IL-17 stimulates differentiation of human anti-inflammatory macrophages and phagocytosis of apoptotic neutrophils in response to il-10 and glucocorticoids

Journal of Immunology

Volumn 190, Issue 10, 2013, Pages 5237-5246

  Zizzo, Gaetano ^a,b   Cohen, Philip L ^a,b  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; PROTEIN TYROSINE KINASE;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; DRUG RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE; NEUTROPHIL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

ANTI-INFLAMMATORY AGENTS; ANTIGENS, CD95; APOPTOSIS; CELL DIFFERENTIATION; CELLS, CULTURED; GLUCOCORTICOIDS; HUMANS; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKIN-4; MACROPHAGES; MONOCYTES; NEUTROPHILS; PHAGOCYTOSIS; PROTEIN ISOFORMS;

EID: 84877796414     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203017     Document Type: Article

References (60)

1. Estaquier, J., and J. C. Ameisen. 1997. A role for T-helper type-1 and type-2 cytokines in the regulation of human monocyte apoptosis. Blood 90: 1618-1625. (Pubitemid 27355435)
2. Schmidt, M., N. Lugering, H. G. Pauels, K. Schulze-Osthoff, W. Domschke, and T. Kucharzik. 2000. IL-10 induces apoptosis in human monocytes involving the CD95 receptor/ligand pathway. Eur. J. Immunol. 30: 1769-1777. (Pubitemid 30342821)
3. Schmidt, M., N. Lugering, A. Lugering, H. G. Pauels, K. Schulze-Osthoff, W. Domschke, and T. Kucharzik. 2001. Role of the CD95/CD95 ligand system in glucocorticoid-induced monocyte apoptosis. J. Immunol. 166: 1344-1351. (Pubitemid 32060297)
4. Ottonello, L., M. Bertolotto, F. Montecucco, P. Dapino, and F. Dallegri. 2005. Dexamethasone -induced apoptosis of human monocytes exposed to immune complexes. Intervention of CD95-And XIAP-dependent pathways. Int. J. Immunopathol. Pharmacol. 18: 403-415. (Pubitemid 41532357)
5. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13: 453-461. (Pubitemid 351599757)
6. Ehrchen, J., L. Steinmuller, K. Barczyk, K. Tenbrock, W. Nacken, M. Eisenacher, U. Nordhues, C. Sorg, C. Sunderkotter, and J. Roth. 2007. Glucocorticoids induce differentiation of a specifically activated, anti-inflammatory subtype of human monocytes. Blood 109: 1265-1274. (Pubitemid 46220679)
7. Sabat, R., G. Grutz, K. Warszawska, S. Kirsch, E. Witte, K. Wolk, and J. Geginat. 2010. Biology of interleukin-10. Cytokine Growth Factor Rev. 21: 331-344.
8. Savill, J. S., A. H. Wyllie, J. E. Henson, M. J. Walport, P. M. Henson, and C. Haslett. 1989. Macrophage phagocytosis of aging neutrophils in inflammation: programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83: 865-875. (Pubitemid 19080618)
9. Bratton, D. L., and P. M. Henson. 2011. Neutrophil clearance: when the party is over, clean-up begins. Trends Immunol. 32: 350-357.
10. Zizzo, G., B. A. Hilliard, M. Monestier, and P. L. Cohen. 2012. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J. Immunol. 189: 3508-3520.
11. McColl, A., S. Bournazos, S. Franz, M. Perretti, B. P. Morgan, C. Haslett, and I. Dransfield. 2009. Glucocorticoids induce protein S-dependent phagocytosis of apoptotic neutrophils by human macrophages. J. Immunol. 183: 2167-2175.
12. Zahuczky, G., E. Kristo'f, G. Majai, and L. Fe'sus. 2011. Differentiation and glucocorticoid regulated apopto-phagocytic gene expression patterns in human macrophages: role of Mertk in enhanced phagocytosis. PLoS ONE 6: e21349.
