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Current Topics in Medicinal Chemistry

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ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

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Mini-Review Article

The Role of Purinergic Signaling in Trichomonas vaginalis Infection

Author(s): Micheli Ferla and Tiana Tasca*

Volume 21, Issue 3, 2021

Published on: 04 September, 2020

Page: [181 - 192] Pages: 12

DOI: 10.2174/1568026620999200904122212

Price: $65

Abstract

Trichomoniasis, one of the most common non-viral sexually transmitted infections worldwide, is caused by the parasite Trichomonas vaginalis. The pathogen colonizes the human urogenital tract, and the infection is associated with complications such as adverse pregnancy outcomes, cervical cancer, and an increase in HIV transmission. The mechanisms of pathogenicity are multifactorial, and controlling immune responses is essential for infection maintenance. Extracellular purine nucleotides are released by cells in physiological and pathological conditions, and they are hydrolyzed by enzymes called ecto-nucleotidases. The cellular effects of nucleotides and nucleosides occur via binding to purinoceptors, or through the uptake by nucleoside transporters. Altogether, enzymes, receptors and transporters constitute the purinergic signaling, a cellular network that regulates several effects in practically all systems including mammals, helminths, protozoa, bacteria, and fungi. In this context, this review updates the data on purinergic signaling involved in T. vaginalis biology and interaction with host cells, focusing on the characterization of ecto-nucleotidases and on purine salvage pathways. The implications of the final products, the nucleosides adenosine and guanosine, for human neutrophil response and vaginal epithelial cell damage reveal the purinergic signaling as a potential new mechanism for alternative drug targets.

Keywords: Trichomonas vaginalis, Purinergic signaling, Adenosine, Neutrophils, Vaginal epithelial cells, Immune response.

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[1]
Rowley, J.; Vander Hoorn, S.; Korenromp, E.; Low, N.; Unemo, M.; Abu-Raddad, L.J.; Chico, R.M.; Smolak, A.; Newman, L.; Gottlieb, S.; Thwin, S.S.; Broutet, N.; Taylor, M.M. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull. World Health Organ., 2019, 97(8), 548-562P.
[http://dx.doi.org/10.2471/BLT.18.228486] [PMID: 31384073]
[2]
Poole, D.N.; McClelland, R.S. Global epidemiology of Trichomonas vaginalis. Sex. Transm. Infect., 2013, 89(6), 418-422.
[http://dx.doi.org/10.1136/sextrans-2013-051075] [PMID: 23744960]
[3]
Chapin, K.; Andrea, S. APTIMA® Trichomonas vaginalis, a transcription-mediated amplification assay for detection of Trichomonas vaginalis in urogenital specimens. Expert Rev. Mol. Diagn., 2011, 11(7), 679-688.
[http://dx.doi.org/10.1586/erm.11.53] [PMID: 21902528]
[4]
Edwards, T.; Burke, P.; Smalley, H.; Hobbs, G. Trichomonas vaginalis: Clinical relevance, pathogenicity and diagnosis. Crit. Rev. Microbiol., 2016, 42(3), 406-417.
[http://dx.doi.org/10.3109/1040841X.2014.958050] [PMID: 25383648]
[5]
Mielczarek, E.; Blaszkowska, J. Trichomonas vaginalis: pathogenicity and potential role in human reproductive failure. Infection, 2016, 44(4), 447-458.
[http://dx.doi.org/10.1007/s15010-015-0860-0] [PMID: 26546373]
[6]
Quinlivan, E.B.; Patel, S.N.; Grodensky, C.A.; Golin, C.E.; Tien, H-C.; Hobbs, M.M. Modeling the impact of Trichomonas vaginalis infection on HIV transmission in HIV-infected individuals in medical care. Sex. Transm. Dis., 2012, 39(9), 671-677.
[http://dx.doi.org/10.1097/OLQ.0b013e3182593839] [PMID: 22902662]
[7]
Kissinger, P.; Adamski, A. Trichomoniasis and HIV interactions: a review. Sex. Transm. Infect., 2013, 89(6), 426-433.
[http://dx.doi.org/10.1136/sextrans-2012-051005] [PMID: 23605851]
[8]
Fichorova, R.N. Impact of T. vaginalis infection on innate immune responses and reproductive outcome. J. Reprod. Immunol., 2009, 83(1-2), 185-189.
[http://dx.doi.org/10.1016/j.jri.2009.08.007] [PMID: 19850356]
[9]
Figueroa-Angulo, E.E.; Rendón-Gandarilla, F.J.; Puente-Rivera, J.; Calla-Choque, J.S.; Cárdenas-Guerra, R.E.; Ortega-López, J.; Quintas-Granados, L.I.; Alvarez-Sánchez, M.E.; Arroyo, R. The effects of environmental factors on the virulence of Trichomonas vaginalis. Microbes Infect., 2012, 14(15), 1411-1427.
