Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

DNA Topoisomerases of Leishmania Parasites; Druggable Targets for Drug Discovery

Author(s): Rosa M. Reguera, Ehab K. Elmahallawy, Carlos García-Estrada, Rubén Carbajo-Andrés and Rafael Balaña-Fouce*

Volume 26, Issue 32, 2019

Page: [5900 - 5923] Pages: 24

DOI: 10.2174/0929867325666180518074959

Price: $65

Abstract

DNA topoisomerases (Top) are a group of isomerase enzymes responsible for controlling the topological problems caused by DNA double helix in the cell during the processes of replication, transcription and recombination. Interestingly, these enzymes have been known since long to be key molecular machines in several cellular processes through overwinding or underwinding of DNA in all living organisms. Leishmania, a trypanosomatid parasite responsible for causing fatal diseases mostly in impoverished populations of low-income countries, has a set of six classes of Top enzymes. These are placed in the nucleus and the single mitochondrion and can be deadly targets of suitable drugs. Given the fact that there are clear differences in structure and expression between parasite and host enzymes, numerous studies have reported the therapeutic potential of Top inhibitors as antileishmanial drugs. In this regard, numerous compounds have been described as Top type IB and Top type II inhibitors in Leishmania parasites, such as camptothecin derivatives, indenoisoquinolines, indeno-1,5- naphthyridines, fluoroquinolones, anthracyclines and podophyllotoxins. The aim of this review is to highlight several facts about Top and Top inhibitors as potential antileishmanial drugs, which may represent a promising strategy for the control of this disease of public health importance.

Keywords: Topoisomerases, topoisomerases inhibitors, Leishmania, antileishmanial drugs, drug discovery, neglected tropical diseases.

« Previous Next »
[1]
Leishmaniasis in high-burden countries: an epidemiological update based on data reported in 2014. Wkly. Epidemiol. Rec., 2016, 91(22), 287-296.
[PMID: 27263128]
[2]
Hotez, P.; Aksoy, S. PLOS neglected tropical diseases: ten years of progress in neglected tropical disease control and elimination … More or less. PLoS Negl. Trop. Dis., 2017, 11(4) e0005355
[http://dx.doi.org/10.1371/journal.pntd.0005355] [PMID: 28426662]
[3]
Alvar, J.; Vélez, I.D.; Bern, C.; Herrero, M.; Desjeux, P.; Cano, J.; Jannin, J.; den Boer, M. WHO Leishmaniasis Control Team. Leishmaniasis worldwide and global estimates of its incidence. PLoS One, 2012, 7(5) e35671
[http://dx.doi.org/10.1371/journal.pone.0035671] [PMID: 22693548]
[4]
Millán, J.; Zanet, S.; Gomis, M.; Trisciuoglio, A.; Negre, N.; Ferroglio, E. An investigation into alternative reservoirs of canine leishmaniasis on the endemic island of Mallorca (Spain). Transbound. Emerg. Dis., 2011, 58(4), 352-357.
[http://dx.doi.org/10.1111/j.1865-1682.2011.01212.x] [PMID: 21733133]
[5]
Alexander, B.; Lozano, C.; Barker, D.C.; McCann, S.H.; Adler, G.H. Detection of Leishmania (Viannia) braziliensis complex in wild mammals from Colombian coffee plantations by PCR and DNA hybridization. Acta Trop., 1998, 69(1), 41-50.
[http://dx.doi.org/10.1016/S0001-706X(97)00114-9] [PMID: 9588240]
[6]
Clem, A. A current perspective on leishmaniasis. J. Glob. Infect. Dis., 2010, 2(2), 124-126.
[http://dx.doi.org/10.4103/0974-777X.62863] [PMID: 20606967]
[7]
Oryan, A.; Akbari, M. Worldwide risk factors in leishmaniasis. Asian Pac. J. Trop. Med., 2016, 9(10), 925-932.
[http://dx.doi.org/10.1016/j.apjtm.2016.06.021] [PMID: 27794384]
[8]
Croft, S.L.; Sundar, S.; Fairlamb, A.H. Drug resistance in leishmaniasis. Clin. Microbiol. Rev., 2006, 19(1), 111-126.
[http://dx.doi.org/10.1128/CMR.19.1.111-126.2006] [PMID: 16418526]
[9]
Leishmania/HIV co-infection, south-western Europe, 1990-1998. Wkly. Epidemiol. Rec., 1999, 74(44), 365-375.
[PMID: 10582498]
[10]
Desjeux, P.; Alvar, J. Leishmania/HIV co-infections: epidemiology in Europe. Ann. Trop. Med. Parasitol., 2003, 97(Suppl. 1), 3-15.
[http://dx.doi.org/10.1179/000349803225002499] [PMID: 14678629]
[11]
Balaña-Fouce, R.; Reguera, R.M.; Cubría, J.C.; Ordóñez, D. The pharmacology of leishmaniasis. Gen. Pharmacol., 1998, 30(4), 435-443.
[http://dx.doi.org/10.1016/S0306-3623(97)00268-1] [PMID: 9580315]
[12]
Murray, H.W. Treatment of visceral leishmaniasis (kala-azar): a decade of progress and future approaches. Int. J. Infect. Dis., 2000, 4(3), 158-177.
[http://dx.doi.org/10.1016/S1201-9712(00)90078-X] [PMID: 11179920]
[13]
Guerin, P.J.; Olliaro, P.; Sundar, S.; Boelaert, M.; Croft, S.L.; Desjeux, P.; Wasunna, M.K.; Bryceson, A.D. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect. Dis., 2002, 2(8), 494-501.
[http://dx.doi.org/10.1016/S1473-3099(02)00347-X] [PMID: 12150849]
[14]
Berman, J. Current treatment approaches to leishmaniasis. Curr. Opin. Infect. Dis., 2003, 16(5), 397-401.
[http://dx.doi.org/10.1097/00001432-200310000-00005] [PMID: 14501991]
[15]
Sundar, S.; Chatterjee, M. Visceral leishmaniasis - current therapeutic modalities. Indian J. Med. Res., 2006, 123(3), 345-352.
[PMID: 16778315]
[16]
Alvar, J.; Croft, S.; Olliaro, P. Chemotherapy in the treatment and control of leishmaniasis. Adv. Parasitol., 2006, 61, 223-274.
[http://dx.doi.org/10.1016/S0065-308X(05)61006-8] [PMID: 16735166]
[17]
Mishra, J.; Saxena, A.; Singh, S. Chemotherapy of leishmaniasis: past, present and future. Curr. Med. Chem., 2007, 14(10), 1153-1169.
[http://dx.doi.org/10.2174/092986707780362862] [PMID: 17456028]
[18]
Sundar, S.; Chakravarty, J. Leishmaniasis: an update of current pharmacotherapy. Expert Opin. Pharmacother., 2013, 14(1), 53-63.
[http://dx.doi.org/10.1517/14656566.2013.755515] [PMID: 23256501]
[19]
Nagle, A.S.; Khare, S.; Kumar, A.B.; Supek, F.; Buchynskyy, A.; Mathison, C.J.; Chennamaneni, N.K.; Pendem, N.; Buckner, F.S.; Gelb, M.H.; Molteni, V. Recent developments in drug discovery for leishmaniasis and human African trypanosomiasis. Chem. Rev., 2014, 114(22), 11305-11347.
[http://dx.doi.org/10.1021/cr500365f] [PMID: 25365529]
[20]
Elmahallawy, E.K.; Agil, A. Treatment of leishmaniasis: a review and assessment of recent research. Curr. Pharm. Des., 2015, 21(17), 2259-2275.
[http://dx.doi.org/10.2174/1381612821666141231163053] [PMID: 25543123]
[21]
Singh, K.; Garg, G.; Ali, V. Current therapeutics, their problems and thiol metabolism as potential drug targets in leishmaniasis. Curr. Drug Metab., 2016, 17(9), 897-919.
[http://dx.doi.org/10.2174/1389200217666160819161444] [PMID: 27549807]
[22]
Sundar, S.; Singh, A. Recent developments and future prospects in the treatment of visceral leishmaniasis. Ther. Adv. Infect. Dis., 2016, 3(3-4), 98-109.
[http://dx.doi.org/10.1177/2049936116646063] [PMID: 27536354]
[23]
Croft, S.L. PKDL--a drug related phenomenon? Indian J. Med. Res., 2008, 128(1), 10-11.
[PMID: 18820352]
[24]
Frézard, F.; Demicheli, C.; Ribeiro, R.R. Pentavalent antimonials: new perspectives for old drugs. Molecules, 2009, 14(7), 2317-2336.
[http://dx.doi.org/10.3390/molecules14072317] [PMID: 19633606]
[25]
Perry, M.; Wyllie, S.; Prajapati, V.; Menten, J.; Raab, A.; Feldmann, J.; Chakraborti, D.; Sundar, S.; Boelaert, M.; Picado, A.; Fairlamb, A. Arsenic, antimony, and leishmania: has arsenic contamination of drinking water in India led to treatment- resistant kala-azar? Lancet, 2015, 385(Suppl. 1), S80.
[http://dx.doi.org/10.1016/S0140-6736(15)60395-6] [PMID: 26312902]
[26]
Rodrigo, C.; Weeratunga, P.; Fernando, S.D.; Rajapakse, S. Amphotericin B for treatment of visceral leishmaniasis: Systematic review and meta-analysis of prospective comparative clinical studies including dose-ranging studies. Clin. Microbiol. Infect., 2017, 24(6), 591-598.
[http://dx.doi.org/10.1016/j.cmi.2017.11.008] [PMID: 29138100]
[27]
Balasegaram, M.; Ritmeijer, K.; Lima, M.A.; Burza, S.; Ortiz Genovese, G.; Milani, B.; Gaspani, S.; Potet, J.; Chappuis, F. Liposomal amphotericin B as a treatment for human leishmaniasis. Expert Opin. Emerg. Drugs, 2012, 17(4), 493-510.
[http://dx.doi.org/10.1517/14728214.2012.748036] [PMID: 23167833]
[28]
Sundar, S.; Singh, A.; Rai, M.; Chakravarty, J. Single-dose indigenous liposomal amphotericin B in the treatment of Indian visceral leishmaniasis: a phase 2 study. Am. J. Trop. Med. Hyg., 2015, 92(3), 513-517.
