Leishmania pifanoi amastigotes avoid macrophage production of superoxide by inducing heme degradation

Infection and Immunity

Volumn 73, Issue 12, 2005, Pages 8322-8333

  Pham, Nam Kha ^a   Mouriz, Jennifer ^a   Kima, Peter E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; HEME; HEME OXYGENASE 1; METALLOPORPHYRIN; NITROBLUE TETRAZOLIUM; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; ZYMOSAN;

AMASTIGOTE; ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; ENZYME ACTIVITY; IMMUNOBLOTTING; LEISHMANIA; LEISHMANIA PIFANOI; LEISHMANIASIS; MACROPHAGE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN PROCESSING;

ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; HEME; HEME OXYGENASE-1; LEISHMANIA MEXICANA; LEISHMANIASIS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; NADPH OXIDASE; SUPEROXIDES; VACUOLES;

EID: 28444478749     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.12.8322-8333.2005     Document Type: Article

References (44)

1. Baca, O. G., M. J. Roman, R. H. Glew, R. F. Christner, J. E. Buhler, and A. S. Aragon. 1993. Acid phosphatase activity in Coxiella burnetii: a possible virulence factor. Infect. Immun. 61:4232-4239.
2. phox. J. Immunol. 164:3946-3949.
3. Bios, M., U. Schleicher, F. J. Soares Rocha, U. Meissner, M. Rollinghoff, and C. Bogdan. 2003. Organ-specific and stage-dependent control of Leishmania major infection by inducible nitric oxide synthase and phagocyte NADPH oxidase. Eur. J. Immunol. 33:1224-1234.
4. Brandonisio, O., M. A. Panaro, R. Marzio, A. Marangi, S. M. Faliero, and E. Jirillo. 1994. Impairment of the human phagocyte oxidative responses caused by Leishmania lipophosphoglycan (LPG): in vitro studies. FEMS Immunol. Med. Microbiol. 8:57-62.
5. Burritt, J. B., M. T. Quinn, M. A. Jutila, C. W. Bond, and A. J. Jesaitis. 1995. Topological mapping of neutrophil cytochrome b epitopes with phage-display libraries. J. Biol. Chem. 270:16974-16980.
6. Burritt, J. B., T. R. Foubert, D. Baniulis, C. I. Lord, R. M. Taylor, J. S. Mills, T. D. Baughan, D. Roos, C. A. Parkos, and A. J. Jesaitis. 2003. Functional epitope on human neutrophil flavocytochrome b558. J. Immunol. 170:6082-6089.
7. Carlyon, J. A., D. Abdel-Latif, M. Pypaert, P. Lacy, and E. Fikrig. 2004. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect. Immun. 72:4772-4783.
8. Chakraborty, P, S. Sturgill-Koszvcki, D. G. Russell. 1994. Isolation and characterization of pathogen-containing phagosomes. Methods Cell Biol. 45:261-276.
9. Chang, C. S., and K. P. Chang. 1985. Heme requirement and acquisition by extracellular and intracellular stages of Leishmania mexicana amazonensis. Mol. Biochem. Parasitol. 16:267-276.
10. Channon, J. Y., M. B, Roberts, J. M. Blackwell. 1984. A study of the differential respiratory burst activity elicited by promastigotes and amastigotes of Leishmania donovani in murine resident peritoneal macrophages. Immunology 53:345-355.
11. Chauveau, C., S. Remy, P. J. Royer, M. Hill, S. Tanguy-Royer, F. X. Hubert, L, Tesson, R. Brion, G. Beriou, M. Gregoire, R. Josien, M. C. Cuturi, and I. Anegon. 2005. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106:1694-1702. (First published 26 May 2005; doi:10.1182/blood-2005-02-0494.)
12. Crapo, J. D., T. Oury, C. Rabouille, J. W. Slot, and L.-Y. Chang. 1992. Copper, zinc superoxide dismutase is primarily a cytosolic protein in human cells. Proc. Natl. Acad. Sci. USA 89:10405-10409.
13. Da Silva, R. P., B. F. Hall, K. A. Joiner, and D. L. Sacks. 1989. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J. Immunol. 143:617-622.
14. Debrabant, A., M. B. Joshi, P. F. Pimenta, and D. M. Dwyer. 2004. Generation of Leishmania donovani axenic amastigotes: their growth and biological characteristics. Int. J. Parasitol. 34:205-217.
15. DeLeo, F. R., J. B. Burritt, L. Yu, A. J. Jesaitis, M. C. Dinauer, and W. M. Nauseef. 2000. Processing and maturation of flavocytochrome b558 include incorporation of heme as a prerequisite for heterodimer assembly. J. Biol. Chem. 275:13986-13993.
16. Descoteaux, A., and S. J. Turco. 1993. The lipophosphoglycan of Leishmania and macrophage protein kinase C. Parasitol. Today 9:468-471.
17. Ewing, J. F., S. N. Haber, and M. D. Maines. 1992. Normal and heat-induced patterns of expression of heme oxygenase-1 (HSP32) in rat brain: hyperthermia causes rapid induction of mRNA and protein. J. Neurochem. 58:4023-4029.
18. Gantt, K. R., T. L. Goldman, M. A. Miller, M. L. McCormick, S. M. B. Jeronimo, E. T. Nascimento, B. E. Britigan, and M. E. Wilson. 2001. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J. Immunol. 167:893-901.