[http://dx.doi.org/10.1016/j.micinf.2012.09.004] [PMID: 23022315]
[10]
Lehker, M.W.; Sweeney, D. Trichomonad invasion of the mucous layer requires adhesins, mucinases, and motility. Sex. Transm. Infect., 1999, 75(4), 231-238.
[http://dx.doi.org/10.1136/sti.75.4.231] [PMID: 10615308]
[11]
Twu, O.; de Miguel, N.; Lustig, G.; Stevens, G.C.; Vashisht, A.A.; Wohlschlegel, J.A.; Johnson, P.J. Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host:parasite interactions. PLoS Pathog., 2013, 9(7)e1003482
[http://dx.doi.org/10.1371/journal.ppat.1003482] [PMID: 23853596]
[12]
Lehker, M.W.; Alderete, J.F. Biology of trichomonosis. Curr. Opin. Infect. Dis., 2000, 13(1), 37-45.
[http://dx.doi.org/10.1097/00001432-200002000-00007] [PMID: 11964771]
[13]
Menezes, C.B.; Frasson, A.P.; Tasca, T. Trichomoniasis - are we giving the deserved attention to the most common non-viral sexually transmitted disease worldwide? Microb. Cell, 2016, 3(9), 404-419.
[http://dx.doi.org/10.15698/mic2016.09.526] [PMID: 28357378]
[14]
Mercer, F.; Johnson, P.J. Trichomonas vaginalis: pathogenesis, symbiont interactions, and host cell immune responses. Trends Parasitol., 2018, 34(8), 683-693.
[http://dx.doi.org/10.1016/j.pt.2018.05.006] [PMID: 30056833]
[15]
Hernandez-Gutierrez, R.; Ortega-López, J.; Arroyo, R.A. 39-kDa cysteine proteinase CP39 from Trichomonas vaginalis, which is negatively affected by iron may be involved in trichomonal cytotoxicity. J. Eukaryot. Microbiol., 2003, 50(Suppl.), 696-698.
[http://dx.doi.org/10.1111/j.1550-7408.2003.tb00692.x] [PMID: 14736224]
[16]
Fichorova, R.N.; Yamamoto, H.S.; Fashemi, T.; Foley, E.; Ryan, S.; Beatty, N.; Dawood, H.; Hayes, G.R.; St-Pierre, G.; Sato, S.; Singh, B.N. Trichomonas vaginalis lipophosphoglycan exploits binding to galectin-1 and -3 to modulate epithelial immunity. J. Biol. Chem., 2016, 291(2), 998-1013.
[http://dx.doi.org/10.1074/jbc.M115.651497] [PMID: 26589797]
[17]
Ryu, J.S.; Kang, J.H.; Jung, S.Y.; Shin, M.H.; Kim, J.M.; Park, H.; Min, D.Y. Production of interleukin-8 by human neutrophils stimulated with Trichomonas vaginalis. Infect. Immun., 2004, 72(3), 1326-1332.
[http://dx.doi.org/10.1128/IAI.72.3.1326-1332.2004] [PMID: 14977935]
[18]
Mercer, F.; Ng, S.H.; Brown, T.M.; Boatman, G.; Johnson, P.J. Neutrophils kill the parasite Trichomonas vaginalis using trogocytosis. PLoS Biol., 2018, 16(2)e2003885
[http://dx.doi.org/10.1371/journal.pbio.2003885] [PMID: 29408891]
[19]
Crouch, M.L.; Alderete, J.F. Trichomonas vaginalis interactions with fibronectin and laminin. Microbiology, 1999, 145(Pt 10), 2835-2843.
[http://dx.doi.org/10.1099/00221287-145-10-2835] [PMID: 10537205]
[20]
Kang, J.H.; Song, H.O.; Ryu, J.S.; Shin, M.H.; Kim, J.M.; Cho, Y.S.; Alderete, J.F.; Ahn, M.H.; Min, D.Y. Trichomonas vaginalis promotes apoptosis of human neutrophils by activating caspase-3 and reducing Mcl-1 expression. Parasite Immunol., 2006, 28(9), 439-446.
[http://dx.doi.org/10.1111/j.1365-3024.2006.00884.x] [PMID: 16916367]
[21]
Robinson, S.C. Trichomonal vaginitis resistant to metranidazole. Can. Med. Assoc. J., 1962, 86(14), 665.
