In vitro trypanocidal activities and structure-activity relationships of ciprofloxacin analogs.
1,2,3-Triazole
African trypanosomes
Ciprofloxacin
Trypanocidal activity
Journal
Molecular diversity
ISSN: 1573-501X
Titre abrégé: Mol Divers
Pays: Netherlands
ID NLM: 9516534
Informations de publication
Date de publication:
23 Jul 2023
23 Jul 2023
Historique:
received:
14
03
2023
accepted:
16
07
2023
medline:
23
7
2023
pubmed:
23
7
2023
entrez:
22
7
2023
Statut:
aheadofprint
Résumé
Tropical diseases, such as African trypanosomiasis, by their nature and prevalence lack the necessary urgency regarding drug development, despite the increasing need for novel, structurally diverse antitrypanosomal drugs, using different mechanisms of action that would improve drug efficacy and safety. Traditionally antibacterial agents, the fluoroquinolones, reportedly possess in vitro trypanocidal activities against Trypanosoma brucei organisms. During our research, the fluroquinolone, ciprofloxacin (1), and its analogs (2-24) were tested against bloodstream forms of T. brucei brucei, T. b. gambiense, T. b. rhodesiense, T. evansi, T. equiperdum, and T. congolense and Madin-Darby bovine kidney cells (cytotoxicity). Ciprofloxacin [CPX (1)] demonstrated selective trypanocidal activity against T. congolense (IC
Identifiants
pubmed: 37481633
doi: 10.1007/s11030-023-10704-9
pii: 10.1007/s11030-023-10704-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Japan Society for the Promotion of Science
ID : 16K18793
Organisme : Japan Society for the Promotion of Science
ID : 148781
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Switzerland AG.
Références
Altamura F, Rajesh R, Catta-Preta CM, Moretti NS, Cestari I (2022) The current drug discovery landscape for trypanosomiasis and leishmaniasis: challenges and strategies to identify drug targets. Drug Dev Res 83(2):225–252. https://doi.org/10.1002/ddr.21664
doi: 10.1002/ddr.21664
pubmed: 32249457
Brun R, Blum J, Chappuis F, Burri C (2010) Human African trypanosomiasis. Lancet 375(9709):148–159. https://doi.org/10.1016/S0140-6736(09)60829-1
doi: 10.1016/S0140-6736(09)60829-1
pubmed: 19833383
Büscher P, Cecchi G, Jamonneau V, Priotto G (2017) Human African trypanosomiasis. Lancet 390(10110):2397–2409. https://doi.org/10.1016/S0140-6736(17)31510-6
doi: 10.1016/S0140-6736(17)31510-6
pubmed: 28673422
Cayla M, Rojas F, Silvester E, Venter F, Matthews KR (2019) African trypanosomes. Parasit Vectors 12(1):1–8. https://doi.org/10.1186/s13071-019-3355-5
doi: 10.1186/s13071-019-3355-5
Desquesnes M, Gonzatti M, Sazmand A, Thévenon S, Bossard G, Boulangé A, Gimonneau G, Truc P, Herder S, Ravel S (2022) A review on the diagnosis of animal trypanosomoses. Parasit Vectors 15(1):1–24. https://doi.org/10.1186/s13071-022-05190-1
doi: 10.1186/s13071-022-05190-1
Giordani F, Morrison LJ, Rowan TG, De Koning HP, Barrett MP (2016) The animal trypanosomiases and their chemotherapy: a review. Parasitology 143(14):1862–1889. https://doi.org/10.1017/S0031182016001268
doi: 10.1017/S0031182016001268
pubmed: 27719692