19. Haidaris, C. G., and P. F. Bonventre. 1982. A role for oxygen-dependent mechanisms in killing of Leishmania donovani tissue forms by activated macrophages. J. Immunol. 129:850-855.
20. Ip, S., M. Chung, J. Kulig, R. O'Brien, R. Sege, S. Glicken, M. J. Maisels, and J. Lau. 2004 An evidence-based review of important issues concerning neonatal hyperbilirubinemia. Pediatrics 114:e130-e153.
21. Kantengwa, S., I. Muller, J. Louis, and B. S. Polla. 1995. Infection of human and murine macrophages with Leishmania major is associated with early parasite heat shock protein synthesis but fails to induce a host cell stress response. Immunol. Cell Biol. 73:73-80.
22. Kappas, A., and G. S. Drummond. 1985. Metalloporphyrins: a class of compounds of pharmacological interests. BioEssays 3:256-259.
23. Kima, P. E., and W. Dunn. 2005. Exploiting calnexin expression on phagosomes to isolate Leishmania parasitophorous vacuoles. Microb. Pathog. 38: 139-145.
24. Maines, M. D. 1981. Zinc-protoporphyrin is a selective inhibitor of heme oxygenase activity in the neonatal rat. Biochim. Biophys. Acta 673:339-350.
25. Maines, M. D. 1997. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37:517-554.
26. Mallinson, D. J., and G. H. Coombs. 1989. Interaction of Leishmania metacyclics with macrophages. Int. J. Parasitol. 19:647-656.
27. McMahon-Pratt, D., and J. Alexander. 2004. Does the Leishmania major paradigm of pathogenesis and protection hold for New World cutaneous leishmaniasis or the visceral disease? Immunol. Rev. 201:206-224.
28. Mott, J., and Y. Rikihisa. 2000. Human granulocytic ehrlichiosis agent inhibits superoxide anion generation by human neutrophils. Infect. Immun. 68:6697-6703.
29. Mott, J., Y. Rikihisa, and S. Tsunawaki. 2002. Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect. Immun. 70:1359-1366.
30. Murray, H. W., and C. F. Nathan. 1999. Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. J. Exp. Med. 189:741-746.
31. Nauseef, W. M. 2004. Assembly of the phagocyte NADPH oxidase. Histochem. Cell Biol. 122:277-291.
32. Passwell, J. H., R. Shor, J. Smolen, and C. L. Jaffe. 1994. Infection of human monocytes by Leishmania results in a defective oxidative burst. Int. J. Exp. Pathol. 75:277-284.
33. Reiner, N. E., and J. W. Kazura. 1982. Oxidant-mediated damage of Leishmania donovani promastigotes. Infect. Immun. 36:1023-1027.
34. Soong, L., S. M. Duboise, P. Kima, and D. McMahon-Pratt. 1995. Leishmania pifanoi amastigote antigens protect mice against cutaneous leishmaniasis. Infect. Immun. 63:3559-3566.
35. Srivastava, P., G. D. Sharma, K. K. Kamboj, A. K. Rastogi, and W. C. Pandey. 1997. Heme metabolism in promastigoies of Leishmania donovani. Mol. Cell. Biochem. 171:65-68.
36. Taille, C., J. El-Benna, S. Lanone, M. C. Dang, E. Ogier-Denis, M. Aubier, and J. Boczkowski. 2004. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J. Biol. Chem. 279:28681-28688.
37. Tan, A. S., and M. V. Berridge. 2000. Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: a simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents. J. Immunol. Methods 238:59-68.
38. 2. Infect. Immun. 57:1108-1112.
39. phox gene expression through altered interferon regulatory factor 1 and PU.1 levels and binding of CCAAT displacement protein. Infect. Immun. 73:208-218.
40. Uchmuller-Rouiller, Y., and J. Mauel. 1987. Impairment of the oxidative metabolism of mouse peritoneal macrophages by intracellular Leishmania spp. Infect. Immun. 55:587-593.
41. Visser, L. G., E. Seijmonsbergen, P. H. Nibbering, P. J. van den Broek, and R. van Furth. 1999. Yops of Yersinia enterocolitica inhibit receptor-dependent superoxide anion production by human granulocytes. Infect. Immun. 67:1245-1250.
42. Vouldoukis, I., P.-A. Becherel, V. Riveros-Moreno, M. Arock, O. da Silva, P. Debre, D. Mazier, and M. D. Mossalayi. 1997. Interleukin-10 and interleukin-4 inhibit intracellular killing of Leishmania infantum and Leishmania major by human macrophages by decreasing nitric oxide generation. Eur. J. Immunol. 27:860-865.
43. Yu, L., F. R. DeLeo, K. J. Biberstine-Kinfcade, J. Renee, W. M. Nauseef, and M. C. Dinauer. 1999. Biosynthesis of flavocytochrome b558. gp91(phox) is synthesized as a 65-kDa precursor (p65) in the endoplasmic reticulum. J. Biol. Chem. 274:4364-4369.
44. Yu, L., L. Zhen, and M. C. Dinnauer. 1997. Biosynthesis of the phagocyte NADPH oxidase cytochrome b558. J. Biol. Chem. 272:27288-27294.