Infection with arginase-deficient Leishmania major reveals a parasite number-dependent and cytokine-independent regulation of host cellular arginase activity and disease pathogenesis

Journal of Immunology

Volumn 183, Issue 12, 2009, Pages 8068-8076

  Muleme, Helen M ^a   Reguera, Rosa M ^b   Berard, Alicia ^a   Azinwi, Richard ^a   Jia, Ping ^a   Okwor, Ifeoma B ^a   Beverley, Stephen ^b   Uzonna, Jude E ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; PROSTAGLANDIN E2; CYTOKINE; IMMUNOLOGICAL ADJUVANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LEISHMANIA MAJOR; LEISHMANIASIS; LYMPH NODE; MOUSE; NONHUMAN; PATHOGENESIS; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL PROLIFERATION; COMPARATIVE STUDY; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYPERARGININEMIA; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; SKIN LEISHMANIASIS;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ARGINASE; BONE MARROW CELLS; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; ENZYME ACTIVATION; FEMALE; HYPERARGININEMIA; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED BALB C;

EID: 76249084931     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803979     Document Type: Article

References (45)

1. Antinori, S., E. Gianelli, S. Calatttini, E. Longhi, M. Gramiccia, and M. Corbellino. 2005. Cutaneous leishmaniasis: an increasing threat for travelers. Clin. Microbiol. Infect. 11: 343-346. (Pubitemid 40575815)
2. Kropf, P., S. Herath, V. Weber, M. Modolell, and I. Muller. 2003. Factors influencing Leishmania major infection in IL-4-deficient BALB/c mice. Parasite Immunol. 25: 439-447. (Pubitemid 38058021)
3. Iniesta, V., L. C. Gomez-Nieto, and I. Corraliza. 2001. The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 193: 777-784. (Pubitemid 32524470)
4. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
5. Kropf, P., J. M. Fuentes, E. Fahnrich, L. Arpa, S. Herath, V. Weber, G. Soler, A. Celada, M. Modolell, and I. Muller. 2005. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J. 19: 1000-1002.
6. Roberts, S. C., M. J. Tancer, M. R. Polinsky, K. M. Gibson, O. Heby, and B. Ullman. 2004. Arginase plays a pivotal role in polyamine precursor metabolism in Leishmania: characterization of gene deletion mutants. J. Biol. Chem. 279: 23668-23678.
7. Iniesta, V., J. Carcelen, I. Molano, P. M. Peixoto, E. Redondo, P. Parra, M. Mangas, I. Monroy, M. L. Campo, C. G. Nieto, and I. Corraliza. 2005. Arginase I induction during Leishmania major infection mediates the development of disease. Infect. Immun. 73: 6085-6090. (Pubitemid 41193047)
8. Iniesta, V., L. C. Gomez-Nieto, I. Molano, A. Mohedano, J. 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: 113-118. (Pubitemid 34451222)
9. Goerdt, S., O. Politz, K. Schledzewski, R. Birk, A. Gratchev, P. Guillot, N. Hakiy, C. D. Klemke, E. Dippel, V. Kodelja, and C. E. Orfanos. 1999. Alternative versus classical activation of macrophages. Pathobiology 67: 222-226. (Pubitemid 30135909)
10. 2) in murine bone-marrow-derived macrophages. Biochem. Biophys. Res. Commun. 206: 667-673.
11. da Silva, E. R., T. M. Castilho, F. C. Pioker, T. de Paula Silva, H. Carlos, and L. M. Floeter-Winter. 2002. Genomic organisation and transcription characterisation of the gene encoding Leishmania (Leishmania) amazonensis arginase and its protein structure prediction. Int. J. Parasitol. 32: 727-737.
12. Bacchi, C. J., and N. Yarlett. 2002. Polyamine metabolism as chemotherapeutic target in protozoan parasites. Mini Rev. Med. Chem. 2: 553-563.
13. Alexander, J., F. Brombacher, H. A. McGachy, A. N. McKenzie, W. Walker, and K. C. Carter. 2002. An essential role for IL-13 in maintaining a non-healing response following Leishmania mexicana infection. Eur. J. Immunol. 32: 2923-2933. (Pubitemid 35238186)
14. Arendse, B., J. Van Snick, and F. Brombacher. 2005. IL-9 is a susceptibility factor in Leishmania major infection by promoting detrimental Th2/type 2 responses. J. Immunol. 174: 2205-2211. (Pubitemid 40223966)
15. Thomas, T., and T. J. Thomas. 2003. Polyamine metabolism and cancer. J. Cell. Mol. Med. 7: 113-126.
16. 2 in Leishmania amazonensis infection of BALB/c mice. Microbes Infect. 8: 1219-1226.
17. Holscher, C., B. Arendse, A. Schwegmann, E. Myburgh, and F. Brombacher. 2006. Impairment of alternative macrophage activation delays cutaneous leishmanisis in nonhealing BALB/c mice. J. Immunol. 176: 1115-1121. (Pubitemid 43099713)
18. Kopf, M., F. Brombacher, G. Kohler, G. Kienzle, K. H. Widmann, K. Lefrang, C. Humborg, B. Ledermann, and W. Solbach. 1996. IL-4-deficient BALB/c mice resist infection with Leishmania major. J. Exp. Med. 184: 1127-1136. (Pubitemid 26313569)
19. Mohrs, M., C. Holscher, and F. Brombacher. 2000. Interleukin-4 receptor α-deficient BALB/c mice show an unimpaired T helper 2 polarization in response to Leishmania major infection. Infect. Immun. 68: 1773-1780. (Pubitemid 30164798)
