Understanding the molecular mechanisms of the multifaceted IL-10-mediated anti-inflammatory response: Lessons from neutrophils

European Journal of Immunology

Volumn 40, Issue 9, 2010, Pages 2360-2368

  Bazzoni, Flavia ^a   Tamassia, Nicola ^a   Rossato, Marzia ^a   Cassatella, Marco A ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

IL 10; LPS; Monocytes; Neutrophils; STAT3

Indexed keywords

ANTIINFLAMMATORY AGENT; AUTACOID; CYTOKINE; INTERLEUKIN 10;

ANIMAL; CHRONIC OBSTRUCTIVE LUNG DISEASE; GENE EXPRESSION REGULATION; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; METABOLISM; NEUTROPHIL; OSTEOARTHRITIS; RHEUMATOID ARTHRITIS; SEPSIS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ARTHRITIS, RHEUMATOID; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; IMMUNOMODULATION; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-10; NEUTROPHILS; OSTEOARTHRITIS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SEPSIS;

EID: 77956494550     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200940294     Document Type: Short Survey

References (85)

1. Moore, K. W., de Waal Malefyt, R., Coffman, R. L. and O'Garra, A., Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 2001. 19: 683-765.
2. Riley, J. K., Takeda, K., Akira, S. and Schreiber, R. D., Interleukin-10 receptor signaling through the JAK-STAT pathway. Requirement for two distinct receptor-derived signals for anti-inflammatory action. J. Biol. Chem. 1999. 274: 16513-16521.
3. Takeda, K., Noguchi, K., Shi, W., Tanaka, T., Matsumoto, M., Yoshida, N., Kishimoto, T. and Akira, S., Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. USA 1997. 94: 3801-3804.
4. Williams, L., Bradley, L., Smith, A. and Foxwell, B., Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J. Immunol. 2004. 172: 567-576. (Pubitemid 38020514)
5. Grutz, G., New insights into the molecular mechanism of interleukin-10-mediated immunosuppression. J. Leukoc. Biol. 2005. 77: 3-15.
6. Cassatella, M. A., Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 1999. 73: 369-509.
7. Cassatella,M.-A. (Ed.) The Neutrophil: An Emerging Regulator of Inflammatory And Immune Response, Karger, Basle 2003.
8. Nathan, C., Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 2006. 6: 173-182.
9. Cassatella, M. A., The neutrophil: one of the cellular targets of interleukin-10. Int. J. Clin. Lab. Res. 1998. 28: 148-161.
10. Cassatella, M. A., Meda, L., Bonora, S., Ceska, M. and Constantin, G., Interleukin 10 (IL-10) inhibits the release of proinflammatory cytokines from human polymorphonuclear leukocytes. Evidence for an autocrine role of tumor necrosis factor and IL-1 beta in mediating the production of IL-8 triggered by lipopolysaccharide. J. Exp. Med. 1993. 178: 2207-2211.
11. Kasama, T., Strieter, R. M., Lukacs, N.W., Burdick, M. D. and Kunkel, S. L., Regulation of neutrophil-derived chemokine expression by IL-10. J. Immunol. 1994. 152: 3559-3569.
12. Cassatella, M. A., Meda, L., Gasperini, S., Calzetti, F. and Bonora, S., Interleukin 10 (IL-10) upregulates IL-1 receptor antagonist production from lipopolysaccharide-stimulated human polymorphonuclear leukocytes by delaying mRNA degradation. J. Exp. Med. 1994. 179: 1695-1699.
13. Crepaldi, L., Gasperini, S., Lapinet, J. A., Calzetti, F., Pinardi, C., Liu, Y., Zurawski, S. et al., Up-regulation of IL-10R1 expression is required to render human neutrophils fully responsive to IL-10. J. Immunol. 2001. 167: 2312-2322.
14. Crepaldi, L., Silveri, L., Calzetti, F., Pinardi, C. and Cassatella, M. A., Molecular basis of the synergistic production of IL-1 receptor antagonist by human neutrophils stimulated with IL-4 and IL-10. Int. Immunol. 2002. 14: 1145-1153.
