Protein disulfide isomerase (PDI) associates with NADPH oxidase and is required for phagocytosis of Leishmania chagasi promastigotes by macrophages

Journal of Leukocyte Biology

Volumn 86, Issue 4, 2009, Pages 989-998

  Santos, Célio X C ^a   Stolf, Beatriz S ^a   Takemoto, Paulo V A ^a   Amanso, Angélica M ^a   Lopes, Lucia R ^a   Souza, Edna B ^a   Goto, Hiro ^a   Laurindo, Francisco R M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Chaperone; Infection; Nox; Parasite; PDI; Thiols

Indexed keywords

ARSENOSOBENZENE; BACITRACIN; BREFELDIN A; CATALASE; COMPLEMENTARY RNA; ENZYME ANTIBODY; PROTEIN DISULFIDE ISOMERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA;

AMASTIGOTE; ANIMAL CELL; ARTICLE; BINDING ASSAY; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME SUBUNIT; GENE OVEREXPRESSION; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; IN VITRO STUDY; LEISHMANIA CHAGASI; MACROPHAGE; MALE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROMASTIGOTE; WILD TYPE;

LEISHMANIA DONOVANI CHAGASI; PROTOZOA;

EID: 70349643912     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0608354     Document Type: Article

References (55)

1. Noiva, R. (1999) Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Semin. Cell Dev. Biol. 10, 481-493. (Pubitemid 129513639)
2. Clissold, P. M., Bicknell, R. (2003) The thioredoxin-like fold: hidden domains in protein disulfide isomerases and other chaperone proteins. Bioessays 25, 603-611.
3. Wetterau, J. R., Combs, K. A., Spinner, S. N., Joiner, B. J. (1990) Protein disulfide isomerase is a component of the microsomal triglyceride transfer protein complex. J. Biol. Chem. 265, 9800-9807. (Pubitemid 20194327)
4. Terada, K., Manchikalapudi, P., Noiva, R., Jauregui, H. O., Stockert, R. J., Schilsky, M. L. (1995) Secretion, surface localization, turnover, and steady state expression of protein disulfide isomerase in rat hepatocytes. J. Biol. Chem. 270, 20410-20416.
5. Conant, C. G., Stephens, R. S. (2007) Chlamydia attachment to mammalian cells requires protein disulfide isomerase. Cell. Microbiol. 9, 222-232. (Pubitemid 44896847)
6. Tsai, B., Rodighiero, C., Lencer, W. I., Rapoport, T. A. (2001) Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104, 937-948. (Pubitemid 32289285)
7. Ryser, H. J., Mandel, R., Ghani, F. (1991) Cell surface sulfhydryls are required for the cytotoxicity of diphtheria toxin but not of ricin in Chinese hamster ovary cells. J. Biol. Chem. 266, 18439-18442. (Pubitemid 21908102)
8. Abell, B. A., Brown, D. T. (1993) Sindbis virus membrane fusion is mediated by reduction of glycoprotein disulfide bridges at the cell surface. J. Virol. 67, 5496-5501.
9. Gallina, A., Hanley, T. M., Mandel, R., Trahey, M., Broder, C. C., Viglianti, G. A., Ryser, H. J. (2002) Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J. Biol. Chem. 277, 50579-50588. (Pubitemid 36042217)
10. Matthias, L. J., Yam, P. T., Jiang, X. M., Vandegraaff, N., Li, P., Poumbourios, P., Donoghue, N., Hogg, P. J. (2002) Disulfide exchange in domain 2 of CD4 is required for entry of HIV-1. Nat. Immunol. 3, 727-732. (Pubitemid 34884828)
11. Garin, J., Diez, R., Kieffer, S., Dermine, J. F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C., Desjardins, M. (2001) The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152, 165-180.
12. Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P. H., Mortimer, O. S., Paiement, J., Bergeron, J. M., Desjardins, M. (2002) Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110, 119-131. (Pubitemid 34874611)
13. Roy, C. R., Salcedo, S. P., Gorvel, J. P. (2006) Pathogen-endoplasmic- reticulum interactions: in through the out door. Nat. Rev. Immunol. 6, 136-147.
14. Kima, P. E., Dunn, W. (2005) Exploiting calnexin expression on phagosomes to isolate Leishmania parasitophorous vacuoles. Microb. Pathog. 38, 139-145.
