Oxidative stress resistance genes contribute to the pathogenic potential of the anaerobic protozoan parasite, Entamoeba histolytica

International Journal for Parasitology

Volumn 42, Issue 11, 2012, Pages 1007-1015

  Rastew, Elena ^a   Vicente, João B ^a,b   Singh, Upinder ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

Author keywords

Cytotoxicity; Entamoeba histolytica; Reactive nitrogen species; Reactive oxygen species; Virulence

Indexed keywords

HYDROGEN PEROXIDE; MESSENGER RNA; PROTOZOAL PROTEIN; REACTIVE OXYGEN METABOLITE; STRESS INDUCED ADHESION FACTOR; UNCLASSIFIED DRUG;

CYTOLOGY; ENZYME ACTIVITY; GENE EXPRESSION; GENOME; HOST-PARASITE INTERACTION; OXIDATION; PARASITE INFESTATION; PATHOGENICITY; PROTEIN; PROTOZOAN; TOXICITY; VIRULENCE;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; ENTAMOEBA HISTOLYTICA; ERYTHROPHAGOCYTOSIS; GENE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE OVEREXPRESSION; HOST CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; MAMMAL CELL; MOLECULAR DYNAMICS; NITROSATIVE STRESS; NITROSATIVE STRESS RESISTANCE GENE; NONHUMAN; OXIDATIVE STRESS; OXIDATIVE STRESS RESISTANCE GENE; PARASITE IDENTIFICATION; PARASITE SURVIVAL; PARASITE VIRULENCE; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION;

ANAEROBIOSIS; ENTAMOEBA HISTOLYTICA; ERYTHROCYTES; GENE EXPRESSION REGULATION; HOT TEMPERATURE; HUMANS; OXIDATIVE STRESS; PHAGOCYTOSIS; PROTOZOAN PROTEINS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; VIRULENCE;

ENTAMOEBA HISTOLYTICA; MAMMALIA; PROTOZOA;

EID: 84868140885     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.08.006     Document Type: Article

References (44)

