L-arginine and cationic amino acid transporter 2B regulate growth and survival of Leishmania amazonensis amastigotes in macrophages

Infection and Immunity

Volumn 75, Issue 6, 2007, Pages 2802-2810

  Wanasen, Nanchaya ^a   MacLeod, Carol L ^b   Ellies, Lesley G ^b   Soong, Lynn ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; ARGINASE; ARGININE; CATIONIC AMINO ACID TRANSPORTER 2B; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 4; MESSENGER RNA; UNCLASSIFIED DRUG;

ADOLESCENT; AMASTIGOTE; AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE; GENE EXPRESSION; HOST RESISTANCE; LEISHMANIA; LEISHMANIASIS; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PARASITE DEVELOPMENT; PARASITE SURVIVAL; PRIORITY JOURNAL; SLC7A2 GENE; TH1 CELL;

ANIMALS; ARGININE; CATIONIC AMINO ACID TRANSPORTER 2; CYTOTOXICITY, IMMUNOLOGIC; LEISHMANIA MEXICANA; LEISHMANIASIS; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C;

EID: 34249898879     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00026-07     Document Type: Article

References (40)

1. Antoine, J. C., T. Lang, E. Prina, N. Courret, and R. Hellio. 1999. H-2M molecules, like MHC class II molecules, are targeted to parasitophorous vacuoles of Leishmania-infected macrophages and internalized by amastigotes of L. amazonensis and L. mexicana. J. Cell Sci. 112(Pt. 15):2559-2570.
2. Baydoun, A. R., and G. E. Mann. 1994. Selective targeting of nitric oxide synthase inhibitors to system y+ in activated macrophages. Biochem. Biophys. Res. Commun. 200:726-731.
3. Boutard, V., R. Havouis, B. Fouqueray, C. Philippe, J. P. Moulinoux, and L. Baud. 1995. Transforming growth factor-beta stimulates arginase activity in macrophages: implications for the regulation of macrophage cytotoxicity. J. Immunol. 155:2077-2084.
4. Bussiere, F. I., R. Chaturvedi, Y. Cheng, A. P. Gobert, M. Asim, D. R. Blumberg, H. Xu, P. Y. Kim, A. Hacker, R. A. Casero, Jr., and K. T. Wilson. 2005. Spermine causes loss of innate immune response to Helicobacter pylori by inhibition of inducible nitric-oxide synthase translation. J. Biol. Chem. 280:2409-2412.
5. Closs, E. I., L. M. Albritton, J. W. Kim, and J. M. Cunningham. 1993. Identification of a low affinity, high capacity transporter of cationic amino acids in mouse liver. J. Biol. Chem. 268:7538-7544.
6. Closs, E. I., F. Z. Basha, A. Habermeier, and U. Forstermann. 1997. Interference of L-arginine analogues with L-arginine transport mediated by the y+ carrier hCAT-2B. Nitric Oxide 1:65-73.
7. Closs, E. I., A. Simon, N. Vekony, and A. Rotmann. 2004. Plasma membrane transporters for arginine. J. Nutr. 134:2752S-2759S; 2765S-2767S.
8. 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.
9. da Silva, E. R., T. M. Castilho, F. C. Pioker, C. H. Tomich de Paula Silva, 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.
10. Dutta, S., D. Ray, B. K. Kolli, and K. P. Chang. 2005. Photodynamic sensitization of Leishmania amazonensis in both extracellular and intracellular stages with aluminum phthalocyanine chloride for photolysis in vitro. Antimicrob. Agents Chemother. 49:4474-4484.
11. Eckmann, L., F. Laurent, T. D. Langford, M. L. Hetsko, J. R. Smith, M. F. Kagnoff, and F. D. Gillin. 2000. Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J. Immunol. 164:1478-1487.
12. Gomes, I. N., A. F. Calabrich, S. Tavares Rda, J. Wietzerbin, L. A. de Freitas, and P. S. Veras. 2003. Differential properties of CBA/J mononuclear phagocytes recovered from an inflammatory site and probed with two different species of Leishmania. Microbes Infect. 5:251-260.
13. Gotoh, T., and M. Mori. 1999. Arginase II downregulates nitric oxide (NO) production and prevents NO-mediated apoptosis in murine macrophage-derived RAW 264.7 cells. J. Cell Biol. 144:427-434.
14. 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.
15. 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.
16. Iniesta, V., L. C. Gomez-Nieto, and I. Corraliza. 2001. The inhibition of arginase by N(omega)-hydroxy-1-arginine controls the growth of Leishmania inside macrophages. J. Exp. Med. 193:777-784.