[http://dx.doi.org/10.4269/ajtmh.14-0259] [PMID: 25510715]
[29]
Sindermann, H.; Engel, J. Development of miltefosine as an oral treatment for leishmaniasis. Trans. R. Soc. Trop. Med. Hyg., 2006, 100(Suppl. 1), S17-S20.
[http://dx.doi.org/10.1016/j.trstmh.2006.02.010] [PMID: 16730362]
[30]
Sundar, S.; Singh, A.; Rai, M.; Prajapati, V.K.; Singh, A.K.; Ostyn, B.; Boelaert, M.; Dujardin, J.C.; Chakravarty, J. Efficacy of miltefosine in the treatment of visceral leishmaniasis in India after a decade of use. Clin. Infect. Dis., 2012, 55(4), 543-550.
[http://dx.doi.org/10.1093/cid/cis474] [PMID: 22573856]
[31]
Mondal, D.; Hasnain, M.G.; Hossain, M.S.; Ghosh, D.; Ghosh, P.; Hossain, H.; Baker, J.; Nath, R.; Haque, R.; Matlashewski, G.; Hamano, S. Study on the safety and efficacy of miltefosine for the treatment of children and adolescents with post-kala-azar dermal leishmaniasis in Bangladesh, and an association of serum vitamin E and exposure to arsenic with post-kala-azar dermal leishmaniasis: an open clinical trial and case-control study protocol. BMJ Open, 2016, 6(5)e010050
[http://dx.doi.org/10.1136/bmjopen-2015-010050] [PMID: 27188804]
[32]
Sinha, P.K.; Jha, T.K.; Thakur, C.P.; Nath, D.; Mukherjee, S.; Aditya, A.K.; Sundar, S. Phase 4 pharmacovigilance trial of paromomycin injection for the treatment of visceral leishmaniasis in India. J. Trop. Med., 2011. 2011645203
[http://dx.doi.org/10.1155/2011/645203] [PMID: 22174722]
[33]
Monge-Maillo, B.; López-Vélez, R. Therapeutic options for old world cutaneous leishmaniasis and new world cutaneous and mucocutaneous leishmaniasis. Drugs, 2013, 73(17), 1889-1920.
[http://dx.doi.org/10.1007/s40265-013-0132-1] [PMID: 24170665]
[34]
Roussel, M.; Nacher, M.; Frémont, G.; Rotureau, B.; Clyti, E.; Sainte-Marie, D.; Carme, B.; Pradinaud, R.; Couppié, P. Comparison between one and two injections of pentamidine isethionate, at 7 mg/kg in each injection, in the treatment of cutaneous leishmaniasis in French Guiana. Ann. Trop. Med. Parasitol., 2006, 100(4), 307-314.
[http://dx.doi.org/10.1179/136485906X105561] [PMID: 16762111]
[35]
Diro, E.; Ritmeijer, K.; Boelaert, M.; Alves, F.; Mohammed, R.; Abongomera, C.; Ravinetto, R.; De Crop, M.; Fikre, H.; Adera, C.; Colebunders, R.; van Loen, H.; Menten, J.; Lynen, L.; Hailu, A.; van Griensven, J. Use of pentamidine as secondary prophylaxis to prevent visceral leishmaniasis relapse in HIV infected patients, the first twelve months of a prospective cohort study. PLoS Negl. Trop. Dis., 2015, 9(10) e0004087
[http://dx.doi.org/10.1371/journal.pntd.0004087] [PMID: 26431253]
[36]
Singh, S.; Sivakumar, R. Challenges and new discoveries in the treatment of leishmaniasis. J. Infect. Chemother., 2004, 10(6), 307-315.
[http://dx.doi.org/10.1007/s10156-004-0348-9] [PMID: 15614453]
[37]
Nassiri-Kashani, M.; Firooz, A.; Khamesipour, A.; Mojtahed, F.; Nilforoushzadeh, M.; Hejazi, H.; Bouzari, N.; Dowlati, Y. A randomized, double-blind, placebo-controlled clinical trial of itraconazole in the treatment of cutaneous leishmaniasis. J. Eur. Acad. Dermatol. Venereol., 2005, 19(1), 80-83.
[http://dx.doi.org/10.1111/j.1468-3083.2004.01133.x] [PMID: 15649196]
[38]
Asilian, A.; Sadeghinia, A.; Faghihi, G.; Momeni, A. Comparative study of the efficacy of combined cryotherapy and intralesional meglumine antimoniate (Glucantime) vs. cryotherapy and intralesional meglumine antimoniate (Glucantime) alone for the treatment of cutaneous leishmaniasis. Int. J. Dermatol., 2004, 43(4), 281-283.
[http://dx.doi.org/10.1111/j.1365-4632.2004.02002.x] [PMID: 15090013]
[39]
Machado, P.R.; Lessa, H.; Lessa, M.; Guimarães, L.H.; Bang, H.; Ho, J.L.; Carvalho, E.M. Oral pentoxifylline combined with pentavalent antimony: a randomized trial for mucosal leishmaniasis. Clin. Infect. Dis., 2007, 44(6), 788-793.
[http://dx.doi.org/10.1086/511643] [PMID: 17304449]
[40]
van Griensven, J.; Diro, E.; Lopez-Velez, R.; Boelaert, M.; Lynen, L.; Zijlstra, E.; Dujardin, J.C.; Hailu, A. HIV-1 protease inhibitors for treatment of visceral leishmaniasis in HIV-co-infected individuals. Lancet Infect. Dis., 2013, 13(3), 251-259.
[http://dx.doi.org/10.1016/S1473-3099(12)70348-1] [PMID: 23427890]
[41]
Vologodskii, A.V.; Cozzarelli, N.R. Conformational and thermodynamic properties of supercoiled DNA. Annu. Rev. Biophys. Biomol. Struct., 1994, 23, 609-643.
[http://dx.doi.org/10.1146/annurev.bb.23.060194.003141] [PMID: 7919794]
[42]
Mirkin, S.M. DNA topology: Fundamentals. Encyclopedia of Life Sciences; John Wiley & Sons, 2001, pp. 1-11.
[43]
Deweese, J.E.; Osheroff, M.A.; Osheroff, N. DNA topology and topoisomerases: teaching a “knotty” subject. Biochem. Mol. Biol. Educ., 2008, 37(1), 2-10.
[http://dx.doi.org/10.1002/bmb.20244] [PMID: 19225573]
[44]
Holmes, V.F.; Cozzarelli, N.R. Closing the ring: links between SMC proteins and chromosome partitioning, condensation, and supercoiling. Proc. Natl. Acad. Sci. USA, 2000, 97(4), 1322-1324.
[http://dx.doi.org/10.1073/pnas.040576797] [PMID: 10677457]
[45]
Postow, L.; Peter, B.J.; Cozzarelli, N.R. Knot what we thought before: the twisted story of replication. BioEssays, 1999, 21(10), 805-808.
[http://dx.doi.org/10.1002/(SICI)1521-1878(199910)21:10<805:AID-BIES1>3.0.CO;2-7] [PMID: 10497329]
[46]
Champoux, J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 2001, 70, 369-413.
[http://dx.doi.org/10.1146/annurev.biochem.70.1.369] [PMID: 11395412]
[47]
Wang, J.C. Interaction between DNA and an Escherichia coli protein omega. J. Mol. Biol., 1971, 55(3), 523-533.
[http://dx.doi.org/10.1016/0022-2836(71)90334-2] [PMID: 4927945]
[48]
Roca, J. The mechanisms of DNA topoisomerases. Trends Biochem. Sci., 1995, 20(4), 156-160.
[http://dx.doi.org/10.1016/S0968-0004(00)88993-8] [PMID: 7770916]
[49]
Wang, J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol., 2002, 3(6), 430-440.
[http://dx.doi.org/10.1038/nrm831] [PMID: 12042765]
[50]
Wang, J.C. DNA topoisomerases: why so many? J. Biol. Chem., 1991, 266(11), 6659-6662.
[PMID: 1849888]
[51]
Baker, N.M.; Rajan, R.; Mondragón, A. Structural studies of type I topoisomerases. Nucleic Acids Res., 2009, 37(3), 693-701.
[http://dx.doi.org/10.1093/nar/gkn1009] [PMID: 19106140]
[52]
Slesarev, A.I.; Stetter, K.O.; Lake, J.A.; Gellert, M.; Krah, R.; Kozyavkin, S.A. DNA topoisomerase V is a relative of eukaryotic topoisomerase I from a hyperthermophilic prokaryote. Nature, 1993, 364(6439), 735-737.
[http://dx.doi.org/10.1038/364735a0] [PMID: 8395022]
[53]
Forterre, P.; Gribaldo, S.; Gadelle, D.; Serre, M.C. Origin and evolution of DNA topoisomerases. Biochimie, 2007, 89(4), 427-446.
[http://dx.doi.org/10.1016/j.biochi.2006.12.009] [PMID: 17293019]
[54]
Forterre, P. DNA topoisomerase V: a new fold of mysterious origin. Trends Biotechnol., 2006, 24(6), 245-247.
[http://dx.doi.org/10.1016/j.tibtech.2006.04.006] [PMID: 16650908]
[55]
Slesarev, A.I.; Zaitzev, D.A.; Kopylov, V.M.; Stetter, K.O.; Kozyavkin, S.A. DNA topoisomerase III from extremely thermophilic archaebacteria. ATP-independent type I topoisomerase from Desulfurococcus amylolyticus drives extensive unwinding of closed circular DNA at high temperature. J. Biol. Chem., 1991, 266(19), 12321-12328.
[PMID: 1648092]
[56]
Iyer, L.M.; Balaji, S.; Koonin, E.V.; Aravind, L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res., 2006, 117(1), 156-184.
[http://dx.doi.org/10.1016/j.virusres.2006.01.009] [PMID: 16494962]
[57]
Raoult, D.; Audic, S.; Robert, C.; Abergel, C.; Renesto, P.; Ogata, H.; La Scola, B.; Suzan, M.; Claverie, J.M. The 1.2-megabase genome sequence of Mimivirus. Science, 2004, 306(5700), 1344-1350.
[http://dx.doi.org/10.1126/science.1101485] [PMID: 15486256]
[58]
Garnier, F.; Debat, H.; Nadal, M. Type IA DNA Topoisomerases: a universal core and multiple activities. Methods Mol. Biol., 2018, 1703, 1-20.
