Thiazolides inhibit growth and induce glutathione-S-transferase Pi (GSTP1)-dependent cell death in human colon cancer cells

International Journal of Cancer

Volumn 123, Issue 8, 2008, Pages 1797-1806

  Müller, Joachim ^a   Sidler, Daniel ^a   Nachbur, Ueli ^a   Wastling, Jonathan ^b   Brunner, Thomas ^a   Hemphill, Andrew ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Apoptosis; Cell cycle; Colon cancer; Oncogene

Indexed keywords

ANTIINFECTIVE AGENT; ANTINEOPLASTIC AGENT; DNA; GLUTATHIONE TRANSFERASE P1; NITAZOXANIDE; PHOSPHATIDYLSERINE; RM 4819; RM 4825; SMALL INTERFERING RNA; THIAZOLIDE; TIZOXANIDE; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER THERAPY; CELL CYCLE; CELL CYCLE ARREST; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; COLON CANCER; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA FRAGMENTATION; DRUG ACTIVITY; DRUG EFFECT; DRUG INHIBITION; EMBRYO; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; POLYMERIZATION; PREPUCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN FIBROBLAST;

APOPTOSIS; BENZAMIDES; CACO-2 CELLS; CELL GROWTH PROCESSES; COLONIC NEOPLASMS; DOXORUBICIN; FLOW CYTOMETRY; GLUTATHIONE S-TRANSFERASE PI; HUMANS; PHOSPHATIDYLSERINES; RNA, SMALL INTERFERING; THIAZOLES;

EID: 51949104566     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23755     Document Type: Article

References (44)

