Heme oxygenase-1 promotes the persistence of Leishmania chagasi infection

Journal of Immunology

Volumn 188, Issue 9, 2012, Pages 4460-4467

  Luz, Nívea F ^a,b   Andrade, Bruno B ^c   Feijó, Daniel F ^d   Araújo Santos, Théo ^a,b   Carvalho, Graziele Q ^a,b   Andrade, Daniela ^a,b   Abánades, Daniel R ^a,b   Melo, Enaldo V ^e   Silva, Angela M ^e   Brodskyn, Cláudia I ^a,b,f   Barral Netto, Manoel ^a,b,f   Barral, Aldina ^a,b,f   Soares, Rodrigo P ^a   Almeida, Roque P ^e,f   Bozza, Marcelo T ^d   Borges, Valéria M ^a,b,f  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF BAHIA   (Brazil)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^e FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^f Instituto Nacional de Ciência e Tecnologia INCT em Imunologia III   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

COBALT; COPPER ZINC SUPEROXIDE DISMUTASE; HEME OXYGENASE 1; LIPOPHOSPHOGLYCAN; PROTOPORPHYRIN COBALT; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BRAZIL; CELL STRESS; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE CONTROL; DISEASE PREDISPOSITION; ENZYME SYNTHESIS; FEMALE; LEISHMANIA CHAGASI; LEISHMANIA INFANTUM; LEISHMANIASIS; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; PROMASTIGOTE; UPREGULATION; VISCERAL LEISHMANIASIS; WILD TYPE;

ANIMALS; BRAZIL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOSPHINGOLIPIDS; HEME OXYGENASE-1; HUMANS; LEISHMANIA; LEISHMANIASIS, VISCERAL; MACROPHAGES, PERITONEAL; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, SCID; PHOTOSENSITIZING AGENTS; PROTOPORPHYRINS; UP-REGULATION;

EID: 84860330759     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103072     Document Type: Article

References (67)

1. Saha, S., S. Mondal, A. Banerjee, J. Ghose, S. Bhowmick, and N. Ali. 2006. Immune responses in kala-azar. Indian J. Med. Res. 123: 245-266. (Pubitemid 43905567)
2. Caldas, A., C. Favali, D. Aquino, V. Vinhas, J. van Weyenbergh, C. Brodskyn, J. Costa, M. Barral-Netto, and A. Barral. 2005. Balance of IL-10 and interferon-gamma plasma levels in human visceral leishmaniasis: implications in the pathogenesis. BMC Infect. Dis. 5: 113.
3. Chappuis, F., S. Sundar, A. Hailu, H. Ghalib, S. Rijal, R. W. Peeling, J. Alvar, and M. Boelaert. 2007. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat. Rev. Microbiol. 5: 873-882. (Pubitemid 47578388)
4. Olivier, M., D. J. Gregory, and G. Forget. 2005. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin. Microbiol. Rev. 18: 293-305. (Pubitemid 40548295)
5. Gantt, K. R., T. L. Goldman, M. L. McCormick, M. A. Miller, S. M. 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. (Pubitemid 32660845)
6. Becker, I., N. Salaiza, M. Aguirre, J. Delgado, N. Carrillo-Carrasco, L. G. Kobeh, A. Ruiz, R. Cervantes, A. P. Torres, N. Cabrera, et al. 2003. Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol. Biochem. Parasitol. 130: 65-74. (Pubitemid 37289124)
7. de Veer, M. J., J. M. Curtis, T. M. Baldwin, J. A. DiDonato, A. Sexton, M. J. McConville, E. Handman, and L. Schofield. 2003. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Tolllike receptor 2 signaling. Eur. J. Immunol. 33: 2822-2831. (Pubitemid 37337148)
8. Bogdan, C., and M. Rollinghoff. 1999. How do protozoan parasites survive inside macrophages? Parasitol. Today 15: 22-28. (Pubitemid 29246041)
9. Dermine, J. F., S. Scianimanico, C. Prive, A. Descoteaux, and M. Desjardins. 2000. Leishmania promastigotes require lipophosphoglycan to actively modulate the fusion properties of phagosomes at an early step of phagocytosis. Cell. Microbiol. 2: 115-126. (Pubitemid 30368026)
10. Brittingham, A., and D. M. Mosser. 1996. Exploitation of the complement system by Leishmania promastigotes. Parasitol. Today 12: 444-447. (Pubitemid 26353795)
11. Proudfoot, L., A. V. Nikolaev, G. J. Feng, W. Q. Wei, M. A. Ferguson, J. S. Brimacombe, and F. Y. Liew. 1996. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc. Natl. Acad. Sci. USA 93: 10984-10989. (Pubitemid 26333104)
12. Piedrafita, D., L. Proudfoot, A. V. Nikolaev, D. Xu, W. Sands, G. J. Feng, E. Thomas, J. Brewer, M. A. Ferguson, J. Alexander, and F. Y. Liew. 1999. Regulation of macrophage IL-12 synthesis by Leishmania phosphoglycans. Eur. J. Immunol. 29: 235-244. (Pubitemid 29043541)
13. Coelho-Finamore, J. M., V. C. Freitas, R. R. Assis, M. N. Melo, N. Novozhilova, N. F. Secundino, P. F. Pimenta, S. J. Turco, and R. P. Soares. 2011. Leishmania infantum: Lipophosphoglycan intraspecific variation and interaction with vertebrate and invertebrate hosts. Int. J. Parasitol. 41: 333-342.
