Adenosine augments IL-10-induced STAT3 signaling in M2c macrophages

Journal of Leukocyte Biology

Volumn 94, Issue 6, 2013, Pages 1309-1315

  Koscsó, Balázs ^a   Csóka, Balázs ^a   Kókai, Endre ^a   Németh, Zoltán H ^c   Pacher, Pál ^d   Virág, László ^e   Joseph Leibovich, S ^a   Haskó, György ^a,b,e  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b The State University of New Jersey   (United States)

^c MORRISTOWN MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^e UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Alternative activation; Arginase; TIMP 1

Indexed keywords

ADENOSINE; ADENOSINE RECEPTOR; ARGINASE 1; INTERLEUKIN 10; SERUM AMYLOID A; SERUM AMYLOID A3; SMALL INTERFERING RNA; STAT3 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION REGULATION; HYPOXIA; INFLAMMATION; KNOCKOUT MOUSE; MACROPHAGE; MACROPHAGE ACTIVATION; METABOLIC DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WILD TYPE;

ALTERNATIVE ACTIVATION; ARGINASE; TIMP-1;

ADENOSINE; ADENOSINE A2 RECEPTOR AGONISTS; AMINOPYRIDINES; ANALGESICS; ANIMALS; ARGINASE; CELL LINE; GENE EXPRESSION REGULATION; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-4; INTERLEUKIN-6; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; RECEPTOR, ADENOSINE A2B; SERUM AMYLOID A PROTEIN; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84888781899     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0113043     Document Type: Article

References (53)