15. Janiszewski, M., Lopes, L. R., Carmo, A. O., Pedro, M. A., Brandes, R. P., Santos, C. X., Laurindo, F. R. (2005) Regulation of NAD(P)H oxidase by associated protein disulfide isomerase in vascular smooth muscle cells. J. Biol. Chem. 280, 40813-40819. (Pubitemid 41780573)
16. Laurindo, F. R., Fernandes, D. C., Amanso, A. M., Santos, C. X. (2008) Novel role of protein disulfide isomerase in the regulation of NADPH oxidase activity: pathophysiological implications in vascular diseases. Antioxid. Redox Signal. 10, 1101-1113.
17. Murray, H. W., Berman, J. D., Davies, C. R., Saravia, N. G. (2005) Advances in Leishmaniasis. Lancet 366, 1561-1577.
18. Posada-Vergara, M. P., Lindoso, J. A., Tolezano, J. E., Pereira-Chioccola, V. L., Silva, M. V., Goto, H. (2005) Tegumentary leishmaniasis as a manifestation of immune reconstitution inflammatory syndrome in 2 patients with AIDS. J. Infect. Dis. 192, 1819-1822. (Pubitemid 41587835)
19. Shaw, J. J. (2006) Further thoughts on the use of the name Leishmania (Leishmania) infantum chagasi for the aethiological agent of American visceral Leishmaniasis. Mem. Inst. Oswaldo Cruz 101, 577-579.
20. McConville, M. J., Handman, E. (2007) The molecular basis of Leishmania pathogenesis. Int. J. Parasitol. 37, 1047-1051.
21. McMahon-Pratt, D., Alexander, J. (2004) Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniases or the visceral disease? Immunol. Rev. 201, 206-224. (Pubitemid 39318454)
22. Pham, N. K., Mouriz, J., Kima, P. E. (2005) Leishmania pifanoi amastigotes avoid macrophage production of superoxide by inducing heme degradation. Infect. Immun. 73, 8322-8333. (Pubitemid 41740323)
23. Sacks, D., Sher, A. (2002) Evasion of innate immunity by parasitic protozoa. Nat. Immunol. 3, 1041-1047. (Pubitemid 35363655)
24. Babior, B. M., Lambeth, J. D., Nauseef, W. (2002) The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397, 342-344.
25. Kawahara, T., Lambeth, J. D. (2007) Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evol. Biol. 7, 178. (Pubitemid 350233621)
26. Hurst, J. K., Lymar, S. V. (1999) Cellularly-generated inorganic oxidants as natural microbicidal agents. Acc. Chem. Res. 32, 520-528.
27. Winterbourn, C. C. (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278-286. (Pubitemid 351550893)
28. Rabinovitch, M. (1995) Professional and nonprofessional phagocytes: an introduction. Trends Cell Biol. 5, 85-87.
29. Desjardins, M. (2003) ER-mediated phagocytosis: a new membrane for new functions. Nat. Rev. Immunol. 3, 280-291.
30. Cross, A. R. (1990) Inhibitors of the leukocyte superoxide generating oxidase. Free Radic. Biol. Med. 8, 71-93.
31. Janiszewski, M., Pedro, M. A., Scheffer, R. C., van Asseldonk, J. H., Souza, L. C., da Luz, P. L., Augusto, O., Laurindo, F. R. (2000) Inhibition of vascular NADH/NADPH oxidase activity by thiol reagents: lack of correlation with cellular glutathione redox status. Free Radic. Biol. Med. 29, 889-899. (Pubitemid 30785818)
32. Lodge, R., Diallo, T. O., Descoteaux, A. (2006) Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane. Cell. Microbiol. 8, 1922-1931. (Pubitemid 44687332)
33. Goto, H., Gomes, C. M., Corbett, C. E., Monteiro, H. P., Gidlund, M. (1998) Insulin-like growth factor I is a growth-promoting factor for Leishmania promastigotes and amastigotes. Proc. Natl. Acad. Sci. USA 95, 13211-13216. (Pubitemid 28509550)
34. Giorgio, S., Barao, S. C., Augusto, O., Kwee, J. K. (1998) Leishmania amazonensis infection is reduced in macrophages treated with guanine ribonucleosides. Acta Trop. 70, 119-122. (Pubitemid 28254779)
35. Lodge, R., Descoteaux, A. (2006) Phagocytosis of Leishmania donovani amastigotes is Rac1 dependent and occurs in the absence of NADPH oxidase activation. Eur. J. Immunol. 36, 2735-2744. (Pubitemid 44608457)
36. Lodge, R., Descoteaux, A. (2005) Leishmania donovani promastigotes induce periphagosomal F-actin accumulation through retention of the GTPase Cdc42. Cell. Microbiol. 7, 1647-1658. (Pubitemid 41511921)