[http://dx.doi.org/10.1007/978-1-4939-7459-7_1] [PMID: 29177730]
[59]
Kozyavkin, S.A.; Krah, R.; Gellert, M.; Stetter, K.O.; Lake, J.A.; Slesarev, A.I. A reverse gyrase with an unusual structure. A type I DNA topoisomerase from the hyperthermophile Methanopyrus kandleri is a two-subunit protein. J. Biol. Chem., 1994, 269(15), 11081-11089.
[PMID: 8157633]
[60]
Krah, R.; O’Dea, M.H.; Gellert, M. Reverse gyrase from Methanopyrus kandleri. Reconstitution of an active extremozyme from its two recombinant subunits. J. Biol. Chem., 1997, 272(21), 13986-13990.
[http://dx.doi.org/10.1074/jbc.272.21.13986] [PMID: 9153263]
[61]
Tse-Dinh, Y.C.; Beran-Steed, R.K. Escherichia coli DNA topoisomerase I is a zinc metalloprotein with three repetitive zinc-binding domains. J. Biol. Chem., 1988, 263(31), 15857-15859.
[PMID: 2846526]
[62]
Krogh, B.O.; Shuman, S. A poxvirus-like type IB topoisomerase family in bacteria. Proc. Natl. Acad. Sci. USA, 2002, 99(4), 1853-1858.
[http://dx.doi.org/10.1073/pnas.032613199] [PMID: 11830640]
[63]
Champoux, J.J. DNA is linked to the rat liver DNA nicking-closing enzyme by a phosphodiester bond to tyrosine. J. Biol. Chem., 1981, 256(10), 4805-4809.
[PMID: 6262303]
[64]
Leppard, J.B.; Champoux, J.J. Human DNA topoisomerase I: relaxation, roles, and damage control. Chromosoma, 2005, 114(2), 75-85.
[http://dx.doi.org/10.1007/s00412-005-0345-5] [PMID: 15830206]
[65]
Fujimoto, D.F.; Pinilla, C.; Segall, A.M. New peptide inhibitors of type IB topoisomerases: similarities and differences vis-a-vis inhibitors of tyrosine recombinases. J. Mol. Biol., 2006, 363(5), 891-907.
[http://dx.doi.org/10.1016/j.jmb.2006.08.052] [PMID: 16996084]
[66]
Tse-Dinh, Y.C. Bacterial and archeal type I topoisomerases. Biochim. Biophys. Acta, 1998, 1400(1-3), 19-27.
[http://dx.doi.org/10.1016/S0167-4781(98)00125-0] [PMID: 9748482]
[67]
Taneja, B.; Schnurr, B.; Slesarev, A.; Marko, J.F.; Mondragón, A. Topoisomerase V relaxes supercoiled DNA by a constrained swiveling mechanism. Proc. Natl. Acad. Sci. USA, 2007, 104(37), 14670-14675.
[http://dx.doi.org/10.1073/pnas.0701989104] [PMID: 17804808]
[68]
Wang, J.C. Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q. Rev. Biophys., 1998, 31(2), 107-144.
[http://dx.doi.org/10.1017/S0033583598003424] [PMID: 9794033]
[69]
Corbett, K.D.; Berger, J.M. Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu. Rev. Biophys. Biomol. Struct., 2004, 33, 95-118.
[http://dx.doi.org/10.1146/annurev.biophys.33.110502.140357] [PMID: 15139806]
[70]
Schoeffler, A.J.; Berger, J.M. DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys., 2008, 41(1), 41-101.
[http://dx.doi.org/10.1017/S003358350800468X] [PMID: 18755053]
[71]
Berger, J.M.; Gamblin, S.J.; Harrison, S.C.; Wang, J.C. Structure and mechanism of DNA topoisomerase II. Nature, 1996, 379(6562), 225-232.
[http://dx.doi.org/10.1038/379225a0] [PMID: 8538787]
[72]
Nitiss, J.L. DNA topoisomerase II and its growing repertoire of biological functions. Nat. Rev. Cancer, 2009, 9(5), 327-337.
[http://dx.doi.org/10.1038/nrc2608] [PMID: 19377505]
[73]
Bollimpelli, V.S.; Dholaniya, P.S.; Kondapi, A.K. Topoisomerase IIβ and its role in different biological contexts. Arch. Biochem. Biophys., 2017, 633, 78-84.
[http://dx.doi.org/10.1016/j.abb.2017.06.021] [PMID: 28669856]
[74]
Kreuzer, K.N. Bacteriophage T4, a model system for understanding the mechanism of type II topoisomerase inhibitors. Biochim. Biophys. Acta, 1998, 1400(1-3), 339-347.
[http://dx.doi.org/10.1016/S0167-4781(98)00145-6] [PMID: 9748648]
[75]
Gadelle, D.; Filée, J.; Buhler, C.; Forterre, P. Phylogenomics of type II DNA topoisomerases. BioEssays, 2003, 25(3), 232-242.
[http://dx.doi.org/10.1002/bies.10245] [PMID: 12596227]
[76]
Gubaev, A.; Klostermeier, D. The mechanism of negative DNA supercoiling: a cascade of DNA-induced conformational changes prepares gyrase for strand passage. DNA Repair (Amst.), 2014, 16, 23-34.
[http://dx.doi.org/10.1016/j.dnarep.2014.01.011] [PMID: 24674625]
[77]
Bergerat, A.; de Massy, B.; Gadelle, D.; Varoutas, P.C.; Nicolas, A.; Forterre, P. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature, 1997, 386(6623), 414-417.
[http://dx.doi.org/10.1038/386414a0] [PMID: 9121560]
[78]
Shapiro, T.A.; Englund, P.T. The structure and replication of kinetoplast DNA. Annu. Rev. Microbiol., 1995, 49, 117-143.
[http://dx.doi.org/10.1146/annurev.mi.49.100195.001001] [PMID: 8561456]
[79]
Stuart, K.; Panigrahi, A.K. RNA editing: complexity and complications. Mol. Microbiol., 2002, 45(3), 591-596.
[http://dx.doi.org/10.1046/j.1365-2958.2002.03028.x] [PMID: 12139607]
[80]
Shlomai, J. The structure and replication of kinetoplast DNA. Curr. Mol. Med., 2004, 4(6), 623-647.
[http://dx.doi.org/10.2174/1566524043360096] [PMID: 15357213]
[81]
Liu, B.; Liu, Y.; Motyka, S.A.; Agbo, E.E.E.; Englund, P.T. Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol., 2005, 21(8), 363-369.
[http://dx.doi.org/10.1016/j.pt.2005.06.008] [PMID: 15967722]
[82]
Jensen, R.E.; Englund, P.T. Network news: the replication of kinetoplast DNA. Annu. Rev. Microbiol., 2012, 66, 473-491.
[http://dx.doi.org/10.1146/annurev-micro-092611-150057] [PMID: 22994497]
[83]
Balaña-Fouce, R.; Alvarez-Velilla, R.; Fernández-Prada, C.; García-Estrada, C.; Reguera, R.M. Trypanosomatids topoisomerase re-visited. New structural findings and role in drug discovery. Int. J. Parasitol. Drugs Drug Resist., 2014, 4(3), 326-337.
[http://dx.doi.org/10.1016/j.ijpddr.2014.07.006] [PMID: 25516844]
[84]
Reguera, R.M.; Redondo, C.M.; Gutierrez de Prado, R.; Pérez-Pertejo, Y.; Balaña-Fouce, R. DNA topoisomerase I from parasitic protozoa: a potential target for chemotherapy. Biochim. Biophys. Acta, 2006, 1759(3-4), 117-131.
[http://dx.doi.org/10.1016/j.bbaexp.2006.03.006] [PMID: 16757380]
[85]
Broccoli, S.; Marquis, J.F.; Papadopoulou, B.; Olivier, M.; Drolet, M. Characterization of a Leishmania donovani gene encoding a protein that closely resembles a type IB topoisomerase. Nucleic Acids Res., 1999, 27(13), 2745-2752.
[http://dx.doi.org/10.1093/nar/27.13.2745] [PMID: 10373592]
[86]
Bodley, A.L.; Chakraborty, A.K.; Xie, S.; Burri, C.; Shapiro, T.A. An unusual type IB topoisomerase from African trypanosomes. Proc. Natl. Acad. Sci. USA, 2003, 100(13), 7539-7544.
[http://dx.doi.org/10.1073/pnas.1330762100] [PMID: 12810956]
[87]
Villa, H.; Otero Marcos, A.R.; Reguera, R.M.; Balaña-Fouce, R.; García-Estrada, C.; Pérez-Pertejo, Y.; Tekwani, B.L.; Myler, P.J.; Stuart, K.D.; Bjornsti, M.A.; Ordóñez, D. A novel active DNA topoisomerase I in Leishmania donovani. J. Biol. Chem., 2003, 278(6), 3521-3526.
[http://dx.doi.org/10.1074/jbc.M203991200] [PMID: 12444094]
[88]
Díaz González, R.; Pérez Pertejo, Y.; Redondo, C.M.; Pommier, Y.; Balaña-Fouce, R.; Reguera, R.M. Structural insights on the small subunit of DNA topoisomerase I from the unicellular parasite Leishmania donovani. Biochimie, 2007, 89(12), 1517-1527.
[http://dx.doi.org/10.1016/j.biochi.2007.07.015] [PMID: 17900785]
[89]
Díaz González, R.; Pérez Pertejo, Y.; Ordóñez, D.; Balaña-Fouce, R.; Reguera, R.M. Deletion study of DNA topoisomerase IB from Leishmania donovani: searching for a minimal functional heterodimer. PLoS One, 2007, 2(11) e1177
[http://dx.doi.org/10.1371/journal.pone.0001177] [PMID: 18000548]
[90]
Das, B.B.; Sen, N.; Ganguly, A.; Majumder, H.K. Reconstitution and functional characterization of the unusual bi-subunit type I DNA topoisomerase from Leishmania donovani. FEBS Lett., 2004, 565(1-3), 81-88.
[http://dx.doi.org/10.1016/j.febslet.2004.03.078] [PMID: 15135057]
[91]
Bakshi, R.P.; Shapiro, T.A. DNA topoisomerases as targets for antiprotozoal therapy. Mini Rev. Med. Chem., 2003, 3(6), 597-608.
[http://dx.doi.org/10.2174/1389557033487863] [PMID: 12871162]
[92]
Redinbo, M.R.; Stewart, L.; Kuhn, P.; Champoux, J.J.; Hol, W.G. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science, 1998, 279(5356), 1504-1513.