13. Sierra-Filardi, E., M. A. Vega, P. Sánchez-Mateos, A. L. Corbí, and A. Puig-Kroger. 2010. Heme oxygenase-1 expression in M-CSF-polarized M2 macrophages contributes to LPS-induced IL-10 release. Immunobiology 215: 788-795.
14. Alciato, F., P. P. Sainaghi, D. Sola, L. Castello, and G. C. Avanzi. 2010. TNF-A, IL-6, and IL-1 expression is inhibited by GAS6 in monocytes/macrophages. J. Leukoc. Biol. 87: 869-875.
15. Denny, M. F., P. Chandaroy, P. D. Killen, R. Caricchio, E. E. Lewis, B. C. Richardson, K. D. Lee, J. Gavalchin, and M. J. Kaplan. 2006. Accelerated macrophage apoptosis induces autoantibody formation and organ damage in systemic lupus erythematosus. J. Immunol. 176: 2095-2104. (Pubitemid 43201656)
16. Eken, C., P. J. Martin, S. Sadallah, S. Treves, M. Schaller, and J. A. Schifferli. 2010. Ectosomes released by polymorphonuclear neutrophils induce a MerTKdependent anti-inflammatory pathway in macrophages. J. Biol. Chem. 285: 39914-39921.
17. Fuchs, T. A., U. Abed, C. Goosmann, R. Hurwitz, I. Schulze, V. Wahn, Y.Weinrauch, V. Brinkmann, and A. Zychlinsky. 2007. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176: 231-241. (Pubitemid 46143263)
18. Cohen, P. L., R. Caricchio, V. Abraham, T. D. Camenisch, J. C. Jennette, R. A. Roubey, H. S. Earp, G. Matsushima, and E. A. Reap. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196: 135-140. (Pubitemid 34747319)
19. Munoz, L. E., C. Janko, G. E. Grossmayer, B. Frey, R. E. Voll, P. Kern, J. R. Kalden, G. Schett, R. Fietkau, M. Herrmann, and U. S. Gaipl. 2009. Remnants of secondarily necrotic cells fuel inflammation in systemic lupus erythematosus. Arthritis Rheum. 60: 1733-1742.
20. Rydell-Tormanen, K., L. Uller, and J. S. Erjefalt. 2006. Direct evidence of secondary necrosis of neutrophils during intense lung inflammation. Eur. Respir. J. 28: 268-274. (Pubitemid 44914224)
21. Krysko, O., P. Vandenabeele, D. V. Krysko, and C. Bachert. 2010. Impairment of phagocytosis of apoptotic cells and its role in chronic airway diseases. Apoptosis 15: 1137-1146.
22. Caudrillier, A., K. Kessenbrock, B. M. Gilliss, J. X. Nguyen, M. B. Marques, M. Monestier, P. Toy, Z. Werb, and M. R. Looney. 2012. Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury. J. Clin. Invest. 122: 2661-2671.
23. Villanueva, E., S. Yalavarthi, C. C. Berthier, J. B. Hodgin, R. Khandpur, A. M. Lin, C. J. Rubin, W. Zhao, S. H. Olsen, M. Klinker, et al. 2011. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 187: 538-552.
24. Kaplan, M. J. 2011. Neutrophils in the pathogenesis and manifestations of SLE. Nat. Rev. Rheumatol. 7: 691-699.
25. Lin, A. M., C. J. Rubin, R. Khandpur, J. Y. Wang, M. Riblett, S. Yalavarthi, E. C. Villanueva, P. Shah, M. J. Kaplan, and A. T. Bruce. 2011. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187: 490-500.
26. Ren, Y., J. Tang, M. Y. Mok, A. W. Chan, A. Wu, and C. S. Lau. 2003. Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum. 48: 2888-2897. (Pubitemid 37280618)
27. Suh, C. H., B. Hilliard, S. Li, J. T. Merrill, and P. L. Cohen. 2010. TAM receptor ligands in lupus: protein S but not Gas6 levels reflect disease activity in systemic lupus erythematosus. Arthritis Res. Ther. 12: R146.
28. Ambarus, C. A., S. Krausz, M. van Eijk, J. Hamann, T. R. Radstake, K. A. Reedquist, P. P. Tak, and D. L. Baeten. 2012. Systematic validation of specific phenotypic markers for in vitro polarized human macrophages. J. Immunol. Methods 375: 196-206.
