Reduced nitric oxide synthase 2 (NOS2) promoter activity in the Syrian hamster renders the animal functionally deficient in NOS2 activity and unable to control an intracellular pathogen

Journal of Immunology

Volumn 176, Issue 9, 2006, Pages 5519-5528

  Perez, Luis E ^a,b   Chandrasekar, Bysani ^a,b   Saldarriaga, Omar A ^b,c   Zhao, Weiguo ^a,b   Arteaga, Lourdes T ^a,b   Travi, Bruno L ^d   Melby, Peter C ^a,b,c,e  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d CENTRO INTERNACIONAL DE ENTRENAMIENTO E INVESTIGACIONES MÉDICAS CIDEIM   (Colombia)

^e SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRIC OXIDE;

ADOLESCENT; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENE; GENE ACTIVITY; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; INFECTION CONTROL; LEISHMANIA DONOVANI; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; NOS2 GENE; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORTHOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; SYRIAN HAMSTER; VISCERAL LEISHMANIASIS;

EID: 33645960117     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.9.5519     Document Type: Article

References (51)

1. 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.
2. Squires, K. E., R. D. Schreiber, M. J. McElrath, B. Y. Rubin, S. L. Anderson, and H. W. Murray. 1989. Experimental visceral leishmaniasis: role of endogenous IFN-γ in host defense and tissue granulomatous response. J. Immunol. 143: 4244-4249.
3. + cells in experimental visceral leishmaniasis. J. Immunol. 140: 3971-3977.
4. Melby, P. C., B. Chandrasekar, W. Zhao, and J. E. Coe. 2001. The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like response. J. Immunol. 166: 1912-1920.
5. Kenney, R. T., D. L. Sacks, A. A. Gam, H. W. Murray, and S. Sundar. 1998. Splenic cytokine responses in Indian kala-azar before and after treatment. J. Infect. Dis. 177: 815-818.
6. Karp, C. L., S. H. el-Safi, T. A. Wynn, M. M. Satti, A. M. Kordofani, F. A. Hashim, M. Hag-Ali, F. A. Neva, T. B. Nutman, and D. L. Sacks. 1993. In vivo cytokine profiles in patients with kala-azar: marked elevation of both interleukin-10 and interferon-γ. J. Clin. Invest. 91: 1644-1648.
7. Wei, X. Q., I. G. Charles, A. Smith, J. Ure, G. J. Feng, F. P. Huang, D. Xu, W. Muller, S. Moncada, and F. Y. Liew. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375: 408-411.
8. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15: 323-350.
9. Green, S. J., M. S. Meltzer, J. B. Hibbs, Jr., and C. A. Nacy. 1990. Activated macrophages destroy intracellular Leishmania major amastigotes by an L-arginine-dependent killing mechanism. J. Immunol. 144: 278-283.
10. 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.
11. Liew, F. Y., Y. Li, D. Moss, C. Parkinson, M. V. Rogers, and S. Moncada. 1991. Resistance to Leishmania major infection correlates with the induction of nitric oxide synthase in murine macrophages. Eur. J. Immunol. 21: 3009-3014.
12. Stenger, S., H. Thuring, M. Rollinghoff, and C. Bogdan. 1994. Tissue expression of inducible nitric oxide synthase is closely associated with resistance to Leishmania major. J. Exp. Med. 180: 783-793.
13. Stenger, S., N. Donhauser, H. Thuring, M. Rollinghoff, and C. Bogdan. 1996. Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J. Exp. Med. 183: 1501-1514.
14. Bories, C., C. Coffin, D. Mathieu, P. N. Bones, E. Scherman, D. Rivollet, and M. Deniau. 1998. Lack of a nitric-oxide response during the course of Leishmania infantum infection in the golden hamster (Mesocricetus auratus), with or without treatment with liposomal amphotericin B. Ann. Trop. Med. Parasitol. 92: 685-692.
