Login Register Cart 0
Generic placeholder image

Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Phage-choline Kinase Inhibitor Combination to Control Pseudomonas aeruginosa: A Promising Combo

Author(s): Moad Khalifa, Ling Ling Few and Wei Cun See Too*

Volume 22, Issue 9, 2022

Published on: 18 January, 2022

Page: [1281 - 1288] Pages: 8

DOI: 10.2174/1389557521666211213160256

Price: $65

Abstract

Background: Pseudomonas aeruginosa is one of the most prevalent opportunistic pathogens in humans that has thrived and proved to be difficult to control in this “post-antibiotic era.” Antibiotic alternatives are necessary for fighting against this resilient bacterium. Even though phages might not be “the wonder drug” that solves everything, they still provide a viable option to combat P. aeruginosa and curb the threat it imposes.

Main Findings: The combination of antibiotics with phages, however, poses a propitious treatment option for P. aeruginosa. Choline kinase (ChoK) is the enzyme that synthesizes phosphorylcholine subsequently incorporated into lipopolysaccharide located at the outer membrane of gram-negative bacteria. Recently, inhibition of ChoKs has been proposed as a promising antibacterial strategy. Successful docking of Hemicholinium-3, a choline kinase inhibitor, to the model structure of P. aeruginosa ChoK also supports the use of this inhibitor or its derivatives to inhibit the growth of this microorganism.

Conclusion: Therefore, the combination of the novel antimicrobial “choline kinase inhibitors (ChoKIs)” with a phage cocktail or synthetic phages as a potential treatment for P. aeruginosa infection has been proposed.

Keywords: Choline kinase inhibitor, phage therapy, Pseudomonas aeruginosa, antibiotic resistance, infection, combined therapy.

