Nitazoxanide: Nematicidal mode of action and drug combination studies

Molecular and Biochemical Parasitology

Volumn 193, Issue 1, 2014, Pages 1-8

  Somvanshi, Vishal S ^a,b   Ellis, Brian L ^a,c   Hu, Yan ^a   Aroian, Raffi V ^a  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b INDIAN AGRICULTURAL RESEARCH INSTITUTE   (India)

^c Tarrant County College NW ^*  (United States)

Author keywords

Anthelmintic; avr 14; Caenorhabditis elegans; Glutamate gated chloride channels; Nitazoxanide; Soil transmitted helminths

Indexed keywords

ALBENDAZOLE; CHLORIDE CHANNEL; IVERMECTIN; NITAZOXANIDE; PYRANTEL; ANTHELMINTIC AGENT; GLUTAMATE-GATED CHLORIDE CHANNELS; THIAZOLE DERIVATIVE;

ANTIBIOTIC SENSITIVITY; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DRUG EFFICACY; DRUG RESISTANCE; GENETIC SCREENING; MUTANT; NONHUMAN; PARASITE ISOLATION; PRIORITY JOURNAL; PROTOZOAL INFECTION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG POTENTIATION; ENZYMOLOGY;

CAENORHABDITIS ELEGANS; NEMATODA; PROTOZOA; VERMES;

ALBENDAZOLE; ANIMALS; ANTHELMINTICS; CAENORHABDITIS ELEGANS; CHLORIDE CHANNELS; DRUG SYNERGISM; PYRANTEL; THIAZOLES;

EID: 84893178251     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2013.12.002     Document Type: Article

References (64)