15. Tamassia, N., Calzetti, F., Menestrina, N., Rossato, M., Bazzoni, F., Gottin, L. and Cassatella, M. A., Circulating neutrophils of septic patients constitutively express IL-10R1 and are promptly responsive to IL-10. Int. Immunol. 2008. 20: 535-541.
16. Petit-Bertron, A. F., Tabary, O., Corvol, H., Jacquot, J., Clement, A., Cavaillon, J. M. and Adib-Conquy, M., Circulating and airway neutrophils in cystic fibrosis display different TLR expression and responsiveness to interleukin-10. Cytokine 2008. 41: 54-60.
17. Pang, G., Ortega, M., Zighang, R., Reeves, G. and Clancy, R., Autocrine modulation of IL-8 production by sputum neutrophils in chronic bronchial sepsis. Am. J. Respir. Crit. Care Med. 1997. 155: 726-731.
18. Du, Z., Kelly, E., Mecklenbrauker, I., Agle, L., Herrero, C., Paik, P. and Ivashkiv, L. B., Selective regulation of IL-10 signaling and function by zymosan. J. Immunol. 2006. 176: 4785-4792.
19. Ji, J. D., Tassiulas, I., Park-Min, K. H., Aydin, A., Mecklenbrauker, I., Tarakhovsky, A., Pricop, L. et al., Inhibition of interleukin 10 signaling after Fc receptor ligation and during rheumatoid arthritis. J. Exp. Med. 2003. 197: 1573-1583.
20. Corinti, S., Albanesi, C., la Sala, A., Pastore, S. and Girolomoni, G., Regulatory activity of autocrine IL-10 on dendritic cell functions. J. Immunol. 2001. 166: 4312-4318. (Pubitemid 32233711)
21. Thomas, R. and Quinn, C., Functional differentiation of dendritic cells in rheumatoid arthritis: role of CD86 in the synovium. J. Immunol. 1996. 156: 3074-3086. (Pubitemid 126660659)
22. MacDonald, K. P., Pettit, A. R., Quinn, C., Thomas, G. J. and Thomas, R., Resistance of rheumatoid synovial dendritic cells to the immunosuppressive effects of IL-10. J. Immunol. 1999. 163: 5599-5607.
23. Moniuszko, M., Bodzenta-Lukaszyk, A. and Dabrowska, M., Oral glucocorticoid treatment decreases interleukin-10 receptor expression on peripheral blood leucocyte subsets. Clin. Exp. Immunol. 2009. 156: 328-335.
24. Stelmach, I., Jerzynska, J. and Kuna, P., A randomized, double-blind trial of the effect of glucocorticoid, antileukotriene and beta-agonist treatment on IL-10 serum levels in children with asthma. Clin. Exp. Allergy 2002. 32: 264-269.
25. Murray, P. J., The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc. Natl. Acad. Sci. USA 2005. 102: 8686-8691.
26. Rossato, M., Cencig, S., Gasperini, S., Cassatella, M. A. and Bazzoni, F., IL-10 modulates cytokine gene transcription by protein synthesis-independent and dependent mechanisms in lipopolysaccharide-treated neutrophils. Eur. J. Immunol. 2007. 37: 3176-3189.
27. Ji, J. D., Kim, H. J., Rho, Y. H., Choi, S. J., Lee, Y. H., Cheon, H. J., Sohn, J. and Song, G. G., Inhibition of IL-10-induced STAT3 activation by 15-deoxy-Delta12,14-prostaglandin J2. Rheumatology (Oxford) 2005. 44: 983-988. (Pubitemid 41487169)
28. Murray, P. J., The JAK-STAT signaling pathway: input and output integration. J. Immunol. 2007. 178: 2623-2629.
29. Yoshimura, A., Naka, T. and Kubo, M., SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 2007. 7: 454-465.
30. El Kasmi, K. C., Holst, J., Coffre, M., Mielke, L., de Pauw, A., Lhocine, N. et al., General nature of the STAT3-activated anti-inflammatory response. J. Immunol. 2006. 177: 7880-7888. (Pubitemid 44846303)
31. Yasukawa, H., Ohishi, M., Mori, H., Murakami, M., Chinen, T., Aki, D., Hanada, T. et al., IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 2003. 4: 551-556.
32. Kuwata, H., Watanabe, Y., Miyoshi, H., Yamamoto, M., Kaisho, T., Takeda, K. and Akira, S., IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-alpha production in macrophages. Blood 2003. 102: 4123-4129. (Pubitemid 37486997)
