Differential requirements for L-citrulline and L-arginine during antimycobacterial macrophage activity

Journal of Immunology

Volumn 195, Issue 7, 2015, Pages 3293-3300

  Rapovy, Shannon M ^a   Zhao, Junfang ^a   Bricker, Rebecca L ^a   Schmidt, Stephanie M ^a   Setchell, Kenneth D R ^a   Qualls, Joseph E ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; ARGININE; CITRULLINE; NITRIC OXIDE; ORNITHINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE;

AMINO ACID METABOLISM; AMINO ACID SYNTHESIS; AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; BACTERIAL IMMUNITY; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR SPACE; MACROPHAGE; MACROPHAGE CULTURE; MOUSE; MYCOBACTERIUM BOVIS BCG; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; IMMUNOLOGY; MACROPHAGE ACTIVATION; METABOLISM; MICROBIOLOGY; MYCOBACTERIUM BOVIS; TRANSGENIC MOUSE; TUBERCULOSIS;

ANIMALS; ARGINASE; ARGININE; CELLS, CULTURED; CITRULLINE; INTERFERON-GAMMA; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYCOBACTERIUM BOVIS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; TUBERCULOSIS;

EID: 84942446689     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500800     Document Type: Article

References (47)

1. Garcia, I., R. Guler, D. Vesin, M. L. Olleros, P. Vassalli, Y. Chvatchko, M. Jacobs, and B. Ryffel. 2000. Lethal Mycobacterium bovis Bacillus Calmette Guérin infection in nitric oxide synthase 2-deficient mice: cellmediated immunity requires nitric oxide synthase 2. Lab. Invest. 80: 1385-1397.
2. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94: 5243-5248.
3. Thomas, A. C., and J. T. Mattila. 2014. "Of mice and men": arginine metabolism in macrophages. Front. Immunol. 5: 479.
4. Azad, A. K., W. Sadee, and L. S. Schlesinger. 2012. Innate immune gene polymorphisms in tuberculosis. Infect. Immun. 80: 3343-3359.
5. Gómez, L. M., J. M. Anaya, J. R. Vilchez, J. Cadena, R. Hinojosa, L. Vélez, M. A. Lopez-Nevot, and J. Martín. 2007. A polymorphism in the inducible nitric oxide synthase gene is associated with tuberculosis. Tuberculosis (Edinb.) 87: 288-294.
6. Jamieson, S. E., E. N. Miller, G. F. Black, C. S. Peacock, H. J. Cordell, J. M. Howson, M. A. Shaw, D. Burgner, W. Xu, Z. Lins-Lainson, et al. 2004. Evidence for a cluster of genes on chromosome 17q11-q21 controlling susceptibility to tuberculosis and leprosy in Brazilians. Genes Immun. 5: 46-57.
7. Möller, M., A. Nebel, R. Valentonyte, P. D. van Helden, S. Schreiber, and E. G. Hoal. 2009. Investigation of chromosome 17 candidate genes in susceptibility to TB in a South African population. Tuberculosis (Edinb.) 89: 189-194.
8. Velez, D. R., W. F. Hulme, J. L. Myers, J. B. Weinberg, M. C. Levesque, M. E. Stryjewski, E. Abbate, R. Estevan, S. G. Patillo, J. R. Gilbert, et al. 2009. NOS2A, TLR4, and IFNGR1 interactions influence pulmonary tuberculosis susceptibility in African-Americans. Hum. Genet. 126: 643-653.
9. Ralph, A. P., T. W. Yeo, C. M. Salome, G. Waramori, G. J. Pontororing, E. Kenangalem, E. Sandjaja, E. Tjitra, R. Lumb, G. P. Maguire, et al. 2013. Impaired pulmonary nitric oxide bioavailability in pulmonary tuberculosis: association with disease severity and delayed mycobacterial clearance with treatment. J. Infect. Dis. 208: 616-626.
10. Nicholson, S., Mda. G. Bonecini-Almeida, J. R. Lapa e Silva, C. Nathan, Q. W. Xie, R. Mumford, J. R. Weidner, J. Calaycay, J. Geng, N. Boechat, et al. 1996. Inducible nitric oxide synthase in pulmonary alveolar macrophages from patients with tuberculosis. J. Exp. Med. 183: 2293-2302.
11. Rich, E. A., M. Torres, E. Sada, C. K. Finegan, B. D. Hamilton, and Z. Toossi. 1997. Mycobacterium tuberculosis (MTB)-stimulated production of nitric oxide by human alveolar macrophages and relationship of nitric oxide production to growth inhibition of MTB. Tuber. Lung Dis. 78: 247-255.
