Mouse Strain Susceptibility to Trypanosome Infection: An Arginase-Dependent Effect

Journal of Immunology

Volumn 172, Issue 10, 2004, Pages 6298-6303

  Duleu, Sébastien ^a,b   Vincendeau, Philippe ^a   Courtois, Pierrette ^a   Semballa, Silla ^a   Lagroye, Isabelle ^b   Daulouède, Sylvie ^a   Boucher, Jean Luc ^c   Wilson, Keith T ^d   Veyret, Bernard ^b   Gobert, Alain P ^e  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; ARGININE; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; N(G) HYDROXYARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIAGNOSTIC VALUE; DISEASE MARKER; ENZYME ACTIVITY; HOST RESISTANCE; HOST SUSCEPTIBILITY; INFECTION RESISTANCE; INFECTION SENSITIVITY; MACROPHAGE; MOUSE; MOUSE STRAIN; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; TRYPANOSOMA BRUCEI; TRYPANOSOMIASIS;

EID: 2442496241     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.10.6298     Document Type: Article

References (37)

1. Legros, D., G. Ollivier, M. Gastellu-Etchegorry, C. Paquet, C. Burri, J. Jannin, and P. Büscher. 2002. Treatment of human African trypanosomiasis: present situation and needs for research and development. Lancet Infect. Dis. 2:437.
2. Hertz, C. J., H. Filutowicz, and J. M. Mansfield. 1998. Resistance to the African trypanosomes is IFN-γ dependent. J. Immunol. 161:6775.
3. + T cells correlates with Th1/Th2 phenotype. J. Immunol. 160:5347.
4. Wang, W. W., C. P. Jenkinson, J. M. Oriscavage, R. M. Kern, N. S. Arabolos, R. E. Byrns, S. D. Cederbaum, and L. J. Ignarro. 1995. Co-induction of arginase and nitric oxide synthase in murine macrophages activated by lipopolysaccharide. Biochem. Biophys. Res. Commun. 25:1009.
5. Gobert, A. P., B. D. Mersey, Y. Cheng, D. R. Blumberg, J. C. Newton, and K. T. Wilson. 2002. Cutting edge: urease release by Helicobacter pylori stimulates macrophage inducible nitric oxide synthase. J. Immunol. 168:6002.
6. Fang, F. C. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99:2818.
7. Gobert, A. P., S. Semballa, S. Daulouede, S. Lesthelle, M. Taxile, B. Veyret, and P. Vincendeau. 1998. Murine macrophages use oxygen and nitric oxide dependent mechanisms to synthesize S-nitroso albumin and to kill extracellular trypanosomes. Infect. Immun. 56:4068.
8. Gobert, A. P., Y. Cheng, J.-Y. Wang, J. L. Boucher, R. K. Iyer, S. D. Cederbaum, R. A. Casero, Jr., J. C. Newton, and K. T. Wilson. 2002. Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J. Immunol. 168:4692.
9. Hesse, M., M. Modolell, A. La Flamme, M. Schito, J. M. Fuentes, A. W. Cheever, E. J. Pearce, and T. A. Wynn. 2001. Differential regulation of nitric oxide synthase-2 and arginase-I by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 167:6533.
10. Vincendeau, P., A. P. Gobert, S. Daulouede, D. Moynet, and M. D. Mossalayi. 2003. Arginases in parasitic diseases. Trends Parasitol. 19:9.
11. Gobert, A. P., S. Daulouede, M. Lepoivre, J. L. Boucher, B. Boutcille, A. Buguet, R. Cespuglio, B. Veyret, and P. Vincendeau. 2000. L-arginine availability modulates local nitric oxide production and parasite killing in experimental trypanosomiasis. Infect. Immun. 68:4653.
12. Suzuki, Y., A. Sher, G. Yap, D. Park, L. E. Neyer, O. Liesenfeld, M. Fort, H. Kang, and E. Gufwoli. 2000. IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii. J. Immunol. 164:5375.
13. Aguilar Torrentera, F., M. A. Lambot, J. D. Laman, M. Van Meurs, R. Kiss, J. C. Noel, and Y. Carlier. 2002. Parasitic load and histopathology of cutaneous lesions, lymph node, spleen, and liver from BALB/c and C57BL/6 mice infected with Leishmania mexicana. Am. J. Trop. Med. Hyg. 66:273.
14. Noel, W., G. Hassanzadeh, G. Raes, B. Namangala, I. Daems, L. Brys, F. Brombacher, P. De Baetselier, and A. Beschin. 2002. Infection stage-dependent modulation of macrophage activation in Trypanosoma congolense-resistant and susceptible mice. Infect. Immun. 70:6180.
15. 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.