[22]
Dunne, R.L.; Dunn, L.A.; Upcroft, P.; O’Donoghue, P.J.; Upcroft, J.A. Drug resistance in the sexually transmitted protozoan Trichomonas vaginalis. Cell Res., 2003, 13(4), 239-249.
[http://dx.doi.org/10.1038/sj.cr.7290169] [PMID: 12974614]
[23]
Schwebke, J.R.; Barrientes, F.J. Prevalence of Trichomonas vaginalis isolates with resistance to metronidazole and tinidazole. Antimicrob. Agents Chemother., 2006, 50(12), 4209-4210.
[http://dx.doi.org/10.1128/AAC.00814-06] [PMID: 17000740]
[24]
Secor, W.E.; Meites, E.; Starr, M.C.; Workowski, K.A. Neglected parasitic infections in the United States: trichomoniasis. Am. J. Trop. Med. Hyg., 2014, 90(5), 800-804.
[http://dx.doi.org/10.4269/ajtmh.13-0723] [PMID: 24808247]
[25]
Muzny, C.; Barnes, A.; Mena, L. Symptomatic Trichomonas vaginalis infection in the setting of severe nitroimidazole allergy: successful treatment with boric acid. Sex. Health, 2012, 9(4), 389-391.
[http://dx.doi.org/10.1071/SH11114] [PMID: 22877600]
[26]
Küng, E.; Fürnkranz, U.; Walochnik, J. Chemotherapeutic options for the treatment of human trichomoniasis. Int. J. Antimicrob. Agents, 2019, 53(2), 116-127.
[http://dx.doi.org/10.1016/j.ijantimicag.2018.10.016] [PMID: 30612993]
[27]
Lauri, N.; Bazzi, Z.; Alvarez, C.L.; Leal Denis, M.F.; Schachter, J.; Herlax, V.; Ostuni, M.A.; Schwarzbaum, P.J. ATPe dynamics in protozoan parasites. adapt or perish. Genes (Basel), 2018, 10(1), 16.
[http://dx.doi.org/10.3390/genes10010016] [PMID: 30591699]
[28]
Figueiredo, A.B.; Souza-Testasicca, M.C.; Afonso, L.C.C. Purinergic signaling and infection by Leishmania: A new approach to evasion of the immune response. Biomed. J., 2016, 39(4), 244-250.
[http://dx.doi.org/10.1016/j.bj.2016.08.004] [PMID: 27793266]
[29]
Burnstock, G. Purinergic signalling: from discovery to current developments. Exp. Physiol., 2014, 99(1), 16-34.
[http://dx.doi.org/10.1113/expphysiol.2013.071951] [PMID: 24078669]
[30]
Burnstock, G. Introduction: P2 receptors. Curr. Top. Med. Chem., 2004, 4(8), 793-803.
[http://dx.doi.org/10.2174/1568026043451014] [PMID: 15078211]
[31]
Burnstock, G. A Basis for distinguishing two types of purinergic receptor. Cell Membrane Receptors for Drugs and Hormone: A Multidisciplinary Approach, 1978, 107-118.
[32]
Burnstock, G.; Kennedy, C. Is there a basis for distinguishing two types of P2-purinoceptor? Gen. Pharmacol., 1985, 16(5), 433-440.
[http://dx.doi.org/10.1016/0306-3623(85)90001-1] [PMID: 2996968]
[33]
Burnstock, G. Purine and pyrimidine receptors. Cell. Mol. Life Sci., 2007, 64(12), 1471-1483.
[http://dx.doi.org/10.1007/s00018-007-6497-0] [PMID: 17375261]
[34]
Abbracchio, M.P.; Burnstock, G.; Boeynaems, J-M.; Barnard, E.A.; Boyer, J.L.; Kennedy, C.; Knight, G.E.; Fumagalli, M.; Gachet, C.; Jacobson, K.A.; Weisman, G.A. International union of pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev., 2006, 58(3), 281-341.
[http://dx.doi.org/10.1124/pr.58.3.3] [PMID: 16968944]
[35]
Lazarowski, E.R.; Sesma, J.I.; Seminario-Vidal, L.; Kreda, S.M. Molecular mechanisms of purine and pyrimidine nucleotide release. In:Pharmacology of Purine and Pyrimidine Receptors. Advances in Pharmacology; Jacobson, K.A.; Linden, J.; Enna, S.J., Eds.; Elsevier: Amsterdam, 2011, Vol. 61, pp. 221-261.
[http://dx.doi.org/10.1016/B978-0-12-385526-8.00008-4]
[36]
Fredholm, B.B.; IJzerman, A.P.; Jacobson, K.A.; Linden, J.; Müller, C.E. International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors--an update. Pharmacol. Rev., 2011, 63(1), 1-34.