12. Wang, C. H., C. Y. Liu, H. C. Lin, C. T. Yu, K. F. Chung, and H. P. Kuo. 1998. Increased exhaled nitric oxide in active pulmonary tuberculosis due to inducible NO synthase upregulation in alveolar macrophages. Eur. Respir. J. 11: 809-815.
13. Jagannath, C., J. K. Actor, and R. L. Hunter, Jr. 1998. Induction of nitric oxide in human monocytes and monocyte cell lines by Mycobacterium tuberculosis. Nitric Oxide 2: 174-186.
14. Choi, H. S., P. R. Rai, H. W. Chu, C. Cool, and E. D. Chan. 2002. Analysis of nitric oxide synthase and nitrotyrosine expression in human pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 166: 178-186.
15. Nozaki, Y., Y. Hasegawa, S. Ichiyama, I. Nakashima, and K. Shimokata. 1997. Mechanism of nitric oxide-dependent killing of Mycobacterium bovis BCG in human alveolar macrophages. Infect. Immun. 65: 3644-3647.
16. Pessanha, A. P., R. A. Martins, A. L. Mattos-Guaraldi, A. Vianna, and L. O. Moreira. 2012. Arginase-1 expression in granulomas of tuberculosis patients. FEMS Immunol. Med. Microbiol. 66: 265-268.
17. Mattila, J. T., O. O. Ojo, D. Kepka-Lenhart, S. Marino, J. H. Kim, S. Y. Eum, L. E. Via, C. E. Barry, III, E. Klein, D. E. Kirschner, et al. 2013. Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms. J. Immunol. 191: 773-784.
18. Duque-Correa, M. A., A. A. Kühl, P. C. Rodriguez, U. Zedler, S. Schommer-Leitner, M. Rao, J. Weiner, III, R. Hurwitz, J. E. Qualls, G. A. Kosmiadi, et al. 2014. Macrophage arginase-1 controls bacterial growth and pathology in hypoxic tuberculosis granulomas. Proc. Natl. Acad. Sci. USA 111: E4024-E4032.
19. Qualls, J. E., G. Neale, A. M. Smith, M. S. Koo, A. A. DeFreitas, H. Zhang, G. Kaplan, S. S. Watowich, and P. J. Murray. 2010. Arginine usage in mycobacteria-infected macrophages depends on autocrine-paracrine cytokine signaling. Sci. Signal. 3: ra62.
20. El Kasmi, K. C., J. E. Qualls, J. T. Pesce, A. M. Smith, R. W. Thompson, M. Henao-Tamayo, R. J. Basaraba, T. König, U. Schleicher, M. S. Koo, et al. 2008. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 9: 1399-1406.
21. Wu, G. Y., and J. T. Brosnan. 1992. Macrophages can convert citrulline into arginine. Biochem. J. 281: 45-48.
22. Qualls, J. E., C. Subramanian, W. Rafi, A. M. Smith, L. Balouzian, A. A. DeFreitas, K. A. Shirey, B. Reutterer, E. Kernbauer, S. Stockinger, et al. 2012. Sustained generation of nitric oxide and control of mycobacterial infection requires argininosuccinate synthase 1. Cell Host Microbe 12: 313-323.
23. El-Bassossy, H. M., R. El-Fawal, A. Fahmy, and M. L. Watson. 2013. Arginase inhibition alleviates hypertension in the metabolic syndrome. Br. J. Pharmacol. 169: 693-703.
24. Shearer, J. D., J. R. Richards, C. D. Mills, and M. D. Caldwell. 1997. Differential regulation of macrophage arginine metabolism: a proposed role in wound healing. Am. J. Physiol. 272: E181-E190.
25. Romero, M. J., D. H. Platt, R. B. Caldwell, and R. W. Caldwell. 2006. Therapeutic use of citrulline in cardiovascular disease. Cardiovasc. Drug Rev. 24: 275-290.
26. Erez, A., S. C. Nagamani, O. A. Shchelochkov, M. H. Premkumar, P. M. Campeau, Y. Chen, H. K. Garg, L. Li, A. Mian, T. K. Bertin, et al. 2011. Requirement of argininosuccinate lyase for systemic nitric oxide production. Nat. Med. 17: 1619-1626.
27. Ashenafi, S., G. Aderaye, A. Bekele, M. Zewdie, G. Aseffa, A. T. Hoang, B. Carow, M. Habtamu, M. Wijkander, M. Rottenberg, et al. 2014. Progression of clinical tuberculosis is associated with a Th2 immune response signature in combination with elevated levels of SOCS3. Clin. Immunol. 151: 84-99.
28. Heitmann, L., M. Abad Dar, T. Schreiber, H. Erdmann, J. Behrends, A. N. Mckenzie, F. Brombacher, S. Ehlers, and C. Hölscher. 2014. The IL-13/IL-4Ra axis is involved in tuberculosis-associated pathology. J. Pathol. 234: 338-350.