1. M. Cappello Global health impact of soil-transmitted nematodes Pediatr Infect Dis J 23 2004 663 664 (Pubitemid 38924892)
2. N.R. de Silva, S. Brooker, P.J. Hotez, A. Montresor, D. Engels, and L. Savioli Soil-transmitted helminth infections: updating the global picture Trends Parasitol 19 2003 547 551 (Pubitemid 37464800)
3. J. Bethony, S. Brooker, M. Albonico, S.M. Geiger, A. Loukas, and D. Diemert et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm Lancet 367 2006 1521 1532
4. P.J. Hotez, D.A.P. Bundy, K. Beegle, S. Brooker, L. Drake, and N. de Silva et al. Helminth infections: Soil-transmitted helminth infections and schistosomiasis D.T. Jamison, J.G. Breman, A.R. Measham, Disease Control Priorities in Developing Countries 2nd edition 2006 World Bank Washington (DC) 467 482
5. P.J. Hotez Hookworm disease in children Pediatr Infect Dis J 8 1989 516 520 (Pubitemid 19213086)
6. J. Keiser, and J. Utzinger Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis J Am Med Assoc 299 2008 1937 1948 (Pubitemid 351574924)
7. T.G. Geary, K. Woo, J.S. McCarthy, C.D. Mackenzie, J. Horton, and R.K. Prichard et al. Unresolved issues in anthelmintic pharmacology for helminthiases of humans Int J Parasitol 40 2010 1 13
8. L. Holden-Dye, and R.J. Walker Anthelmintic drugs WormBook 2007 1 13
9. D. Humphries, E. Mosites, J. Otchere, W.A. Twum, L. Woo, and H. Jones-Sanpei et al. Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure Am J Trop Med Hyg 84 2011 792 800
10. P.A. Soukhathammavong, S. Sayasone, K. Phongluxa, V. Xayaseng, J. Utzinger, and P. Vounatsou et al. Low efficacy of single-dose albendazole and mebendazole against hookworm and effect on concomitant helminth infection in Lao PDR PLoS Negl Trop Dis 6 2012 e1417
11. J.R. Stothard, D. Rollinson, E. Imison, and I.S. Khamis A spot-check of the efficacies of albendazole or levamisole, against soil-transmitted helminthiases in young Ungujan children, reveals low frequencies of cure Ann Trop Med Parasitol 103 2009 357 360
12. P. Steinmann, X.N. Zhou, Z.W. Du, J.Y. Jiang, S.H. Xiao, and Z.X. Wu et al. Tribendimidine and albendazole for treating soil-transmitted helminths Strongyloides stercoralis and Taenia spp.: open-label randomized trial PLoS Negl Trop Dis 2 2008 e322
13. J.F. Rossignol, and H. Maisonneuve Nitazoxanide in the treatment of Taenia saginata and Hymenolepis nana infections Am J Trop Med Hyg 33 1984 511 512 (Pubitemid 14075656)
14. J.F. Rossignol, H. Hidalgo, M. Feregrino, F. Higuera, W.H. Gomez, and J.L. Romero et al. A double-'blind' placebo-controlled study of nitazoxanide in the treatment of cryptosporidial diarrhoea in AIDS patients in Mexico Trans R Soc Trop Med Hyg 92 1998 663 666 (Pubitemid 29015224)
15. J.F. Rossignol, A. Ayoub, and M.S. Ayers Treatment of diarrhea caused by Giardia intestinalis and Entamoeba histolytica or E. dispar: a randomized, double-blind, placebo-controlled study of nitazoxanide J Infect Dis 184 2001 381 384 (Pubitemid 32662190)
16. I.S. Adagu, D. Nolder, D.C. Warhurst, and J.F. Rossignol In vitro activity of nitazoxanide and related compounds against isolates of Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis J Antimicrob Chemother 49 2002 103 111 (Pubitemid 34100652)
17. T.Z. Jodlowski, R. Oehler, L.W. Kam, and I. Melnychuk Emerging therapies in the treatment of Clostridium difficile-associated disease Ann Pharmacother 40 2006 2164 2169 (Pubitemid 44954435)
18. D.M. Musher, N. Logan, R.J. Hamill, H.L. Dupont, A. Lentnek, and A. Gupta et al. Nitazoxanide for the treatment of Clostridium difficile colitis Clin Infect Dis 43 2006 421 427 (Pubitemid 44157148)
19. D.A. Bobak Nitazoxanide to treat persistent Clostridium difficile colitis Curr Infect Dis Rep 10 2008 89 91
20. F. Megraud, A. Occhialini, and J.F. Rossignol Nitazoxanide, a potential drug for eradication of Helicobacter pylori with no cross-resistance to metronidazole Antimicrob Agents Chemother 42 1998 2836 2840 (Pubitemid 28501212)
21. J.F. Rossignol, M. Abu-Zekry, A. Hussein, and M.G. Santoro Effect of nitazoxanide for treatment of severe rotavirus diarrhoea: randomised double-blind placebo-controlled trial Lancet 368 2006 124 129 (Pubitemid 43994153)