[http://dx.doi.org/10.1124/pr.110.003285] [PMID: 21303899]
[37]
Zimmermann, H. Ectonucleotidases: some recent developments and a note on nomenclature. Drug Dev. Res., 2001, 52, 44-56.
[http://dx.doi.org/10.1002/ddr.1097]
[38]
Yegutkin, G.G. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim. Biophys. Acta, 2008, 1783(5), 673-694.
[http://dx.doi.org/10.1016/j.bbamcr.2008.01.024] [PMID: 18302942]
[39]
Franco, R.; Casadó, V.; Ciruela, F.; Saura, C.; Mallol, J.; Canela, E.I.; Lluis, C. Cell surface adenosine deaminase: much more than an ectoenzyme. Prog. Neurobiol., 1997, 52(4), 283-294.
[http://dx.doi.org/10.1016/S0301-0082(97)00013-0] [PMID: 9247966]
[40]
Koeppen, M.; Eckle, T.; Eltzschig, H.K. Interplay of hypoxia and a2b adenosine receptors in tissue protection. In:Pharmacology of Purine and Pyrimidine Receptors. Advances in Pharmacology; Jacobson, K.A.; Linden, J.; Enna, S.J., Eds.; Elsevier: Amsterdam, 2011, Vol. 61, pp. 145-186.
[http://dx.doi.org/10.1016/B978-0-12-385526-8.00006-0]
[41]
Menezes, C.B.; Frasson, A.P.; Meirelles, L.C.; Tasca, T. Adenosine, but not guanosine, protects vaginal epithelial cells from Trichomonas vaginalis cytotoxicity. Microbes Infect., 2017, 19(2), 122-131.
[http://dx.doi.org/10.1016/j.micinf.2016.11.001] [PMID: 27871906]
[42]
Gorodeski, G.I. P2X7 receptors and epithelial cancers. Purinergic Signal., 2009, 5(3), 351-368.
[43]
Aliagas, E.; Vidal, A.; Texidó, L.; Ponce, J.; Condom, E.; Martín-Satué, M. High expression of ecto-nucleotidases CD39 and CD73 in human endometrial tumors. Mediators Inflamm., 2014, 2014509027
[http://dx.doi.org/10.1155/2014/509027] [PMID: 24707115]
[44]
Su, R.Y.; Ho, L.J.; Yang, H.Y.; Chung, C.H.; Yang, S.S.; Cheng, C.Y.; Chien, W.C.; Lin, H.C. Association between Trichomonas vaginalis infection and cervical lesions: a population-based, nested case-control study in Taiwan. Parasitol. Res., 2020, 119(8), 2649-2657.
[http://dx.doi.org/10.1007/s00436-020-06759-4] [PMID: 32583161]
[45]
Burnstock, G. Purinergic signalling in the reproductive system in health and disease. Purinergic Signal., 2014, 10, 157-187.
[http://dx.doi.org/10.1007/s11302-013-9399-7]
[46]
Li, X.; Qi, X.; Zhou, L.; Fu, W.; Abdul-Karim, F.W.; Maclennan, G.; Gorodeski, G.I. P2X(7) receptor expression is decreased in epithelial cancer cells of ectodermal, uro-genital sinus, and distal paramesonephric duct origin. Purinergic Signal., 2009, 5(3), 351-368.
[http://dx.doi.org/10.1007/s11302-009-9161-3] [PMID: 19399640]
[47]
Gorodeski, G.I. Regulation of paracellular permeability in low-resistance human vaginal-cervical epithelia. In:Biotechnology, pharmaceutical aspects, drug absorption studies in situ, in vitro, and in silico models; Ehrhardt, C.; Kim, K.J., Eds.; Springer: Berlin, 2008, pp. 339-367.
[http://dx.doi.org/10.1007/978-0-387-74901-3_15]
[48]
Gorodeski, G.I. Purinergic signalling in the reproductive system. Auton. Neurosci., 2015, 191, 82-101.
[http://dx.doi.org/10.1016/j.autneu.2015.04.008] [PMID: 25981553]
[49]
Burnstock, G.; Di Virgilio, F. Purinergic signalling and cancer. Purinergic Signal., 2013, 9(4), 491-540.
[http://dx.doi.org/10.1007/s11302-013-9372-5] [PMID: 23797685]
[50]
Wang, X.; Chen, D. Purinergic regulation of neutrophil function. Front. Immunol., 2018, 9, 399.
[http://dx.doi.org/10.3389/fimmu.2018.00399] [PMID: 29545806]
[51]
Funaro, A.; Ortolan, E.; Bovino, P.; Lo Buono, N.; Nacci, G.; Parrotta, R.; Ferrero, E.; Malavasi, F. Ectoenzymes and innate immunity: the role of human CD157 in leukocyte trafficking. Front. Biosci., 2009, 14, 929-943.