« Previous Next »
Graphical Abstract

[1]
Parkins, M.D.; Somayaji, R.; Waters, V.J. Epidemiology, biology, and impact of clonal Pseudomonas aeruginosa infections in cystic fibrosis. Clin. Microbiol. Rev., 2018, 31(4), e00019-e18.
[http://dx.doi.org/10.1128/CMR.00019-18] [PMID: 30158299]
[2]
Brüggemann, H.; Migliorini, L.B.; Sales, R.O.; Koga, P.C.M.; Souza, A.V.; Jensen, A.; Poehlein, A.; Brzuszkiewicz, E.; Doi, A.M.; Pasternak, J.; Martino, M.D.V.; Severino, P. Comparative genomics of nonoutbreak Pseudomonas aeruginosa strains underlines genome plasticity and geographic relatedness of the global clone ST235. Genome Biol. Evol., 2018, 10(7), 1852-1857.
[http://dx.doi.org/10.1093/gbe/evy139] [PMID: 29982603]
[3]
Meradji, S.; Barguigua, A.; Zerouali, K.; Mazouz, D.; Chettibi, H.; Elmdaghri, N.; Timinouni, M. Epidemiology of carbapenem non-susceptible Pseudomonas aeruginosa isolates in Eastern Algeria. Antimicrob. Resist. Infect. Control, 2015, 4(1), 27.
[http://dx.doi.org/10.1186/s13756-015-0067-2] [PMID: 26075066]
[4]
Vincent, J.L.; Rello, J.; Marshall, J.; Silva, E.; Anzueto, A.; Martin, C.D.; Moreno, R.; Lipman, J.; Gomersall, C.; Sakr, Y.; Reinhart, K. International study of the prevalence and outcomes of infection in intensive care units. JAMA, 2009, 302(21), 2323-2329.
[http://dx.doi.org/10.1001/jama.2009.1754] [PMID: 19952319]
[5]
Bagge, N.; Schuster, M.; Hentzer, M.; Ciofu, O.; Givskov, M.; Greenberg, E.P.; Høiby, N. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob. Agents Chemother., 2004, 48(4), 1175-1187.
[http://dx.doi.org/10.1128/AAC.48.4.1175-1187.2004] [PMID: 15047518]
[6]
Ciofu, O.; Tolker-Nielsen, T. Tolerance and resistance of Pseudomonas aeruginosa Biofilms to antimicrobial agents-how P. aeruginosa can escape Antibiotics. Front. Microbiol., 2019, 10, 913.
[http://dx.doi.org/10.3389/fmicb.2019.00913] [PMID: 31130925]
[7]
Gellatly, S.L.; Hancock, R.E.W. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses. Pathog. Dis., 2013, 67(3), 159-173.
[http://dx.doi.org/10.1111/2049-632X.12033] [PMID: 23620179]
[8]
Tashiro, Y.; Inagaki, A.; Ono, K.; Inaba, T.; Yawata, Y.; Uchiyama, H.; Nomura, N. Low concentrations of ethanol stimulate biofilm and pellicle formation in Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem., 2014, 78(1), 178-181.
[http://dx.doi.org/10.1080/09168451.2014.877828] [PMID: 25036502]
[9]
Duval, R.E.; Grare, M.; Demoré, B. Fight against antimicrobial resistance: We always need new antibacterials but for right bacteria. Molecules, 2019, 24(17), 3152.
[http://dx.doi.org/10.3390/molecules24173152] [PMID: 31470632]
[10]
Guo, Z.; Lin, H.; Ji, X.; Yan, G.; Lei, L.; Han, W.; Gu, J.; Huang, J. Therapeutic applications of lytic phages in human medicine. Microb. Pathog., 2020, 142, 104048.
[http://dx.doi.org/10.1016/j.micpath.2020.104048] [PMID: 32035104]
[11]
De Sordi, L.; Lourenço, M.; Debarbieux, L. The battle within: Interactions of bacteriophages and bacteria in the gastrointestinal tract. Cell Host Microbe, 2019, 25(2), 210-218.
[http://dx.doi.org/10.1016/j.chom.2019.01.018] [PMID: 30763535]
[12]
Labrie, S.J.; Samson, J.E.; Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol., 2010, 8(5), 317-327.
[http://dx.doi.org/10.1038/nrmicro2315] [PMID: 20348932]
[13]