29. Rook, G. A., R. Hernandez-Pando, K. Dheda, and G. Teng Seah. 2004. IL-4 in tuberculosis: implications for vaccine design. Trends Immunol. 25: 483-488.
30. Flam, B. R., P. J. Hartmann, M. Harrell-Booth, L. P. Solomonson, and D. C. Eichler. 2001. Caveolar localization of arginine regeneration enzymes, argininosuccinate synthase, and lyase, with endothelial nitric oxide synthase. Nitric Oxide 5: 187-197.
31. Xu, W., F. T. Kaneko, S. Zheng, S. A. Comhair, A. J. Janocha, T. Goggans, F. B. Thunnissen, C. Farver, S. L. Hazen, C. Jennings, et al. 2004. Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J. 18: 1746-1748.
32. Zhang, C., T. W. Hein, W. Wang, M. W. Miller, T. W. Fossum, M. M. McDonald, J. D. Humphrey, and L. Kuo. 2004. Upregulation of vascular arginase in hypertension decreases nitric oxide-mediated dilation of coronary arterioles. Hypertension 44: 935-943.
33. White, A. R., S. Ryoo, D. Li, H. C. Champion, J. Steppan, D. Wang, D. Nyhan, A. A. Shoukas, J. M. Hare, and D. E. Berkowitz. 2006. Knockdown of arginase I restores NO signaling in the vasculature of old rats. Hypertension 47: 245-251.
34. Flam, B. R., D. C. Eichler, and L. P. Solomonson. 2007. Endothelial nitric oxide production is tightly coupled to the citrulline-NO cycle. Nitric Oxide 17: 115-121.
35. Mun, G. I., I. S. Kim, B. H. Lee, and Y. C. Boo. 2011. Endothelial argininosuccinate synthetase 1 regulates nitric oxide production and monocyte adhesion under static and laminar shear stress conditions. J. Biol. Chem. 286: 2536-2542.
36. Yu, H., R. K. Iyer, R. M. Kern, W. I. Rodriguez, W. W. Grody, and S. D. Cederbaum. 2001. Expression of arginase isozymes in mouse brain. J. Neurosci. Res. 66: 406-422.
37. Xu, L., B. Hilliard, R. J. Carmody, G. Tsabary, H. Shin, D. W. Christianson, and Y. H. Chen. 2003. Arginase and autoimmune inflammation in the central nervous system. Immunology 110: 141-148.
38. Knott, A. B., and E. Bossy-Wetzel. 2009. Nitric oxide in health and disease of the nervous system. Antioxid. Redox Signal. 11: 541-554.
39. Que, L. G., S. E. George, T. Gotoh, M. Mori, and Y. C. Huang. 2002. Effects of arginase isoforms on NO production by nNOS. Nitric Oxide 6: 1-8.
40. Simic, G., P. J. Lucassen, Z. Krsnik, B. Kruslin, I. Kostovic, B. Winblad, and Bogdanovi. 2000. nNOS expression in reactive astrocytes correlates with increased cell death related DNA damage in the hippocampus and entorhinal cortex in Alzheimer's disease. Exp. Neurol. 165: 12-26.
41. Caggiano, A. O., and R. P. Kraig. 1998. Neuronal nitric oxide synthase expression is induced in neocortical astrocytes after spreading depression. J. Cereb. Blood Flow Metab. 18: 75-87.
42. Schmidlin, A., and H. Wiesinger. 1998. Argininosuccinate synthetase: localization in astrocytes and role in the production of glial nitric oxide. Glia 24: 428-436.
43. Wiesinger, H. 2001. Arginine metabolism and the synthesis of nitric oxide in the nervous system. Prog. Neurobiol. 64: 365-391.
44. Schön, T., D. Elias, F. Moges, E. Melese, T. Tessema, O. Stendahl, S. Britton, and T. Sundqvist. 2003. Arginine as an adjuvant to chemotherapy improves clinical outcome in active tuberculosis. Eur. Respir. J. 21: 483-488.
45. Ralph, A. P., G. Waramori, G. J. Pontororing, E. Kenangalem, A. Wiguna, E. Tjitra, D. B. Sandjaja, T. W. Lolong, M. D. Yeo, Chatfield, et al. 2013. Larginine and vitamin D adjunctive therapies in pulmonary tuberculosis: a randomised, double-blind, placebo-controlled trial. PLoS One 8: e70032.
46. Curis, E., I. Nicolis, C. Moinard, S. Osowska, N. Zerrouk, S. Bénazeth, and L. Cynober. 2005. Almost all about citrulline in mammals. Amino Acids 29: 177-205.
47. Bahri, S., N. Zerrouk, C. Aussel, C. Moinard, P. Crenn, E. Curis, J. C. Chaumeil, L. Cynober, and S. Sfar. 2013. Citrulline: from metabolism to therapeutic use. Nutrition 29: 479-484.