1. Hemphill A, Müller J, Esposito M. Nitazoxanide, a broad-spectrum thiazolide anti-infective agent for the treatment of gastrointestinal infections. Expert Opin Pharmacother 2006;7:953-64.
2. Hemphill A, Müller N, Müller J. Structure-function relationship of thiazolides, a novel class of anti-parasitic drugs, investigated in intracellular and extracellular protozoan parasites and larval-stage cestodes. Antiinf Agents Med Chem 2007;6:273-82.
3. Rossignol JF, Maisonneuve H. Nitazoxanide in the treatment of Taenia saginata and Hymenolepis nana. Am J Trop Med Hyg 1984;33:511-12.
4. Adagu IS, Nolder D, Warhurst D, Rossignol JF. In vitro activity of nitazoxanide and related compounds against isolates of Giardia intestinalis. Entamoeba histolytica and Trichomonas vaginalis. J Antimicrob Chemother 2002;49:103-111.
5. Gardner TB, Hill DR. Treatment of Giardiasis. Clin Microbiol Rev 2001;14:114-28.
6. Müller J, Rüttle G, Müller N, Rossignol JF, Hemphill A. In vitro effects of thiazolides on Giardia lamblia WB C6 cultured axenically and in co-culture with Caco2 cells. Antimicrob Agents Chemother 2006;50:162-70.
7. Fox LM, Saravolatz LD. Nitazoxanide: a new thiazolide antiparasitic agent. Clin Inf Dis 2005;40:1173-80.
8. Gilles HM, Hoffman PS. Treatment of intestinal parasitic infections: a review of nitazoxanide. Trends Parasitol 2002;18:95-7.
9. McClure S, Palma K. Treatment of equine protozoal myeloencephalitis with Nitazoxanide. J Eq Vet Sci 1999;19:639-41.
10. White CA, Jr. Nitazoxanide: a new broad spectrum antiparasitic agent. Expert Rev Anti Infect Ther 2004;2:43-9.
11. Rossignol JF, Abu-Zekry M, Hussein A, Santoro MG. Effect of nitazoxanide for treatment of severe rotavirus diarrhoea: randomized double-blind placebo-controlled trial. Lancet 2006;368:124-9.
12. Esposito M, Moores S, Naguleswaran A, Müller J, Hemphill A. Induction of tachyzoite egress from cells infected with the protozoan Neospora caninum by nitro- and bromo-thiazolides, a class of broad-spectrum anti-parasitic drugs. Int J Parasitol 2007;37:1143-52.
13. Esposito M, Müller N, Hemphill A. Structure-activity relationships from in vitro efficacies of the thiazolide series against the intracellular apicomplexan protozoan Neospora caninum. Int J Parasitol 2007;37:183-90.
14. Esposito M, Stettier R, Moores SL, Pidathala C, Müller N, Stachulski A, Berry NG, Rossignol JF, Hemphill A. In vitro efficacies of nitazoxanide and other thiazolides against Neospora caninum tachyzoites reveal antiparasitic activity independent of the nitro group. Antimicrob Agents Chemother 2005;49:3715-23.
15. Cortes HCE, Müller N, Esposito M, Leitào A, Naguleswaran A, Hemphill A. In vitro efficacy of nitro- and bromo-thiazolyl-salicylamide compounds (thiazolides) against Besnoitia besnoiti infection in Vero cells. Parasitology 2007;134:975-85.
16. Broekhuysen J, Stockts A, Lins R, De Graeve J, Rossignol JF. Nitazoxanide: pharmacokinetics and metabolism in man. Int J Clin Pharmacol Ther 2000;38:387-94.
17. Hoffman PS, Sisson G, Croxen MA, Welch K, Dean Harman W, Cremades N, Morash M. Antiparasitic drug nitazoxanide inhibits the pyruvate oxidoreductases of Helicobacter pylori and selected anaerobic bacteria and parasites, and Campylobacter jejuni. Antimicrob Agents Chemother 2007;51:868-76.
18. Sisson G, Goodwin A, Raudonikiene A, Hughes NJ, Mukhopadhyay AK, Berg DA, Hoffman PS. Enzymes associated with reductive activation and action of nitazoxanide, nitrofurans, and metronidazole in Helicobacter pylori. Antimicrob Agents Chemother 2002;46:2116-23.
19. Müller J, Wastling J, Sanderson S, Müller N, Hemphill A. A novel Giardia lamblia nitroreductase. GlNR1, interacts with nitazoxanide and other thiazolides. Antimicrob Agents Chemother 2007;51:1979-86.
20. Müller J, Naguleswaran A, Müller N, Hemphill A. Neospora caninum: functional inhibition of protein disulfide isomerase by the broad-spectrum anti-parasitic drug nitazoxanide and other thiazolides. Exp Parasitol 2008;118:80-8.
21. Müller J, Sterck M, Hemphill A, Müller N. Characterization of Giardia lamblia WB C6 clones resistant to nitazoxanide and to metronidazole. J Antimicrob Chemother 2007;60:280-7.
22. Guthenberg C, Jensson H, Nystrom L, Osterlund E, Tahir MK, Mannervik B. Isoenzymes of glutathione transferase in rat kidney cytosol. Biochem J 1985;230:609-15.
23. Mannervik B, Alin P, Guthenberg C, Jensson H, Tahir MK, Warholm M, Jörnvall H. Identification of three classes of cytosolic glutathione transferase common to several mammalian species: correlation between structural data and enzymatic properties. Proc Natl Acad Sci USA 1985;82:7202-6.
24. Tew KD. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res 1994;54:4313-4320.
25. Hemphill A, Croft SL. Electron microscopy in parasitology. In: Rogan PM, ed. Analytical parasitology. Heidelberg: Springer Verlag, 1997:227-68.
26. Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995;182:1545-56.
27. Corazza N, Jakob S, Schaer C, Frese S, Keogh A, Stroka D, Kassahn D, Torgler R, Mueller C, Schneider P, Brunner T. TRAIL receptor-mediated JNK activation and Bim phosphorylation critically regulate Fas-mediated liver damage and lethality. J Clin Invest 2006;116:2493-9.
28. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680-5.
29. Blum H, Beier H, Gross HJ. Improved silver staining of plant proteins. RNA and DNA in polyacrylamide gels. Electrophoresis 1987;8:93-9.
30. Ali-Osman F, Akande O, Antoun G, Mao JX, Buolamwini J. Molecular cloning, characterization, and expression in Escherichia coli of full-length cDNAs of three human glutathione S-transferase Pi gene variants. J Biol Chem 1997;272:10004-12.
31. Habig WH, Pabst MJ, Jakoby WB. Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974;249:7130-9.
32. Parkin DP. Purine-specific nucleoside N-ribohydrolase from Trypanosoma brucei brucei. J Biol Chem 1996;271:21713-19.
33. Lo Bello M, Oakley AJ, Battistoni A, Mazzetti AP, Nuccetelli M, Mazzarese G, Rossjohn J, Parker MW, Ricci G. Multifunctional role of Tyr 108 in the catalytic mechanism of human glutathione transferase P1-1. Crystallographic and kinetic studies on the Y108F mutant enzyme. Biochemistry 1997;36:6207-17.
34. Jiao L, Bondy ML, Hassan MM, Chang DZ, Abbruzzese JL, Evans DB, Smolensky MH, Li D. Glutathione S-transferase gene polymorphisms and risk and survival of pancreatic cancer. Cancer 2007;109:840-8.
35. Lu C, Spitz MR, Zhao H, Dong Q, Truong M, Chang JY, Blumenschein GR, Hong WK, Wu X. Association between glutathione S- transferase pi polymorphisms and survival in patients with advanced nonsmall cell lung carcinoma. Cancer 2006;106:441-7.
36. Schneider J, Bernges U, Philipp M, Woitowitz HJ. GSTM1, GSTT1, and GSTP1 polymorphism and lung cancer risk in relation to tobacco smoking. Cancer Lett 2004;208:65-74.
37. Wrensch M, Kelsey KT, Liu M, Miike R, Moghadassi M, Aldape K, McMillan A, Wiencke JK. Glutathione-S-transferase variants and adult glioma. Cancer Epidemiol Biomarkers Prev 2004;13:461-7.
38. Ritchie KJ, Henderson CJ, Wang XJ, Vassieva O, Carrie D, Farmer PB, Gaskell M, Park K, Wolf CR. Glutathione transferase π plays a critical role in the development of lung carcinogenesis following exposure to tobacco-related carcinogens and urethane. Cancer Res 2007;67:9248-57.
39. Kruh GD. Introduction to resistance to anticancer agents. Oncogene 2003;22:7262-4.
40. Rooseboom M, Commandeur JNM, Vermeulen NPE. Enzyme-catalyzed activation of anticancer prodrugs. Pharmacol Rev 2004;56:53-102.
41. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CL, Wolf CR, Davis RJ, Ronai Z. Regulation of JNK sienaling by GSTp. EMBO J 1999;18:1321-34.
42. Turella P, Cerella C, Filomeni G, Bullo A, De Maria F, Ghibelli L, Ciriolo MR, Cianfriglia M, Mattei M, Federici G, Ricci G, Caccuri AM. Proapoptotic activity of new glutathione S-transferase inhibitors. Cancer Res 2005;65:3751-61.
43. Klinkert MQ, Heussler V. The use of anticancer drugs in antiparasitic chemotherapy. Mini Rev Med Chem 2006;6:131-43.
44. Mukanganyama S, Widersten M, Naik YS, Mannervik B, Hasler JA. Inhibition of glutathione-S-transferases by antimalarial drugs possible implications for circumventing anticancer drug resistance. Int J Cancer 2002;97:700-5.