33. Lee, T. S. and Chau, L. Y., Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 2002. 8: 240-246.
34. Weaver, B. K., Bohn, E., Judd, B. A., Gil, M. P. and Schreiber, R. D., ABIN-3: a molecular basis for species divergence in interleukin-10-induced anti-inflammatory actions. Mol. Cell. Biol. 2007. 27: 4603-4616.
35. Hirotani, T., Lee, P. Y., Kuwata, H., Yamamoto, M.,Matsumoto,M., Kawase, I., Akira, S. and Takeda, K., The nuclear IkappaB protein IkappaBNS selectively inhibits lipopolysaccharide-induced IL-6 production in macrophages of the colonic lamina propria. J. Immunol. 2005. 174: 3650-3657. (Pubitemid 40354075)
36. Kuwata, H., Matsumoto, M., Atarashi, K., Morishita, H., Hirotani, T., Koga, R. and Takeda, K., IkappaBNS inhibits induction of a subset of Toll-like receptor-dependent genes and limits inflammation. Immunity 2006. 24: 41-51.
37. El Kasmi, K. C., Smith, A. M., Williams, L., Neale, G., Panopoulos, A. D., Watowich, S. S., Hacker, H. et al., Cutting edge: a transcriptional repressor and corepressor induced by the STAT3-regulated anti-inflammatory signaling pathway. J. Immunol. 2007. 179: 7215-7219.
38. Cassatella, M. A., Gasperini, S., Bovolenta, C., Calzetti, F., Vollebregt, M., Scapini, P., Marchi, M. et al., Interleukin-10 (IL-10) selectively enhances CIS3/SOCS3 mRNA expression in human neutrophils: evidence for an IL-10-induced pathway that is independent of STAT protein activation. Blood 1999. 94: 2880-2889.
39. Ito, S., Ansari, P., Sakatsume, M., Dickensheets, H., Vazquez, N., Donnelly, R. P., Larner, A. C. and Finbloom, D. S., Interleukin-10 inhibits expression of both interferon alpha- and interferon gamma-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 1999. 93: 1456-1463.
40. Berlato, C., Cassatella, M. A., Kinjyo, I., Gatto, L., Yoshimura, A. and Bazzoni, F., Involvement of suppressor of cytokine signaling-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol. 2002. 168: 6404-6411.
41. Lang, R., Pauleau, A. L., Parganas, E., Takahashi, Y., Mages, J., Ihle, J. N., Rutschman, R. and Murray, P. J., SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 2003. 4: 546-550.
42. Cassatella, M. A., Tamassia, N., Crepaldi, L., McDonald, P. P., Ear, T., Calzetti, F., Gasperini, S. et al., Lipopolysaccharide primes neutrophils for a rapid response to IL-10. Eur. J. Immunol. 2005. 35: 1877-1885.
43. Hoentjen, F., Sartor, R. B., Ozaki, M. and Jobin, C., STAT3 regulates NF-kappaB recruitment to the IL-12p40 promoter in dendritic cells. Blood 2005. 105: 689-696.
44. Jenkins, J. K., Malyak, M. and Arend, W. P., The effects of interleukin-10 on interleukin-1 receptor antagonist and interleukin-1 beta production in human monocytes and neutrophils. Lymphokine Cytokine Res. 1994. 13: 47-54.
45. Balavoine, J. F., de Rochemonteix, B., Williamson, K., Seckinger, P., Cruchaud, A. and Dayer, J. M., Prostaglandin E2 and collagenase production by fibroblasts and synovial cells is regulated by urine-derived human interleukin 1 and inhibitor(s). J. Clin. Invest. 1986. 78: 1120-1124.
46. Arend, W. P., The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev. 2002. 13: 323-340.
47. Horai, R., Saijo, S., Tanioka, H., Nakae, S., Sudo, K., Okahara, A., Ikuse, T. et al., Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J. Exp. Med. 2000. 191: 313-320.
48. Nicklin, M. J., Hughes, D. E., Barton, J. L., Ure, J. M. and Duff, G. W., Arterial inflammation in mice lacking the interleukin 1 receptor antagonist gene. J. Exp. Med. 2000. 191: 303-312.