22. J.F. Rossignol, S.M. Kabil, Y. El-Gohary, A. Elfert, and E.B. Keeffe Clinical trial: randomized, double-blind, placebo-controlled study of nitazoxanide monotherapy for the treatment of patients with chronic hepatitis C genotype 4 Aliment Pharmacol Ther 28 2008 574 580
23. F. Bihl, and F. Negro Treatment of chronic hepatitis C Minerva Med 100 2009 459 465
24. B.E. Korba, A.B. Montero, K. Farrar, K. Gaye, S. Mukerjee, and M.S. Ayers et al. Nitazoxanide, tizoxanide and other thiazolides are potent inhibitors of hepatitis B virus and hepatitis C virus replication Antiviral Res 77 2008 56 63
25. A. Hemphill, J. Mueller, and M. Esposito Nitazoxanide, a broad-spectrum thiazolide anti-infective agent for the treatment of gastrointestinal infections Expert Opin Pharmacother 7 2006 953 964
26. J.F. Rossignol Nitazoxanide in the treatment of acquired immune deficiency syndrome-related cryptosporidiosis: results of the United States compassionate use program in 365 patients Aliment Pharmacol Ther 24 2006 887 894
27. I. Abubakar, S.H. Aliyu, C. Arumugam, P.R. Hunter, and N.K. Usman Prevention and treatment of cryptosporidiosis in immunocompromised patients Cochrane Database Syst Rev 1 2007 CD004932
28. D.R. Abraham, H. Rabie, and M.F. Cotton Nitazoxanide for severe cryptosporidial diarrhea in human immunodeficiency virus infected children Pediatr Infect Dis J 27 2008 1040 1041
29. H. Abaza, A.R. El-Zayadi, S.M. Kabil, and H. Rizk Nitazoxanide in the treatment of patients with intestinal protozoan and helminthic infections: a report on 546 patients in Egypt Curr Ther Res 59 1998 116 121 (Pubitemid 28126264)
30. T.G. Geary, N.C. Sangster, and D.P. Thompson Frontiers in anthelmintic pharmacology Vet Parasitol 84 1999 275 295 (Pubitemid 29320035)
31. C.E. Davila-Gutierrez, C. Vasquez, B. Trujillo-Hernandez, and M. Huerta Nitazoxanide compared with quinfamide and mebendazole in the treatment of helminthic infections and intestinal protozoa in children Am J Trop Med Hyg 66 2002 251 254 (Pubitemid 34756092)
32. J.O. Juan, N. Lopez Chegne, G. Gargala, and L. Favennec Comparative clinical studies of nitazoxanide, albendazole and praziquantel in the treatment of ascariasis, trichuriasis and hymenolepiasis in children from Peru Trans R Soc Trop Med Hyg 96 2002 193 196 (Pubitemid 34846567)
33. L.M. Fox, and L.D. Saravolatz Nitazoxanide: a new thiazolide antiparasitic agent Clin Infect Dis 40 2005 1173 1180 (Pubitemid 40490245)
34. E. Diaz, J. Mondragon, E. Ramirez, and R. Bernal Epidemiology and control of intestinal parasites with nitazoxanide in children in Mexico Am J Trop Med Hyg 68 2003 384 385 (Pubitemid 38230634)
35. R. Romero Cabello, L.R. Guerrero, M.R. Munoz Garcia, and A. Geyne Cruz Nitazoxanide for the treatment of intestinal protozoan and helminthic infections in Mexico Trans R Soc Trop Med Hyg 91 1997 701 703 (Pubitemid 28019920)
36. B. Speich, S.M. Ame, S.M. Ali, R. Alles, J. Hattendorf, and J. Utzinger et al. Efficacy and safety of nitazoxanide, albendazole, and nitazoxanide-albendazole against Trichuris trichiura infection: a randomized controlled trial PLoS Negl Trop Dis 6 2012 e1685
37. Y. Hu, B.L. Ellis, Y.Y. Yiu, M.M. Miller, J.F. Urban, and L.Z. Shi et al. An extensive comparison of the effect of anthelmintic classes on diverse nematodes PLoS ONE 8 2013 e70702
38. P.S. Hoffman, G. Sisson, M.A. Croxen, K. Welch, W.D. Harman, and N. Cremades et al. Antiparasitic drug nitazoxanide inhibits the pyruvate oxidoreductases of Helicobacter pylori, selected anaerobic bacteria and parasites, and Campylobacter jejuni Antimicrob Agents Chemother 51 2007 868 876 (Pubitemid 46355269)
39. J. Muller, M. Sterk, A. Hemphill, and N. Muller Characterization of Giardia lamblia WB C6 clones resistant to nitazoxanide and to metronidazole J Antimicrob Chemother 60 2007 280 287 (Pubitemid 47243875)
40. J. Muller, S. Ley, I. Felger, A. Hemphill, and N. Muller Identification of differentially expressed genes in a Giardia lamblia WB C6 clone resistant to nitazoxanide and metronidazole J Antimicrob Chemother 62 2008 72 82 (Pubitemid 351865876)
41. J. Muller, J. Wastling, S. Sanderson, N. Muller, and A. Hemphill A novel Giardia lamblia nitroreductase, GlNR1, interacts with nitazoxanide and other thiazolides Antimicrob Agents Chemother 51 2007 1979 1986 (Pubitemid 46903083)