1. Sica, A., Mantovani, A. (2012) Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 122, 787-795.
2. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686.
3. Gordon, S., Martinez, F. O. (2010) Alternative activation of macrophages: mechanism and functions. Immunity 32, 593-604.
4. Sabat, R., Grutz, G., Warszawska, K., Kirsch, S., Witte, E., Wolk, K., Geginat, J. (2010) Biology of interleukin-10. Cytokine Growth Factor Rev. 21, 331-344.
5. Lacraz, S., Nicod, L. P., Chicheportiche, R., Welgus, H. G., Dayer, J. M. (1995) IL-10 inhibits metalloproteinase and stimulates TIMP-1 production in human mononuclear phagocytes. J. Clin. Invest. 96, 2304-2310.
6. Williams, L., Bradley, L., Smith, A., Foxwell, B. (2004) Signal transducer and activator of transcription 3 is the dominant mediator of the antiinflammatory effects of IL-10 in human macrophages. J. Immunol. 172, 567-576.
7. Moore, L., Fan, D., Basu, R., Kandalam, V., Kassiri, Z. (2012) Tissue inhibitor of metalloproteinases (TIMPs) in heart failure. Heart Fail. Rev. 17, 693-706.
8. Moore, C. S., Crocker, S. J. (2012) An alternate perspective on the roles of TIMPs and MMPs in pathology. Am. J. Pathol. 180, 12-16.
9. Moore, K. W., de Waal Malefyt, R., Coffman, R. L., O'Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683-765.
10. Murray, P. J. (2006) Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6, 379-386.
11. Dhingra, S., Bagchi, A. K., Ludke, A. L., Sharma, A. K., Singal, P. K. (2011) Akt regulates IL-10 mediated suppression of TNF-induced cardiomyocyte apoptosis by upregulating Stat3 phosphorylation. PLoS One 6, e25009.
12. Scheller, J., Chalaris, A., Schmidt-Arras, D., Rose-John, S. (2011) The proand anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 1813, 878-888.
13. Gabay, C., Kushner, I. (1999) Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340, 448-454.
14. King, V. L., Thompson, J., Tannock, L. R. (2011) Serum amyloid A in atherosclerosis. Curr. Opin. Lipidol. 22, 302-307.
15. Schuett, H., Luchtefeld, M., Grothusen, C., Grote, K., Schieffer, B. (2009) How much is too much? Interleukin-6 and its signalling in atherosclerosis. Thromb. Haemost. 102, 215-222.
16. Migita, K., Kawabe, Y., Tominaga, M., Origuchi, T., Aoyagi, T., Eguchi, K. (1998) Serum amyloid A protein induces production of matrix metalloproteinases by human synovial fibroblasts. Lab. Invest. 78, 535-539.
17. Connolly, M., Marrelli, A., Blades, M., McCormick, J., Maderna, P., Godson, C., Mullan, R., FitzGerald, O., Bresnihan, B., Pitzalis, C., Veale, D. J., Fearon, U. (2010) Acute serum amyloid A induces migration, angiogenesis, and inflammation in synovial cells in vitro and in a human rheumatoid arthritis/SCID mouse chimera model. J. Immunol. 184, 6427-6437.
18. Migita, K., Koga, T., Komori, A., Torigoshi, T., Maeda, Y., Izumi, Y., Sato, J., Jiuchi, Y., Miyashita, T., Yamasaki, S., Kawakami, A., Nakamura, M., Motokawa, S., Ishibashi, H. (2011) Influence of Janus kinase inhibition on interleukin 6-mediated induction of acute-phase serum amyloid A in rheumatoid synovium. J. Rheumatol. 38, 2309-2317.
19. Meek, R. L., Eriksen, N., Benditt, E. P. (1992) Murine serum amyloid A3 is a high density apolipoprotein and is secreted by macrophages. Proc. Natl. Acad. Sci. USA 89, 7949-7952.
20. Chiba, T., Han, C. Y., Vaisar, T., Shimokado, K., Kargi, A., Chen, M. H., Wang, S., McDonald, T. O., O'Brien, K. D., Heinecke, J. W., Chait, A. (2009) Serum amyloid A3 does not contribute to circulating SAA levels. J. Lipid Res. 50, 1353-1362.
21. Hiratsuka, S., Watanabe, A., Aburatani, H., Maru, Y. (2006) Tumourmediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat. Cell Biol. 8, 1369-1375.
22. Haskó, G., Pacher, P. (2012) Regulation of macrophage function by adenosine. Arterioscler. Thromb. Vasc. Biol. 32, 865-869.
23. Haskó, G., Cronstein, B. N. (2004) Adenosine: an endogenous regulator of innate immunity. Trends Immunol. 25, 33-39.
24. Colgan, S. P., Eltzschig, H. K., Eckle, T., Thompson, L. F. (2006) Physiological roles for ecto-5′-nucleotidase (CD73). Purinergic Signal. 2, 351-360.
25. Fredholm, B. B., IJzerman, A. P., Jacobson, K. A., Klotz, K. N., Linden, J. (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 53, 527-552.
26. Szabo, C., Scott, G. S., Virag, L., Egnaczyk, G., Salzman, A. L., Shanley, T. P., Haskó, G. (1998) Suppression of macrophage inflammatory protein (MIP)-1 production and collagen-induced arthritis by adenosine receptor agonists. Br. J. Pharmacol. 125, 379-387.
27. Haskó, G., Szabo, C., Nemeth, Z. H., Kvetan, V., Pastores, S. M., Vizi, E. S. (1996) Adenosine receptor agonists differentially regulate IL-10, TNF-, and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J. Immunol. 157, 4634-4640.
28. Haskó, G., Kuhel, D. G., Chen, J. F., Schwarzschild, M. A., Deitch, E. A., Mabley, J. G., Marton, A., Szabo, C. (2000) Adenosine inhibits IL-12 and TNF-production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J. 14, 2065-2074.
29. Chen, H., Yang, D., Carroll, S. H., Eltzschig, H. K., Ravid, K. (2009) Activation of the macrophage A2b adenosine receptor regulates tumor necrosis factorlevels following vascular injury. Exp. Hematol. 37, 533-538.
30. Csoka, B., Selmeczy, Z., Koscso, B., Nemeth, Z. H., Pacher, P., Murray, P. J., Kepka-Lenhart, D., Morris S. M., Jr., Gause, W. C., Leibovich, S. J., Haskó, G. (2012) Adenosine promotes alternative macrophage activation via A2A and A2B receptors. FASEB J. 26, 376-386.