[http://dx.doi.org/10.2741/3287] [PMID: 19273109]
[52]
Gounaris, K.; Selkirk, M.E. Parasite nucleotide-metabolizing enzymes and host purinergic signalling. Trends Parasitol., 2005, 21(1), 17-21.
[http://dx.doi.org/10.1016/j.pt.2004.10.005] [PMID: 15639736]
[53]
Idzko, M.; Ferrari, D.; Eltzschig, H.K. Nucleotide signalling during inflammation. Nature, 2014, 509(7500), 310-317.
[http://dx.doi.org/10.1038/nature13085] [PMID: 24828189]
[54]
Sansom, F.M. The role of the NTPDase enzyme family in parasites: what do we know, and where to from here? Parasitology, 2012, 139(8), 963-980.
[http://dx.doi.org/10.1017/S003118201200025X] [PMID: 22423612]
[55]
de Aguiar Matos, J.A.; Borges, F.P.; Tasca, T.; Bogo, M.R.; De Carli, G.A.; da Graça Fauth, M.; Dias, R.D.; Bonan, C.D. Characterisation of an ATP diphosphohydrolase (Apyrase, EC 3.6.1.5) activity in Trichomonas vaginalis. Int. J. Parasitol., 2001, 31(8), 770-775.
[http://dx.doi.org/10.1016/S0020-7519(01)00191-6] [PMID: 11403767]
[56]
Tasca, T.; Bonan, C.D.; Carli, G.A.D.; Battastini, A.M.O.; Sarkis, J.J.F. Characterization of an ecto-5′-nucleotidase (EC 3.1.3.5) activity in intact cells of Trichomonas vaginalis. Exp. Parasitol., 2003, 105(2), 167-173.
[http://dx.doi.org/10.1016/j.exppara.2003.12.001] [PMID: 14969694]
[57]
Weizenmann, M.; Frasson, A.P.; de Barros, M.P.; Vieira, P. de B.; Rosemberg, D.B.; De Carli, G.A.; Bogo, M.R.; Bonan, C.D.; Tasca, T. Kinetic characterization and gene expression of adenosine deaminase in intact trophozoites of Trichomonas vaginalis. FEMS Microbiol. Lett., 2011, 319(2), 115-124.
[http://dx.doi.org/10.1111/j.1574-6968.2011.02283.x] [PMID: 21477257]
[58]
Tasca, T.; Bonan, C.D.; De Carli, G.A.; Sarkis, J.J.F. Trichomonas vaginalis: cytochemical localization of a NTPDase1 and an ecto-5′-nucleotidase and effects of adenine nucleotides on cellular viability. Parasitol. Res., 2004, 93(4), 300-303.
[http://dx.doi.org/10.1007/s00436-004-1126-4] [PMID: 15175877]
[59]
Frasson, A.P.; Dos Santos, O.; Meirelles, L.C.; Macedo, A.J.; Tasca, T. Five putative nucleoside triphosphate diphosphohydrolase genes are expressed in Trichomonas vaginalis. FEMS Microbiol. Lett., 2016, 363(2)fnv221
[http://dx.doi.org/10.1093/femsle/fnv221] [PMID: 26590960]
[60]
Zimmermann, H. 5′-Nucleotidase: molecular structure and functional aspects. Biochem. J., 1992, 285(Pt 2), 345-365.
[http://dx.doi.org/10.1042/bj2850345] [PMID: 1637327]
[61]
Zimmermann, H.; Zebisch, M.; Sträter, N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal., 2012, 8(3), 437-502.
[http://dx.doi.org/10.1007/s11302-012-9309-4] [PMID: 22555564]
[62]
Adinolfi, E.; Giuliani, A.L.; De Marchi, E.; Pegoraro, A.; Orioli, E.; Di Virgilio, F. The P2X7 receptor: A main player in inflammation. Biochem. Pharmacol., 2018, 151, 234-244.
[http://dx.doi.org/10.1016/j.bcp.2017.12.021] [PMID: 29288626]
[63]
Munagala, N.R.; Wang, C.C. Adenosine is the primary precursor of all purine nucleotides in Trichomonas vaginalis. Mol. Biochem. Parasitol., 2003, 127(2), 143-149.
[http://dx.doi.org/10.1016/S0166-6851(02)00330-4] [PMID: 12672523]
[64]
Tasca, T.; Borges, F.P.; Bonan, C.D.; De Carli, G.A.; Battastini, A.M.; Sarkis, J.J. Effects of metronidazole and tinidazole on NTPDase1 and ecto-5′-nucleotidase from intact cells of Trichomonas vaginalis. FEMS Microbiol. Lett., 2003, 226(2), 379-384.