20. Mohrs, M., B. Ledermann, G. Kohler, A. Dorfmuller, A. Gessner, and F. Brombacher. 1999. Differences between IL-4- and IL-4 receptor α-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 162: 7302-7308. (Pubitemid 29277704)
21. Reguera, R. M., R. Balana-Fouce, M. Showalter, S. Hickerson, and S. M. Beverley. 2009. Leishmania major lacking arginase (ARG) are auxotrophic for polyamines but retain infectivity to susceptible BALB/c mice. Mol. Biochem. Parasitol. 165: 48-56.
22. Gaur, U., S. C. Roberts, R. P. Dalvi, I. Corraliza, B. Ullman, and M. E. Wilson. 2007. An effect of parasite-encoded arginase on the outcome of murine cutaneous leishmaniasis. J. Immunol. 179: 8446-8453.
23. Colmenares, M., S. Kar, K. Goldsmith-Pestana, and D. McMahon-Pratt. 2002. Mechanisms of pathogenesis: differences amongst Leishmania species. Trans. R. Soc. Trop. Med. Hyg. 96, Supplement 1: S3-S7.
24. McMahon-Pratt, D., and J. Alexander. 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.
25. 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.
26. Spath, G. F., L. Lye, H. Segawa, D. L. Sacks, S. J. Turco, and S. M. Beverley. 2003. Persistence without pathology in phosphoglycan-deficient Leishmania major. Science 301: 1241-1243.
27. Buffet, P. A., A. Sulahian, Y. J. Garin, N. Nassar, and F. Derouin. 1995. Culture microtitration: a sensitive method for quantifying Leishmania infantum in tissues of infected mice. Antimicrob. Agents Chemother. 39: 2167-2168.
28. Titus, R. G., M. Marchand, T. Boon, and J. A. Louis. 1985. A limiting dilution assay for quantifying Leishmania major in tissues of infected mice. Parasite Immunol. 7: 545-555.
29. Zaph, C., J. Uzonna, S. M. Beverley, and P. Scott. 2004. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat. Med. 10: 1104-1110.
30. Ding, A. H., C. F. Nathan, and D. J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production. J. Immunol. 141: 2407-2412.
31. + Th1 cell development and resistance to Leishmania major. J. Immunol. 170: 1995-2003.
32. Corraliza, I. M., M. L. Campo, G. Soler, and M. Modolell. 1994. Determination of arginase activity in macrophages: a micromethod. J. Immunol. Methods 174: 231-235.
33. Baetselier, P. D., B. Namangala, W. Noel, L. Brys, E. Pays, and A. Beschin. 2001. Alternative versus classical macrophage activation during experimental African trypanosomosis. Int. J. Parasitol. 31: 575-587.
34. Modolell, M., I. M. Corraliza, F. Link, G. Soler, and K. Eichmann. 1995. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur. J. Immunol. 25: 1101-1104.
35. Titus, R. G., F. J. Gueiros-Filho, L. A. de Freitas, and S. M. Beverley. 1995. Development of a safe live Leishmania vaccine line by gene replacement. Proc. Natl. Acad. Sci. USA 92: 10267-10271.
36. Uzonna, J. E., G. F. Spath, S. M. Beverley, and P. Scott. 2004. Vaccination with phosphoglycan-deficient Leishmania major protects highly susceptible mice from virulent challenge without inducing a strong Th1 response. J. Immunol. 172: 3793-3797.
37. Peranzoni, E., I. Marigo, L. Dolcetti, S. Ugel, N. Sonda, E. Taschin, B. Mantelli, V. Bronte, and P. Zanovello. 2007. Role of arginine metabolism in immunity and immunopathology. Immunobiology 212: 795-812. (Pubitemid 350246262)
38. Samuelsson, B., R. Morgenstern, and P. J. Jakobsson. 2007. Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol. Rev. 59: 207-224. (Pubitemid 47481434)
39. Kojima, F., H. Naraba, Y. Sasaki, M. Beppu, H. Aoki, and S. Kawai. 2003. Prostaglandin E2 is an enhancer of interleukin-1-induced expression of membrane-associated prostaglandin E synthase in rheumatoid synovial fibroblasts. Arthritis Rheum. 48: 2819-2828. (Pubitemid 37280610)
40. Capul, A. A., S. Hickerson, T. Barron, S. J. Turco, and S. M. Beverley. 2007. Comparisons of mutants lacking the Golgi UDP-galactose or GDP-mannose transporters establish that phosphoglycans are important for promastigote but not amastigote virulence in Leishmania major. Infect. Immun. 75: 4629-4637.
41. Wanasen, N., and L. Soong. 2008. L-arginine metabolism and its impact on host immunity against Leishmania major. Immunol. Res. 41: 15-25.
42. Nylen, S., K. Maasho, K. Soderstrom, T. Ilg, and H. Akuffo. 2003. Leishmania promastigotes can directly activate primary human natural killer cells to produce interferon-γ. Clin. Exp. Immunol. 131: 457-467. (Pubitemid 36324137)
43. Giordanengo, L., N. Guinazu, C. Stempin, R. Fretes, F. Cerban, and S. Gea. 2002. Cruzipain, a major Trypanosoma cruzi antigen, conditions the host immune response in favor of parasite. Eur. J. Immunol. 32: 1003-1011. (Pubitemid 34428815)
44. Stempin, C., L. Giordanengo, S. Gea, and F. Cerban. 2002. Alternative activation and increase of Trypanosoma cruzi survival in murine macrophages stimulated by cruzipain, a parasite antigen. J. Leukocyte Biol. 72: 727-734. (Pubitemid 36277844)
45. Donnelly, S., S. M. O'Neill, M. Sekiya, G. Mulcahy, and J. P. Dalton. 2005. Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infect. Immun. 73: 166-173. (Pubitemid 40041106)