42. D. Nillius, J. Muller, and N. Muller Nitroreductase (GlNR1) increases susceptibility of Giardia lamblia and Escherichia coli to nitro drugs J Antimicrob Chemother 66 2011 1029 1035
43. J.F. Rossignol, S. La Frazia, L. Chiappa, A. Ciucci, and M.G. Santoro Thiazolides, a new class of anti-influenza molecules targeting viral hemagglutinin at the post-translational level J Biol Chem 284 2009 29798 29808
44. Y. Yamamoto, A. Hakki, H. Friedman, S. Okubo, T. Shimamura, and P.S. Hoffman et al. Nitazoxanide, a nitrothiazolide antiparasitic drug, is an anti-Helicobacter pylori agent with anti-vacuolating toxin activity Chemotherapy 45 1999 303 312 (Pubitemid 29292366)
45. Y. Hu, S.H. Xiao, and R.V. Aroian The new anthelmintic tribendimidine is an l-type (levamisole and pyrantel) nicotinic acetylcholine receptor agonist PLoS Negl Trop Dis 3 2009 e499
46. L.J. Bischof, D.L. Huffman, and R.V. Aroian Assays for toxicity studies in C. elegans with Bt crystal proteins Methods Mol Biol 351 2006 139 154
47. S. Brenner The genetics of Caenorhabditis elegans Genetics 77 1974 71 94
48. J.A. Dent, M.W. Davis, and L. Avery avr-15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans EMBO J 16 1997 5867 5879 (Pubitemid 27427283)
49. J.Z. Wei, K. Hale, L. Carta, E. Platzer, C. Wong, and S.C. Fang et al. Bacillus thuringiensis crystal proteins that target nematodes Proc Natl Acad Sci U S A 100 2003 2760 2765 (Pubitemid 36297572)
50. Y. Hu, E.G. Platzer, A. Bellier, and R.V. Aroian Discovery of a highly synergistic anthelmintic combination that shows mutual hypersusceptibility Proc Natl Acad Sci U S A 107 2010 5955 5960
51. J. Sulston, and J. Hodgkin Methods W.B. Wood, The nematode Caenorhabditis elegans 1988 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 587 606
52. B.D. Williams, B. Schrank, C. Huynh, R. Shownkeen, and R.H. Waterston A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites Genetics 131 1992 609 624
53. T.C. Chou Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies Pharmacol Rev 58 2006 621 681
54. T.C. Chou Drug combination studies and their synergy quantification using the Chou-Talalay method Cancer Res 70 2010 440 446
55. F. Fonseca-Salamanca, M.M. Martinez-Grueiro, and A.R. Martinez-Fernandez Nematocidal activity of nitazoxanide in laboratory models Parasitol Res 91 2003 321 324 (Pubitemid 37363628)
56. J.A. Dent, M.M. Smith, D.K. Vassilatis, and L. Avery The genetics of ivermectin resistance in Caenorhabditis elegans Proc Natl Acad Sci U S A 97 2000 2674 2679 (Pubitemid 30159230)
57. E. Ruiz-Lancheros, C. Viau, T. Walter, A. Francis, and T. Geary Activity of novel nicotinic anthelmintics in cut preparations of Caenorhabditis elegans Int J Parasitol 41 2011 455 461
58. A. Burns, I. Wallace, J. Wildenhain, M. Tyers, G. Giaever, and G. Bader et al. A predictive model for drug bioaccumulation and bioactivity in Caenorhabditis elegans Nat Chem Biol 6 2010 549 557
59. D.L. Laughton, G.G. Lunt, and A.J. Wolstenholme Reporter gene constructs suggest the Caenorhabditis elegans avermectin receptor b-subunit is expressed solely in the pharynx J Exp Biol 200 1997 1509 1514 (Pubitemid 27253226)
60. S. Jagannathan, D.L. Laughton, C.L. Critten, T.M. Skinner, L. Horoszok, and A.J. Wolstenholme Ligand-gated chloride channel subunits encoded by the Haemonchus contortus and Ascaris suum orthologues of the Caenorhabditis elegans gbr-2 (avr-14) gene Mol Biochem Parasitol 103 1999 129 140 (Pubitemid 29469768)
61. D.M. Yates, and A.J. Wolstenholme An ivermectin-sensitive glutamate-gated chloride channel subunit from Dirofilaria immitis Int J Parasitol 34 2004 1075 1081 (Pubitemid 39093807)
62. A. El-Abdellati, J. De-Graef, A. Van-Zeveren, A. Donnan, P. Skuce, and T. Walsh et al. Altered avr-14B gene transcription patterns in ivermectin-resistant isolates of the cattle parasites, Cooperia oncophora and Ostertagia ostertagi Int J Parasitol 41 2011 951 957
63. A.J. Wolstenholme, and A.T. Rogers Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics Parasitology 131 2005 S85 S95
64. L. Tritten, A. Silbereisen, and J. Keiser Nitazoxanide: in vitro and in vivo drug effects against Trichuris muris and Ancylostoma ceylanicum, alone or in combination Int J Parasitol: Drugs Drug Resist 2 2012 98 105