Orzechowska, B.; Mohammed, M. The War between Bacteria and Bacteriophages. In: Growing and Handling of Bacterial Cultures; IntechOpen: London, UK, 2019.
[http://dx.doi.org/10.5772/intechopen.87247]
[14]
Stern, A.; Sorek, R. The phage-host arms race: Shaping the evolution of microbes. BioEssays, 2011, 33(1), 43-51.
[http://dx.doi.org/10.1002/bies.201000071] [PMID: 20979102]
[15]
Rohde, C.; Wittmann, J.; Kutter, E. bacteriophages: a therapy concept against multi-drug-resistant bacteria. Surg. Infect. (Larchmt.), 2018, 19(8), 737-744.
[http://dx.doi.org/10.1089/sur.2018.184] [PMID: 30256176]
[16]
Harper, D.R. Criteria for selecting suitable infectious diseases for phage therapy. Viruses, 2018, 10(4), 177.
[http://dx.doi.org/10.3390/v10040177] [PMID: 29621149]
[17]
Koskella, B.; Meaden, S. Understanding bacteriophage specificity in natural microbial communities. Viruses, 2013, 5(3), 806-823.
[http://dx.doi.org/10.3390/v5030806] [PMID: 23478639]
[18]
Sillankorva, S.M.; Oliveira, H.; Azeredo, J. Bacteriophages and their role in food safety. Int. J. Microbiol., 2012, 2012, 863945.
[http://dx.doi.org/10.1155/2012/863945] [PMID: 23316235]
[19]
Matilla, M.A.; Salmond, G.P.C. Bacteriophage ϕMAM1, a viunalikevirus, is a broad-host-range, high-efficiency generalized transducer that infects environmental and clinical isolates of the enterobacterial genera Serratia and Kluyvera. Appl. Environ. Microbiol., 2014, 80(20), 6446-6457.
[http://dx.doi.org/10.1128/AEM.01546-14] [PMID: 25107968]
[20]
Jault, P.; Leclerc, T.; Jennes, S.; Pirnay, J.P.; Que, Y.A.; Resch, G.; Rousseau, A.F.; Ravat, F.; Carsin, H.; Le Floch, R.; Schaal, J.V.; Soler, C.; Fevre, C.; Arnaud, I.; Bretaudeau, L.; Gabard, J. Efficacy and tolerability of a cocktail of bacteriophages to treat burn wounds infected by Pseudomonas aeruginosa (PhagoBurn): A randomised, controlled, double-blind phase 1/2 trial. Lancet Infect. Dis., 2019, 19(1), 35-45.
[http://dx.doi.org/10.1016/S1473-3099(18)30482-1] [PMID: 30292481]
[21]
Kutter, E.; De Vos, D.; Gvasalia, G.; Alavidze, Z.; Gogokhia, L.; Kuhl, S.; Abedon, S.T. Phage therapy in clinical practice: Treatment of human infections. Curr. Pharm. Biotechnol., 2010, 11(1), 69-86.
[http://dx.doi.org/10.2174/138920110790725401] [PMID: 20214609]
[22]
Principi, N.; Silvestri, E.; Esposito, S. Advantages and limitations of bacteriophages for the treatment of bacterial infections. Front. Pharmacol., 2019, 10, 513.
[http://dx.doi.org/10.3389/fphar.2019.00513] [PMID: 31139086]
[23]
Salmond, G.P.C.; Fineran, P.C. A century of the phage: Past, present and future. Nat. Rev. Microbiol., 2015, 13(12), 777-786.
[http://dx.doi.org/10.1038/nrmicro3564] [PMID: 26548913]
[24]
Payne, D.J.; Gwynn, M.N.; Holmes, D.J.; Pompliano, D.L. Drugs for bad bugs: Confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov., 2007, 6(1), 29-40.
[http://dx.doi.org/10.1038/nrd2201] [PMID: 17159923]
[25]
Furfaro, L.L.; Payne, M.S.; Chang, B.J. Bacteriophage therapy: Clinical trials and regulatory hurdles. Front. Cell. Infect. Microbiol., 2018, 8, 376.
[http://dx.doi.org/10.3389/fcimb.2018.00376] [PMID: 30406049]
[26]
Roach, D.R.; Debarbieux, L. Phage therapy: Awakening a sleeping giant. Emerg. Top. Life Sci., 2017, 1(1), 93-103.
[http://dx.doi.org/10.1042/ETLS20170002] [PMID: 33525818]
[27]