Venturelli A, Tagliazucchi L, Lima C, Venuti F, Malpezzi G, Magoulas GE, Santarem N, Calogeropoulou T, Cordeiro-da-Silva A, Costi MP (2022) Current treatments to control African trypanosomiasis and one health perspective. Microorganisms 10(7):1298. https://doi.org/10.3390/microorganisms10071298
doi: 10.3390/microorganisms10071298
pubmed: 35889018
pmcid: 9321528
Simarro PP, Cecchi G, Paone M, Franco JR, Diarra A, Ruiz JA, Fèvre EM, Courtin F, Mattioli RC, Jannin JG (2010) The atlas of human African trypanosomiasis: a contribution to global mapping of neglected tropical diseases. Int J Health Geogr 9(1):1–18. https://doi.org/10.1186/1476-072X-9-57
doi: 10.1186/1476-072X-9-57
Peacock L, Cook S, Ferris V, Bailey M, Gibson W (2012) The life cycle of Trypanosoma (nannomonas) congolense in the tsetse fly. Parasit Vectors 5(1):1–13. https://doi.org/10.1186/1756-3305-5-109
doi: 10.1186/1756-3305-5-109
Desquesnes M, Holzmuller P, Lai DH, Dargantes A, Lun ZR, Jittaplapong S (2013) Trypanosoma evansi and surra: a review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects. Biomed Res Int. https://doi.org/10.1155/2013/194176
doi: 10.1155/2013/194176
pubmed: 24151595
pmcid: 3789323
WHO. Trypanosomiasis, human African (sleeping sickness). https://www.who.int/news-room/fact-sheets/detail/trypanosomiasis-human-african-(sleeping-sickness ). Accessed on 23 Nov 2022
Kasozi KI, MacLeod ET, Ntulume I, Welburn SC (2022) An update on African trypanocide pharmaceutics and resistance. Front Vet Sci. https://doi.org/10.3389/fvets.2022.828111
doi: 10.3389/fvets.2022.828111
pubmed: 36686196
pmcid: 8959112
Horn D (2014) Antigenic variation in African trypanosomes. Mol Biochem Parasitol 195(2):123–129. https://doi.org/10.1101/cshperspect.a025320
doi: 10.1101/cshperspect.a025320
pubmed: 24859277
pmcid: 4155160
Field MC, Horn D, Fairlamb AH, Ferguson MA, Gray DW, Read KD, De Rycker M, Torrie LS, Wyatt PG, Wyllie S (2017) Anti-trypanosomatid drug discovery: an ongoing challenge and a continuing need. Nat Rev Microbiol 15(4):217–231. https://doi.org/10.1038/nrmicro.2016.193
doi: 10.1038/nrmicro.2016.193
pubmed: 28239154
pmcid: 5582623
Kourbeli V, Chontzopoulou E, Moschovou K, Pavlos D, Mavromoustakos T, Papanastasiou IP (2021) An overview on target-based drug design against kinetoplastid protozoan infections: human African trypanosomiasis, chagas disease and leishmaniases. Molecules 26(15):4629. https://doi.org/10.3390/molecules26154629
doi: 10.3390/molecules26154629
pubmed: 34361781
pmcid: 8348971
Imran M, Khan SA, Alshammari MK, Alqahtani AM, Alanazi TA, Kamal M, Jawaid T, Ghoneim MM, Alshehri S, Shakeel F (2022) Discovery, development, inventions and patent review of fexinidazole: the first all-oral therapy for human African trypanosomiasis. Pharmaceuticals 15(2):128. https://doi.org/10.3390/ph15020128
doi: 10.3390/ph15020128
pubmed: 35215241
pmcid: 8878566
Sokolova AY, Wyllie S, Patterson S, Oza SL, Read KD, Fairlamb AH (2010) Cross-resistance to nitro drugs and implications for treatment of human African trypanosomiasis. Antimicrob Agents Chemother 54(7):2893–2900. https://doi.org/10.1128/AAC.00332-10
doi: 10.1128/AAC.00332-10
pubmed: 20439607
pmcid: 2897277
