Microenvironments in tuberculous granulomas are delineated by distinct populations of macrophage subsets and expression of nitric oxide synthase and arginase isoforms

Journal of Immunology

Volumn 191, Issue 2, 2013, Pages 773-784

  Mattila, Joshua T ^a   Ojo, Olabisi O ^a   Kepka Lenhart, Diane ^a   Marino, Simeone ^b   Kim, Jin Hee ^c   Eum, Seok Yong ^d   Via, Laura E ^e   Barry III, Clifton E ^e   Klein, Edwin ^f   Kirschner, Denise E ^b   Morris, Sidney M ^a   Lin, Philana Ling ^g   Flynn, JoAnne L ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c National Masan Tuberculosis Hospital   (South Korea)

^d International Tuberculosis Research Center   (South Korea)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f UNIVERSITY OF PITTSBURGH   (United States)

^g CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE; ARGINASE 1; ARGINASE 2; CALGRANULIN; CD163 ANTIGEN; CD209 ANTIGEN; CD68 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCOPROTEIN P 15095; INDUCIBLE NITRIC OXIDE SYNTHASE; LYMPHOCYTE ANTIGEN; PROTEIN HAM56; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL COUNT; BACTERIUM IDENTIFICATION; BONE MARROW CELL; CONTROLLED STUDY; ENZYME ACTIVITY; GRANULOMA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; INNATE IMMUNITY; MACACA; MACROPHAGE FUNCTION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TUBERCULOSIS; TUBERCULOUS GRANULOMA; TUMOR MICROENVIRONMENT; UPREGULATION;

EID: 84880126124     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300113     Document Type: Article

References (70)