Yehl, K.; Lemire, S.; Yang, A.C.; Ando, H.; Mimee, M.; Torres, M.T.; de la Fuente-Nunez, C.; Lu, T.K. Engineering phage host-range and suppressing bacterial resistance through phage tail fiber mutagenesis. Cell, 2019, 179(2), 459-469.e9.
[http://dx.doi.org/10.1016/j.cell.2019.09.015] [PMID: 31585083]
[28]
Borges, A.L.; Davidson, A.R.; Bondy-Denomy, J. The discovery, mechanisms, and evolutionary impact of anti-CRISPRs. Annu. Rev. Virol., 2017, 4(1), 37-59.
[http://dx.doi.org/10.1146/annurev-virology-101416-041616] [PMID: 28749735]
[29]
Merril, C.R.; Biswas, B.; Carlton, R.; Jensen, N.C.; Creed, G.J.; Zullo, S.; Adhya, S. Long-circulating bacteriophage as antibacterial agents. Proc. Natl. Acad. Sci. USA, 1996, 93(8), 3188-3192.
[http://dx.doi.org/10.1073/pnas.93.8.3188] [PMID: 8622911]
[30]
Vitiello, C.L.; Merril, C.R.; Adhya, S. An amino acid substitution in a capsid protein enhances phage survival in mouse circulatory system more than a 1000-fold. Virus Res., 2005, 114(1-2), 101-103.
[http://dx.doi.org/10.1016/j.virusres.2005.05.014] [PMID: 16055223]
[31]
Matsuda, T.; Freeman, T.A.; Hilbert, D.W.; Duff, M.; Fuortes, M.; Stapleton, P.P.; Daly, J.M. Lysis-deficient bacteriophage therapy decreases endotoxin and inflammatory mediator release and improves survival in a murine peritonitis model. Surgery, 2005, 137(6), 639-646.
[http://dx.doi.org/10.1016/j.surg.2005.02.012] [PMID: 15933632]
[32]
Paul, V.D.; Sundarrajan, S.; Rajagopalan, S.S.; Hariharan, S.; Kempashanaiah, N.; Padmanabhan, S.; Sriram, B.; Ramachandran, J. Lysis-deficient phages as novel therapeutic agents for controlling bacterial infection. BMC Microbiol., 2011, 11(1), 195.
[http://dx.doi.org/10.1186/1471-2180-11-195] [PMID: 21880144]
[33]
Hagens, S.; Bläsi, U. Genetically modified filamentous phage as bactericidal agents: A pilot study. Lett. Appl. Microbiol., 2003, 37(4), 318-323.
[http://dx.doi.org/10.1046/j.1472-765X.2003.01400.x] [PMID: 12969496]
[34]
Little, J.W.; Harper, J.E. Identification of the lexA gene product of Escherichia coli K-12. Proc. Natl. Acad. Sci. USA, 1979, 76(12), 6147-6151.
[http://dx.doi.org/10.1073/pnas.76.12.6147] [PMID: 160562]
[35]
Lu, T.K.; Collins, J.J. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc. Natl. Acad. Sci. USA, 2009, 106(12), 4629-4634.
[http://dx.doi.org/10.1073/pnas.0800442106] [PMID: 19255432]
[36]
Barbu, E.M.; Cady, K.C.; Hubby, B. Phage therapy in the era of synthetic biology. Cold Spring Harb. Perspect. Biol., 2016, 8(10), a023879.
[http://dx.doi.org/10.1101/cshperspect.a023879] [PMID: 27481531]
[37]
Kilcher, S.; Loessner, M.J. Engineering bacteriophages as versatile biologics. Trends Microbiol., 2019, 27(4), 355-367.
[http://dx.doi.org/10.1016/j.tim.2018.09.006] [PMID: 30322741]
[38]
Lenneman, B.R.; Fernbach, J.; Loessner, M.J.; Lu, T.K.; Kilcher, S. Enhancing phage therapy through synthetic biology and genome engineering. Curr. Opin. Biotechnol., 2021, 68, 151-159.
[http://dx.doi.org/10.1016/j.copbio.2020.11.003] [PMID: 33310655]
[39]
Danis-Wlodarczyk, K.; Vandenheuvel, D.; Jang, H.B.; Briers, Y.; Olszak, T.; Arabski, M.; Wasik, S.; Drabik, M.; Higgins, G.; Tyrrell, J.; Harvey, B.J.; Noben, J.P.; Lavigne, R.; Drulis-Kawa, Z. A proposed integrated approach for the preclinical evaluation of phage therapy in Pseudomonas infections. Sci. Rep., 2016, 6, 28115.
[http://dx.doi.org/10.1038/srep28115] [PMID: 27301427]
[40]