29. Migdall-Wilson, J., C. Bates, J. Schlegel, L. Brandao, R. M. Linger, D. DeRyckere, and D. K. Graham. 2012. Prolonged exposure to a Mer ligand in leukemia: Gas6 favors expression of a partial Mer glycoform and reveals a novel role for Mer in the nucleus. PLoS ONE 7: e31635.
30. Giles, K. M., K. Ross, A. G. Rossi, N. A. Hotchin, C. Haslett, and I. Dransfield. 2001. Glucocorticoid augmentation of macrophage capacity for phagocytosis of apoptotic cells is associated with reduced p130Cas expression, loss of paxillin/ pyk2 phosphorylation, and high levels of active Rac. J. Immunol. 167: 976-986. (Pubitemid 32660855)
31. Stout, R. D., C. Jiang, B. Matta, I. Tietzel, S. K. Watkins, and J. Suttles. 2005. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175: 342-349. (Pubitemid 40884337)
32. Heasman, S. J., K. M. Giles, A. G. Rossi, J. E. Allen, C. Haslett, and I. Dransfield. 2004. Interferon g suppresses glucocorticoid augmentation of macrophage clearance of apoptotic cells. Eur. J. Immunol. 34: 1752-1761. (Pubitemid 39256058)
33. Hong, C., Y. Kidani, N. A-Gonzalez, T. Phung, A. Ito, X. Rong, K. Ericson, H. Mikkola, S. W. Beaven, L. S. Miller, et al. 2012. Coordinate regulation of neutrophil homeostasis by liver X receptors in mice. J. Clin. Invest. 122: 337-347.
34. Anwar, A., A. K. Keating, D. Joung, S. Sather, G. K. Kim, K. K. Sawczyn, L. Brandao, P. M. Henson, and D. K. Graham. 2009. Mer tyrosine kinase (MerTK) promotes macrophage survival following exposure to oxidative stress. J. Leukoc. Biol. 86: 73-79.
35. Barbarin, V., Z. Xing, M. Delos, D. Lison, and F. Huaux. 2005. Pulmonary overexpression of IL-10 augments lung fibrosis and Th2 responses induced by silica particles. Am. J. Physiol. Lung Cell. Mol. Physiol. 288: L841-L848. (Pubitemid 40547909)
36. Pechkovsky, D. V., A. Prasse, F. Kollert, K. M. Engel, J. Dentler, W. Luttmann, K. Friedrich, J. Muller-Quernheim, and G. Zissel. 2010. Alternatively activated alveolar macrophages in pulmonary fibrosis-mediator production and intracellular signal transduction. Clin. Immunol. 137: 89-101.
37. Barnes, P. J., and I. M. Adcock. 2009. Glucocorticoid resistance in inflammatory diseases. Lancet 373: 1905-1917.
38. Whitman, S. C., P. Ravisankar, and A. Daugherty. 2002. Interleukin-18 enhances atherosclerosis in apolipoprotein E2/2 mice through release of interferon-g. Circ. Res. 90: E34-E38.
39. Meduri, G. U., D. Annane, G. P. Chrousos, P. E. Marik, and S. E. Sinclair. 2009. Activation and regulation of systemic inflammation in ARDS: rationale for prolonged glucocorticoid therapy. Chest 136: 1631-1643.
40. Farrell, R. J., and D. Kelleher. 2003. Glucocorticoid resistance in inflammatory bowel disease. J. Endocrinol. 178: 339-346. (Pubitemid 37220161)
41. Deng, J., B. R. Younge, R. A. Olshen, J. J. Goronzy, and C. M. Weyand. 2010. Th17 and Th1 T-cell responses in giant cell arteritis. Circulation 121: 906-915.
42. Leung, D. Y., J. D. Spahn, and S. J. Szefler. 2002. Steroid-unresponsive asthma. Semin. Respir. Crit. Care Med. 23: 387-398. (Pubitemid 34971394)
43. Sumi, Y., and Q. Hamid. 2007. Airway remodeling in asthma. Allergol. Int. 56: 341-348. (Pubitemid 350306388)
44. Kumar, R. K., M. Yang, C. Herbert, and P. S. Foster. 2012. Interferon-g, pulmonary macrophages and airway responsiveness in asthma. Inflamm. Allergy Drug Targets 11: 292-297.