1. Lawn, S. D., and A. I. Zumla. 2011. Tuberculosis. Lancet 378: 57-72.
2. Russell, D. G., P. J. Cardona, M. J. Kim, S. Allain, and F. Altare. 2009. Foamy macrophages and the progression of the human tuberculosis granuloma. Nat. Immunol. 10: 943-948.
3. Flynn, J. L., and E. Klein, eds. 2010. Pulmonary Tuberculosis in Monkeys. CRC Press, Taylor & Francis Publishers, Boca Raton, FL.
4. Capuano, S. V., III, D. A. Croix, S. Pawar, A. Zinovik, A. Myers, P. L. Lin, S. Bissel, C. Fuhrman, E. Klein, and J. L. Flynn. 2003. Experimental Mycobacterium tuberculosis infection of cynomolgus macaques closely resembles the various manifestations of human M. tuberculosis infection. Infect. Immun. 71: 5831-5844. (Pubitemid 37205637)
5. Lin, P. L., M. Rodgers, L. Smith, M. Bigbee, A. Myers, C. Bigbee, I. Chiosea, S. V. Capuano, C. Fuhrman, E. Klein, and J. L. Flynn. 2009. Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect. Immun. 77: 4631-4642.
6. Leong, F., E. Seokyong, V. Laura, and B. Clifton. 2010. Pathology of Tuberculosis in the Human Lung. In A Color Atlas of Comparative Pathology of Pulmonary Tuberculosis. F. J. Leong, V. Dartois, and T. Dick, eds. CRC Press, Boca Raton, FL, p. 53-81.
7. Marino, S., J. J. Linderman, and D. E. Kirschner. 2011. A multifaceted approach to modeling the immune response in tuberculosis. Wiley Interdiscip Rev Syst Biol Med 3: 479-489.
8. Ray, J. C., J. L. Flynn, and D. E. Kirschner. 2009. Synergy between individual TNF-dependent functions determines granuloma performance for controlling Mycobacterium tuberculosis infection. J. Immunol. 182: 3706-3717.
9. Adams, L. B., M. C. Dinauer, D. E. Morgenstern, and J. L. Krahenbuhl. 1997. Comparison of the roles of reactive oxygen and nitrogen intermediates in the host response to Mycobacterium tuberculosis using transgenic mice. Tuber. Lung Dis. 78: 237-246. (Pubitemid 28389093)
10. 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.
11. Scanga, C. A., V. P. Mohan, K. Tanaka, D. Alland, J. L. Flynn, and J. Chan. 2001. The inducible nitric oxide synthase locus confers protection against aerogenic challenge of both clinical and laboratory strains of Mycobacterium tuberculosis in mice. Infect. Immun. 69: 7711-7717. (Pubitemid 33086601)
12. 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. (Pubitemid 34765454)
13. Schön, T., G. Elmberger, Y. Negesse, R. H. Pando, T. Sundqvist, and S. Britton. 2004. Local production of nitric oxide in patients with tuberculosis. Int. J. Tuberc. Lung Dis. 8: 1134-1137. (Pubitemid 39201262)
14. 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.
15. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97: 8841-8848. (Pubitemid 30626635)
16. Gordon, S., and F. O. Martinez. 2010. Alternative activation of macrophages: mechanism and functions. Immunity 32: 593-604.
17. Byers, D. E., and M. J. Holtzman. 2011. Alternatively activated macrophages and airway disease. Chest 140: 768-774.
18. Morris, S. M., Jr. 2007. Arginine metabolism: boundaries of our knowledge. J. Nutr. 137(Suppl 2)1602S-1609S.
19. 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.
20. Pesce, J. T., T. R. Ramalingam, M. M. Mentink-Kane, M. S. Wilson, K. C. El Kasmi, A. M. Smith, R. W. Thompson, A. W. Cheever, P. J. Murray, and T. A. Wynn. 2009. Arginase-1-expressing macrophages suppress Th2 cytokinedriven inflammation and fibrosis. PLoS Pathog. 5: e1000371.
21. Pegg, A. E. 2009. Mammalian polyamine metabolism and function. IUBMB Life 61: 880-894.
22. Barron, L., and T. A.Wynn. 2011. Macrophage activation governs schistosomiasisinduced inflammation and fibrosis. Eur. J. Immunol. 41: 2509-2514.
23. 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.
24. Schreiber, T., S. Ehlers, L. Heitmann, A. Rausch, J. Mages, P. J. Murray, R. Lang, and C. Hölscher. 2009. Autocrine IL-10 induces hallmarks of alternative activation in macrophages and suppresses antituberculosis effector mechanisms without compromising T cell immunity. J. Immunol. 183: 1301-1312.
25. 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.
26. Zea, A. H., K. S. Culotta, J. Ali, C. Mason, H. J. Park, J. Zabaleta, L. F. Garcia, and A. C. Ochoa. 2006. Decreased expression of CD3zeta and nuclear transcription factor kappa B in patients with pulmonary tuberculosis: potential mechanisms and reversibility with treatment. J. Infect. Dis. 194: 1385-1393. (Pubitemid 44706506)