[http://dx.doi.org/10.1016/S0378-1097(03)00637-2] [PMID: 14553936]
[65]
Fietto, J.L.R.; DeMarco, R.; Nascimento, I.P.; Castro, I.M.; Carvalho, T.M.U.; de Souza, W.; Bahia, M.T.; Alves, M.J.M.; Verjovski-Almeida, S. Characterization and immunolocalization of an NTP diphosphohydrolase of Trypanosoma cruzi. Biochem. Biophys. Res. Commun., 2004, 316(2), 454-460.
[http://dx.doi.org/10.1016/j.bbrc.2004.02.071] [PMID: 15020239]
[66]
Tasca, T.; Bonan, C.D.; De Carli, G.A.; Sarkis, J.J.F.; Alderete, J.F. Heterogeneity in extracellular nucleotide hydrolysis among clinical isolates of Trichomonas vaginalis. Parasitology, 2005, 131(Pt 1), 71-78.
[http://dx.doi.org/10.1017/S0031182005007377] [PMID: 16038398]
[67]
Heyworth, P.G.; Gutteridge, W.E.; Ginger, C.D. Purine metabolism in Trichomonas vaginalis. FEBS Lett., 1982, 141(1), 106-110.
[http://dx.doi.org/10.1016/0014-5793(82)80026-4] [PMID: 6282644]
[68]
Heyworth, P.G.; Gutteridge, W.E.; Ginger, C.D. Pyrimidine metabolism in Trichomonas vaginalis. FEBS Lett., 1984, 176(1), 55-60.
[http://dx.doi.org/10.1016/0014-5793(84)80910-2] [PMID: 6333357]
[69]
Bouma, M.G.; van den Wildenberg, F.A.J.M.; Buurman, W.A. The anti-inflammatory potencial of adenosine in ischemia-reperfusion injury: established and putative beneficial action of retaliatory metabolite. Shock, 1997, 8(5), 313-320.
[70]
Haskó, G.; Cronstein, B.N. Adenosine: an endogenous regulator of innate immunity. Trends Immunol., 2004, 25(1), 33-39.
[http://dx.doi.org/10.1016/j.it.2003.11.003] [PMID: 14698282]
[71]
Demirezen, S.; Safi, Z.; Beksaç, S. The interaction of Trichomonas vaginalis with epithelial cells, polymorphonuclear leucocytes and erythrocytes on vaginal smears: light microscopic observation. Cytopathology, 2000, 11(5), 326-332.
[http://dx.doi.org/10.1046/j.1365-2303.2000.00237.x] [PMID: 11014660]
[72]
Kukulski, F.; Ben Yebdri, F.; Lecka, J.; Kauffenstein, G.; Lévesque, S.A.; Martín-Satué, M.; Sévigny, J. Extracellular ATP and P2 receptors are required for IL-8 to induce neutrophil migration. Cytokine, 2009, 46(2), 166-170.
[http://dx.doi.org/10.1016/j.cyto.2009.02.011] [PMID: 19303321]
[73]
Arroyo, R.; Ochoa, T.; Tai, J-H.; de la Garza, M. Iron and parasites. BioMed Res. Int., 2015, 2015291672
[http://dx.doi.org/10.1155/2015/291672] [PMID: 26078944]
[74]
Vieira, Pde. B.; Silva, N.L.F.; Kist, L.W.; Oliveira, G.M. de T.; Bogo, M.R.; Carli, G.A.; Macedo, A.J.; Tasca, T. Iron from haemoglobin and haemin modulates nucleotide hydrolysis in Trichomonas vaginalis. Mem. Inst. Oswaldo Cruz, 2015, 110(2), 201-208.
[http://dx.doi.org/10.1590/0074-02760140320] [PMID: 25946243]
[75]
Primon-Barros, M.; Rigo, G.V.; Frasson, A.P.; Santos, Od.; Smiderle, L.; Almeida, S.; Macedo, A.J.; Tasca, T. Modulatory effect of iron chelators on adenosine deaminase activity and gene expression in Trichomonas vaginalis. Mem. Inst. Oswaldo Cruz, 2015, 110(7), 877-883.
[http://dx.doi.org/10.1590/0074-02760150076] [PMID: 26517498]
[76]
Frasson, A.P.; Charão, M.F.; Rosemberg, D.B.; de Souza, A.P.; Garcia, S.C.; Bonorino, C.; Bogo, M.R.; De Carli, G.A.; Tasca, T. Analysis of the NTPDase and ecto-5′-nucleotidase profiles in serum-limited Trichomonas vaginalis. Mem. Inst. Oswaldo Cruz, 2012, 107(2), 170-177.