Trouiller P, Olliaro PL (1999) Drug development output: what proportion for tropical diseases? Lancet 354(9173):164. https://doi.org/10.1016/S0140-6736(05)75299-5
doi: 10.1016/S0140-6736(05)75299-5
pubmed: 10408518
Pink R, Hudson A, Mouriès MA, Bendig M (2005) Opportunities and challenges in antiparasitic drug discovery. Nat Rev Drug Discovery 4(9):727–740. https://doi.org/10.1038/nrd1824
doi: 10.1038/nrd1824
pubmed: 16138106
Guha R (2013) On exploring structure-activity relationships. In Silico Models Drug Discov. https://doi.org/10.1007/978-1-62703-342-8_6
doi: 10.1007/978-1-62703-342-8_6
Keiser J, Burri C (2001) Evaluation of quinolone derivatives for antitrypanosomal activity. Tropical Med Int Health 6(5):369–389. https://doi.org/10.1046/j.1365-3156.2001.00713.x
doi: 10.1046/j.1365-3156.2001.00713.x
King DE, Malone R, Lilley SH (2000) New classification and update on the quinolone antibiotics. Am Fam Physician 61(9):2741–2748
pubmed: 10821154
Sharma PC, Jain A, Jain S, Pahwa R, Yar MS (2010) Ciprofloxacin: review on developments in synthetic, analytical, and medicinal aspects. J Enzyme Inhib Med Chem 25(4):577–589. https://doi.org/10.3109/14756360903373350
doi: 10.3109/14756360903373350
pubmed: 20235755
Dalhoff A (2015) Antiviral, antifungal, and antiparasitic activities of fluoroquinolones optimized for treatment of bacterial infections: a puzzling paradox or a logical consequence of their mode of action? Eur J Clin Microbiol Infect Dis 34(4):661–668. https://doi.org/10.1007/s10096-014-2296-3
doi: 10.1007/s10096-014-2296-3
pubmed: 25515946
Betbeder D, Hutchison D, Baltz T, Cros S (1988) Trypanocidal and antitumor activities of nalidixic and oxolinic acid derivatives. Med Sci Res 16:141–142
Hiltensperger G, Hecht N, Kaiser M, Rybak JC, Hoerst A, Dannenbauer N, Müller-Buschbaum K, Bruhn H, Esch H, Lehmann L (2016) Quinolone amides as antitrypanosomal lead compounds with in vivo activity. Antimicrob Agents Chemother 60(8):4442–4452. https://doi.org/10.1128/AAC.01757-15
doi: 10.1128/AAC.01757-15
pubmed: 27139467
pmcid: 4958235
Nenortas E, Kulikowicz T, Burri C, Shapiro TA (2003) Antitrypanosomal activities of fluoroquinolones with pyrrolidinyl substitutions. Antimicrob Agents Chemother 47(9):3015–3017. https://doi.org/10.1128/AAC.47.9.3015-3017.2003
doi: 10.1128/AAC.47.9.3015-3017.2003
pubmed: 12937017
pmcid: 182618
Tang SC, Shapiro TA (2010) Newly identified antibacterial compounds are topoisomerase poisons in African trypanosomes. Antimicrob Agents Chemother 54(2):620–626. https://doi.org/10.1128/AAC.01025-09
doi: 10.1128/AAC.01025-09
pubmed: 20008775
Nenortas E, Burri C, Shapiro TA (1999) Antitrypanosomal activity of fluoroquinolones. Antimicrob Agents Chemother 43(8):2066–2068. https://doi.org/10.1128/AAC.43.8.2066
doi: 10.1128/AAC.43.8.2066
pubmed: 10428939
pmcid: 89417
Hooper DC, Jacoby GA (2016) Topoisomerase inhibitors: fluoroquinolone mechanisms of action and resistance. Cold Spring Harb Perspect Med 6(9):a025320
doi: 10.1101/cshperspect.a025320
pubmed: 27449972
pmcid: 5008060
Balaña-Fouce R, Álvarez-Velilla R, Fernández-Prada C, García-Estrada C, Reguera RM (2014) Trypanosomatids topoisomerase re-visited: new structural findings and role in drug discovery. Int J Parasitol Drugs Drug Resist 4(3):326–337. https://doi.org/10.1016/j.ijpddr.2014.07.006