15. Dasgupta, S., A. Mookerjee, S. K. Chowdhury, and A. C. Ghose. 1999. Immunosuppression in hamsters with progressive visceral leishmaniasis: an evaluation of the role of nitric oxide toward impairment of the lymphoproliferative response. Parasitol. Res. 85: 594-596.
16. Denis, M. 1994. Human monocytes/macrophages: NO or NO? J. Leukocyte Biol. 55: 682-684.
17. Schneemann, M., G. Schoedon, S. Hofer, N. Blau, L. Guerrero, and A. Schaffner. 1993. Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J. Infect. Dis. 167: 1358-1363.
18. Padgett, E. L., and S. B. Pruett. 1992. Evaluation of nitrite production by human monocyte-derived macrophages. Biochem. Biophys. Res. Commun. 186: 775-781.
19. Chu, S. C., J. Marks-Konczalik, H. P. Wu, T. C. Banks, and J. Moss. 1998. Analysis of the cytokine-stimulated human inducible nitric oxide synthase (iNOS) gene: characterization of differences between human and mouse iNOS promoters. Biochem. Biophys. Res. Commun. 248: 871-878.
20. 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.
21. Lowenstein, C. J., E. W. Alley, P. Raval, A. M. Snowman, S. H. Snyder, S. W. Russell, and W. J. Murphy. 1993. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon γ and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 90: 9730-9734.
22. Zhang, X., V. E. Laubach, E. W. Alley, K. A. Edwards, P. A. Sherman, S. W. Russell, and W. J. Murphy. 1996. Transcriptional basis for hyporesponsiveness of the human inducible nitric oxide synthase gene to lipopolysaccharide/ interferon-γ. J. Leukocyte Biol. 59: 575-585.
23. McDowell, M. A., D. M. Lucas, C. M. Nicolet, and D. M. Paulnock. 1995. Differential utilization of IFN-γ-responsive elements in two maturationally distinct macrophage cell lines. J. Immunol. 155: 4933-4938.
24. Taylor, B. S., M. E. de Vera, R. W. Ganster, Q. Wang, R. A. Shapiro, S. M. Morris, Jr., T. R. Billiar, and D. A. Geller. 1998. Multiple NF-κB enhancer elements regulate cytokine induction of the human inducible nitric oxide synthase gene. J. Biol. Chem. 273: 15148-15156.
25. Xie, Q. W., R. Whisnant, and C. Nathan. 1993. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon γ and bacterial lipopolysaccharide. J. Exp. Med. 177: 1779-1784.
26. Gao, J., D. C. Morrison, T. J. Parmely, S. W. Russell, and W. J. Murphy. 1997. An interferon-γ-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-γ and lipopolysaccharide. J. Biol. Chem. 272: 1226-1230.
27. Sacks, D., and P. Melby. 1998. Animal models for the analysis of immune responses to leishmaniasis. In Current Protocols in Immunology. J. Coligan, A. Kruisbeek, D. Margulies, E. Shevach, and W. Strober, eds. John Wiley and Sons, New York, pp. 19.12.11-19.12.20.
28. Melby, P. C., V. V. Tryon, B. Chandrasekar, and G. L. Freeman. 1998. Cloning of Syrian hamster (Mesocricetus auratus) cytokine cDNAs and analysis of cytokine mRNA expression in experimental visceral leishmaniasis. Infect. Immun. 66: 2135-2142.
29. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
30. + CXC chemokine LIX (CXCL5) amplifies a proinflammatory cytokine response via a phosphatidylinositol 3-kinase-NF-κB pathway. J. Biol. Chem. 278: 4675-4686.
31. Chandrasekar, B., J. E. Streitman, J. T. Colston, and G. L. Freeman. 1998. Inhibition of nuclear factor kappa B attenuates proinflammatory cytokine and inducible nitric-oxide synthase expression in postischemic myocardium. Biochim. Biophys. Acta 1406: 91-106.
32. Boehm, U., T. Klamp, M. Groot, and J. C. Howard. 1997. Cellular responses to interferon-γ. Annu. Rev. Immunol. 15: 749-795.
33. Taylor, A. P., and H. W. Murray. 1998. Therapeutic effect of interferon-γ gene transfer in experimental visceral leishmaniasis. J. Infect. Dis. 178: 908-911.