[http://dx.doi.org/10.1126/science.279.5356.1504] [PMID: 9488644]
[93]
Das, B.B.; Sen, N.; Dasgupta, S.B.; Ganguly, A.; Majumder, H.K. N-terminal region of the large subunit of Leishmania donovani bisubunit topoisomerase I is involved in DNA relaxation and interaction with the smaller subunit. J. Biol. Chem., 2005, 280(16), 16335-16344.
[http://dx.doi.org/10.1074/jbc.M412417200] [PMID: 15711017]
[94]
Diaz-González, R.; Pérez-Pertejo, Y.; Pommier, Y.; Balaña-Fouce, R.; Reguera, R.M. Mutational study of the “catalytic tetrad” of DNA topoisomerase IB from the hemoflagellate Leishmania donovani: Role of Asp-353 and Asn-221 in camptothecin resistance. Biochem. Pharmacol., 2008, 76(5), 608-619.
[http://dx.doi.org/10.1016/j.bcp.2008.06.019] [PMID: 18655776]
[95]
Ganguly, A.; Sengupta, S.; Bosedasgupta, S.; Roy, A.; Majumder, H.K. Mutational studies reveal lysine 352 on the large subunit is indispensable for catalytic activity of bi-subunit topoisomerase I from Leishmania donovani. Mol. Biochem. Parasitol., 2009, 165(1), 57-66.
[http://dx.doi.org/10.1016/j.molbiopara.2009.01.002] [PMID: 19393162]
[96]
Sengupta, S.; Ganguly, A.; Roy, A.; Bosedasgupta, S.; D’Annessa, I.; Desideri, A.; Majumder, H.K. ATP independent type IB topoisomerase of Leishmania donovani is stimulated by ATP: an insight into the functional mechanism. Nucleic Acids Res., 2011, 39(8), 3295-3309.
[http://dx.doi.org/10.1093/nar/gkq1284] [PMID: 21186185]
[97]
Prada, C.F.; Álvarez-Velilla, R.; Díaz-Gozález, R.; Pérez-Pertejo, Y.; Balaña-Fouce, R.; Reguera, R.M. Identification and characterization of the regions involved in the nuclear translocation of the heterodimeric leishmanial DNA topoisomerase IB. PLoS One, 2013, 8(9) e73565
[http://dx.doi.org/10.1371/journal.pone.0073565] [PMID: 24023887]
[98]
Stewart, L.; Ireton, G.C.; Champoux, J.J. A functional linker in human topoisomerase I is required for maximum sensitivity to camptothecin in a DNA relaxation assay. J. Biol. Chem., 1999, 274(46), 32950-32960.
[http://dx.doi.org/10.1074/jbc.274.46.32950] [PMID: 10551862]
[99]
Ireton, G.C.; Stewart, L.; Parker, L.H.; Champoux, J.J. Expression of human topoisomerase I with a partial deletion of the linker region yields monomeric and dimeric enzymes that respond differently to camptothecin. J. Biol. Chem., 2000, 275(33), 25820-25830.
[http://dx.doi.org/10.1074/jbc.M002144200] [PMID: 10827183]
[100]
Das, B.B.; Bose Dasgupta, S.; Ganguly, A.; Mazumder, S.; Roy, A.; Majumder, H.K. Leishmania donovani bisubunit topoisomerase I gene fusion leads to an active enzyme with conserved type IB enzyme function. FEBS J., 2007, 274(1), 150-163.
[http://dx.doi.org/10.1111/j.1742-4658.2006.05572.x] [PMID: 17222179]
[101]
Bosedasgupta, S.; Das, B.B.; Sengupta, S.; Ganguly, A.; Roy, A.; Tripathi, G.; Majumder, H.K. Amino acids 39-456 of the large subunit and 210-262 of the small subunit constitute the minimal functionally interacting fragments of the unusual heterodimeric topoisomerase IB of Leishmania. Biochem. J., 2008, 409(2), 481-489.
[http://dx.doi.org/10.1042/BJ20071358] [PMID: 17924857]
[102]
Prada, C.F.; Alvarez-Velilla, R.; Diaz-González, R.; Prieto, C.; Pérez-Pertejo, Y.; Balaña-Fouce, R.; Reguera, R.M. A pentapeptide signature motif plays a pivotal role in Leishmania DNA topoisomerase IB activity and camptothecin sensitivity. Biochim. Biophys. Acta, 2012, 1820(12), 2062-2071.
[http://dx.doi.org/10.1016/j.bbagen.2012.09.005] [PMID: 23000572]
[103]
Roy, A.; Tesauro, C.; Frøhlich, R.; Hede, M.S.; Nielsen, M.J.; Kjeldsen, E.; Bonven, B.; Stougaard, M.; Gromova, I.; Knudsen, B.R. Decreased camptothecin sensitivity of the stem-cell-like fraction of Caco2 cells correlates with an altered phosphorylation pattern of topoisomerase I. PLoS One, 2014, 9(6) e99628
[http://dx.doi.org/10.1371/journal.pone.0099628] [PMID: 24960044]
[104]
Campbell, D.A.; Thomas, S.; Sturm, N.R. Transcription in kinetoplastid protozoa: why be normal? Microbes Infect., 2003, 5(13), 1231-1240.
[http://dx.doi.org/10.1016/j.micinf.2003.09.005] [PMID: 14623019]
[105]
Martínez-Calvillo, S.; Vizuet-de-Rueda, J.C.; Florencio-Martínez, L.E.; Manning-Cela, R.G.; Figueroa-Angulo, E.E. Gene expression in trypanosomatid parasites. J. Biomed. Biotechnol., 2010, 2010 525241
[http://dx.doi.org/10.1155/2010/525241] [PMID: 20169133]
[106]
Bakshi, R.P.; Shapiro, T.A. RNA interference of Trypanosoma brucei topoisomerase IB: both subunits are essential. Mol. Biochem. Parasitol., 2004, 136(2), 249-255.
[http://dx.doi.org/10.1016/j.molbiopara.2004.04.006] [PMID: 15478803]
[107]
Balaña-Fouce, R.; García-Estrada, C.; Pérez-Pertejo, Y.; Reguera, R.M. Gene disruption of the DNA topoisomerase IB small subunit induces a non-viable phenotype in the hemoflagellate Leishmania major. BMC Microbiol., 2008, 8, 113.
[http://dx.doi.org/10.1186/1471-2180-8-113] [PMID: 18611247]
[108]
Li, Z.; Mondragón, A.; Hiasa, H.; Marians, K.J.; DiGate, R.J. Identification of a unique domain essential for Escherichia coli DNA topoisomerase III-catalysed decatenation of replication intermediates. Mol. Microbiol., 2000, 35(4), 888-895.
[http://dx.doi.org/10.1046/j.1365-2958.2000.01763.x] [PMID: 10692165]
[109]
Viard, T.; de la Tour, C.B. Type IA topoisomerases: a simple puzzle? Biochimie, 2007, 89(4), 456-467.
[http://dx.doi.org/10.1016/j.biochi.2006.10.013] [PMID: 17141394]
[110]
Scocca, J.R.; Shapiro, T.A. A mitochondrial topoisomerase IA essential for late theta structure resolution in African trypanosomes. Mol. Microbiol., 2008, 67(4), 820-829.
[http://dx.doi.org/10.1111/j.1365-2958.2007.06087.x] [PMID: 18179422]
[111]
Banerjee, B.; Sen, N.; Majumder, H.K. Identification of a functional type IA topoisomerase, LdTopIIIβ, from kinetoplastid parasite Leishmania donovani. Enzyme Res., 2011. 2011230542
[http://dx.doi.org/10.4061/2011/230542] [PMID: 21637326]
[112]
Kim, H.S.; Cross, G.A. TOPO3alpha influences antigenic variation by monitoring expression-site-associated VSG switching in Trypanosoma brucei. PLoS Pathog., 2010, 6(7)e1000992
[http://dx.doi.org/10.1371/journal.ppat.1000992] [PMID: 20628569]
[113]
Shapiro, T.A.; Klein, V.A.; Englund, P.T. Drug-promoted cleavage of kinetoplast DNA minicircles. Evidence for type II topoisomerase activity in trypanosome mitochondria. J. Biol. Chem., 1989, 264(7), 4173-4178.
[PMID: 2537308]
[114]
Shapiro, T.A. Mitochondrial topoisomerase II activity is essential for kinetoplast DNA minicircle segregation. Mol. Cell. Biol., 1994, 14(6), 3660-3667.
[http://dx.doi.org/10.1128/MCB.14.6.3660] [PMID: 8196610]
[115]
Kulikowicz, T.; Shapiro, T.A. Distinct genes encode type II Topoisomerases for the nucleus and mitochondrion in the protozoan parasite Trypanosoma brucei. J. Biol. Chem., 2006, 281(6), 3048-3056.
[http://dx.doi.org/10.1074/jbc.M505977200] [PMID: 16316982]
[116]
Sengupta, T.; Mukherjee, M.; Mandal, C.; Das, A.; Majumder, H.K. Functional dissection of the C-terminal domain of type II DNA topoisomerase from the kinetoplastid hemoflagellate Leishmania donovani. Nucleic Acids Res., 2003, 31(18), 5305-5316.
[http://dx.doi.org/10.1093/nar/gkg727] [PMID: 12954766]
[117]
Hanke, T.; Ramiro, M.J.; Trigueros, S.; Roca, J.; Larraga, V. Cloning, functional analysis and post-transcriptional regulation of a type II DNA topoisomerase from Leishmania infantum. A new potential target for anti-parasite drugs. Nucleic Acids Res., 2003, 31(16), 4917-4928.
[http://dx.doi.org/10.1093/nar/gkg671] [PMID: 12907735]
[118]
Sengupta, T.; Mukherjee, M.; Das, A.; Mandal, C.; Das, R.; Mukherjee, T.; Majumder, H.K. Characterization of the ATPase activity of topoisomerase II from Leishmania donovani and identification of residues conferring resistance to etoposide. Biochem. J., 2005, 390(Pt 2), 419-426.
[http://dx.doi.org/10.1042/BJ20042128] [PMID: 15901238]
[119]
Sengupta, T.; Mukherjee, M.; Das, R.; Das, A.; Majumder, H.K. Characterization of the DNA-binding domain and identification of the active site residue in the ‘Gyr A’ half of Leishmania donovani topoisomerase II. Nucleic Acids Res., 2005, 33(8), 2364-2373.