Torres-Barceló, C.; Arias-Sánchez, F.I.; Vasse, M.; Ramsayer, J.; Kaltz, O.; Hochberg, M.E. A window of opportunity to control the bacterial pathogen Pseudomonas aeruginosa combining antibiotics and phages. PLoS One, 2014, 9(9), e106628.
[http://dx.doi.org/10.1371/journal.pone.0106628] [PMID: 25259735]
[41]
Yang, Y.; Shen, W.; Zhong, Q.; Chen, Q.; He, X.; Baker, J.L.; Xiong, K.; Jin, X.; Wang, J.; Hu, F.; Le, S. DDevelopment of a bacteriophage cocktail to constrain the emergence of phage-resistant Pseudomonas aeruginosa. Front. Microbiol., 2020, 11, 327.
[http://dx.doi.org/10.3389/fmicb.2020.00327] [PMID: 32194532]
[42]
Wright, R.C.T.; Friman, V.P.; Smith, M.C.M.; Brockhurst, M.A. Resistance evolution against phage combinations depends on the timing and order of exposure. MBio, 2019, 10(5), e01652-e19.
[http://dx.doi.org/10.1128/mBio.01652-19] [PMID: 31551330]
[43]
Akturk, E.; Oliveira, H.; Santos, S.B.; Costa, S.; Kuyumcu, S.; Melo, L.D.R.; Azeredo, J. Synergistic action of phage and antibiotics: Parameters to enhance the killing efficacy against mono and dual-species biofilms. Antibiotics (Basel), 2019, 8(3), E103.
[44]
Cui, Z.; Guo, X.; Feng, T.; Li, L. Exploring the Whole Standard Operating Procedure for Phage Therapy in Clinical Practice. J. Transl. Med., 2019, 17(1), 373.
[http://dx.doi.org/10.1186/s12967-019-2120-z] [PMID: 31727099]
[45]
Górski, A.; Borysowski, J.; Międzybrodzki, R. Phage Therapy: Towards a Successful Clinical Trial. Antibiot. (Basel, Switzerland), 2020, 9(11), 827.
[http://dx.doi.org/10.3390/antibiotics9110827] [PMID: 33227949]
[46]
Darch, S.E.; Kragh, K.N.; Abbott, E.A.; Bjarnsholt, T.; Bull, J.J.; Whiteley, M. Phage inhibit pathogen dissemination by targeting bacterial migrants in a chronic infection model. MBio, 2017, 8(2), e00240-e17.
[http://dx.doi.org/10.1128/mBio.00240-17] [PMID: 28377527]
[47]
Rodriguez-Gonzalez, R.A.; Leung, C.Y.; Chan, B.K.; Turner, P.E.; Weitz, J.S. Quantitative models of phage-antibiotic combination therapy. mSystems, 2020, 5(1), e00756-e19.
[http://dx.doi.org/10.1128/mSystems.00756-19] [PMID: 32019835]
[48]
Chan, B.K.; Sistrom, M.; Wertz, J.E.; Kortright, K.E.; Narayan, D.; Turner, P.E. Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci. Rep., 2016, 6(1), 26717.
[http://dx.doi.org/10.1038/srep26717] [PMID: 27225966]
[49]
Comeau, A.M.; Tétart, F.; Trojet, S.N.; Prère, M.F.; Krisch, H.M. Phage-Antibiotic Synergy (PAS): β-lactam and quinolone antibiotics stimulate virulent phage growth. PLoS One, 2007, 2(8), e799.
[http://dx.doi.org/10.1371/journal.pone.0000799] [PMID: 17726529]
[50]
Oechslin, F.; Piccardi, P.; Mancini, S.; Gabard, J.; Moreillon, P.; Entenza, J.M.; Resch, G.; Que, Y.A. interaction between phage therapy and antibiotics clears Pseudomonas aeruginosa infection in endocarditis and reduces virulence. J. Infect. Dis., 2017, 215(5), 703-712.
[http://dx.doi.org/10.1093/infdis/jiw632] [PMID: 28007922]
[51]
Cafora, M.; Deflorian, G.; Forti, F.; Ferrari, L.; Binelli, G.; Briani, F.; Ghisotti, D.; Pistocchi, A. Phage therapy against Pseudomonas aeruginosa infections in a cystic fibrosis zebrafish model. Sci. Rep., 2019, 9(1), 1527.
[http://dx.doi.org/10.1038/s41598-018-37636-x] [PMID: 30728389]
[52]
Chaudhry, W.N.; Concepción-Acevedo, J.; Park, T.; Andleeb, S.; Bull, J.J.; Levin, B.R. Synergy and order effects of antibiotics and phages in killing Pseudomonas aeruginosa biofilms. PLoS One, 2017, 12(1), e0168615.