34. + effector cells default to the Th2 pathway in interferon γ-deficient mice infected with Leishmania major. J. Exp. Med. 179: 1367-1371.
35. Martin, E., C. Nathan, and Q. W. Xie. 1994. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp. Med. 180: 977-984.
36. Xie, Q. W., Y. Kashiwabara, and C. Nathan. 1994. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269: 4705-4708.
37. Weinberg, J. B., M. A. Misukonis, P. J. Shami, S. N. Mason, D. L. Sauls, W. A. Dittman, E. R. Wood, G. K. Smith, B. McDonald, K. E. Bachus, et al. 1995. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood 86: 1184-1195.
38. Geller, D. A., C. J. Lowenstein, R. A. Shapiro, A. K. Nussler, M. Di Silvio, S. C. Wang, D. K. Nakayama, R. L. Simmons, S. H. Snyder, and T. R. Billiar. 1993. Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc. Natl. Acad. Sci. USA 90: 3491-3495.
39. Geller, D. A., A. K. Nussler, M. Di Silvio, C. J. Lowenstein, R. A. Shapiro, S. C. Wang, R. L. Simmons, and T. R. Billiar. 1993. Cytokines, endotoxin, and glucocorticoids regulate the expression of inducible nitric oxide synthase in hepatocytes. Proc. Natl. Acad. Sci. USA 90: 522-526.
40. 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.
41. Lohoff, M., D. Ferrick, H. W. Mittrucker, G. S. Duncan, S. Bischof, M. Rollinghoff, and T. W. Mak. 1997. Interferon regulatory factor-1 is required for a T helper 1 immune response in vivo. Immunity 6: 681-689.
42. + T cell response. J. Exp. Med. 181: 961-971.
43. Taylor, A. P., and H. W. Murray. 1997. Intracellular antimicrobial activity in the absence of interferon-γ: effect of interleukin-12 in experimental visceral leishmaniasis in interferon-γ gene-disrupted mice. J. Exp. Med. 185: 1231-1239.
44. Marks-Konczalik, J., S. C. Chu, and J. Moss. 1998. Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor κB-binding sites. J. Biol. Chem. 273: 22201-22208.
45. de Vera, M. E., R. A. Shapiro, A. K. Nussler, J. S. Mudgett, R. L. Simmons, S. M. Morris, Jr., T. R. Billiar, and D. A. Geller. 1996. Transcriptional regulation of human inducible nitric oxide synthase (NOS2) gene by cytokines: initial analysis of the human NOS2 promoter. Proc. Natl. Acad. Sci. USA 93: 1054-1059.
46. Huang, J., F. J. DeGraves, S. D. Lenz, D. Gao, P. Feng, D. Li, T. Schlapp, and B. Kaltenboeck. 2002. The quantity of nitric oxide released by macrophages regulates Chlamydia-induced disease. Proc. Natl. Acad. Sci. USA 99: 3914-3919.
47. Basu, R., S. Bhaumik, J. M. Basu, K. Naskar, T. De, and S. Roy: 2005. Kineto-plastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and -resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: evidence for mixed Th1- and Th2-like responses in visceral leishmaniasis. J. Immunol. 174: 7160-7171.
48. Farrell, J. P. 1976. Leishmania donovani: acquired resistance to visceral leishmaniasis in the golden hamster. Exp. Parasitol. 40: 89-94.
49. Garg, R., J. K. Srivastava, A. Pal, S. Naik, and A. Dube. 2005. Isolation of integral membrane proteins of Leishmania promastigotes and evaluation of their prophylactic potential in hamsters against experimental visceral leishmaniasis. Vaccine 23: 1189-1196.
50. Gifawesen, C., and J. P. Farrell. 1989. Comparison of T-cell responses in self-limiting versus progressive visceral Leishmania donovani infections in golden hamsters. Infect. Immun. 57: 3091-3096.
51. Srivastava, J. K., A. Misra, P. Sharma, B. Srivastava, S. Naik, and A. Dube. 2003. Prophylactic potential of autoclaved Leishmania donovani with BCG against experimental visceral leishmaniasis. Parasitology 127: 107-114.