14. Giorgione, J. R., S. J. Turco, and R. M. Epand. 1996. Transbilayer inhibition of protein kinase C by the lipophosphoglycan from Leishmania donovani. Proc. Natl. Acad. Sci. USA 93: 11634-11639. (Pubitemid 26347174)
15. Guimaraes-Costa, A. B., M. T. Nascimento, G. S. Froment, R. P. Soares, F. N. Morgado, F. Conceicao-Silva, and E. M. Saraiva. 2009. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc. Natl. Acad. Sci. USA 106: 6748-6753.
16. Vivarini Ade, C., M. Pereira Rde, K. L. Teixeira, T. C. Calegari-Silva, M. Bellio, M. D. Laurenti, C. E. Corbett, C. M. Gomes, R. P. Soares, A. M. Silva, et al. 2011. Human cutaneous leishmaniasis: interferon-dependent expression of double-stranded RNA-dependent protein kinase (PKR) via TLR2. FASEB J. 25: 4162-4173.
17. Andrade, B. B., T. Araujo-Santos, N. F. Luz, R. Khouri, M. T. Bozza, L. M. Camargo, A. Barral, V. M. Borges, and M. Barral-Netto. 2010. Heme impairs prostaglandin E2 and TGF-beta production by human mononuclear cells via Cu/Zn superoxide dismutase: insight into the pathogenesis of severe malaria. J. Immunol. 185: 1196-1204.
18. Tenhunen, R., H. S. Marver, and R. Schmid. 1968. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl. Acad. Sci. USA 61: 748-755.
19. Soares, M. P., I. Marguti, A. Cunha, and R. Larsen. 2009. Immunoregulatory effects of HO-1: how does it work? Curr. Opin. Pharmacol. 9: 482-489.
20. Pamplona, A., A. Ferreira, J. Balla, V. Jeney, G. Balla, S. Epiphanio, A. Chora, C. D. Rodrigues, I. P. Gregoire, M. Cunha-Rodrigues, et al. 2007. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat. Med. 13: 703-710. (Pubitemid 46889755)
21. Seixas, E., R. Gozzelino, A. Chora, A. Ferreira, G. Silva, R. Larsen, S. Rebelo, C. Penido, N. R. Smith, A. Coutinho, and M. P. Soares. 2009. Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proc. Natl. Acad. Sci. USA 106: 15837-15842.
22. Shen, X. D., B. Ke, Y. Zhai, F. Gao, R. W. Busuttil, G. Cheng, and J. W. Kupiec-Weglinski. 2005. Toll-like receptor and heme oxygenase-1 signaling in hepatic ischemia/reperfusion injury. Am. J. Transplant. 5: 1793-1800. (Pubitemid 41039851)
23. Zenclussen, M. L., P. A. Casalis, T. El-Mousleh, S. Rebelo, S. Langwisch, N. Linzke, H. D. Volk, S. Fest, M. P. Soares, and A. C. Zenclussen. 2011. Haem oxygenase-1 dictates intrauterine fetal survival in mice via carbon monoxide. J. Pathol. 225: 293-304.