[http://dx.doi.org/10.1093/nar/gki527] [PMID: 15860773]
[120]
Das, A.; Dasgupta, A.; Sharma, S.; Ghosh, M.; Sengupta, T.; Bandopadhyay, S.; Majumder, H.K. Characterisation of the gene encoding type II DNA topoisomerase from Leishmania donovani: a key molecular target in antileishmanial therapy. Nucleic Acids Res., 2001, 29(9), 1844-1851.
[http://dx.doi.org/10.1093/nar/29.9.1844] [PMID: 11328867]
[121]
Lindsay, M.E.; Gluenz, E.; Gull, K.; Englund, P.T. A new function of Trypanosoma brucei mitochondrial topoisomerase II is to maintain kinetoplast DNA network topology. Mol. Microbiol., 2008, 70(6), 1465-1476.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06493.x] [PMID: 19019151]
[122]
Pommier, Y.; Leo, E.; Zhang, H.; Marchand, C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol., 2010, 17(5), 421-433.
[http://dx.doi.org/10.1016/j.chembiol.2010.04.012] [PMID: 20534341]
[123]
Pommier, Y. Drugging topoisomerases: lessons and challenges. ACS Chem. Biol., 2013, 8(1), 82-95.
[http://dx.doi.org/10.1021/cb300648v] [PMID: 23259582]
[124]
Kohn, K.W.; Pommier, Y. Molecular and biological determinants of the cytotoxic actions of camptothecins. Perspective for the development of new topoisomerase I inhibitors. Ann. N. Y. Acad. Sci., 2000, 922, 11-26.
[http://dx.doi.org/10.1111/j.1749-6632.2000.tb07021.x] [PMID: 11193886]
[125]
Pommier, Y. Camptothecins and topoisomerase I: a foot in the door. Targeting the genome beyond topoisomerase I with camptothecins and novel anticancer drugs: importance of DNA replication, repair and cell cycle checkpoints. Curr. Med. Chem. Anticancer Agents, 2004, 4(5), 429-434.
[http://dx.doi.org/10.2174/1568011043352777] [PMID: 15379698]
[126]
Nitiss, J.L. DNA topoisomerases in cancer chemotherapy: using enzymes to generate selective DNA damage. Curr. Opin. Investig. Drugs, 2002, 3(10), 1512-1516.
[PMID: 12431029]
[127]
Chen, T.; Sun, Y.; Ji, P.; Kopetz, S.; Zhang, W. Topoisomerase IIα in chromosome instability and personalized cancer therapy. Oncogene, 2015, 34(31), 4019-4031.
[http://dx.doi.org/10.1038/onc.2014.332] [PMID: 25328138]
[128]
Balaña-Fouce, R.; Redondo, C.M.; Pérez-Pertejo, Y.; Díaz-González, R.; Reguera, R.M. Targeting atypical trypanosomatid DNA topoisomerase I. Drug Discov. Today, 2006, 11(15-16), 733-740.
[http://dx.doi.org/10.1016/j.drudis.2006.06.014] [PMID: 16846801]
[129]
Das, B.B.; Sengupta, T.; Ganguly, A.; Majumder, H.K. Topoisomerases of kinetoplastid parasites: why so fascinating? Mol. Microbiol., 2006, 62(4), 917-927.
[http://dx.doi.org/10.1111/j.1365-2958.2006.05428.x] [PMID: 17042788]
[130]
Chen, S.H.; Chan, N.L.; Hsieh, T.S. New mechanistic and functional insights into DNA topoisomerases. Annu. Rev. Biochem., 2013, 82, 139-170.
[http://dx.doi.org/10.1146/annurev-biochem-061809-100002] [PMID: 23495937]
[131]
Wall, M.E.; Wani, M.C.; Cook, C.E.; Palmer, K.H.; McPhail, A.T.; Sim, G.A. Plant antitumor agents. I. The isolation and structure of camptothecin, a novel alkaloidal leukemia and tumor inhibitor from Camptotheca acuminate. J. Am. Chem. Soc., 1966, 18(16), 3888-3890.
[http://dx.doi.org/10.1021/ja00968a057]
[132]
Wall, M.E.; Wani, M.C. Camptothecin and taxol: discovery to clinic--thirteenth Bruce F. Cain Memorial Award Lecture. Cancer Res., 1995, 55(4), 753-760.
[PMID: 7850785]
[133]
Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer, 2006, 6(10), 789-802.
[http://dx.doi.org/10.1038/nrc1977] [PMID: 16990856]
[134]
Ulukan, H.; Swaan, P.W. Camptothecins: a review of their chemotherapeutic potential. Drugs, 2002, 62(14), 2039-2057.
[http://dx.doi.org/10.2165/00003495-200262140-00004] [PMID: 12269849]
[135]
Li, Q.Y.; Zu, Y.G.; Shi, R.Z.; Yao, L.P. Review camptothecin: current perspectives. Curr. Med. Chem., 2006, 13(17), 2021-2039.
[http://dx.doi.org/10.2174/092986706777585004] [PMID: 16842195]
[136]
Mamidala, R.; Majumdar, P.; Jha, K.K.; Bathula, C.; Agarwal, R.; Chary, M.T.; Majumder, H.K.; Munshi, P.; Sen, S. Identification of Leishmania donovani Topoisomerase 1 inhibitors via intuitive scaffold hopping and bioisosteric modification of known Top 1 inhibitors. Sci. Rep., 2016, 6, 26603.
[http://dx.doi.org/10.1038/srep26603] [PMID: 27221589]
[137]
Fassberg, J.; Stella, V.J. A kinetic and mechanistic study of the hydrolysis of camptothecin and some analogues. J. Pharm. Sci., 1992, 81(7), 676-684.
[http://dx.doi.org/10.1002/jps.2600810718] [PMID: 1403703]
[138]
Denny, W.A. Emerging DNA topisomerase inhibitors as anticancer drugs. Expert Opin. Emerg. Drugs, 2004, 9(1), 105-133.
[http://dx.doi.org/10.1517/eoed.9.1.105.32948] [PMID: 15155139]
[139]
Liu, L.F.; Desai, S.D.; Li, T.K.; Mao, Y.; Sun, M.; Sim, S.P. Mechanism of action of camptothecin. Ann. N. Y. Acad. Sci., 2000, 922, 1-10.
[http://dx.doi.org/10.1111/j.1749-6632.2000.tb07020.x] [PMID: 11193884]
[140]
Pommier, Y. DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem. Rev., 2009, 109(7), 2894-2902.
[http://dx.doi.org/10.1021/cr900097c] [PMID: 19476377]
[141]
Tomicic, M.T.; Kaina, B. Topoisomerase degradation, DSB repair, p53 and IAPs in cancer cell resistance to camptothecin-like topoisomerase I inhibitors. Biochim. Biophys. Acta, 2013, 1835(1), 11-27.
[PMID: 23006513]
[142]
Staker, B.L.; Hjerrild, K.; Feese, M.D.; Behnke, C.A.; Burgin, A.B., Jr; Stewart, L. The mechanism of topoisomerase I poisoning by a camptothecin analog. Proc. Natl. Acad. Sci. USA, 2002, 99(24), 15387-15392.
[http://dx.doi.org/10.1073/pnas.242259599] [PMID: 12426403]
[143]
Bodley, A.L.; Shapiro, T.A. Molecular and cytotoxic effects of camptothecin derivatives, a topoisomerase IB leading to a strong leishmanicide effect. Biochem. Pharmacol., 2013, 85(10), 1433-1440.
[http://dx.doi.org/10.1016/j.bcp.2013.02.024] [PMID: 23466420]
[144]
Banerjee, B.; Roy, A.; Sen, N.; Majumder, H.K. A tyrosyl DNA phosphodiesterase 1 from kinetoplastid parasite Leishmania donovani (LdTdp1) capable of removing topo I-DNA covalent complexes. Mol. Microbiol., 2010, 78(1), 119-137.
[http://dx.doi.org/10.1111/j.1365-2958.2010.07318.x] [PMID: 20659295]
[145]
Sen, N.; Das, B.B.; Ganguly, A.; Mukherjee, T.; Tripathi, G.; Bandyopadhyay, S.; Rakshit, S.; Sen, T.; Majumder, H.K. Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. Cell Death Differ., 2004, 11(8), 924-936.
[http://dx.doi.org/10.1038/sj.cdd.4401435] [PMID: 15118764]
[146]
Kollmannsberger, C.; Mross, K.; Jakob, A.; Kanz, L.; Bokemeyer, C. Topotecan - A novel topoisomerase I inhibitor: pharmacology and clinical experience. Oncology, 1999, 56(1), 1-12.
[http://dx.doi.org/10.1159/000011923] [PMID: 9885371]
[147]
Schiller, J.H. Future role of topotecan in the treatment of lung cancer. Oncology, 2001, 61(Suppl. 1), 55-59.
[http://dx.doi.org/10.1159/000055393] [PMID: 11598416]
[148]
Masuda, N.; Fukuoka, M.; Kusunoki, Y.; Matsui, K.; Takifuji, N.; Kudoh, S.; Negoro, S.; Nishioka, M.; Nakagawa, K.; Takada, M. CPT-11: a new derivative of camptothecin for the treatment of refractory or relapsed small-cell lung cancer. J. Clin. Oncol., 1992, 10(8), 1225-1229.
[http://dx.doi.org/10.1200/JCO.1992.10.8.1225] [PMID: 1321891]
[149]
Rivory, L.P. Irinotecan (CPT-11): a brief overview. Clin. Exp. Pharmacol. Physiol., 1996, 23(10-11), 1000-1004.
[http://dx.doi.org/10.1111/j.1440-1681.1996.tb01158.x] [PMID: 8911750]
[150]
Das, B.B.; Sen, N.; Roy, A.; Dasgupta, S.B.; Ganguly, A.; Mohanta, B.C.; Dinda, B.; Majumder, H.K. Differential induction of Leishmania donovani bi-subunit topoisomerase I-DNA cleavage complex by selected flavones and camptothecin: activity of flavones against camptothecin-resistant topoisomerase I. Nucleic Acids Res., 2006, 34(4), 1121-1132.
[http://dx.doi.org/10.1093/nar/gkj502] [PMID: 16488884]
[151]
Das, B.B.; Sen, N.; Dasgupta, S.B.; Ganguly, A.; Das, R.; Majumder, H.K. Topoisomerase research of kinetoplastid parasite Leishmania, with special reference to development of therapeutics. Indian J. Med. Res., 2006, 123(3), 221-232.