[http://dx.doi.org/10.1371/journal.pone.0168615] [PMID: 28076361]
[53]
Tagliaferri, T.L.; Jansen, M.; Horz, H.P. Fighting pathogenic bacteria on two fronts: Phages and antibiotics as combined strategy. Front. Cell. Infect. Microbiol., 2019, 9, 22.
[http://dx.doi.org/10.3389/fcimb.2019.00022] [PMID: 30834237]
[54]
Torres-Barceló, C.; Gurney, J.; Gougat-Barberá, C.; Vasse, M.; Hochberg, M.E. Transient negative effects of antibiotics on phages do not jeopardise the advantages of combination therapies. FEMS Microbiol. Ecol., 2018, 94(8)
[http://dx.doi.org/10.1093/femsec/fiy107] [PMID: 29878184]
[55]
Uchiyama, J.; Shigehisa, R.; Nasukawa, T.; Mizukami, K.; Takemura-Uchiyama, I.; Ujihara, T.; Murakami, H.; Imanishi, I.; Nishifuji, K.; Sakaguchi, M.; Matsuzaki, S. Piperacillin and ceftazidime produce the strongest synergistic phage-antibiotic effect in Pseudomonas aeruginosa. Arch. Virol., 2018, 163(7), 1941-1948.
[http://dx.doi.org/10.1007/s00705-018-3811-0] [PMID: 29550930]
[56]
Zimmerman, T.; Ibrahim, S. Choline kinase, a novel drug target for the inhibition of Streptococcus pneumoniae. Antibiotics (Basel), 2017, 6(4), 20.
[http://dx.doi.org/10.3390/antibiotics6040020] [PMID: 28946671]
[57]
Serino, L.; Virji, M. Phosphorylcholine decoration of lipopolysaccharide differentiates commensal Neisseriae from pathogenic strains: Identification of licA-type genes in commensal Neisseriae. Mol. Microbiol., 2000, 35(6), 1550-1559.
[http://dx.doi.org/10.1046/j.1365-2958.2000.01825.x] [PMID: 10760154]
[58]
Elswaifi, S.F.; St Michael, F.; Sreenivas, A.; Cox, A.; Carman, G.M.; Inzana, T.J. Molecular characterization of phosphorylcholine expression on the lipooligosaccharide of Histophilus somni. Microb. Pathog., 2009, 47(4), 223-230.
[http://dx.doi.org/10.1016/j.micpath.2009.08.001] [PMID: 19682567]
[59]
Whiting, G.C.; Gillespie, S.H. Incorporation of choline into Streptococcus pneumoniae cell wall antigens: Evidence for choline kinase activity. FEMS Microbiol. Lett., 1996, 138(2-3), 141-145.
[http://dx.doi.org/10.1111/j.1574-6968.1996.tb08147.x] [PMID: 9026440]
[60]
Brundish, D.E.; Baddiley, J. Pneumococcal C-substance, a ribitol teichoic acid containing choline phosphate. Biochem. J., 1968, 110(3), 573-582.
[http://dx.doi.org/10.1042/bj1100573] [PMID: 4387389]
[61]
Seo, H.S.; Cartee, R.T.; Pritchard, D.G.; Nahm, M.H. A new model of pneumococcal lipoteichoic acid structure resolves biochemical, biosynthetic, and serologic inconsistencies of the current model. J. Bacteriol., 2008, 190(7), 2379-2387.
[http://dx.doi.org/10.1128/JB.01795-07] [PMID: 18245291]
[62]
Clark, S.E.; Snow, J.; Li, J.; Zola, T.A.; Weiser, J.N. Phosphorylcholine allows for evasion of bactericidal antibody by Haemophilus influenzae. PLoS Pathog., 2012, 8(3), e1002521.
[http://dx.doi.org/10.1371/journal.ppat.1002521] [PMID: 22396641]
[63]
Lysenko, E.S.; Gould, J.; Bals, R.; Wilson, J.M.; Weiser, J.N. Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/hCAP18 expressed in the upper respiratory tract. Infect. Immun., 2000, 68(3), 1664-1671.
[http://dx.doi.org/10.1128/IAI.68.3.1664-1671.2000] [PMID: 10678986]
[64]
