Proteomic and transcriptional analyses of genes differentially expressed in Giardia duodenalis clones resistant to albendazole

Infection, Genetics and Evolution

Volumn 15, Issue , 2013, Pages 10-17

  Paz Maldonado, María Teresita ^a   Argüello García, Raúl ^a   Cruz Soto, Maricela ^a,c   Mendoza Hernández, Guillermo ^b   Ortega Pierres, Guadalupe ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c Probiomed SA de CV   (Mexico)

Author keywords

Albendazole; Drug resistance; Giardia; Proteomics; Transcriptional analysis

Indexed keywords

ALBENDAZOLE; ALPHA 2 GIARDIN PROTEIN; HELMINTH PROTEIN; MESSENGER RNA; ORNITHINE CARBAMOYLTRANSFERASE; PHOSPHOGLYCERATE KINASE; RANBP1 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GIARDIA LAMBLIA; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MOLECULAR CLONING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; TROPHOZOITE; UPREGULATION;

GIARDIA; GIARDIA INTESTINALIS;

EID: 84878125851     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.08.021     Document Type: Article

References (51)

1. Adam R.D. Biology of Giardia lamblia. Clin. Microbiol. Rev. 2001, 14:447-475.
2. Alvarez L.I., Solana H.D., Mottier M.L., et al. Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 2005, 131:1-10.
3. Argüello-García R., Cruz-Soto M., Romero-Montoya L., et al. In vitro resistance to 5-nitroimidazoles and benzimidazoles in Giardia duodenalis: variability and variation in gene expression. Infect. Genet. Evol. 2009, 9:1057-1064.
4. Baum K.F., Berens R.L., Jones R.H., et al. A new method for cloning Giardia lamblia, with a discussion of the statistical considerations of limiting dilution. J. Parasitol. 1988, 74:267-269.
5. 2O-producing NADH oxidase from the protozoan parasite Giardia duodenalis. Eur. J. Biochem. 1996, 241:155-161.
6. Brown D.M., Upcroft J.A., Edwards M.R., et al. Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. Int. J. Parasitol. 1998, 28:149-164.
7. Chavez B., Cedillo-Rivera R., Martinez-Palomo A. Giardia lamblia: ultrastructural study of the in vitro effect of benzimidazoles. J. Protozool. 1992, 39:510-515.
8. Darbon A., Portal A., Girier L., et al. Treatment of giardiasis (lambliasis) with metronidazole. apropos of 100 cases. Presse Med. 1962, 70:15-16.
9. Drummelsmith J., Brochu V., Girard I., et al. Proteome mapping of the protozoan parasite Leishmania and application to the study of drug targets and resistance mechanisms. Mol. Cell. Proteomics 2003, 2:146-155.
10. Duan Z., Lamendola D.E., Yusuf R.Z., et al. Overexpression of human phosphoglycerate kinase 1 (PGK1) induces a multidrug resistance phenotype. Anticancer Res. 2002, 22:1933-1941.
11. Farthing M.J.G. Host-parasite interactions in human giardiasis. Q. J Med. 1989, 70:191-204.
12. Fox L.M., Saravolatz L.D. Nitazoxanide: a new thiazolide antiparasitic agent. Clin. Infect. Dis. 2005, 40:1173-1180.
13. Gardner H., Hill D.R. Treatment of Giardiasis. Clin. Microbiol. Rev. 2001, 14:114-128.
14. Gerke V., Moss S.E. Annexins: from structure to function. Physiol. Rev. 2002, 82:331-371.
15. Greenbaum D., Jansen R., Gerstein M. Analysis of mRNA expression and protein abundance data: an approach for the comparison of enrichment of features in the cellular population of protein and transcripts. Bioinformatics 2002, 18:585-596.
16. Katelaris P.H., Naeem A., Farthing M.J. Attachment of Giardia lamblia trophozoites to a cultured human intestinal cell line. Gut 1995, 37:512-518.
17. Katiyar S.K., Gordon V.R., McLaughlin G.L., et al. Antiprotozoal activities of benzimidazoles and correlations with beta-tubulin sequence. Antimicrob. Agents Chemother. 1994, 38:2086-2090.
18. Keister D.B. Axenic cultivation of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans. R. Soc. Trop. Med. Hyg. 1983, 77:487-488.
19. Lin X., Li H., Wang C., et al. Proteomic analysis of nalidixic acid resistance in Escherichia coli: identification and functional characterization of OM proteins. J. Proteome Res. 2008, 7:2399-2405.
20. Lindquist H.D. Induction of albendazole resistance in Giardia lamblia. Microbiol. Drug Resist. 1996, 2:433-434.
21. Longley D.B., Johnston P.G. Molecular mechanisms of drug resistance. J. Pathol. 2005, 205:275-292.
22. Lowry O.H., Rosebrough N.J., Farr A.L., et al. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
23. Meloni B.P., Thompson R.C.A., Reynoldson J.A., et al. Albendazole: a more effective antigiardial agent in vitro than metronidazole or tinidazole. Trans. R. Soc. Trop. Med. Hyg. 1990, 84:375-379.
24. Merino G., Alvarez A.I., Prieto J.G., Kim R.B. The anthelminthic agent albendazole does not interact with p-glycoprotein. Drug Metab. Dispos. 2002, 30:365-369.