49. Palmer, G., Talabot-Ayer, D., Kaya, G. and Gabay, C., Type I IL-1 receptor mediates IL-1 and intracellular IL-1 receptor antagonist effects in skin inflammation. J. Invest. Dermatol. 2007. 127: 1938-1946.
50. Lamacchia, C., Palmer, G., Seemayer, C. A., Talabot-Ayer, D. and Gabay, C., Enhanced Th1 and Th17 responses and arthritis severity in mice with a deficiency of myeloid cell-specific interleukin-1 receptor antagonist. Arthritis Rheum. 2010. 62: 452-462.
51. Aksentijevich, I., Masters, S. L., Ferguson, P. J., Dancey, P., Frenkel, J., van Royen-Kerkhoff, A., Laxer, R. et al., An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N. Engl. J. Med. 2009. 360: 2426-2437.
52. Reddy, S., Jia, S., Geoffrey, R., Lorier, R., Suchi, M., Broeckel, U., Hessner, M. J. and Verbsky, J., An autoinflammatory disease due to homozygous deletion of the IL1RN locus. N. Engl. J. Med. 2009. 360: 2438-2444.
53. Tamassia, N., Castellucci, M., Rossato, M., Gasperini, S., Bosisio, D., Giacomelli, M., Badolato, R. et al., Uncovering an IL-10-dependent NF-{kappa} B recruitment to the IL-1ra promoter that is impaired in STAT3 functionally defective patients. FASEB J. 2010. 24: 1365-1375.
54. Lang, R., Patel, D., Morris, J. J., Rutschman, R. L. and Murray, P. J., Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 2002. 169: 2253-2263.
55. Minegishi, Y., Saito, M., Tsuchiya, S., Tsuge, I., Takada, H., Hara, T., Kawamura, N. et al., Dominant-negative mutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 2007. 448: 1058-1062.
56. Carl, V. S., Gautam, J. K., Comeau, L. D. and Smith, M. F., Jr., Role of endogenous IL-10 in LPS-induced STAT3 activation and IL-1 receptor antagonist gene expression. J. Leukoc. Biol. 2004. 76: 735-742.
57. Cheung,W. L., Briggs, S. D. and Allis, C. D., Acetylation and chromosomal functions. Curr. Opin. Cell. Biol. 2000. 12: 326-333.
58. Strahl, B. D. and Allis, C. D., The language of covalent histone modifications. Nature 2000. 403: 41-45.
59. Tse, C., Sera, T.,Wolffe, A. P. and Hansen, J. C., Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol. Cell. Biol. 1998. 18: 4629-4638.
60. Natoli, G., Tuning up inflammation: how DNA sequence and chromatin organization control the induction of inflammatory genes by NF-kappaB. FEBS Lett. 2006. 580: 2843-2849.
61. Li, B., Carey, M. and Workman, J. L., The role of chromatin during transcription. Cell 2007. 128: 707-719.
62. Cloutier, A., Guindi, C., Larivee, P., Dubois, C. M., Amrani, A. and McDonald, P. P., Inflammatory cytokine production by human neutrophils involves C/EBP transcription factors. J. Immunol. 2009. 182: 563-571.
63. Bober, L. A., Rojas-Triana, A., Jackson, J. V., Leach, M. W., Manfra, D., Narula, S. K. and Grace, M. J., Regulatory effects of interleukin-4 and interleukin-10 on human neutrophil function ex vivo and on neutrophil influx in a rat model of arthritis. Arthritis Rheum. 2000. 43: 2660-2667.
64. Murakami, Y., Akahoshi, T., Kawai, S., Inoue, M. and Kitasato, H., Antiinflammatory effect of retrovirally transfected interleukin-10 on monosodium urate monohydrate crystal-induced acute inflammation in murine air pouches. Arthritis Rheum. 2002. 46: 2504-2513.
65. Ajuebor, M. N., Das, A. M., Virag, L., Szabo, C. and Perretti, M., Regulation of macrophage inflammatory protein-1 alpha expression and function by endogenous interleukin-10 in a model of acute inflammation. Biochem. Biophys. Res. Commun. 1999. 255: 279-282.
66. Inoue, G., Effect of interleukin-10 (IL-10) on experimental LPS-induced acute lung injury. J. Infect. Chemother. 2000. 6: 51-60.
67. Mulligan, M. S., Warner, R. L., Foreback, J. L., Shanley, T. P. and Ward, P. A., Protective effects of IL-4, IL-10, IL-12, and IL-13 in IgG immune complex-induced lung injury: role of endogenous IL-12. J. Immunol. 1997. 159: 3483-3489.