Serrán-Aguilera, L.; Denton, H.; Rubio-Ruiz, B.; López-Gutiérrez, B.; Entrena, A.; Izquierdo, L.; Smith, T.K.; Conejo-García, A.; Hurtado-Guerrero, R. Plasmodium falciparum choline kinase inhibition leads to a major decrease in phosphatidylethanolamine causing parasite death. Sci. Rep., 2016, 6, 33189.
[http://dx.doi.org/10.1038/srep33189] [PMID: 27616047]
[65]
Zimmerman, T.; Moneriz, C.; Diez, A.; Bautista, J.M.; Gómez Del Pulgar, T.; Cebrián, A.; Lacal, J.C. Antiplasmodial activity and mechanism of action of RSM-932A, a promising synergistic inhibitor of Plasmodium falciparum choline kinase. Antimicrob. Agents Chemother., 2013, 57(12), 5878-5888.
[http://dx.doi.org/10.1128/AAC.00920-13] [PMID: 24041883]
[66]
Kall, S.L.; Delikatny, E.J.; Lavie, A. Identification of a unique inhibitor-binding site on choline kinase α. Biochemistry, 2018, 57(8), 1316-1325.
[http://dx.doi.org/10.1021/acs.biochem.7b01257] [PMID: 29389115]
[67]
Sanchez-Lopez, E.; Zimmerman, T.; Gomez del Pulgar, T.; Moyer, M.P.; Lacal Sanjuan, J.C.; Cebrian, A. Choline kinase inhibition induces exacerbated endoplasmic reticulum stress and triggers apoptosis via CHOP in cancer cells. Cell Death Dis., 2013, 4(11), e933.
[http://dx.doi.org/10.1038/cddis.2013.453] [PMID: 24287694]
[68]
Zimmerman, T.; Lacal, J.C.; Ibrahim, S.A. Choline kinase emerges as a promising drug target in gram-positive bacteria. Front. Microbiol., 2019, 6, 2146.
[http://dx.doi.org/10.3389/fmicb.2019.02146] [PMID: 31681254]
[69]
Trousil, S.; Kaliszczak, M.; Schug, Z.; Nguyen, Q.D.; Tomasi, G.; Favicchio, R.; Brickute, D.; Fortt, R.; Twyman, F.J.; Carroll, L.; Kalusa, A.; Navaratnam, N.; Adejumo, T.; Carling, D.; Gottlieb, E.; Aboagye, E.O. The novel choline kinase inhibitor ICL-CCIC-0019 reprograms cellular metabolism and inhibits cancer cell growth. Oncotarget, 2016, 7(24), 37103-37120.
[http://dx.doi.org/10.18632/oncotarget.9466] [PMID: 27206796]
[70]
Sola-Leyva, A.; López-Cara, L.C.; Ríos-Marco, P.; Ríos, A.; Marco, C.; Carrasco-Jiménez, M.P. Choline kinase inhibitors EB-3D and EB-3P interferes with lipid homeostasis in HepG2 cells. Sci. Rep., 2019, 9(1), 5109.
[http://dx.doi.org/10.1038/s41598-019-40885-z] [PMID: 30911014]
[71]
Lacal, J.C.; Campos, J.M. Preclinical characterization of RSM-932A, a novel anticancer drug targeting the human choline kinase alpha, an enzyme involved in increased lipid metabolism of cancer cells. Mol. Cancer Ther., 2015, 14(1), 31-39.
[http://dx.doi.org/10.1158/1535-7163.MCT-14-0531] [PMID: 25487918]
[72]
Zimmerman, T.; Chasten, V.; Lacal, J.C.; Ibrahim, S.A. Identification and validation of novel and more effective choline kinase inhibitors against Streptococcus pneumoniae. Sci. Rep., 2020, 10(1), 15418.
[http://dx.doi.org/10.1038/s41598-020-72165-6] [PMID: 32963303]
[73]
Dar, A.M.; Mir, S. Molecular docking: Approaches, types, applications and basic challenges. J. Anal. Bioanal. Tech., 2017, 08(02), 1-3.
[http://dx.doi.org/10.4172/2155-9872.1000356]
[74]
Kolluru, S.; Momoh, R.; Lin, L.; Mallareddy, J.R.; Krstenansky, J.L. Identification of potential binding pocket on viral oncoprotein HPV16 E6: A promising anti-cancer target for small molecule drug discovery. BMC Mol. Cell Biol., 2019, 20(1), 30.
[http://dx.doi.org/10.1186/s12860-019-0214-3] [PMID: 31387520]
[75]
Grosdidier, A.; Zoete, V.; Michielin, O. Fast docking using the CHARMM force field with EADock DSS. J. Comput. Chem., 2011, 32(10), 2149-2159.
[http://dx.doi.org/10.1002/jcc.21797] [PMID: 21541955]