27. Mosser, D. M. 2003. The many faces of macrophage activation. J. Leukoc. Biol. 73: 209-212. (Pubitemid 36158295)
28. Fallahi-Sichani, M., M. A. Schaller, D. E. Kirschner, S. L. Kunkel, and J. J. Linderman. 2010. Identification of key processes that control tumor necrosis factor availability in a tuberculosis granuloma. PLOS Comput. Biol. 6: e1000778.
29. Kepka-Lenhart, D., D. E. Ash, and S. M. Morris. 2008. Determination of mammalian arginase activity. Methods Enzymol. 440: 221-230.
30. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. (Pubitemid 34164012)
31. Pawar, S. N., J. T. Mattila, T. J. Sturgeon, P. L. Lin, O. Narayan, R. C. Montelaro, and J. L. Flynn. 2008. Comparison of the effects of pathogenic simian human immunodeficiency virus strains SHIV-89.6P and SHIV-KU2 in cynomolgus macaques. AIDS Res. Hum. Retroviruses 24: 643-654. (Pubitemid 351571043)
32. El-Zammar, O. A., and A. L. Katzenstein. 2007. Pathological diagnosis of granulomatous lung disease: a review. Histopathology 50: 289-310. (Pubitemid 46169414)
33. Jones, T. C., R. D. Hunt, and N. W. King. 1997. Veterinary Pathology. Williams & Wilkins, Baltimore, MD.
34. Turk, J. L., and R. B. Narayanan. 1982. The origin, morphology, and function of epithelioid cells. Immunobiology 161: 274-282. (Pubitemid 12120150)
35. Hamann, J., N. Koning, W. Pouwels, L. H. Ulfman, M. van Eijk, M. Stacey, H. H. Lin, S. Gordon, and M. J. Kwakkenbos. 2007. EMR1, the human homolog of F4/80, is an eosinophil-specific receptor. Eur. J. Immunol. 37: 2797-2802. (Pubitemid 47578299)
36. Chan, E. D., J. Chan, and N. W. Schluger. 2001. What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. Am. J. Respir. Cell Mol. Biol. 25: 606-612. (Pubitemid 33087112)
37. Nathan, C. 2006. Role of iNOS in human host defense. Science 312: 1874-1875; author reply 1874-1875.
38. Nathan, C. 2002. Inducible nitric oxide synthase in the tuberculous human lung. Am. J. Respir. Crit. Care Med. 166: 130-131. (Pubitemid 34765444)
39. Lee, W. L., B. Gold, C. Darby, N. Brot, X. Jiang, L. P. de Carvalho, D. Wellner, G. St John, W. R. Jacobs, Jr., and C. Nathan. 2009. Mycobacterium tuberculosis expresses methionine sulphoxide reductases A and B that protect from killing by nitrite and hypochlorite. Mol. Microbiol. 71: 583-593.
40. Ohno, H., G. Zhu, V. P. Mohan, D. Chu, S. Kohno, W. R. Jacobs, Jr., and J. Chan. 2003. The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell. Microbiol. 5: 637-648. (Pubitemid 37080674)
41. Darwin, K. H., S. Ehrt, J. C. Gutierrez-Ramos, N.Weich, and C. F. Nathan. 2003. The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302: 1963-1966. (Pubitemid 37523503)
42. Werner, E. R., A. C. Gorren, R. Heller, G. Werner-Felmayer, and B. Mayer. 2003. Tetrahydrobiopterin and nitric oxide: mechanistic and pharmacological aspects. Exp. Biol. Med. (Maywood) 228: 1291-1302. (Pubitemid 37549234)
43. Alp, N. J., and K. M. Channon. 2004. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler. Thromb. Vasc. Biol. 24: 413-420. (Pubitemid 38326132)
44. Xu, J., Z. Xie, R. Reece, D. Pimental, and M. H. Zou. 2006. Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: role of NAD(P)H oxidase-derived superoxide and peroxynitrite. Arterioscler. Thromb. Vasc. Biol. 26: 2688-2695.
45. Yu, K., C. Mitchell, Y. Xing, R. S. Magliozzo, B. R. Bloom, and J. Chan. 1999. Toxicity of nitrogen oxides and related oxidants on mycobacteria: M. tuberculosis is resistant to peroxynitrite anion. Tuber. Lung Dis. 79: 191-198. (Pubitemid 29446005)
46. Rodriguez, P. C., A. H. Zea, J. DeSalvo, K. S. Culotta, J. Zabaleta, D. G. Quiceno, J. B. Ochoa, and A. C. Ochoa. 2003. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J. Immunol. 171: 1232-1239. (Pubitemid 36900052)
47. Zea, A. H., P. C. Rodriguez, K. S. Culotta, C. P. Hernandez, J. DeSalvo, J. B. Ochoa, H. J. Park, J. Zabaleta, and A. C. Ochoa. 2004. L-Arginine modulates CD3zeta expression and T cell function in activated human T lymphocytes. Cell. Immunol. 232: 21-31. (Pubitemid 40732717)
48. Choi, B. S., I. C. Martinez-Falero, C. Corset, M. Munder, M. Modolell, I. Müller, and P. Kropf. 2009. Differential impact of L-arginine deprivation on the activation and effector functions of T cells and macrophages. J. Leukoc. Biol. 85: 268-277.
49. Mishra, B. B., V. A. Rathinam, G. W. Martens, A. J. Martinot, H. Kornfeld, K. A. Fitzgerald, and C. M. Sassetti. 2013. Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1 b. Nat. Immunol. 14: 52-60.