[http://dx.doi.org/10.1590/S0074-02762012000200004] [PMID: 22415254]
[77]
Menezes, C.B.; Durgante, J.; de Oliveira, R.R.; Dos Santos, V.H.J.M.; Rodrigues, L.F.; Garcia, S.C.; Dos Santos, O.; Tasca, T. Trichomonas vaginalis NTPDase and ecto-5′-nucleotidase hydrolyze guanine nucleotides and increase extracellular guanosine levels under serum restriction. Mol. Biochem. Parasitol., 2016, 207(1), 10-18.
[http://dx.doi.org/10.1016/j.molbiopara.2016.04.003] [PMID: 27150347]
[78]
Lustig, G.; Ryan, C.M.; Secor, W.E.; Johnson, P.J. Trichomonas vaginalis contact-dependent cytolysis of epithelial cells. Infect. Immun., 2013, 81(5), 1411-1419.
[http://dx.doi.org/10.1128/IAI.01244-12] [PMID: 23429535]
[79]
Sharma, P.; Malla, N.; Gupta, I.; Ganguly, N.K.; Mahajan, R.C. Anti-trichomonad IgA antibodies in trichomoniasis before and after treatment. Folia Microbiol. (Praha), 1991, 36(3), 302-304.
[http://dx.doi.org/10.1007/BF02814365] [PMID: 1841864]
[80]
Kaur, S.; Khurana, S.; Bagga, R.; Wanchu, A.; Malla, N. Anti-Trichomonas IgG, IgM, IgA, and IgG subclass responses in human intravaginal trichomoniasis. Parasitol. Res., 2008, 103(2), 305-312.
[http://dx.doi.org/10.1007/s00436-008-0971-y] [PMID: 18437425]
[81]
Bastida-Corcuera, F.D.; Singh, B.N.; Gray, G.C.; Stamper, P.D.; Davuluri, M.; Schlangen, K.; Corbeil, R.R.; Corbeil, L.B. Antibodies to Trichomonas vaginalis surface glycolipid. Sex. Transm. Infect., 2013, 89(6), 467-472.
[http://dx.doi.org/10.1136/sextrans-2012-051013] [PMID: 23785040]
[82]
Yadav, M.; Dubey, M.L.; Gupta, I.; Malla, N. Cysteine proteinase 30 (CP30) and antibody response to CP30 in serum and vaginal washes of symptomatic and asymptomatic Trichomonas vaginalis-infected women. Parasite Immunol., 2007, 29(7), 359-365.
[http://dx.doi.org/10.1111/j.1365-3024.2007.00952.x] [PMID: 17576365]
[83]
Shaio, M.F.; Lin, P.R.; Liu, J.Y.; Yang, K.D. Generation of interleukin-8 from human monocytes in response to Trichomonas vaginalis stimulation. Infect. Immun., 1995, 63(10), 3864-3870.
[http://dx.doi.org/10.1128/IAI.63.10.3864-3870.1995] [PMID: 7558293]
[84]
Forman, H.J.; Torres, M. Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am. J. Respir. Crit. Care Med., 2002, 166(12), S4-S8.
[85]
Burnstock, G.; Boeynaems, J-M. Purinergic signalling and immune cells. Purinergic Signal., 2014, 10(4), 529-564.
[http://dx.doi.org/10.1007/s11302-014-9427-2] [PMID: 25352330]
[86]
Frasson, A.P.; De Carli, G.A.; Bonan, C.D.; Tasca, T. Involvement of purinergic signaling on nitric oxide production by neutrophils stimulated with Trichomonas vaginalis. Purinergic Signal., 2012, 8(1), 1-9.
[http://dx.doi.org/10.1007/s11302-011-9254-7] [PMID: 21833696]
[87]
Frasson, A.P.; Menezes, C.B.; Goelzer, G.K.; Gnoatto, S.C.B.; Garcia, S.C.; Tasca, T. Adenosine reduces reactive oxygen species and interleukin-8 production by Trichomonas vaginalis-stimulated neutrophils. Purinergic Signal., 2017, 13(4), 569-577.
[http://dx.doi.org/10.1007/s11302-017-9584-1] [PMID: 28879644]
[88]
de Brum Vieira, P.; Tasca, T.; Secor, W.E. Challenges and persistent questions in the treatment of trichomoniasis. Curr. Top. Med. Chem., 2017, 17(11), 1249-1265.
[http://dx.doi.org/10.2174/1568026616666160930150429] [PMID: 27697044]
[89]
Bala, V.; Chhonker, Y.S. Recent developments in anti-Trichomonas research: An update review. Eur. J. Med. Chem., 2018, 143, 232-243.