17. 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.
18. Kandpal, M., R. B. Fouce, A. Pal, P. Y. Guru, and B. L. Tekwani. 1995. Kinetics and molecular characteristics of arginine transport by Leishmania donovani promastigotes. Mol. Biochem. Parasitol. 71:193-201.
19. Kane, M. M., and D. M. Mosser. 2001. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166:1141- 1147.
20. Kim, J. W., E. I. Closs, L. M. Albritton, and J. M. Cunningham. 1991. Transport of cationic amino acids by the mouse ecotropic retrovirus receptor. Nature 352:725-728.
21. 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.
22. Lang, T., C. de Chastellier, C. Frehel, R. Hellio, P. Metezeau, S. Leao Sde, and J. C. Antoine. 1994. Distribution of MHC class I and of MHC class II molecules in macrophages infected with Leishmania amazonensis. J. Cell Sci. 107(Pt. 1):69-82.
23. 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.
24. Lin, J. Y., R. Seguin, K. Keller, and K. Chadee. 1994. Tumor necrosis factor alpha augments nitric oxide-dependent macrophage cytotoxicity against Entamoeba histolytica by enhanced expression of the nitric oxide synthase gene. Infect. Immun. 62:1534-1541.
25. Nicholson, B., C. K. Manner, J. Kleeman, and C. L. MacLeod. 2001. Sustained nitric oxide production in macrophages requires the arginine transporter CAT2. J. Biol. Chem. 276:15881-15885.
26. Peluffo, G., L. Piacenza, F. Irigoin, M. N. Alvarez, and R. Radi. 2004. L-Arginine metabolism during interaction of Trypanosoma cruzi with host cells. Trends Parasitol. 20:363-369.
27. Qi, H., J. Ji, N. Wanasen, and L. Soong. 2004. Enhanced replication of Leishmania amazonensis amastigotes in gamma interferon-stimulated murine macrophages: implications for the pathogenesis of cutaneous leishmaniasis. Infect. Immun. 72:988-995.
28. + T cells in vivo. J. Immunol. 167:4534-4542.
29. Reiner, S. L., and R. M. Locksley. 1995. The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 13:151-177.
30. 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.
31. Stevens, B. R., D. K. Kakuda, K. Yu, M. Waters, C. B. Vo, and M. K. Raizada. 1996. Induced nitric oxide synthesis is dependent on induced alternatively spliced CAT-2 encoding L-arginine transport in brain astrocytes. J. Biol. Chem. 271:24017-24022.
32. Stuehr, D. J., S. S. Gross, I. Sakuma, R. Levi, and C. F. Nathan. 1989. Activated murine macrophages secrete a metabolite of arginine with the bioactivity of endothelium-derived relaxing factor and the chemical reactivity of nitric oxide. J. Exp. Med. 169:1011-1020.
33. Talaue, M. T., V. Venketaraman, M. H. Hazbon, M. Peteroy-Kelly, A. Seth, R. Colangeli, D. Alland, and N. D. Connell. 2006. Arginine homeostasis in J774.1 macrophages in the context of Mycobacterium bovis BCG infection. J. Bacteriol. 188:4830-4840.
34. Teixeira, M. J., C. R. Teixeira, B. B. Andrade, M. Barral-Netto, and A. Barral. 2006. Chemokines in host-parasite interactions in leishmaniasis. Trends Parasitol. 22:32-40.
35. Vasquez, R. E., and L. Soong. 2006. CXCL10/gamma interferon-inducible protein 10-mediated protection against Leishmania amazonensis infection in mice. Infect. Immun. 74:6769-6777.
36. Verrey, F., E. I. Closs, C. A. Wagner, M. Palacin, H. Endou, and Y. Kanai. 2004. CATs and HATs: the SLC7 family of amino acid transporters. Pflugers Arch. 447:532-542.
37. Vinetz, J. M., and L. Soong. 2006. Leishmania mexicana infection of the eyelid in a traveler to Belize. Braz. J. Infect. Dis. 10:304-307.
38. Wu, G., and S. M. Morris, Jr. 1998 Arginine metabolism: nitric oxide and beyond. Biochem. J. 336(Pt. 1):1-17.
39. Yeramian, A., L. Martin, L. Arpa, J. Bertran, C. Soler, C. McLeod, M. Modolell, M. Palacin, J. Lloberas, and A. Celada. 2006. Macrophages require distinct arginine catabolism and transport systems for proliferation and for activation. Eur. J. Immunol. 36:1516-1526.
40. Yoshida, N., and E. P. Camargo. 1978. Ureotelism and ammonotelism in trypanosomatids. J. Bacteriol. 136:1184-1186.