[PMID: 16778306]
[152]
Deterding, A.; Dungey, F.A.; Thompson, K.A.; Steverding, D. Anti-trypanosomal activities of DNA topoisomerase inhibitors. Acta Trop., 2005, 93(3), 311-316.
[http://dx.doi.org/10.1016/j.actatropica.2005.01.005] [PMID: 15715983]
[153]
D’Annessa, I.; Castelli, S.; Desideri, A. Topoisomerase 1B as a target against leishmaniasis. Mini Rev. Med. Chem., 2015, 15(3), 203-210.
[http://dx.doi.org/10.2174/138955751503150312120912] [PMID: 25769969]
[154]
Pratesi, G.; Beretta, G.L.; Zunino, F. Gimatecan, a novel camptothecin with a promising preclinical profile. Anticancer Drugs, 2004, 15(6), 545-552.
[http://dx.doi.org/10.1097/01.cad.0000131687.08175.14] [PMID: 15205595]
[155]
Di Francesco, A.M.; Riccardi, A.; Barone, G.; Rutella, S.; Meco, D.; Frapolli, R.; Zucchetti, M.; D’Incalci, M.; Pisano, C.; Carminati, P.; Riccardi, R. The novel lipophilic camptothecin analogue gimatecan is very active in vitro in human neuroblastoma: a comparative study with SN38 and topotecan. Biochem. Pharmacol., 2005, 70(8), 1125-1136.
[http://dx.doi.org/10.1016/j.bcp.2005.07.009] [PMID: 16139802]
[156]
Prada, C.F.; Alvarez-Velilla, R.; Balaña-Fouce, R.; Prieto, C.; Calvo-Álvarez, E.; Escudero-Martínez, J.M.; Requena, J.M.; Ordóñez, C.; Desideri, A.; Pérez-Pertejo, Y.; Reguera, R.M. Gimatecan and other camptothecin derivatives poison Leishmania DNA-topoisomerase IB leading to a strong leishmanicidal effect. Biochem. Pharmacol., 2013, 85(10), 1433-1440.
[http://dx.doi.org/10.1016/j.bcp.2013.02.024] [PMID: 23466420]
[157]
Armand, J.P. CPT-11: clinical experience in phase I studies. Semin. Oncol., 1996, 23(1)(Suppl. 3), 27-33.
[PMID: 8633250]
[158]
Sánchez, C.; Méndez, C.; Salas, J.A. Indolocarbazole natural products: occurrence, biosynthesis, and biological activity. Nat. Prod. Rep., 2006, 23(6), 1007-1045.
[http://dx.doi.org/10.1039/B601930G] [PMID: 17119643]
[159]
Prudhomme, M. Rebeccamycin analogues as anti-cancer agents. Eur. J. Med. Chem., 2003, 38(2), 123-140.
[http://dx.doi.org/10.1016/S0223-5234(03)00011-4] [PMID: 12620658]
[160]
Zuma, A.A.; Cavalcanti, D.P.; Maia, M.C.; de Souza, W.; Motta, M.C. Effect of topoisomerase inhibitors and DNA-binding drugs on the cell proliferation and ultrastructure of Trypanosoma cruzi. Int. J. Antimicrob. Agents, 2011, 37(5), 449-456.
[http://dx.doi.org/10.1016/j.ijantimicag.2010.11.031] [PMID: 21292448]
[161]
Meng, L.H.; Liao, Z.Y.; Pommier, Y. Non-camptothecin DNA topoisomerase I inhibitors in cancer therapy. Curr. Top. Med. Chem., 2003, 3(3), 305-320.
[http://dx.doi.org/10.2174/1568026033452546] [PMID: 12570765]
[162]
Antony, S.; Jayaraman, M.; Laco, G.; Kohlhagen, G.; Kohn, K.W.; Cushman, M.; Pommier, Y. Differential induction of topoisomerase I-DNA cleavage complexes by the indenoisoquinoline MJ-III-65 (NSC 706744) and camptothecin: base sequence analysis and activity against camptothecin-resistant topoisomerases I. Cancer Res., 2003, 63(21), 7428-7435.
[PMID: 14612542]
[163]
Strumberg, D.; Pommier, Y.; Paull, K.; Jayaraman, M.; Nagafuji, P.; Cushman, M. Synthesis of cytotoxic indenoisoquinoline topoisomerase I poisons. J. Med. Chem., 1999, 42(3), 446-457.
[http://dx.doi.org/10.1021/jm9803323] [PMID: 9986716]
[164]
Pommier, Y.; Cushman, M. The indenoisoquinoline noncamptothecin topoisomerase I inhibitors: update and perspectives. Mol. Cancer Ther., 2009, 8(5), 1008-1014.
[http://dx.doi.org/10.1158/1535-7163.MCT-08-0706] [PMID: 19383846]
[165]
Conda-Sheridan, M.; Reddy, P.V.; Morrell, A.; Cobb, B.T.; Marchand, C.; Agama, K.; Chergui, A.; Renaud, A.; Stephen, A.G.; Bindu, L.K.; Pommier, Y.; Cushman, M. Synthesis and biological evaluation of indenoisoquinolines that inhibit both tyrosyl-DNA phosphodiesterase I (Tdp1) and topoisomerase I (Top1). J. Med. Chem., 2013, 56(1), 182-200.
[http://dx.doi.org/10.1021/jm3014458] [PMID: 23259865]
[166]
Bakshi, R.P.; Sang, D.; Morrell, A.; Cushman, M.; Shapiro, T.A. Activity of indenoisoquinolines against African trypanosomes. Antimicrob. Agents Chemother., 2009, 53(1), 123-128.
[http://dx.doi.org/10.1128/AAC.00650-07] [PMID: 18824603]
[167]
Balaña-Fouce, R.; Prada, C.F.; Requena, J.M.; Cushman, M.; Pommier, Y.; Álvarez-Velilla, R.; Escudero-Martínez, J.M.; Calvo-Álvarez, E.; Pérez-Pertejo, Y.; Reguera, R.M. Indotecan (LMP400) and AM13-55: two novel indenoisoquinolines show potential for treating visceral leishmaniasis. Antimicrob. Agents Chemother., 2012, 56(10), 5264-5270.
[http://dx.doi.org/10.1128/AAC.00499-12] [PMID: 22850521]
[168]
Hussain, H.; Krohn, K.; Uddin Ahmad, V.U.; Miana, G.A.; Greend, I.R. Lapachol: an overview. ARKIVOC, 2007, 2, 145-171.
[169]
Riffel, A.; Medina, L.F.; Stefani, V.; Santos, R.C.; Bizani, D.; Brandelli, A. In vitro antimicrobial activity of a new series of 1,4-naphthoquinones. Braz. J. Med. Biol. Res., 2002, 35(7), 811-818.
[http://dx.doi.org/10.1590/S0100-879X2002000700008] [PMID: 12131921]
[170]
Pinto, A.V.; de Castro, S.L. The trypanocidal activity of naphthoquinones: a review. Molecules, 2009, 14(11), 4570-4590.
[http://dx.doi.org/10.3390/molecules14114570] [PMID: 19924086]
[171]
Hussain, H.; Green, I.R. Lapachol and lapachone analogs: a journey of two decades of patent research(1997-2016). Expert Opin. Ther. Pat., 2017, 27(10), 1111-1121.
[http://dx.doi.org/10.1080/13543776.2017.1339792] [PMID: 28586252]
[172]
Lopes, J.N.; Cruz, F.S.; Docampo, R.; Vasconcellos, M.E.; Sampaio, M.C.R.; Pinto, A.V.; Gilbert, B. In vitro and in vivo evaluation of the toxicity of 1,4-naphthoquinone and 1,2-naphthoquinone derivatives against Trypanosoma cruzi. Ann. Trop. Med. Parasitol., 1978, 72(6), 523-531.
[http://dx.doi.org/10.1080/00034983.1978.11719356] [PMID: 367298]
[173]
Pinto, A.V.; Ferreira, V.F.; Capella, R.S.; Gilbert, B.; Pinto, M.C.F.R.; da Silva, J.S. Activity of some naphthoquinones on blood stream forms of Trypanosoma cruzi. Trans. R. Soc. Trop. Med. Hyg., 1987, 81(4), 609-610.
[http://dx.doi.org/10.1016/0035-9203(87)90427-5] [PMID: 3127962]
[174]
Moreno, E.; Schwartz, J.; Larrea, E.; Conde, I.; Font, M.; Sanmartín, C.; Irache, J.M.; Espuelas, S. Assessment of β-lapachone loaded in lecithin-chitosan nanoparticles for the topical treatment of cutaneous Leishmaniasis in L. major infected BALB/c mice. Nanomedicine (Lond.), 2015, 11(8), 2003-2012.
[http://dx.doi.org/10.1016/j.nano.2015.07.011] [PMID: 26282379]
[175]
Li, C.J.; Averboukh, L.; Pardee, A.B. beta-Lapachone, a novel DNA topoisomerase I inhibitor with a mode of action different from camptothecin. J. Biol. Chem., 1993, 268(30), 22463-22468.
[PMID: 8226754]
[176]
Hazra, B.; Sur, P.; Roy, D.K.; Sur, B.; Banerjee, A. Biological activity of diospyrin towards Ehrlich ascites carcinoma in Swiss A mice. Planta Med., 1984, 50(4), 295-297.
[http://dx.doi.org/10.1055/s-2007-969713] [PMID: 6505078]
[177]
Hazra, B.; Saha, A.K.; Ray, R.; Roy, D.K.; Sur, P.; Banerjee, A. Antiprotozoal activity of diospyrin towards Leishmania donovani promastigotes in vitro. Trans. R. Soc. Trop. Med. Hyg., 1987, 81(5), 738-741.
[http://dx.doi.org/10.1016/0035-9203(87)90013-7] [PMID: 3449989]
[178]
Ray, S.; Hazra, B.; Mittra, B.; Das, A.; Majumder, H.K. Diospyrin, a bisnaphthoquinone: a novel inhibitor of type I DNA topoisomerase of Leishmania donovani. Mol. Pharmacol., 1998, 54(6), 994-999.
[http://dx.doi.org/10.1124/mol.54.6.994] [PMID: 9855627]
[179]
Mukherjee, P.; Majee, S.B.; Ghosh, S.; Hazra, B. Apoptosis-like death in Leishmania donovani promastigotes induced by diospyrin and its ethanolamine derivative. Int. J. Antimicrob. Agents, 2009, 34(6), 596-601.
