Involvement of the Leishmania donovani virulence factor A2 in protection against heat and oxidative stress

Experimental Parasitology

Volumn 132, Issue 2, 2012, Pages 109-115

  McCall, Laura Isobel ^a   Matlashewski, Greg ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

A2; Heat shock; Leishmania donovani; Oxidative stress; Stress response; Virulence

Indexed keywords

COMPLEMENTARY RNA; DITHIOTHREITOL; HYDROGEN PEROXIDE; NITRIC OXIDE; PARASITE ANTIGEN; PROTEIN A2; UNCLASSIFIED DRUG;

AMASTIGOTE; ANTIOXIDANT ACTIVITY; ANTISENSE VECTOR; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; HEAT SHOCK RESPONSE; HEAT STRESS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; LEISHMANIA DONOVANI; LEISHMANIASIS; NONHUMAN; OXIDATIVE STRESS; PARASITE CULTIVATION; PARASITE SURVIVAL; PARASITE VIABILITY; PARASITE VIRULENCE; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANTIGENS, PROTOZOAN; AXENIC CULTURE; DOWN-REGULATION; HEAT-SHOCK RESPONSE; LEISHMANIA DONOVANI; OXIDATIVE STRESS; PLASMIDS; PROTOZOAN PROTEINS; TUBULIN; VIRULENCE FACTORS;

LEISHMANIA DONOVANI; MAMMALIA; PROTOZOA;

EID: 84866377565     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2012.06.001     Document Type: Article

References (51)