doi: 10.1016/j.ijpddr.2014.07.006
pubmed: 25516844
pmcid: 4266802
Andersson MI, MacGowan AP (2003) Development of the quinolones. J Antimicrob Chemother 51(suppl_1):1–11. https://doi.org/10.1093/jac/dkg212
doi: 10.1093/jac/dkg212
pubmed: 12702698
Ma X, Zhou W, Brun R (2009) Synthesis, in vitro antitrypanosomal and antibacterial activity of phenoxy, phenylthio or benzyloxy substituted quinolones. Bioorg Med Chem Lett 19(3):986–989. https://doi.org/10.1016/j.bmcl.2008.11.078
doi: 10.1016/j.bmcl.2008.11.078
pubmed: 19095449
Martinez M, McDermott P, Walker R (2006) Pharmacology of the fluoroquinolones: a perspective for the use in domestic animals. Vet J 172(1):10–28
doi: 10.1016/j.tvjl.2005.07.010
pubmed: 16154368
Chu DT, Fernandes PB (1991) Recent developments in the field of quinolone antibacterial agents. Adv Drug Res 21:39–144. https://doi.org/10.1016/B978-0-12-013321-5.50007-2
doi: 10.1016/B978-0-12-013321-5.50007-2
Sharma PC, Jain A, Jain S (2009) Fluoroquinolone antibacterials: a review on chemistry, microbiology and therapeutic prospects. Acta Pol Pharm 66(6):587–604
pubmed: 20050522
Cilliers P, Seldon R, Smit FJ, Aucamp J, Jordaan A, Warner DF, N’Da DD (2019) Design, synthesis, and antimycobacterial activity of novel ciprofloxacin derivatives. Chem Biol Drug Des 94(2):1518–1536. https://doi.org/10.1111/cbdd.13534
doi: 10.1111/cbdd.13534
pubmed: 31033220
Meunier B (2008) Hybrid molecules with a dual mode of action: dream or reality? Acc Chem Res 41(1):69–77. https://doi.org/10.1016/j.tvjl.2005.07.010
doi: 10.1016/j.tvjl.2005.07.010
pubmed: 17665872
Ali AA (2020) 1, 2, 3-triazoles: synthesis and biological application. IntechOpen. https://doi.org/10.5772/intechopen.92692
doi: 10.5772/intechopen.92692
Kharb R, Sharma PC, Yar MS (2011) Pharmacological significance of triazole scaffold. J Enzyme Inhib Med Chem 26(1):1–21. https://doi.org/10.3109/14756360903524304
doi: 10.3109/14756360903524304
pubmed: 20583859
Tarawneh AH, Al-Momani L, León F, Jain SK, Gadetskaya AV, Abu-Orabi ST, Tekwani BL, Cutler SJ (2018) Evaluation of triazole and isoxazole derivatives as potential anti-infective agents. Med Chem Res 27(4):1269–1275. https://doi.org/10.1007/s00044-018-2146-4
doi: 10.1007/s00044-018-2146-4
pubmed: 30374214
pmcid: 6203334
Lepesheva GI, Waterman MR (2011) Sterol 14alpha-demethylase (CYP51) as a therapeutic target for human trypanosomiasis and leishmaniasis. Curr Top Med Chem 11(16):2060–2071. https://doi.org/10.2174/156802611796575902
doi: 10.2174/156802611796575902
pubmed: 21619513
pmcid: 3391166
Batiha GES, Tayebwa DS, Beshbishy AM, N’Da DD, Yokoyama N, Igarashi I (2020) Inhibitory effects of novel ciprofloxacin derivatives on the growth of four Babesia species and Theileria equi. Parasitol Res 119(9):3061–3073. https://doi.org/10.1007/s00436-020-06796-z
doi: 10.1007/s00436-020-06796-z
pubmed: 32677000
Suganuma K, Allamanda P, Hakimi H, Zhou M, Angeles JM, Kawazu SI, Inoue N (2014) Establishment of ATP-based luciferase viability assay in 96-well plate for Trypanosoma congolense. J Vet Med Sci. https://doi.org/10.1292/jvms.14-0273