24. Chung, S. W., X. Liu, A. A. Macias, R. M. Baron, and M. A. Perrella. 2008. Heme oxygenase-1-derived carbon monoxide enhances the host defense response to microbial sepsis in mice. J. Clin. Invest. 118: 239-247.
25. Larsen, R., R. Gozzelino, V. Jeney, L. Tokaji, F. A. Bozza, A. M. Japiassu, D. Bonaparte, M. M. Cavalcante, A. Chora, A. Ferreira, et al. 2010. A central role for free heme in the pathogenesis of severe sepsis. Science Transl. Med. 2: 51ra71.
26. Ke, B., R. Buelow, X. D. Shen, J. Melinek, F. Amersi, F. Gao, T. Ritter, H. D. Volk, R. W. Busuttil, and J. W. Kupiec-Weglinski. 2002. Heme oxygenase 1 gene transfer prevents CD95/Fas ligand-mediated apoptosis and improves liver allograft survival via carbon monoxide signaling pathway. Hum. Gene Ther. 13: 1189-1199. (Pubitemid 34746699)
27. Camara, N. O., and M. P. Soares. 2005. Heme oxygenase-1 (HO-1), a protective gene that prevents chronic graft dysfunction. Free Radic. Biol. Med. 38: 426-435. (Pubitemid 40247434)
28. Nath, K. A., J. P. Grande, J. J. Haggard, A. J. Croatt, Z. S. Katusic, A. Solovey, and R. P. Hebbel. 2001. Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease. Am. J. Pathol. 158: 893-903. (Pubitemid 32221782)
29. Chung, S. W., S. R. Hall, and M. A. Perrella. 2009. Role of haem oxygenase-1 in microbial host defence. Cell. Microbiol. 11: 199-207.
30. Epiphanio, S., S. A. Mikolajczak, L. A. Goncalves, A. Pamplona, S. Portugal, S. Albuquerque, M. Goldberg, S. Rebelo, D. G. Anderson, A. Akinc, et al. 2008. Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine plasmodium liver infection. Cell Host Microbe 3: 331-338. (Pubitemid 351635999)
31. Pham, N. K., J. Mouriz, and P. E. Kima. 2005. Leishmania pifanoi amastigotes avoid macrophage production of superoxide by inducing heme degradation. Infect. Immun. 73: 8322-8333. (Pubitemid 41740323)
32. Maines, M. D., and A. Kappas. 1975. Cobalt stimulation of heme degradation in the liver. Dissociation of microsomal oxidation of heme from cytochrome P-450. J. Biol. Chem. 250: 4171-4177.
33. Gomes, N. A., C. R. Gattass, V. Barreto-De-Souza, M. E. Wilson, and G. A. DosReis. 2000. TGF-beta mediates CTLA-4 suppression of cellular immunity in murine kalaazar. J. Immunol. 164: 2001-2008. (Pubitemid 30108756)
34. Saltzman, B. E. 1954. Colorimetric microdetermination of nitrogen dioxide in the atmosphere. Anal. Chem. 26: 1949-1955.
35. Khouri, R., A. Bafica, P. Silva Mda, A. Noronha, J. P. Kolb, J. Wietzerbin, A. Barral, M. Barral-Netto, and J. Van Weyenbergh. 2009. IFN-beta impairs superoxide-dependent parasite killing in human macrophages: evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. J. Immunol. 182: 2525-2531.
36. Shiloh, M. U., P. Manzanillo, and J. S. Cox. 2008. Mycobacterium tuberculosis senses host-derived carbon monoxide during macrophage infection. Cell Host Microbe 3: 323-330. (Pubitemid 351635997)
37. Murray, H. W. 1982. Cell-mediated immune response in experimental visceral leishmaniasis. II. Oxygen-dependent killing of intracellular Leishmania donovani amastigotes. J. Immunol. 129: 351-357. (Pubitemid 12080715)
38. Novais, F. O., R. C. Santiago, A. Bafica, R. Khouri, L. Afonso, V. M. Borges, C. Brodskyn, M. Barral-Netto, A. Barral, and C. I. de Oliveira. 2009. Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. J. Immunol. 183: 8088-8098.