[http://dx.doi.org/10.1016/j.ijantimicag.2009.08.007] [PMID: 19783125]
[180]
Roy, A.; Chowdhury, S.; Sengupta, S.; Mandal, M.; Jaisankar, P.; D’Annessa, I.; Desideri, A.; Majumder, H.K. Development of derivatives of 3, 3′-diindolylmethane as potent Leishmania donovani bi-subunit topoisomerase IB poisons. PLoS One, 2011, 6(12)e28493
[http://dx.doi.org/10.1371/journal.pone.0028493] [PMID: 22174820]
[181]
Roy, A. BoseDasgupta, S.; Ganguly, A.; Jaisankar, P.; Majumder, H.K. Topoisomerase I gene mutations at F270 in the large subunit and N184 in the small subunit contribute to the resistance mechanism of the unicellular parasite Leishmania donovani towards 3,3′-diindolylmethane. Antimicrob. Agents Chemother., 2009, 53(6), 2589-2598.
[http://dx.doi.org/10.1128/AAC.01648-08] [PMID: 19332675]
[182]
Li, X.C.; Jacob, M.R.; Khan, S.I.; Ashfaq, M.K.; Babu, K.S.; Agarwal, A.K.; Elsohly, H.N.; Manly, S.P.; Clark, A.M. Potent in vitro antifungal activities of naturally occurring acetylenic acids. Antimicrob. Agents Chemother., 2008, 52(7), 2442-2448.
[http://dx.doi.org/10.1128/AAC.01297-07] [PMID: 18458131]
[183]
Siddiq, A.; Dembitsky, V. Acetylenic anticancer agents. Anticancer. Agents Med. Chem., 2008, 8(2), 132-170.
[http://dx.doi.org/10.2174/187152008783497073] [PMID: 18288919]
[184]
Chaudhuri, G.; Ghoshal, K.; Banerjee, A.B. Toxic effects of fatty acids on Leishmania donovani promastigotes. Indian J. Med. Res., 1986, 84, 361-365.
[PMID: 3781591]
[185]
de Á Santos, L.; Cavalheiro, A.J.; Tempone, A.G..; Correa, D.S.; Alexandre, T.R.; Quintiliano, N.F.; Rodrigues-Oliveira, A.F.; Oliveira-Silva, D.; Martins, R.C.; Lago, J.H. Antitrypanosomal acetylene fatty acid derivatives from the seeds of Porcelia macrocarpa (Annonaceae). Molecules, 2015, 20(5), 8168-8180.
[http://dx.doi.org/10.3390/molecules20058168] [PMID: 25961159]
[186]
Carballeira, N.M.; Cartagena, M.M.; Prada, C.F.; Rubio, C.F.; Balaña-Fouce, R. Total synthesis and antileishmanial activity of the natural occurring acetylenic fatty acids 6-heptadecynoic acid and 6-icosynoic acid. Lipids, 2009, 44(10), 953-961.
[http://dx.doi.org/10.1007/s11745-009-3345-z] [PMID: 19789903]
[187]
Carballeira, N.M. Recent developments in the antiprotozoal and anticancer activities of the 2-alkynoic fatty acids. Chem. Phys. Lipids, 2013, 172-173, 58-66.
[http://dx.doi.org/10.1016/j.chemphyslip.2013.05.002] [PMID: 23727443]
[188]
Carballeira, N.M.; Montano, N.; Cintrón, G.A.; Márquez, C.; Rubio, C.F.; Prada, C.F.; Balaña-Fouce, R. First total synthesis and antileishmanial activity of (Z)-16-methyl-11-heptadecenoic acid, a new marine fatty acid from the sponge Dragmaxia undata. Chem. Phys. Lipids, 2011, 164(2), 113-117.
[http://dx.doi.org/10.1016/j.chemphyslip.2010.11.006] [PMID: 21129369]
[189]
Kiselev, E.; Dexheimer, T.S.; Pommier, Y.; Cushman, M. Design, synthesis, and evaluation of dibenzo[c,h][1,6]naphthyridines as topoisomerase I inhibitors and potential anticancer agents. J. Med. Chem., 2010, 53(24), 8716-8726.
[http://dx.doi.org/10.1021/jm101048k] [PMID: 21090809]
[190]
López-Arencibia, A.; García-Velázquez, D.; Martín-Navarro, C.M.; Sifaoui, I.; Reyes-Batlle, M.; Lorenzo-Morales, J.; Gutiérrez-Ravelo, Á.; Piñero, J.E. In vitro activities of hexaazatrinaphthylenes against Leishmania spp. Antimicrob. Agents Chemother., 2015, 59(5), 2867-2874.
[http://dx.doi.org/10.1128/AAC.00226-15] [PMID: 25753635]
[191]
Alonso, C.; Fuertes, M.; González, M.; Rodríguez-Gascón, A.; Rubiales, G.; Palacios, F. Synthesis and biological evaluation of 1,5-naphthyridines as topoisomerase I inhibitors. A new family of antiproliferative agents. Curr. Top. Med. Chem., 2014, 14(23), 2722-2728.
[http://dx.doi.org/10.2174/1568026614666141215152441] [PMID: 25515747]
[192]
Alonso, C.; Fuertes, M.; González, M.; Rubiales, G.; Tesauro, C.; Knudsen, B.R.; Palacios, F. Synthesis and biological evaluation of indeno[1,5]naphthyridines as topoisomerase I (TopI) inhibitors with antiproliferative activity. Eur. J. Med. Chem., 2016, 115, 179-190.
[http://dx.doi.org/10.1016/j.ejmech.2016.03.031] [PMID: 27017547]
[193]
Tejería, A.; Pérez-Pertejo, Y.; Reguera, R.M.; Balaña-Fouce, R.; Alonso, C.; Fuertes, M.; González, M.; Rubiales, G.; Palacios, F. Antileishmanial effect of new indeno-1,5-naphthyridines, selective inhibitors of Leishmania infantum type IB DNA topoisomerase. Eur. J. Med. Chem., 2016, 124, 740-749.
[http://dx.doi.org/10.1016/j.ejmech.2016.09.017] [PMID: 27639365]
[194]
Andersen, M.B.; Tesauro, C.; Gonzalez, M.; Kristoffersen, E.L.; Alonso, C.; Rubiales, G.; Coletta, A.; Frøhlich, R.; Stougaard, M.; Ho, Y.P.; Palacios, F.; Knudsen, B.R. Advantages of an optical nanosensor system for the mechanistic analysis of a novel topoisomerase I targeting drug: a case study. Nanoscale, 2017, 9(5), 1886-1895.
[http://dx.doi.org/10.1039/C6NR06848K] [PMID: 28094391]
[195]
Furet, Y.X.; Pechère, J.C. Newly documented antimicrobial activity of quinolones. Eur. J. Clin. Microbiol. Infect. Dis., 1991, 10(4), 249-254.
[http://dx.doi.org/10.1007/BF01966997] [PMID: 1864284]
[196]
Naeem, A.; Badshah, S.L.; Muska, M.; Ahmad, N.; Khan, K. The current case of quinolones: synthetic approaches and antibacterial activity. Molecules, 2016, 21(4), 268.
[http://dx.doi.org/10.3390/molecules21040268] [PMID: 27043501]
[197]
Hiasa, H. DNA topoisomerases as targets for antibacterial agents. Methods Mol. Biol., 2018, 1703, 47-62.
[http://dx.doi.org/10.1007/978-1-4939-7459-7_3] [PMID: 29177732]
[198]
Raether, W.; Seidenath, H.; Hofmann, J. Potent antibacterial fluoroquinolones with marked activity against Leishmania donovani in vivo. Parasitol. Res., 1989, 75(5), 412-413.
[http://dx.doi.org/10.1007/BF00931138] [PMID: 2726722]
[199]
Romero, I.C.; Saravia, N.G.; Walker, J. Selective action of fluoroquinolones against intracellular amastigotes of Leishmania (Viannia) panamensis in vitro. J. Parasitol., 2005, 91(6), 1474-1479.
[http://dx.doi.org/10.1645/GE-3489.1] [PMID: 16539034]
[200]
Wube, A.; Hüfner, A.; Seebacher, W.; Kaiser, M.; Brun, R.; Bauer, R.; Bucar, F. 1,2-substituted 4-(1H)-quinolones: synthesis, antimalarial and antitrypanosomal activities in vitro. Molecules, 2014, 19(9), 14204-14220.
[http://dx.doi.org/10.3390/molecules190914204] [PMID: 25211002]
[201]
Nenortas, E.; Burri, C.; Shapiro, T.A. Antitrypanosomal activity of fluoroquinolones. Antimicrob. Agents Chemother., 1999, 43(8), 2066-2068.
[http://dx.doi.org/10.1128/AAC.43.8.2066] [PMID: 10428939]
[202]
Nenortas, E.; Kulikowicz, T.; Burri, C.; Shapiro, T.A. Antitrypanosomal activities of fluoroquinolones with pyrrolidinyl substitutions. Antimicrob. Agents Chemother., 2003, 47(9), 3015-3017.
[http://dx.doi.org/10.1128/AAC.47.9.3015-3017.2003] [PMID: 12937017]
[203]
Cortázar, T.M.; Coombs, G.H.; Walker, J. Leishmania panamensis: comparative inhibition of nuclear DNA topoisomerase II enzymes from promastigotes and human macrophages reveals anti-parasite selectivity of fluoroquinolones, flavonoids and pentamidine. Exp. Parasitol., 2007, 116(4), 475-482.
[http://dx.doi.org/10.1016/j.exppara.2007.02.018] [PMID: 17466980]
[204]
Di Marco, A.; Cassinelli, G.; Arcamone, F. The discovery of daunorubicin. Cancer Treat. Rep., 1981, 65(Suppl. 4), 3-8.
[PMID: 7049379]
[205]
Cagel, M.; Grotz, E.; Bernabeu, E.; Moretton, M.A.; Chiappetta, D.A. Doxorubicin: nanotechnological overviews from bench to bedside. Drug Discov. Today, 2017, 22(2), 270-281.
[http://dx.doi.org/10.1016/j.drudis.2016.11.005] [PMID: 27890669]
[206]
Tewey, K.M.; Rowe, T.C.; Yang, L.; Halligan, B.D.; Liu, L.F. Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science, 1984, 226(4673), 466-468.
[http://dx.doi.org/10.1126/science.6093249] [PMID: 6093249]
[207]
Singh, G.; Dey, C.S. Induction of apoptosis-like cell death by pentamidine and doxorubicin through differential inhibition of topoisomerase II in arsenite-resistant L. donovani. Acta Trop., 2007, 103(3), 172-185.