doi: 10.1292/jvms.14-0273
pubmed: 25056575
pmcid: 4272975
Suganuma K, Yamasaki S, Molefe NI, Musinguzi PS, Davaasuren B, Mossaad E, Narantsatsral S, Battur B, Battsetseg B, Inoue N (2017) The establishment of in vitro culture and drug screening systems for a newly isolated strain of Trypanosoma equiperdum. Int J Parasitol Drugs Drug Resist 7(2):200–205. https://doi.org/10.1016/j.ijpddr.2017.04.002
doi: 10.1016/j.ijpddr.2017.04.002
pubmed: 28437733
pmcid: 5403793
Munsimbwe L, Seetsi A, Namangala B, N’Da DD, Inoue N, Suganuma K (2021) In vitro and in vivo trypanocidal efficacy of synthesized nitrofurantoin analogs. Molecules 26(11):3372. https://doi.org/10.3390/molecules26113372
doi: 10.3390/molecules26113372
pubmed: 34199682
pmcid: 8199755
Katsuno K, Burrows JN, Duncan K, Van Huijsduijnen RH, Kaneko T, Kita K, Mowbray CE, Schmatz D, Warner P, Slingsby B (2015) Hit and lead criteria in drug discovery for infectious diseases of the developing world. Nat Rev Drug Discov 14(11):751–758. https://doi.org/10.1038/nrd4683
doi: 10.1038/nrd4683
pubmed: 26435527
Nwaka S, Hudson A (2006) Innovative lead discovery strategies for tropical diseases. Nat Rev Drug Discov 5(11):941–955. https://doi.org/10.1038/nrd2144
doi: 10.1038/nrd2144
pubmed: 17080030
Adewusi EA, Steenkamp P, Fouche G, Steenkamp V (2013) Isolation of cycloeucalenol from Boophone disticha and evaluation of its cytotoxicity. Nat Prod Commun 8(9):906. https://doi.org/10.1177/1934578X13008009
doi: 10.1177/1934578X13008009
Fu J, Chen H, Soroka DN, Warin RF, Sang S (2014) Cysteine-conjugated metabolites of ginger components, shogaols, induce apoptosis through oxidative stress-mediated p53 pathway in human colon cancer cells. J Agric Food Chem 62(20):4632–4642. https://doi.org/10.1021/jf501351r
doi: 10.1021/jf501351r
pubmed: 24786146
pmcid: 4033655
Liu S, Su M, Song SJ, Jung JH (2017) Marine-derived Penicillium species as producers of cytotoxic metabolites. Mar Drugs 15(10):329. https://doi.org/10.3390/md15100329
doi: 10.3390/md15100329
pubmed: 29064452
pmcid: 5666435
Finiuk N, Hreniuh V, Ostapiuk YV, Matiychuk V, Frolov D, Obushak M, Stoika R, Babsky A (2017) Antineoplastic activity of novel thiazole derivatives. Biopolym Cell 33(2):135–146. https://doi.org/10.7124/bc.00094B
doi: 10.7124/bc.00094B
Hay M, Thomas DW, Craighead JL, Economides C, Rosenthal J (2014) Clinical development success rates for investigational drugs. Nat Biotechnol 32(1):40–51. https://doi.org/10.1038/nbt.2786
doi: 10.1038/nbt.2786
pubmed: 24406927
Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (1997) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 23(1–3):3–25. https://doi.org/10.1016/S0169-409X(96)00423-1
doi: 10.1016/S0169-409X(96)00423-1
Talevi A (2022) The ADME Encyclopedia: A Comprehensive Guide on Biopharmacy and Pharmacokinetics. Springer, Cham, pp 725–732. https://doi.org/10.1007/978-3-030-84860-6_11
doi: 10.1007/978-3-030-84860-6_11
MSD Veterinary Manual. Quinolones, Including Fluoroquinolones, Use in Animals. https://www.msdvetmanual.com/pharmacology/antibacterial-agents/quinolones,-including-fluoroquinolones,-use-in-animals . Accessed 20 Jun 2023