1. Bangs J.D., Uyetake L., Brickman M.J., Balber A.E., Boothroyd J.C. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei. Divergent ER retention signals in a lower eukaryote. J. Cell. Sci. 1993, 105(Pt 4):1101-1113.
2. Barak E., Amin-Spector S., Gerliak E., Goyard S., Holland N., Zilberstein D. Differentiation of Leishmania donovani in host-free system: analysis of signal perception and response. Mol. Biochem. Parasitol. 2005, 141:99-108.
3. Castro H., Tomas A.M. Peroxidases of trypanosomatids. Antioxid. Redox Signal. 2008, 10:1593-1606.
4. Chan J., Fujiwara T., Brennan P., Mcneil M., Turco S.J., Sibille J.C., Snapper M., Aisen P., Bloom B.R. Microbial glycolipids - possible virulence factors that scavenge oxygen radicals. Proc. Natl. Acad. Sci. USA 1989, 86:2453-2457.
5. Channon J.Y., Blackwell J.M. A study of the sensitivity of Leishmania-donovani promastigotes and amastigotes to hydrogen-peroxide.1. Differences in sensitivity correlate with parasite-mediated removal of hydrogen-peroxide. Parasitology 1985, 91:197-206.
6. Charest H., Matlashewski G. Developmental gene expression in Leishmania donovani: differential cloning and analysis of an amastigote-stage-specific gene. Mol. Cell. Biol. 1994, 14:2975-2984.
7. Charest H., Zhang W.W., Matlashewski G. The developmental expression of Leishmania donovani A2 amastigote-specific genes is post-transcriptionally mediated and involves elements located in the 3'-untranslated region. J. Biol. Chem. 1996, 271:17081-17090.
8. Gokool S. Sigma 1- and mu 1-adaptin homologues of Leishmania mexicana are required for parasite survival in the infected host. J. Biol. Chem. 2003, 278:29400-29409.
9. Gosline S.J.C., Nascimento M., McCall L.I., Zilberstein D., Thomas D.Y., Matlashewski G., Hallett M. Intracellular eukaryotic parasites have a distinct unfolded protein response. PLoS One 2011, 6.
10. Gupta N., Goyal N., Rastogi A.K. In vitro cultivation and characterization of axenic amastigotes of Leishmania. Trends Parasitol. 2001, 17:150-153.
11. Harding H.P., Zhang Y.H., Zeng H.Q., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
12. Haynes C.M., Titus E.A., Cooper A.A. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell 2004, 15:767-776.
13. Huang L.E., Zhang H., Bae S.W., Liu A.Y. Thiol reducing reagents inhibit the heat shock response. Involvement of a redox mechanism in the heat shock signal transduction pathway. J. Biol. Chem. 1994, 269:30718-30725.
14. Iyer J.P., Kaprakkaden A., Choudhary M.L., Shaha C. Crucial role of cytosolic tryparedoxin peroxidase in Leishmania donovani survival, drug response and virulence. Mol. Microbiol. 2008, 68:372-391.
15. Kampinga H.H. Chaperones in preventing protein denaturation in living cells and protecting against cellular stress. Handb. Exp. Pharmacol. 2006, 1-42.
16. Lemesre J.L., Sereno D., Daulouede S., Veyret B., Brajon N., Vincendeau P. Leishmania spp.: nitric oxide-mediated metabolic inhibition of promastigote and axenically grown amastigote forms. Exp. Parasitol. 1997, 86:58-68.
17. Liu Y., Chang A. Heat shock response relieves ER stress. EMBO J. 2008, 27:1049-1059.
18. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., Kaufman R.J. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl. Acad. Sci. USA 2008, 105:18525-18530.
19. Matsumoto R., Akama K., Rakwal R., Iwahashi H. The stress response against denatured proteins in the deletion of cytosolic chaperones SSA1/2 is different from heat-shock response in Saccharomyces cerevisiae. BMC Genomics 2005, 6.
20. McCall L.I., Matlashewski G. Localization and induction of the A2 virulence factor in Leishmania: evidence that A2 is a stress response protein. Mol. Microbiol. 2010, 77:518-530.
21. Mehlotra R.K. Antioxidant defense mechanisms in parasitic protozoa. Crit. Rev. Microbiol. 1996, 22:295-314.
22. Mikus J., Steverding D. A simple colorimetric method to screen drug cytotoxicity against Leishmania using the dye Alamar Blue. Parasitol. Int. 2000, 48:265-269.
23. Militello K.T., Refour P., Comeaux C.A., Duraisingh M.T. Antisense RNA and RNAi in protozoan parasites: working hard or hardly working?. Mol. Biochem. Parasitol. 2008, 157:117-126.
24. Moreira W., Leblanc E., Ouellette M. The role of reduced pterins in resistance to reactive oxygen and nitrogen intermediates in the protozoan parasite Leishmania. Free Radic. Biol. Med. 2009, 46:367-375.
25. Mukherjee A., Roy G., Guimond C., Ouellette M. The gamma-glutamylcysteine synthetase gene of Leishmania is essential and involved in response to oxidants. Mol. Microbiol. 2009, 74:914-927.