31. Csoka, B., Nemeth, Z. H., Rosenberger, P., Eltzschig, H. K., Spolarics, Z., Pacher, P., Selmeczy, Z., Koscso, B., Himer, L., Vizi, E. S., Blackburn, M. R., Deitch, E. A., Haskó, G. (2010) A2B adenosine receptors protect against sepsis-induced mortality by dampening excessive inflammation. J. Immunol. 185, 542-550.
32. Csoka, B., Nemeth, Z. H., Virag, L., Gergely, P., Leibovich, S. J., Pacher, P., Sun, C. X., Blackburn, M. R., Vizi, E. S., Deitch, E. A., Haskó, G. (2007) A2A adenosine receptors and C/EBP÷ are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood 110, 2685-2695.
33. Koscso, B., Csoka, B., Selmeczy, Z., Himer, L., Pacher, P., Virag, L., Haskó, G. (2012) Adenosine augments IL-10 production by microglial cells through an A2B adenosine receptor-mediated process. J. Immunol. 188, 445-453.
34. Buenestado, A., Grassin Delyle, S., Arnould, I., Besnard, F., Naline, E., Blouquit-Laye, S., Chapelier, A., Bellamy, J. F., Devillier, P. (2010) The role of adenosine receptors in regulating production of tumour necrosis factorand chemokines by human lung macrophages. Br. J. Pharmacol. 159, 1304-1311.
35. Kreckler, L. M., Wan, T. C., Ge, Z. D., Auchampach, J. A. (2006) Adenosine inhibits tumor necrosis factorrelease from mouse peritoneal macrophages via A2A and A2B but not the A3 adenosine receptor. J. Pharmacol. Exp. Ther. 317, 172-180.
36. Ryzhov, S., Zaynagetdinov, R., Goldstein, A. E., Novitskiy, S. V., Blackburn, M. R., Biaggioni, I., Feoktistov, I. (2008) Effect of A2B adenosine receptor gene ablation on adenosine-dependent regulation of proinflammatory cytokines. J. Pharmacol. Exp. Ther. 324, 694-700.
37. Nemeth, Z. H., Lutz, C. S., Csoka, B., Deitch, E. A., Leibovich, S. J., Gause, W. C., Tone, M., Pacher, P., Vizi, E. S., Haskó, G. (2005) Adenosine augments IL-10 production by macrophages through an A2B receptor-mediated posttranscriptional mechanism. J. Immunol. 175, 8260-8270.
38. Ricchetti, G. A., Williams, L. M., Foxwell, B. M. (2004) Heme oxygenase 1 expression induced by IL-10 requires STAT-3 and phosphoinositol-3 kinase and is inhibited by lipopolysaccharide. J. Leukoc. Biol. 76, 719-726.
39. Dien, J., Amin, H. M., Chiu, N., Wong, W., Frantz, C., Chiu, B., Mackey, J. R., Lai, R. (2006) Signal transducers and activators of transcription-3 up-regulates tissue inhibitor of metalloproteinase-1 expression and decreases invasiveness of breast cancer. Am. J. Pathol. 169, 633-642.
40. Antoniv, T. T., Ivashkiv, L. B. (2011) Interleukin-10-induced gene expression and suppressive function are selectively modulated by the PI3KAkt-GSK3 pathway. Immunology 132, 567-577.
41. Li, J., Si, H. F., Lu, X., Guo, A., Jiang, H. (2008) Suppressive effects of leflunomide on leptin-induced TIMP-1 production involves on hepatic stellate cell proliferation and apoptosis. Eur. J. Pharmacol. 580, 63-69.
42. Jovanovic, D. V., Di Battista, J. A., Martel-Pelletier, J., Reboul, P., He, Y., Jolicoeur, F. C., Pelletier, J. P. (2001) Modulation of TIMP-1 synthesis by antiinflammatory cytokines and prostaglandin E2 in interleukin 17 stimulated human monocytes/macrophages. J. Rheumatol. 28, 712-718.
43. Neurath, M. F., Finotto, S. (2011) IL-6 signaling in autoimmunity, chronic inflammation and inflammation-associated cancer. Cytokine Growth Factor Rev. 22, 83-89.
44. Lang, R., Pauleau, A. L., Parganas, E., Takahashi, Y., Mages, J., Ihle, J. N., Rutschman, R., Murray, P. J. (2003) SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 4, 546-550.
45. Eulenfeld, R., Dittrich, A., Khouri, C., Muller, P. J., Mutze, B., Wolf, A., Schaper, F. (2012) Interleukin-6 signalling: more than Jaks and STATs. Eur. J. Cell Biol. 91, 486-495.
46. Duluc, D., Delneste, Y., Tan, F., Moles, M. P., Grimaud, L., Lenoir, J., Preisser, L., Anegon, I., Catala, L., Ifrah, N., Descamps, P., Gamelin, E., Gascan, H., Hebbar, M., Jeannin, P. (2007) Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 110, 4319-4330.
47. Allavena, P., Sica, A., Garlanda, C., Mantovani, A. (2008) The Yin-Yang of tumor-associated macrophages in neoplastic progression and immune surveillance. Immunol. Rev. 222, 155-161.
48. Coffelt, S. B., Hughes, R., Lewis, C. E. (2009) Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim. Biophys. Acta 1796, 11-18.
49. Novitskiy, S. V., Ryzhov, S., Zaynagetdinov, R., Goldstein, A. E., Huang, Y., Tikhomirov, O. Y., Blackburn, M. R., Biaggioni, I., Carbone, D. P., Feoktistov, I., Dikov, M. M. (2008) Adenosine receptors in regulation of dendritic cell differentiation and function. Blood 112, 1822-1831.
50. Ryzhov, S., Novitskiy, S. V., Zaynagetdinov, R., Goldstein, A. E., Carbone, D. P., Biaggioni, I., Dikov, M. M., Feoktistov, I. (2008) Host A(2B) adenosine receptors promote carcinoma growth. Neoplasia 10, 987-995.
51. Kujawski, M., Kortylewski, M., Lee, H., Herrmann, A., Kay, H., Yu, H. (2008) Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice. J. Clin. Invest. 118, 3367-3377.
52. Zhang, L., Alizadeh, D., Van Handel, M., Kortylewski, M., Yu, H., Badie, B. (2009) Stat3 inhibition activates tumor macrophages and abrogates glioma growth in mice. Glia 57, 1458-1467.
53. Cekic, C., Sag, D., Li, Y., Theodorescu, D., Strieter, R. M., Linden, J. (2012) Adenosine A2B receptor blockade slows growth of bladder and breast tumors. J. Immunol. 188, 198-205.