[76]
Grosdidier, A.; Zoete, V.; Michielin, O. SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res., 2011, 39(Suppl. 2), W270-277.
[http://dx.doi.org/10.1093/nar/gkr366] [PMID: 21624888]
[77]
Guex, N.; Peitsch, M.C.; Schwede, T. Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective. Electrophoresis, 2009, 30(Suppl. 1), S162-S173.
[http://dx.doi.org/10.1002/elps.200900140] [PMID: 19517507]
[78]
Waterhouse, A.; Bertoni, M.; Bienert, S.; Studer, G.; Tauriello, G.; Gumienny, R.; Heer, F.T.; de Beer, T.A.P.; Rempfer, C.; Bordoli, L.; Lepore, R.; Schwede, T. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res., 2018, 46(W1), W296-W303.
[http://dx.doi.org/10.1093/nar/gky427] [PMID: 29788355]
[79]
Benkert, P.; Biasini, M.; Schwede, T. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics, 2011, 27(3), 343-350.
[http://dx.doi.org/10.1093/bioinformatics/btq662] [PMID: 21134891]
[80]
Studer, G.; Rempfer, C.; Waterhouse, A.M.; Gumienny, R.; Haas, J.; Schwede, T. QMEANDisCo-distance constraints applied on model quality estimation. Bioinformatics, 2020, 36(6), 1765-1771.
[http://dx.doi.org/10.1093/bioinformatics/btz828] [PMID: 31697312]
[81]
Irwin, J.J.; Shoichet, B.K. ZINC-a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model., 2005, 45(1), 177-182.
[http://dx.doi.org/10.1021/ci049714+] [PMID: 15667143]
[82]
Sterling, T.; Irwin, J.J. ZINC 15-Ligand discovery for everyone. J. Chem. Inf. Model., 2015, 55(11), 2324-2337.
[http://dx.doi.org/10.1021/acs.jcim.5b00559] [PMID: 26479676]
[83]
Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera--a visualization system for exploratory research and analysis. J. Comput. Chem., 2004, 25(13), 1605-1612.
[http://dx.doi.org/10.1002/jcc.20084] [PMID: 15264254]
[84]
Lacal, J.C. Choline kinase: A novel target for antitumor drugs. IDrugs, 2001, 4(4), 419-426.
[PMID: 16015482]
[85]
Zoete, V.; Daina, A.; Bovigny, C.; Michielin, O. Swiss similarity: A web tool for low to ultra high throughput ligand-based virtual screening. J. Chem. Inf. Model., 2016, 56(8), 1399-1404.
[http://dx.doi.org/10.1021/acs.jcim.6b00174] [PMID: 27391578]
[86]
Reynolds, I.J.; Miller, R.J. Ifenprodil is a novel type of N-methyl-D-aspartate receptor antagonist: Interaction with polyamines. Mol. Pharmacol., 1989, 36(5), 758-765.
[PMID: 2555674]
[87]
U.S. National Library of Medicine. Safety and Efficacy of NP-120 (Ifenprodil) for the Treatment of Hospitalized Patient With Confirmed COVID-19 Disease. Available from: https://clinicaltrials.gov/ct2/show/NCT04382924 (Accessed Apr 23, 2021).
[88]
Ojha, P.K.; Kar, S.; Krishna, J.G.; Roy, K.; Leszczynski, J. Therapeutics for COVID-19: from computation to practices-where we are, where we are heading to. Mol. Divers., 2021, 25(1), 625-659.
[http://dx.doi.org/10.1007/s11030-020-10134-x] [PMID: 32880078]
[89]
Fernandes, S.; São-José, C. Enzymes and Mechanisms Employed byTailed Bacteriophages to Breach the Bacterial Cell Barriers. Viruses, 2018, 10(8), 396.
[http://dx.doi.org/10.3390/v10080396] [PMID: 30060520]
[90]
Fokine, A.; Rossmann, M. G. Molecular Architecture of Tailed Double-Stranded DNA Phages. Bacteriophage, 2014, 4(2), e28281.
[http://dx.doi.org/10.4161/bact.28281] [PMID: 24616838]

Rights & Permissions Print Cite
Article Metrics
18
1
© 2024 Bentham Science Publishers | Privacy Policy