25. Morgan R.O., Fernandez M.P. Molecular phylogeny of annexins and identification of a primitive homologue in Giardia lamblia. Mol. Biol. Evol. 1995, 12:967-979.
26. Mottier L., Lanusse C. Pharmaco-parasitological basis of anthelmintic resistance. Rev. Med. Vet. 2001, 82:74-85.
27. Muenster U., Grieshop B., Ickenroth K., Gnoth M.J. Characterization of substrates and inhibitors for the in vitro assessment of Bcrp mediated drug-drug interactions. Pharm. Res. 2008, 25:2320-2326.
28. Müller J., Ley S., Felger I., Hemphill A., Müller N. Identification of differentially expressed genes in a Giardia lamblia WB C6 clone resistant to nitazoxanide and metronidazole. J. Antimicrob. Chemother. 2008, 62:72-82.
29. Nohýnková E., Dráber P., Reischig J., et al. Localization of gamma-tubulin in interphase and mitotic cells of a unicellular eukaryote Giardia intestinalis. Eur. J. Cell Biol. 2000, 79:438-445.
30. Oxberry M.E., Reynoldson J.A., Thompson R.C.A. The binding and distribution of albendazole and its principal metabolites in Giardia duodenalis. J. Vet. Pharmacol. Ther. 2000, 23:113-120.
31. Park B.S., Lee B.H., Kim T.W., et al. Proteomic evaluation of adults of Rhyzopertha dominica resistant to phosphine. Environ. Toxicol. Pharmacol. 2008, 25:121-126.
32. Peattie D.A., Alonso R.A., Hein A., Caulfield J.P. Ultrastructural localization of giardins to the edges of disk micorribbons of Giardia lamblia and the nucleotide and deduced protein sequence of alpha giardin. J. Cell. Biol. 1989, 109:2323-2335.
33. Prieto J.H., Koncarevic S., Park S.K., et al. Large-scale differential proteome analysis in Plasmodium falciparum under drug treatment. PLoS ONE 2008, 3:e4098.
34. Quimby B.B., Dasso M. The small GTPase Ran: interpreting the signs. Curr. Opin. Cell Biol. 2003, 15:338-344.
35. Reynoldson J.A., Thompson R.C.A., Meloni B.P. In vivo efficacy of albendazole against Giardia duodenalis in mice. Parasitol. Res. 1991, 77:325-328.
36. Savioli L., Smith H., Thompson A. Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'. Trend Parasitol. 2006, 22:203-208.
37. Saravanan R.S., Rose J.K.C. A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 2004, 4:2522-2532.
38. Schofield P.J., Edwards M.R., Kranz P. Glucose metabolism in Giardia intestinalis. Mol. Biochem. Parasitol. 1991, 45:39-48.
39. Schwab A.E., Boakye D.A., Kyelem D., et al. Detection of benzimidazole resistance-associated mutations in the filarial nematode Wuchereria bancrofti and evidence for selection by albendazole and ivermectin combination treatment. Am. J. Trop. Med. Hyg. 2005, 2005(73):234-238.
40. Shevchenko A., Wilm M., Vorm O., et al. Mass spectrometry sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
41. Su L.H., Lee G.A., Huang Y.C., et al. Neomycin and puromycin affect gene expression in Giardia lamblia stable transfection. Mol. Biochem. Parasitol. 2007, 156:124-135.
42. Thomas M.E. Observations upon the effects of mepacrine and other substances on Giardia intestinalis. Parasitology 1953, 42:262-268.
43. Turi T.G., Mueller U.W., Sazer S., et al. Characterization of a nuclear protein conferring brefeldin a resistance in Schizosaccharomyces pombe. J. Biol. Chem. 1996, 271:9166-9171.
44. Upcroft J., Mitchell R., Chen N., et al. Albendazole resistance in Giardia is correlated with cytoskeletal changes but not with a mutation at amino acid 200 in beta-tubulin. Microbiol. Drug Resist. 1996, 2:303-308.
45. Upcroft P., Upcroft J.A. Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin. Microbiol. Rev. 2001, 14:150-164.
46. Venkasetan P. Albendazole. J. Antimicrob. Chemother. 1998, 41:145-147.
47. Vinaud M.C., Ferreira C.S., Lino Junior Rde S., et al. Taenia crassiceps: energetic and respiratory metabolism from cysticerci exposed to praziquantel and albendazole in vitro. Exp. Parasitol. 2008, 120:221-226.
48. Wang X., Lu Y., Yang J., et al. Identification of triosephosphate isomerase as an anti-drug resistance agent in human gastric cancer cells using functional proteomic analysis. J. Cancer Res. Clin. Oncol. 2008, 134:995-1003.
49. Weiland M.E.L., Palma J.E.D., Griffiths W.J., et al. Characterisation of alpha-1 giardin: an immunodominant Giardia lamblia annexin with glycosaminoglycan-binding activity. Int. J. Parasitol. 2003, 33:1341-1351.
50. Weiland M.E.L., McArthur A.G., Morrison H.G., et al. Annexin-like alpha giardins: a new cytoskeletal gene family in Giardia lamblia. Int. J. Parasitol. 2005, 35:617-626.
51. Xolalpa W., Vallecillo A.J., Lara M., et al. Identification of novel bacterial plasminogen-binding proteins in the human pathogen Mycobacterium tuberculosis. Proteomics 2007, 7:3332-3341.