1. Akbar M.A., Chatterjee N.S., Sen P., Debnath A., Pal A., Bera T., Das P. Genes induced by a high-oxygen environment in Entamoeba histolytica. Mol. Biochem. Parasitol. 2004, 133:187-196.
2. Barr S.D., Gedamu L. Role of peroxidoxins in Leishmania chagasi survival. Evidence of an enzymatic defense against nitrosative stress. J. Biol. Chem. 2003, 278:10816-10823.
3. Bates S., MacCallum D.M., Bertram G., Munro C.A., Hughes H.B., Buurman E.T., Brown A.J., Odds F.C., Gow N.A. Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. J. Biol. Chem. 2005, 280:23408-23415.
4. Baxt L.A., Baker R.P., Singh U., Urban S. An Entamoeba histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion. Genes Dev. 2008, 22:1636-1646.
5. Baxt L.A., Rastew E., Bracha R., Mirelman D., Singh U. Downregulation of an Entamoeba histolytica rhomboid protease reveals roles in regulating parasite adhesion and phagocytosis. Eukaryot. Cell 2010, 9:1283-1293.
6. Biller L., Davis P.H., Tillack M., Matthiesen J., Lotter H., Stanley S.L., Tannich E., Bruchhaus I. Differences in the transcriptome signatures of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. BMC Genomics 2010, 11:63.
7. Biller L., Schmidt H., Krause E., Gelhaus C., Matthiesen J., Handal G., Lotter H., Janssen O., Tannich E., Bruchhaus I. Comparison of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. Proteomics 2009, 9:4107-4120.
8. Blom N., Sicheritz-Ponten T., Gupta R., Gammeltoft S., Brunak S. Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 2004, 4:1633-1649.
9. Boettner D.R., Huston C.D., Linford A.S., Buss S.N., Houpt E., Sherman N.E., Petri W.A. Entamoeba histolytica phagocytosis of human erythrocytes involves PATMK, a member of the transmembrane kinase family. PLoS Pathog. 2008, 4:e8.
10. Bruchhaus I., Richter S., Tannich E. Removal of hydrogen peroxide by the 29kDa protein of Entamoeba histolytica. Biochem. J. 1997, 326(Pt 3):785-789.
11. Chan H., Babayan V., Blyumin E., Gandhi C., Hak K., Harake D., Kumar K., Lee P., Li T.T., Liu H.Y., Lo T.C., Meyer C.J., Stanford S., Zamora K.S., Saier M.H. The p-type ATPase superfamily. J. Mol. Microbiol. Biotechnol. 2010, 19:5-104.
12. Choi M.H., Sajed D., Poole L., Hirata K., Herdman S., Torian B.E., Reed S.L. An unusual surface peroxiredoxin protects invasive Entamoeba histolytica from oxidant attack. Mo. Biochem. Parasitol. 2005, 143:80-89.
13. Davis P.H., Zhang X., Guo J., Townsend R.R., Stanley S.L. Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amoebic virulence. Mol. Microbiol. 2006, 61:1523-1532.
14. Diamond L.S., Harlow D.R., Cunnick C.C. A new medium for the axenic cultivation of Entamoeba histolytica and other Entamoeba. Trans. R. Soc. Trop. Med. Hyg. 1978, 72:431-432.
15. Ehrenkaufer G.M., Haque R., Hackney J.A., Eichinger D.J., Singh U. Identification of developmentally regulated genes in Entamoeba histolytica: insights into mechanisms of stage conversion in a protozoan parasite. Cell. Microbiol. 2007, 9:1426-1444.
16. Fields J.A., Thompson S.A. Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J. Bacteriol. 2008, 190:3411-3416.
17. Gilchrist C.A., Houpt E., Trapaidze N., Fei Z., Crasta O., Asgharpour A., Evans C., Martino-Catt S., Baba D.J., Stroup S., Hamano S., Ehrenkaufer G., Okada M., Singh U., Nozaki T., Mann B.J., Petri W.A. Impact of intestinal colonization and invasion on the Entamoeba histolytica transcriptome. Mol. Biochem. Parasitol. 2006, 147:163-176.
18. Griffin J.L. Human amebic dysentery. Electron microscopy of Entamoeba histolytica contacting, ingesting, and digesting inflammatory cells. Am. J. Trop. Med. Hyg. 1972, 21:895-906.
19. Hackney J.A., Ehrenkaufer G.M., Singh U. Identification of putative transcriptional regulatory networks in Entamoeba histolytica using Bayesian inference. Nucleic Acids Res. 2007, 35:2141-2152.
20. Hellberg A., Nickel R., Lotter H., Tannich E., Bruchhaus I. Overexpression of cysteine proteinase 2 in Entamoeba histolytica or Entamoeba dispar increases amoeba-induced monolayer destruction in vitro but does not augment amoebic liver abscess formation in gerbils. Cell. Microbiol. 2001, 3:13-20.