16. Kaushik, R. S., J. E. Uzonna, J. R. Gordon, and H. Tabel. 1999. Innate resistance to Trypanosoma congolense infections: differential production of nitric oxide by macrophages from susceptible BALB/c and resistant C57BL/6 mice. Exp. Parasitol. 92:131.
17. ω-hydroxy-nor-L-arginine. Biochemistry 37:10453.
18. Russel, A. S., and U. T. Ruegg. 1980. Arginase production by peritoneal macrophages: a new assay. J. Immunol. Methods 32:375.
19. Louis, C. A., V. Mody, W. L. Henry, Jr., J. S. Reichner, and J. E. Albina. 1999. Regulation of arginase isoforms I and II by IL-4 in cultured murine peritoneal macrophages. Am. J. Physiol. 363:R237.
20. Salimuddin, A. Nagasaki, T. Gotoh, H. Isobe, and M. Mori. 1999. Regulation of the genes for arginase isoforms and related enzymes in mouse macrophages by lipopolysaccharide. Am. J. Physiol. 227:E110.
21. Morris Jr., S. M., D. Kepta-Lenhart, and L.-C. Chen. 1998. Differential regulation of arginase and inducible nitric oxide synthase in murine macrophage cells. Am. J. Physiol. 275:E740.
22. Uzonna, J. E., R. S. Kaushik, J. R. Gordon, and H. Tabel. 1999. Cytokines and antibody responses during Trypanosoma congolense infections in two inbred mouse strains that differ in resistance. Parasite Immunol. 21:57.
23. Boutard, V., R. Havouis, B. Fouqueray, C. Philippe, J. P. Moulinoux, and L. Baud. 1995. Transforming growth factor-β stimulates arginase activity in macrophages: implication for the regulation of macrophage cytotoxicity. J. Immunol. 155:2077.
24. Iniesta, V., L. C. Gomez-Nieto, I. Molano, A. Mohedano, I. Carcelen, C. Miron, C. Alonso, and I. Corraliza. 2002. Arginase I induction in macrophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites. Parasite Immunol. 24:113.
25. Li, J., C. A. Hunter, and J. P. Farrell. 1999. Anti-TGF-β treatment promotes rapid healing of Leishmania major infection in mice by enhancing in vivo nitric oxide production. J. Immunol. 162:974.
26. Mills, C. D., K. Kincaid, J. M. Alt, M. J. Heilman, and A. M. Hill. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164:6166.
27. Gobert, A. P., D. J. McGee, M. Akthar, G. L. Mendz, J. C. Newton, Y. Cheng, H. L. T. Mobley, and K. T. Wilson. 2001. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: a strategy for bacterial survival. Proc. Natl. Acad. Sci. USA 98:13844.
28. Vouldoukis, I., V. Riveros-Moreno, B. Dugas, F. Ouaaz, P. Becharel, P. Debre, S. Moncada, and M. D. Mossalayi. 1995. The killing of Leishmania major by human macrophages is mediated by nitric oxide induced after ligation of the FcεRII/CD23 surface antigen. Proc. Natl. Acad. Sci. USA 92:7804.
29. ω-hydroxy-L-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 193:777.
30. Schleifer, K. W., and J. M. Mansfield. 1993. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. J. Immunol. 151:5492.
31. Millar, A. E., J. Sternberg, C. McSharry, X. Q. Wei, F. Y. Liew, and C. M. Turner. 1999. T-cell responses during Trypanosoma brucei infections in mice deficient in inducible nitric oxide synthase. Infect. Immun. 67:3334.
32. 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.
33. Hertz, C. J., and J. M. Mansfield. 1999. IFN-γ-dependent nitric oxide production is not linked to resistance in experimental African trypanosomiasis. Cell. Immunol. 192:24.
34. Schluter, D., M. Deckert-Schluter, E. Lorenz, T. Meyer, M. Rollingboff, and C. Bogdan. 1999. Inhibition of inducible nitric oxide synthase exacerbates chronic cerebral toxoplasmosis in Toxoplasma gondii-susceptible C57BL/6 mice but does not reactivate the latent disease in T. gondii-resistant BALB/c mice. J. Immunol. 162:3512.
35. McCafferty, D. M., M. Miampamba, E. Sihota, K. A. Sharkey, and P. Kubes. 1999. Role of inducible nitric oxide synthase in trinitrobenzene sulphonic acid induced colitis in mice. Gut 45:864.
36. Saeftel, M., B. Fleischer, and A. Hoerauf. 2001. Stage-dependent role of nitric oxide in control of Trypanosoma cruzi infection. Infect. Immun. 69:2252.
37. Fairlamb, A. H., and A. Cerami. 1992. Metabolism and functions of trypanothione in the Kinetoplastida. Annu. Rev. Microbiol. 46:695.