50. Biswas, S. K., and A. Mantovani. 2010. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11: 889-896.
51. Cassol, E., L. Cassetta, M. Alfano, and G. Poli. 2010. Macrophage polarization and HIV-1 infection. J. Leukoc. Biol. 87: 599-608.
52. Daley, J. M., S. K. Brancato, A. A. Thomay, J. S. Reichner, and J. E. Albina. 2010. The phenotype of murine wound macrophages. J. Leukoc. Biol. 87: 59-67.
53. Hesse, M., M. Modolell, A. C. 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-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 167: 6533-6544. (Pubitemid 33081589)
54. Niino, D., Y. Komohara, T. Murayama, R. Aoki, Y. Kimura, K. Hashikawa, J. Kiyasu, M. Takeuchi, N. Suefuji, Y. Sugita, et al. 2010. Ratio of M2 macrophage expression is closely associated with poor prognosis for Angioimmunoblastic T-cell lymphoma (AITL). Pathol. Int. 60: 278-283.
55. Stumpo, R., M. Kauer, S. Martin, and H. Kolb. 1999. Alternative activation of macrophage by IL-10. Pathobiology 67: 245-248. (Pubitemid 30135915)
56. Niemand, C., A. Nimmesgern, S. Haan, P. Fischer, F. Schaper, R. Rossaint, P. C. Heinrich, and G. Müller-Newen. 2003. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J. Immunol. 170: 3263-3272. (Pubitemid 36302204)
57. Ihling, C., H. R. Göbel, A. Lippoldt, S. Wessels, M. Paul, H. E. Schaefer, and A. M. Zeiher. 1996. Endothelin-1-like immunoreactivity in human atherosclerotic coronary tissue: a detailed analysis of the cellular distribution of endothelin-1. J. Pathol. 179: 303-308. (Pubitemid 26266410)
58. Cummings, T. J., C. M. Hulette, S. H. Bigner, G. J. Riggins, and R. E. McLendon. 2001. Ham56-immunoreactive macrophages in untreated infiltrating gliomas. Arch. Pathol. Lab. Med. 125: 637-641. (Pubitemid 32429810)
59. Oleszak, E. L., E. Zaczynska, M. Bhattacharjee, C. Butunoi, A. Legido, and C. D. Katsetos. 1998. Inducible nitric oxide synthase and nitrotyrosine are found in monocytes/macrophages and/or astrocytes in acute, but not in chronic, multiple sclerosis. Clin. Diagn. Lab. Immunol. 5: 438-445. (Pubitemid 28342866)
60. Peyron, P., J. Vaubourgeix, Y. Poquet, F. Levillain, C. Botanch, F. Bardou, M. Daffé, J. F. Emile, B. Marchou, P. J. Cardona, et al. 2008. Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog. 4: e1000204.
61. Lowe, D. M., P. S. Redford, R. J. Wilkinson, A. O'Garra, and A. R. Martineau. 2012. Neutrophils in tuberculosis: friend or foe? Trends Immunol. 33: 14-25.
62. Nandi, B., and S. M. Behar. 2011. Regulation of neutrophils by interferon-g limits lung inflammation during tuberculosis infection. J. Exp. Med. 208: 2251-2262.
63. Berry, M. P., C. M. Graham, F. W. McNab, Z. Xu, S. A. Bloch, T. Oni, K. A. Wilkinson, R. Banchereau, J. Skinner, R. J. Wilkinson, et al. 2010. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 466: 973-977.
64. Corleis, B., D. Korbel, R. Wilson, J. Bylund, R. Chee, and U. E. Schaible. 2012. Escape of Mycobacterium tuberculosis from oxidative killing by neutrophils. Cell. Microbiol. 14: 1109-1121.
65. Eum, S. Y., J. H. Kong, M. S. Hong, Y. J. Lee, J. H. Kim, S. H. Hwang, S. N. Cho, L. E. Via, and C. E. Barry, III. 2010. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 137: 122-128.
66. Pechkovsky, D. V., O. M. Zalutskaya, G. I. Ivanov, and N. I. Misuno. 2000. Calprotectin (MRP8/14 protein complex) release during mycobacterial infection in vitro and in vivo. FEMS Immunol. Med. Microbiol. 29: 27-33.
67. Scapini, P., J. A. Lapinet-Vera, S. Gasperini, F. Calzetti, F. Bazzoni, and M. A. Cassatella. 2000. The neutrophil as a cellular source of chemokines. Immunol. Rev. 177: 195-203.
68. Kasama, T., Y. Miwa, T. Isozaki, T. Odai, M. Adachi, and S. L. Kunkel. 2005. Neutrophil-derived cytokines: potential therapeutic targets in inflammation. Curr. Drug Targets Inflamm. Allergy 4: 273-279. (Pubitemid 40873111)
69. Tvinnereim, A. R., S. E. Hamilton, and J. T. Harty. 2004. Neutrophil involvement in cross-priming CD8+ T cell responses to bacterial antigens. J. Immunol. 173: 1994-2002. (Pubitemid 38971636)
70. Lin, P. L., V. Dartois, P. J. Johnston, C. Janssen, L. Via, M. B. Goodwin, E. Klein, C. E. Barry, III, and J. L. Flynn. 2012. Metronidazole prevents reactivation of latent Mycobacterium tuberculosis infection in macaques. Proc. Natl. Acad. Sci. USA 109: 14188-14193.