Pacheco MC, Purser S, Gouverneur V (2008) The chemistry of propargylic and allylic fluorides. Chem Rev 108(6):1943–1981. https://doi.org/10.1021/cr068410e
doi: 10.1021/cr068410e
pubmed: 18543877
Purser S, Moore PR, Swallow S, Gouverneur V (2008) Fluorine in medicinal chemistry. Chem Soc Rev 37(2):320–330. https://doi.org/10.1039/B610213C
doi: 10.1039/B610213C
pubmed: 18197348
Testa B, Krämer SD (2007) The biochemistry of drug metabolism: an introduction: part 2: redox reactions and their enzymes. Chem Biodivers 4(3):257–405. https://doi.org/10.1002/cbdv.200790032
doi: 10.1002/cbdv.200790032
pubmed: 17372942
Hollenberg PF (2002) Characteristics and common properties of inhibitors, inducers, and activators of CYP enzymes. Drug Metab Rev 34(1–2):17–35. https://doi.org/10.1081/DMR-120001387
doi: 10.1081/DMR-120001387
pubmed: 11996009
Huang SM, Strong JM, Zhang L, Reynolds KS, Nallani S, Temple R, Abraham S, Habet SA, Baweja RK, Burckart GJ (2008) New era in drug interaction evaluation: US Food and Drug Administration update on CYP enzymes, transporters, and the guidance process. J Clin Pharmacol 48(6):662–670. https://doi.org/10.1177/0091270007312153
doi: 10.1177/0091270007312153
pubmed: 18378963
Lejon V, Bentivoglio M, Franco JR (2013) Human African trypanosomiasis. Handb Clin Neurol 114:169–181. https://doi.org/10.1016/B978-0-444-53490-3.00011-X
doi: 10.1016/B978-0-444-53490-3.00011-X
pubmed: 23829907
Green HP, Portela MD, Jean EN, Lugli EB, Raper J (2003) Evidence for a Trypanosoma brucei lipoprotein scavenger receptor. J Biol Chem 278(1):422–427. https://doi.org/10.1074/jbc.M207215200
doi: 10.1074/jbc.M207215200
pubmed: 12401813
Nok AJ, Nock IH, Bonire JJ (2003) The cholesterol pathway of Trypanosoma congolense could be a target for triphenyltinsalicylate and triphenylsiliconsalicylate inhibition. Appl Organomet Chem 17(1):17–22. https://doi.org/10.1002/aoc.368
doi: 10.1002/aoc.368
Rahman A, O’Sullivan P, Rozas I (2019) Recent developments in compounds acting in the DNA minor groove. Medchemcomm 10(1):26–40. https://doi.org/10.1039/C8MD00425K
doi: 10.1039/C8MD00425K
pubmed: 30774852
Fersing C, Boudot C, Castera-Ducros C, Pinault É, Hutter S, Paoli-Lombardo R, Primas N, Pedron J, Séguy L, Bourgeade-Delmas S, Sournia-Saquet A, Stigliani J, Brossas J, Paris L, Valentin A, Wyllie S, Fairlamb AH, Boutet-Robinet E, Corvaisier S, Since M, Malzert-Fréon A, Destere A, Mazier D, Rathelot P, Courtioux B, Azas N, Verhaeghe P, Vanelle P (2020) 8-Alkynyl-3-nitroimidazopyridines display potent antitrypanosomal activity against both T. b. brucei and cruzi. Eur J Med Chem. https://doi.org/10.1016/j.ejmech.2020.112558
doi: 10.1016/j.ejmech.2020.112558
pubmed: 32795774
Daina A, Michielin O, Zoete V (2017) SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep 7(1):1–13. https://doi.org/10.1038/srep42717
doi: 10.1038/srep42717
Hirumi H, Hirumi K (1991) In vitro cultivation of Trypanosoma congolense bloodstream forms in the absence of feeder cell layers. Parasitology 102(2):225–236. https://doi.org/10.1017/S0031182000062533
doi: 10.1017/S0031182000062533
pubmed: 1852490