26. Murray H.W., Berman J.D., Davies C.R., Saravia N.G. Advances in leishmaniasis. Lancet 2005, 366:1561-1577.
27. Naderer T., Dandash O., McConville M.J. Calcineurin is required for Leishmania major stress response pathways and for virulence in the mammalian host. Mol. Microbiol. 2011, 80:471-480.
28. Nielsen M., Lundegaard C., Lund O., Petersen T.N. CPHmodels-3.0-remote homology modeling using structure-guided sequence profiles. Nucleic Acids Res. 2010, 38:W576-W581.
29. Olivier M., Gregory D.J., Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 2005, 18:293-305.
30. Pal S., Dolai S., Yadav R.K., Adak S. Ascorbate peroxidase from Leishmania major controls the virulence of infective stage of promastigotes by regulating oxidative stress. PLoS One 2010, 5.
31. Park H.G., Han S.I., Oh S.Y., Kang H.S. Cellular responses to mild heat stress. Cell. Mol. Life Sci. 2005, 62:10-23.
32. Pearson R.D., Sousa A.Q. Clinical spectrum of Leishmaniasis. Clin. Infect. Dis. 1996, 22:1-13.
33. Pescher P., Blisnick T., Bastin P., Spath G.F. Quantitative proteome profiling informs on phenotypic traits that adapt Leishmania donovani for axenic and intracellular proliferation. Cell. Microbiol. 2011, 13:978-991.
34. Pimenta P.F., Saraiva E.M., Sacks D.L. The comparative fine structure and surface glycoconjugate expression of three life stages of Leishmania major. Exp. Parasitol. 1991, 72:191-204.
35. Robinson K.A., Beverley S.M. Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol. Biochem. Parasitol. 2003, 128:217-228.
36. Rochette A., Raymond F., Corbeil J., Ouellette M., Papadopoulou B. Whole-genome comparative RNA expression profiling of axenic and intracellular amastigote forms of Leishmania infantum. Mol. Biochem. Parasitol. 2009, 165:32-47.
37. Sanders S.L., Whitfield K.M., Vogel J.P., Rose M.D., Schekman R.W. Sec61p and Bip directly facilitate polypeptide translocation into the Er. Cell 1992, 69:353-365.
38. Sarkar A., Ghosh S., Pakrashi S., Roy D., Sen S., Chatterjee M. Leishmania strains causing self-healing cutaneous leishmaniasis have greater susceptibility towards oxidative stress. Free Radic. Res. 2012, 46:665-673.
39. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
40. Thorne K.J.I., Blackwell J.M. Cell-mediated killing of protozoa, p 85. Advances in Parasitology 1983, vol. 22. Academic Press, London.
41. Toivola D.M., Strnad P., Habtezion A., Omary M.B. Intermediate filaments take the heat as stress proteins. Trends Cell Biol. 2010, 20:79-91.
42. Vince J.E., Tull D.L., Spurck T., Derby M.C., McFadden G.I., Gleeson P.A., Gokool S., McConville M.J. Leishmania adaptor protein-1 subunits are required for normal lysosome traffic, flagellum biogenesis, lipid homeostasis, and adaptation to temperatures encountered in the mammalian host. Eukaryot. Cell 2008, 7:1256-1267.
43. Wei X.Q., Charles I.G., Smith A., Ure J., Feng C.J., Huang F.P., Xu D.M., Muller W., Moncada S., Liew F.Y. Altered immune-responses in mice lacking inducible nitric-oxide synthase. Nature 1995, 375:408-411.
44. Wilson M.E., Andersen K.A., Britigan B.E. Response of Leishmania-chagasi promastigotes to oxidant stress. Infect. Immun. 1994, 62:5133-5141.
45. Wilson M.E., Jeronimo S.M.B., Pearson R.D. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb. Pathog. 2005, 38:147-160.
46. Zarley J.H., Britigan B.E., Wilson M.E. Hydrogen peroxide-mediated toxicity for Leishmania-donovani chagasi promastigotes - role of hydroxyl radical and protection by heat-shock. J. Clin. Invest. 1991, 88:1511-1521.
47. Zhang W.W., Charest H., Ghedin E., Matlashewski G. Identification and overexpression of the A2 amastigote-specific protein in Leishmania donovani. Mol. Biochem. Parasitol. 1996, 78:79-90.
48. Zhang W.W., Matlashewski G. Loss of virulence in Leishmania donovani deficient in an amastigote-specific protein, A2. Proc. Natl. Acad. Sci. USA 1997, 94:8807-8811.
49. Zhang W.W., Matlashewski G. Analysis of antisense and double stranded RNA downregulation of A2 protein expression in Leishmania donovani. Mol. Biochem. Parasitol. 2000, 107:315-319.
50. Zhang W.W., Matlashewski G. Characterization of the A2-A2rel gene cluster in Leishmania donovani: involvement of A2 in visceralization during infection. Mol. Microbiol. 2001, 39:935-948.
51. Zhang W.W., Mendez S., Ghosh A., Myler P., Ivens A., Clos J., Sacks D.L., Matlashewski G. Comparison of the A2 gene locus in Leishmania donovani and Leishmania major and its control over cutaneous infection. J. Biol. Chem. 2003, 278:35508-35515.