21. Hu G., Kronstad J.W. A putative P-type ATPase, Apt1, is involved in stress tolerance and virulence in Cryptococcus neoformans. Eukaryot. Cell 2009, 9:74-83.
22. Hughes M.A., Lee C.W., Holm C.F., Ghosh S., Mills A., Lockhart L.A., Reed S.L., Mann B.J. Identification of Entamoeba histolytica thiol-specific antioxidant as a GalNAc lectin-associated protein. Mol. Biochem. Parasitol. 2003, 127:113-120.
23. Huston C.D., Boettner D.R., Miller-Sims V., Petri W.A. Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infect. Immun. 2003, 71:964-972.
24. Huston C.D., Houpt E.R., Mann B.J., Hahn C.S., Petri W.A. Caspase 3-dependent killing of host cells by the parasite Entamoeba histolytica. Cell. Microbiol. 2000, 2:617-625.
25. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 1999, 292:195-202.
26. Labruyere E., Guillen N. Host tissue invasion by Entamoeba histolytica is powered by motility and phagocytosis. Arch. Med. Res. 2006, 37:253-258.
27. MacFarlane R.C., Singh U. Identification of differentially expressed genes in virulent and nonvirulent Entamoeba species: potential implications for amebic pathogenesis. Infect. Immun. 2006, 74:340-351.
28. MacFarlane R.C., Singh U. Identification of an Entamoeba histolytica serine-, threonine-, and isoleucine-rich protein with roles in adhesion and cytotoxicity. Eukaryot. Cell 2007, 6:2139-2146.
29. Marshall R.D. Glycoproteins. Annu. Rev. Biochem. 1972, 41:673-702.
30. Mora-Galindo J., Gutierrez-Lozano M., Anaya-Velazquez F. Entamoeba histolytica: kinetics of hemolytic activity, erythrophagocytosis and digestion of erythrocytes. Arch. Med. Res. 1997, 28:200-201.
31. Nachin L., Nannmark U., Nystrom T. Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J. Bacteriol. 2005, 187:6265-6272.
32. Nugent T., Jones D.T. Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 2009, 10:159.
33. Petri W.A., Smith R.D., Schlesinger P.H., Murphy C.F., Ravdin J.I. Isolation of the galactose-binding lectin that mediates the in vitro adherence of Entamoeba histolytica. J. Clin. Invest. 1987, 80:1238-1244.
34. Poole L.B., Chae H.Z., Flores B.M., Reed S.L., Rhee S.G., Torian B.E. Peroxidase activity of a TSA-like antioxidant protein from a pathogenic amoeba. Free Radical Biol. Med. 1997, 23:955-959.
35. Ramos-Martinez E., Olivos-Garcia A., Saavedra E., Nequiz M., Sanchez E.C., Tello E., El-Hafidi M., Saralegui A., Pineda E., Delgado J., Montfort I., Perez-Tamayo R. Entamoeba histolytica: oxygen resistance and virulence. Int. J. Parasitol. 2009, 39:693-702.
36. Saffer L.D., Petri W.A. Role of the galactose lectin of Entamoeba histolytica in adherence-dependent killing of mammalian cells. Infect. Immun. 1991, 59:4681-4683.
37. Saito-Nakano Y., Yasuda T., Nakada-Tsukui K., Leippe M., Nozaki T. Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J. Biol. Chem. 2004, 279:49497-49507.
38. Salles J.M., Salles M.J., Moraes L.A., Silva M.C. Invasive amebiasis: an update on diagnosis and management. Expert Rev. Anti. Infect. Ther. 2007, 5:893-901.
39. Santi-Rocca J., Smith S., Weber C., Pineda E., Hon C.C., Saavedra E., Olivos-Garcia A., Rousseau S., Dillies M.A., Coppee J.Y., Guillen N. Endoplasmic reticulum stress-sensing mechanism is activated in Entamoeba histolytica upon treatment with nitric oxide. PLoS One 2012, 7:e31777.
40. Stanley S.L. Amoebiasis. Lancet 2003, 361:1025-1034.
41. Teixeira J.E., Huston C.D. Participation of the serine-rich Entamoeba histolytica protein in amebic phagocytosis of apoptotic host cells. Infect. Immun. 2008, 76:959-966.
42. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface. Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
43. Vicente J.B., Ehrenkaufer G.M., Saraiva L.M., Teixeira M., Singh U. Entamoeba histolytica modulates a complex repertoire of novel genes in response to oxidative and nitrosative stresses: implications for amebic pathogenesis. Cell. Microbiol. 2009, 11:51-69.
44. Voigt H., Guillen N. New insights into the role of the cytoskeleton in phagocytosis of Entamoeba histolytica. Cell. Microbiol. 1999, 1:195-203.