39. Liew, F. Y., S. Millott, C. Parkinson, R. M. Palmer, and S. Moncada. 1990. Macrophage killing of Leishmania parasite in vivo is mediated by nitric oxide from L-arginine. J. Immunol. 144: 4794-4797. (Pubitemid 20224118)
40. Turco, S. J., G. F. Spath, and S. M. Beverley. 2001. Is lipophosphoglycan a virulence factor? A surprising diversity between Leishmania species. Trends Parasitol. 17: 223-226. (Pubitemid 32422166)
41. Spath, G. F., L. Epstein, B. Leader, S. M. Singer, H. A. Avila, S. J. Turco, and S. M. Beverley. 2000. Lipophosphoglycan is a virulence factor distinct from related glycoconjugates in the protozoan parasite Leishmania major. Proc. Natl. Acad. Sci. USA 97: 9258-9263. (Pubitemid 30626706)
42. Kronke, G., A. Kadl, E. Ikonomu, S. Bluml, A. Furnkranz, I. J. Sarembock, V. N. Bochkov, M. Exner, B. R. Binder, and N. Leitinger. 2007. Expression of heme oxygenase-1 in human vascular cells is regulated by peroxisome proliferator-activated receptors. Arterioscler. Thromb. Vasc. Biol. 27: 1276-1282. (Pubitemid 46809415)
43. Adapala, N., and M. M. Chan. 2008. Long-term use of an antiinflammatory, curcumin, suppressed type 1 immunity and exacerbated visceral leishmaniasis in a chronic experimental model. Lab. Invest. 88: 1329-1339.
44. Turkseven, S., A. Kruger, C. J. Mingone, P. Kaminski, M. Inaba, L. F. Rodella, S. Ikehara, M. S. Wolin, and N. G. Abraham. 2005. Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am. J. Physiol. Heart Circ. Physiol. 289: H701-H707. (Pubitemid 41129386)
45. Ahmad, M., X. Zhao, M. R. Kelly, S. Kandhi, O. Perez, N. G. Abraham, and M. S. Wolin. 2009. Heme oxygenase-1 induction modulates hypoxic pulmonary vasoconstriction through upregulation of ecSOD. Am. J. Physiol. Heart Circ. Physiol. 297: H1453-H1461.
46. Nylén, S., and D. Sacks. 2007. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol. 28: 378-384. (Pubitemid 47385375)
47. Ansari, N. A., R. Kumar, S. Gautam, S. Nylen, O. P. Singh, S. Sundar, and D. Sacks. 2011. IL-27 and IL-21 are associated with T cell IL-10 responses in human visceral leishmaniasis. J. Immunol. 186: 3977-3985.
48. Gozzelino, R., V. Jeney, and M. P. Soares. 2010. Mechanisms of cell protection by heme oxygenase-1. Annu. Rev. Pharmacol. Toxicol. 50: 323-354.
49. Ryter, S. W., and R. M. Tyrrell. 2000. The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 28: 289-309. (Pubitemid 30084022)
50. Pae, H. O., and H. T. Chung. 2009. Heme oxygenase-1: its therapeutic roles in inflammatory diseases. Immune Network 9: 12-19.
51. Schneider, D. S., and J. S. Ayres. 2008. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat. Rev. Immunol. 8: 889-895.
52. Ryter, S. W., L. E. Otterbein, D. Morse, and A. M. Choi. 2002. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol. Cell. Biochem. 234-235: 249-263. (Pubitemid 34777864)
53. Seldon, M. P., G. Silva, N. Pejanovic, R. Larsen, I. P. Gregoire, J. Filipe, J. Anrather, and M. P. Soares. 2007. Heme oxygenase-1 inhibits the expression of adhesion molecules associated with endothelial cell activation via inhibition of NF-kappaB RelA phosphorylation at serine 276. J. Immunol. 179: 7840-7851.