[http://dx.doi.org/10.1016/j.ejmech.2017.11.029] [PMID: 29175675]
[90]
Giordani, R.B.; Weizenmann, M.; Rosemberg, D.B.; De Carli, G.A.; Bogo, M.R.; Zuanazzi, J.A.S.; Tasca, T. Trichomonas vaginalis nucleoside triphosphate diphosphohydrolase and ecto-5′-nucleotidase activities are inhibited by lycorine and candimine. Parasitol. Int., 2010, 59(2), 226-231.
[http://dx.doi.org/10.1016/j.parint.2010.02.004] [PMID: 20176129]
[91]
Petró-Silveira, B.; Rigo, G.V.; da Silva Trentin, D.; Macedo, A.J.; Sauer, E.; de Oliveira Alves, E.; Tallini, L.R.; Garcia, S.C.; de Souza Borges, W.; Zuanazzi, J.Â.S.; Tasca, T. Trichomonas vaginalis NTPDase inhibited by lycorine modulates the parasite-neutrophil interaction. Parasitol. Res., 2020, 119(8), 2587-2595.
[http://dx.doi.org/10.1007/s00436-020-06739-8] [PMID: 32524267]
[92]
Menezes, C.B.; Rigo, G.V.; Bridi, H.; Trentin, D.D.S.; Macedo, A.J.; von Poser, G.L.; Tasca, T. The anti-Trichomonas vaginalis phloroglucinol derivative isoaustrobrasilol B modulates extracellular nucleotide hydrolysis. Chem. Biol. Drug Des., 2017, 90(5), 811-819.
[http://dx.doi.org/10.1111/cbdd.13002] [PMID: 28390095]
[93]
Harris, D.I.; Beechey, R.B.; Linstead, D.; Barrett, J. Nucleoside uptake by Trichomonas vaginalis. Mol. Biochem. Parasitol., 1988, 29(2-3), 105-116.
[http://dx.doi.org/10.1016/0166-6851(88)90065-5] [PMID: 2457803]
[94]
El Kouni, M.H. Potential chemotherapeutic targets in the purine metabolism of parasites. Pharmacol. Ther., 2003, 99(3), 283-309.
[http://dx.doi.org/10.1016/S0163-7258(03)00071-8] [PMID: 12951162]
[95]
Wang, C.C.; Cheng, H-W. Salvage of pyrimidine nucleosides by Trichomonas vaginalis. Mol. Biochem. Parasitol., 1984, 10(2), 171-184.
[http://dx.doi.org/10.1016/0166-6851(84)90005-7] [PMID: 6199666]
[96]
Munagala, N.; Wang, C.C. The purine nucleoside phosphorylase from Trichomonas vaginalis is a homologue of the bacterial enzyme. Biochemistry, 2002, 41(33), 10382-10389.
[http://dx.doi.org/10.1021/bi026025n] [PMID: 12173924]
[97]
Zang, Y.; Wang, W-H.; Wu, S-W.; Ealick, S.E.; Wang, C.C. Identification of a subversive substrate of Trichomonas vaginalis purine nucleoside phosphorylase and the crystal structure of the enzyme-substrate complex. J. Biol. Chem., 2005, 280(23), 22318-22325.
[http://dx.doi.org/10.1074/jbc.M501843200] [PMID: 15817485]
[98]
Rinaldo-Matthis, A.; Wing, C.; Ghanem, M.; Deng, H.; Wu, P.; Gupta, A.; Tyler, P.C.; Evans, G.B.; Furneaux, R.H.; Almo, S.C.; Wang, C.C.; Schramm, V.L. Inhibition and structure of Trichomonas vaginalis purine nucleoside phosphorylase with picomolar transition state analogues. Biochemistry, 2007, 46(3), 659-668.
[http://dx.doi.org/10.1021/bi061515r] [PMID: 17223688]
[99]
Evans, G.B.; Tyler, P.C.; Schramm, V.L. Immucillins in infectious diseases. ACS Infect. Dis., 2018, 4(2), 107-117.
[http://dx.doi.org/10.1021/acsinfecdis.7b00172] [PMID: 29151351]
[100]
Alam, R.; Barbarovich, A.T.; Caravan, W.; Ismail, M.; Barskaya, A.; Parkin, D.W.; Stockman, B.J. Druggability of the guanosine/adenosine/cytidine nucleoside hydrolase from Trichomonas vaginalis. Chem. Biol. Drug Des., 2018, 92(4), 1736-1742.
[http://dx.doi.org/10.1111/cbdd.13341] [PMID: 29808562]

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