[http://dx.doi.org/10.1016/j.actatropica.2007.06.004] [PMID: 17655815]
[208]
Gutierrez-Corbo, C.; Dominguez-Asenjo, B.; Vossen, L.I.; Pérez-Pertejo, Y.; Muñoz-Fenández, M.A.; Balaña-Fouce, R.; Calderón, M.; Reguera, R.M. PEGylated dendritic polyglycerol conjugate delivers doxorubicin to the parasitophorous vacuole in Leishmania infantum infections. Macromol. Biosci., 2017, 17(10)1700098
[http://dx.doi.org/10.1002/mabi.201700098] [PMID: 28683183]
[209]
Hande, K.R. Etoposide: four decades of development of a topoisomerase II inhibitor. Eur. J. Cancer, 1998, 34(10), 1514-1521.
[http://dx.doi.org/10.1016/S0959-8049(98)00228-7] [PMID: 9893622]
[210]
Leroy, D.; Kajava, A.V.; Frei, C.; Gasser, S.M. Analysis of etoposide binding to subdomains of human DNA topoisomerase II alpha in the absence of DNA. Biochemistry, 2001, 40(6), 1624-1634.
[http://dx.doi.org/10.1021/bi0019141] [PMID: 11327821]
[211]
Shapiro, T.A.; Showalter, A.F. In vivo inhibition of trypanosome mitochondrial topoisomerase II: effects on kinetoplast DNA maxicircles. Mol. Cell. Biol., 1994, 14(9), 5891-5897.
[http://dx.doi.org/10.1128/MCB.14.9.5891] [PMID: 8065322]
[212]
Escudero-Martínez, J.M.; Pérez-Pertejo, Y.; Reguera, R.M.; Castro, M.Á.; Rojo, M.V.; Santiago, C.; Abad, A.; García, P.A.; López-Pérez, J.L.; San Feliciano, A.; Balaña-Fouce, R. Antileishmanial activity and tubulin polymerization inhibition of podophyllotoxin derivatives on Leishmania infantum. Int. J. Parasitol. Drugs Drug Resist., 2017, 7(3), 272-285.
[213]
Ríos, J.L.; Máñez, S. New pharmacological opportunities for betulinic acid. Planta Med., 2018, 84(1), 8-19.
[http://dx.doi.org/10.1055/s-0043-123472] [PMID: 29202513]
[214]
Alakurtti, S.; Heiska, T.; Kiriazis, A.; Sacerdoti-Sierra, N.; Jaffe, C.L.; Yli-Kauhaluoma, J. Synthesis and anti-leishmanial activity of heterocyclic betulin derivatives. Bioorg. Med. Chem., 2010, 18(4), 1573-1582.
[http://dx.doi.org/10.1016/j.bmc.2010.01.003] [PMID: 20116263]
[215]
Sousa, M.C.; Varandas, R.; Santos, R.C.; Santos-Rosa, M.; Alves, V.; Salvador, J.A. Antileishmanial activity of semisynthetic lupane triterpenoids betulin and betulinic acid derivatives: synergistic effects with miltefosine. PLoS One, 2014, 9(3)e89939
[http://dx.doi.org/10.1371/journal.pone.0089939] [PMID: 24643019]
[216]
Alcazar, W.; López, A.S.; Alakurtti, S.; Tuononen, M.L.; Yli-Kauhaluoma, J.; Ponte-Sucre, A. Betulin derivatives impair Leishmania braziliensis viability and host-parasite interaction. Bioorg. Med. Chem., 2014, 22(21), 6220-6226.
[http://dx.doi.org/10.1016/j.bmc.2014.08.023] [PMID: 25240731]
[217]
Chowdhury, A.R.; Mandal, S.; Mittra, B.; Sharma, S.; Mukhopadhyay, S.; Majumder, H.K. Betulinic acid, a potent inhibitor of eukaryotic topoisomerase I: identification of the inhibitory step, the major functional group responsible and development of more potent derivatives. Med. Sci. Monit., 2002, 8(7), BR254-BR265.
[PMID: 12118187]
[218]
Chowdhury, A.R.; Mandal, S.; Goswami, A.; Ghosh, M.; Mandal, L.; Chakraborty, D.; Ganguly, A.; Tripathi, G.; Mukhopadhyay, S.; Bandyopadhyay, S.; Majumder, H.K. Dihydrobetulinic acid induces apoptosis in Leishmania donovani by targeting DNA topoisomerase I and II: implications in antileishmanial therapy. Mol. Med., 2003, 9(1-2), 26-36.
[http://dx.doi.org/10.1007/BF03402104] [PMID: 12765337]
[219]
Wong, I.L.; Chan, K.F.; Chen, Y.F.; Lun, Z.R.; Chan, T.H.; Chow, L.M. In vitro and in vivo efficacy of novel flavonoid dimers against cutaneous leishmaniasis. Antimicrob. Agents Chemother., 2014, 58(6), 3379-3388.
[http://dx.doi.org/10.1128/AAC.02425-13] [PMID: 24687505]
[220]
Ribeiro, F.F.; Junior, F.J.; da Silva, M.S.; Scotti, M.T.; Scotti, L. Computational and investigative study of flavonoids active against Typanosoma cruzi and Leishmania spp. Nat. Prod. Commun., 2015, 10(6), 917-920.
[http://dx.doi.org/10.1177/1934578X1501000630] [PMID: 26197515]
[221]
Mittra, B.; Saha, A.; Chowdhury, A.R.; Pal, C.; Mandal, S.; Mukhopadhyay, S.; Bandyopadhyay, S.; Majumder, H.K. Luteolin, an abundant dietary component is a potent anti-leishmanial agent that acts by inducing topoisomerase II-mediated kinetoplast DNA cleavage leading to apoptosis. Mol. Med., 2000, 6(6), 527-541.
[http://dx.doi.org/10.1007/BF03401792] [PMID: 10972088]
[222]
Chowdhury, A.R.; Sharma, S.; Mandal, S.; Goswami, A.; Mukhopadhyay, S.; Majumder, H.K. Luteolin, an emerging anti-cancer flavonoid, poisons eukaryotic DNA topoisomerase I. Biochem. J., 2002, 366(Pt 2), 653-661.
[http://dx.doi.org/10.1042/bj20020098] [PMID: 12027807]
[223]
Cantero, G.; Campanella, C.; Mateos, S.; Cortés, F. Topoisomerase II inhibition and high yield of endoreduplication induced by the flavonoids luteolin and quercetin. Mutagenesis, 2006, 21(5), 321-325.
[http://dx.doi.org/10.1093/mutage/gel033] [PMID: 16950806]
[224]
Chan, A.L.; Chang, W.S.; Chen, L.M.; Lee, C.M.; Chen, C.E.; Lin, C.M.; Hwang, J.L. Evodiamine stabilizes topoisomerase I-DNA cleavable complex to inhibit topoisomerase I activity. Molecules, 2009, 14(4), 1342-1352.
[http://dx.doi.org/10.3390/molecules14041342] [PMID: 19384267]
[225]
Pan, X.; Hartley, J.M.; Hartley, J.A.; White, K.N.; Wang, Z.; Bligh, S.W. Evodiamine, a dual catalytic inhibitor of type I and II topoisomerases, exhibits enhanced inhibition against camptothecin resistant cells. Phytomedicine, 2012, 19(7), 618-624.
[http://dx.doi.org/10.1016/j.phymed.2012.02.003] [PMID: 22402246]
[226]
BoseDasgupta, S.; Das, B.B.; Sengupta, S.; Ganguly, A.; Roy, A.; Dey, S.; Tripathi, G.; Dinda, B.; Majumder, H.K. The caspase-independent algorithm of programmed cell death in Leishmania induced by baicalein: the role of LdEndoG, LdFEN-1 and LdTatD as a DNA ‘degradesome’. Cell Death Differ., 2008, 15(10), 1629-1640.
[http://dx.doi.org/10.1038/cdd.2008.85] [PMID: 18566607]
[227]
Singh, A.K.; Lown, J.W. Design, synthesis and antitumor cytotoxicity of novel bis-benzimidazoles. Anticancer Drug Des., 2000, 15(4), 265-275.
[PMID: 11200502]
[228]
Wilson, W.D.; Nguyen, B.; Tanious, F.A.; Mathis, A.; Hall, J.E.; Stephens, C.E.; Boykin, D.W. Dications that target the DNA minor groove: compound design and preparation, DNA interactions, cellular distribution and biological activity. Curr. Med. Chem. Anticancer Agents, 2005, 5(4), 389-408.
[http://dx.doi.org/10.2174/1568011054222319] [PMID: 16101490]
[229]
Beerman, T.A.; McHugh, M.M.; Sigmund, R.; Lown, J.W.; Rao, K.E.; Bathini, Y. Effects of analogs of the DNA minor groove binder Hoechst 33258 on topoisomerase II and I mediated activities. Biochim. Biophys. Acta, 1992, 1131(1), 53-61.
[http://dx.doi.org/10.1016/0167-4781(92)90098-K] [PMID: 1374646]
[230]
Walker, J.; Saravia, N.G. Inhibition of Leishmania donovani promastigote DNA topoisomerase I and human monocyte DNA topoisomerases I and II by antimonial drugs and classical antitopoisomerase agents. J. Parasitol., 2004, 90(5), 1155-1162.
[http://dx.doi.org/10.1645/GE-3347] [PMID: 15562618]
[231]
Correia Soeiro, M.N.; de Souza, E.M.; Boykin, D.W. Antiparasitic activity of aromatic diamidines and their patented literature. Expert Opin. Ther. Pat., 2007, 17(8), 927-939.
[http://dx.doi.org/10.1517/13543776.17.8.927]
[232]
Werbovetz, K. Diamidines as antitrypanosomal, antileishmanial and antimalarial agents. Curr. Opin. Investig. Drugs, 2006, 7(2), 147-157.
[PMID: 16499285]
[233]
Yang, G.; Choi, G.; No, J.H. Antileishmanial mechanism of diamidines involves targeting kinetoplasts. Antimicrob. Agents Chemother., 2016, 60(11), 6828-6836.
[http://dx.doi.org/10.1128/AAC.01129-16] [PMID: 27600039]

Rights & Permissions Print Cite
Article Metrics
39
1
© 2024 Bentham Science Publishers | Privacy Policy