54. Wagener, F. A., H. D. Volk, D. Willis, N. G. Abraham, M. P. Soares, G. J. Adema, and C. G. Figdor. 2003. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol. Rev. 55: 551-571. (Pubitemid 37013215)
55. Lodge, R., T. O. Diallo, and A. Descoteaux. 2006. Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane. Cell. Microbiol. 8: 1922-1931. (Pubitemid 44687332)
56. Odegaard, J. I., R. R. Ricardo-Gonzalez, M. H. Goforth, C. R. Morel, V. Subramanian, L. Mukundan, A. Red Eagle, D. Vats, F. Brombacher, A. W. Ferrante, and A. Chawla. 2007. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447: 1116-1120. (Pubitemid 47014427)
57. Green, S. J., R. M. Crawford, J. T. Hockmeyer, M. S. Meltzer, and C. A. Nacy. 1990. Leishmania major amastigotes initiate the L-arginine-dependent killing mechanism in IFN-gamma-stimulated macrophages by induction of tumor necrosis factor-alpha. J. Immunol. 145: 4290-4297.
58. Engwerda, C. R., M. Ato, S. Stager, C. E. Alexander, A. C. Stanley, and P. M. Kaye. 2004. Distinct roles for lymphotoxin-alpha and tumor necrosis factor in the control of Leishmania donovani infection. Am. J. Pathol. 165: 2123-2133. (Pubitemid 39578389)
59. Barral-Netto, M., R. Badaro, A. Barral, R. P. Almeida, S. B. Santos, F. Badaro, D. Pedral-Sampaio, E. M. Carvalho, E. Falcoff, and R. Falcoff. 1991. Tumor necrosis factor (cachectin) in human visceral leishmaniasis. J. Infect. Dis. 163: 853-857.
60. Peruhype-Magalhaes, V., O. A. Martins-Filho, A. Prata, A. Silva Lde, A. Rabello, A. Teixeira-Carvalho, R. M. Figueiredo, S. F. Guimaraes-Carvalho, T. C. Ferrari, J. Van Weyenbergh, and R. Correa-Oliveira. 2006. Mixed inflammatory/regulatory cytokine profile marked by simultaneous raise of interferon-gamma and interleukin-10 and low frequency of tumour necrosis factor-alpha(+) monocytes are hallmarks of active human visceral Leishmaniasis due to Leishmania chagasi infection. Clin. Exp. Immunol. 146: 124-132. (Pubitemid 44393847)
61. Santos-Oliveira, J. R., E. G. Regis, C. R. B. Leal, R. V. Cunha, P. T. Bozza, and A. M. Da-Cruz. 2011. Evidence That Lipopolisaccharide May Contribute to the Cytokine Storm and Cellular Activation in Patients with Visceral Leishmaniasis. PLoS Negl. Trop. Dis. 5: e1198.
62. Yoshinaga, T., S. Sassa, and A. Kappas. 1982. The oxidative degradation of heme c by the microsomal heme oxygenase system. J. Biol. Chem. 257: 7803-7807.
63. Chen, T., Z. P. Guo, Y. H. Zhang, Y. Gao, H. J. Liu, and J. Y. Li. 2009. Elevated serum heme oxygenase-1 and insulin-like growth factor-1 levels in patients with Henoch-Schonlein purpura. Rheumatol. Int. 31: 321-326.
64. Kirino, Y., M. Takeno, M. Iwasaki, A. Ueda, S. Ohno, A. Shirai, H. Kanamori, K. Tanaka, and Y. Ishigatsubo. 2005. Increased serum HO-1 in hemophagocytic syndrome and adult-onset Still's disease: use in the differential diagnosis of hyperferritinemia. Arthritis Res. Ther. 7: R616-R624.
65. Miyazaki, T., Y. Kirino, M. Takeno, M. Hama, A. Ushihama, R. Watanabe, K. Takase, T. Tachibana, K. Matsumoto, M. Tanaka, et al. 2010. Serum HO-1 is useful to make differential diagnosis of secondary hemophagocytic syndrome from other similar hematological conditions. Int. J. Hematol. 91: 229-237.
66. Bao, W., F. Song, X. Li, S. Rong, W. Yang, M. Zhang, P. Yao, L. Hao, N. Yang, F. B. Hu, and L. Liu. 2010. Plasma Heme Oxygenase-1 Concentration Is Elevated in Individuals with Type 2 Diabetes Mellitus. PLoS ONE 5: e12371.
67. Blann, A. D., B. Balakrishnan, P. Ryan, and G. Y. Lip. 2011. Increased levels of plasma haemoxygenase-1 in prostate cancer. Prostate Cancer Prostatic Dis. 14: 114-117.