45. Sergejeva, S., S. Ivanov, J. Lotvall, and A. Lindén. 2005. Interleukin-17 as a recruitment and survival factor for airway macrophages in allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 33: 248-253. (Pubitemid 41254291)
46. Curtis, M. M., and S. S. Way. 2009. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126: 177-185.
47. Wong, C. K., L. C. Lit, L. S. Tam, E. K. Li, P. T. Wong, and C. W. Lam. 2008. Hyperproduction of IL-23 and IL-17 in patients with systemic lupus erythematosus: implications for Th17-mediated inflammation in auto-immunity. Clin. Immunol. 127: 385-393.
48. Zizzo, G., M. De Santis, S. L. Bosello, A. L. Fedele, G. Peluso, E. Gremese, B. Tolusso, and G. Ferraccioli. 2011. Synovial fluid-derived T helper 17 cells correlate with inflammatory activity in arthritis, irrespectively of diagnosis. Clin. Immunol. 138: 107-116.
49. Schwarzenberger, P., V. La Russa, A. Miller, P. Ye, W. Huang, A. Zieske, S. Nelson, G. J. Bagby, D. Stoltz, R. L. Mynatt, et al. 1998. IL-17 stimulates granulopoiesis in mice: use of an alternate, novel gene therapy-derived method for in vivo evaluation of cytokines. J. Immunol. 161: 6383-6389. (Pubitemid 28536015)
50. Laan, M., Z. H. Cui, H. Hoshino, J. Lotvall, M. Sjostrand, D. C. Gruenert, B. E. Skoogh, and A. Lindén. 1999. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J. Immunol. 162: 2347-2352. (Pubitemid 29288861)
51. Dragon, S., A. S. Saffar, L. Shan, and A. S. Gounni. 2008. IL-17 attenuates the anti-Apoptotic effects of GM-CSF in human neutrophils. Mol. Immunol. 45: 160-168. (Pubitemid 47331645)
52. Zhang, Z. G., Q. Y. He, X. M. Liu, X. Y. Tang, and L. Z. Chen. 2006. [Effect of interleukin-17 on neutrophil apoptosis]. Beijing Da Xue Xue Bao 38: 305-309.
53. Silverpil, E., P. Glader, M. Hansson, and A. Lindén. 2011. Impact of interleukin-17 on macrophage phagocytosis of apoptotic neutrophils and particles. Inflammation 34: 1-9.
54. Chanteux, H., A. C. Guisset, C. Pilette, and Y. Sibille. 2007. LPS induces IL-10 production by human alveolar macrophages via MAPKinases-And Sp1-dependent mechanisms. Respir. Res. 8: 71.
55. Jovanovic, D. V., J. A. Di Battista, J. Martel-Pelletier, F. C. Jolicoeur, Y. He, M. Zhang, F. Mineau, and J. P. Pelletier. 1998. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-b and TNF-A, by human macrophages. J. Immunol. 160: 3513-3521. (Pubitemid 28164746)
56. McGeachy, M. J., K. S. Bak-Jensen, Y. Chen, C. M. Tato, W. Blumenschein, T. McClanahan, and D. J. Cua. 2007. TGF-b and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397. (Pubitemid 350138974)
57. Naundorf, S., M. Schroder, C. Hoflich, N. Suman, H. D. Volk, and G. Grutz. 2009. IL-10 interferes directly with TCR-induced IFN-g but not IL-17 production in memory T cells. Eur. J. Immunol. 39: 1066-1077.
58. Fransen, J. H., L. B. Hilbrands, J. Ruben, M. Stoffels, G. J. Adema, J. van der Vlag, and J. H. Berden. 2009. Mouse dendritic cells matured by ingestion of apoptotic blebs induce T cells to produce interleukin-17. Arthritis Rheum. 60: 2304-2313.
59. Njoroge, J. M., L. B. Mitchell, M. Centola, D. Kastner, M. Raffeld, and J. L. Miller. 2001. Characterization of viable autofluorescent macrophages among cultured peripheral blood mononuclear cells. Cytometry 44: 38-44. (Pubitemid 32434001)
60. Reiter, C. 1986. Fluorescence test to identify deep smokers. Forensic Sci. Int. 31: 21-26. (Pubitemid 16105559)