37. Mandel, R., Ryser, H. J., Ghani, F., Wu, M., Peak, D. (1993) Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc. Natl. Acad. Sci. USA 90, 4112-4116. (Pubitemid 23134176)
38. Ben Achour, Y., Chenik, M., Louzir, H., Dellagi, K. (2002) Identification of a disulfide isomerase protein of Leishmania major as a putative virulence factor. Infect. Immun. 70, 3576-3585. (Pubitemid 34665995)
39. Hong, B. X., Soong, L. (2008) Identification and enzymatic activities of four protein disulfide isomerase (PDI) isoforms of Leishmania amazonensis. Parasitol. Res. 102, 437-446.
40. Touret, N., Paroutis, P., Terebiznik, M., Harrison, R. E., Trombetta, S., Pypaert, M., Chow, A., Jiang, A., Shaw, J., Yip, C., Moore, H. P., van der Wel, N., Houben, D., Peters, P. J., de Chastellier, C., Mellman, I., Grinstein, S. (2005) Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123, 157-170. (Pubitemid 41414536)
41. Gagnon, E., Bergeron, J. J., Desjardins, M. (2005) ER-mediated phagocytosis: myth or reality? J. Leukoc. Biol. 77, 843-845. (Pubitemid 40770833)
42. Müller-Taubenberger, A., Lupas, A. N., Li, H., Ecke, M., Simmeth, E., Gerisch, G. (2001) Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J. 20, 6772-6782. (Pubitemid 33134207)
43. Park, B., Lee, S., Kim, E., Cho, K., Riddell, S. R., Cho, S., Ahn, K. (2006) Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127, 369-382. (Pubitemid 44572373)
44. Park, J. B. (2003) Phagocytosis induces superoxide formation and apoptosis in macrophages. Exp. Mol. Med. 35, 325-335.
45. Tian, G., Xiang, S., Noiva, R., Lennarz, W. J., Schindelin, H. (2006) The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124, 61-73. (Pubitemid 43069310)
46. Zarley, J. H., Britigan, B. E., Wilson, M. E. (1991) Hydrogen peroxide-mediated toxicity for Leishmania donovani chagasi promastigotes. Role of hydroxyl radical and protection by heat shock. J. Clin. Invest. 88, 1511-1521.
47. Pham, N. K., Mouriz, J., Kima, P. E. (2005) Leishmania pifanoi amastigotes avoid macrophage production of superoxide by inducing heme degradation. Infect. Immun. 73, 8322-8333. (Pubitemid 41740323)
48. Channon, J. Y., Blackwell, J. M. (1985) A study of the sensitivity of Leishmania donovani promastigotes and amastigotes to hydrogen peroxide. II. Possible mechanisms involved in protective H2O2 scavenging. Parasitology 91, 207-217. (Pubitemid 16232373)
49. Wilson, M. E., Andersen, K. A., Britigan, B. E. (1994) Response of Leishmania chagasi promastigotes to oxidant stress. Infect. Immun. 62, 5133-5141.
50. Murray, H. W. (1981) Interaction of Leishmania with a macrophage cell line. Correlation between intracellular killing and the generation of oxygen intermediates. J. Exp. Med. 153, 1690-1695.
51. Ashutosh, Sundar, S., Goyal, N. (2007) Molecular mechanisms of antimony resistance in Leishmania. J. Med. Microbiol. 56, 143-153. (Pubitemid 46302715)
52. Miller, M. A., McGowan, S. E., Gantt, K. R., Champion, M., Novick, S. L., Andersen, K. A., Bacchi, C. J., Yarlett, N., Britigan, B. E., Wilson, M. E. (2000) Inducible resistance to oxidant stress in the protozoan Leishmania chagasi. J. Biol. Chem. 275, 33883-33889. (Pubitemid 30808614)
53. Finzi, J. K, Chiavegatto, C. W., Corat, K. F., Lopez, J. A., Cabrera, O. G., Mielniczki-Pereira, A. A., Colli, W., Alves, M. J., Gadelha, F. R (2004) Trypanosoma cruzi response to the oxidative stress generated by hydrogen peroxide. Mol. Biochem. Parasitol. 133, 37-43. (Pubitemid 37510306)
54. Wyllie, S., Cunningham, M. L., Fairlamb, A. H. (2004) Dual action of antimonial drugs on thiol redox metabolism in the human pathogen Leishmania donovani. J. Biol. Chem. 279, 39925-39932. (Pubitemid 39258265)
55. Akerboom, T. P., Sies, H. (1981) Assay of glutathione, glutathione disul- fide, and glutathione mixed disulfides in biological samples. Methods Enzymol. 77, 373-383.