68. Shanley, T. P., Schmal, H., Friedl, H. P., Jones, M. L. and Ward, P. A., Regulatory effects of intrinsic IL-10 in IgG immune complex-induced lung injury. J. Immunol. 1995. 154: 3454-3460.
69. Roilides, E., Katsifa, H., Tsaparidou, S., Stergiopoulou, T., Panteliadis, C. and Walsh, T. J., Interleukin 10 suppresses phagocytic and antihyphal activities of human neutrophils. Cytokine 2000. 12: 379-387.
70. Sun, L., Guo, R. F., Newstead, M. W., Standiford, T. J., Macariola, D. R. and Shanley, T. P., Effect of IL-10 on neutrophil recruitment and survival after Pseudomonas aeruginosa challenge. Am. J. Respir. Cell. Mol. Biol. 2009. 41: 76-84.
71. van der Sluijs, K. F., van Elden, L. J., Nijhuis, M., Schuurman, R., Pater, J. M., Florquin, S., Goldman, M. et al., IL-10 is an important mediator of the enhanced susceptibility to pneumococcal pneumonia after influenza infection. J. Immunol. 2004. 172: 7603-7609.
72. Hayward, R., Nossuli, T. O., Scalia, R. and Lefer, A. M., Cardioprotective effect of interleukin-10 in murine myocardial ischemia-reperfusion. Eur. J. Pharmacol. 1997. 334: 157-163.
73. Dinant, S., Vetelainen, R. L., Florquin, S., van Vliet, A. K. and van Gulik, T. M., IL-10 attenuates hepatic I/R injury and promotes hepatocyte proliferation. J. Surg. Res. 2007. 141: 176-182.
74. Lane, J. S., Todd, K. E., Lewis, M. P., Gloor, B., Ashley, S. W., Reber, H. A., McFadden, D.W. and Chandler, C. F., Interleukin-10 reduces the systemic inflammatory response in a murine model of intestinal ischemia/reperfusion. Surgery 1997. 122: 288-294.
75. Hess, P. J., Seeger, J. M., Huber, T. S., Welborn, M. B., Martin, T. D., Harward, T. R., Duschek, S. et al., Exogenously administered interleukin-10 decreases pulmonary neutrophil infiltration in a tumor necrosis factor-dependent murine model of acute visceral ischemia. J. Vasc. Surg. 1997. 26: 113-118.
76. Fine, J. S., Rojas-Triana, A., Jackson, J. V., Engstrom, L. W., Deno, G. S., Lundell, D. J. and Bober, L. A., Impairment of leukocyte trafficking in amurine pleuritismodel by IL-4 and IL-10. Inflammation 2003. 27: 161-174.
77. Fu, C. L., Chuang, Y. H., Chau, L. Y. and Chiang, B. L., Effects of adenovirus-expressing IL-10 in alleviating airway inflammation in asthma. J. Gene. Med. 2006. 8: 1393-1399.
78. Kobbe, P., Schmidt, J., Stoffels, B., Chanthaphavong, R. S., Bauer, A. J. and Pape, H. C., IL-10 administration attenuates pulmonary neutrophil infiltration and alters pulmonary iNOS activation following hemorrhagic shock. Inflamm. Res. 2009. 58: 170-174.
79. Cox, G., IL-10 enhances resolution of pulmonary inflammation in vivo by promoting apoptosis of neutrophils. Am. J. Physiol. 1996. 271: L566-L571.
80. Shanley, T. P., Vasi, N. and Denenberg, A., Regulation of chemokine expression by IL-10 in lung inflammation. Cytokine 2000. 12: 1054-1064.
81. Ajuebor, M. N., Das, A. M., Virag, L., Flower, R. J., Szabo, C. and Perretti, M., Role of resident peritoneal macrophages and mast cells in chemokine production and neutrophil migration in acute inflammation: evidence for an inhibitory loop involving endogenous IL-10. J. Immunol. 1999. 162: 1685-1691.
82. Louis, H., Van Laethem, J. L., Wu, W., Quertinmont, E., Degraef, C., Van den Berg, K., Demols, A. et al., Interleukin-10 controls neutrophilic infiltration, hepatocyte proliferation, and liver fibrosis induced by carbon tetrachloride in mice. Hepatology 1998. 28: 1607-1615.
83. Ismail, H. F., Fick, P., Zhang, J., Lynch, R. G. and Berg, D. J., Depletion of neutrophils in IL-10(-/-) mice delays clearance of gastric Helicobacter infection and decreases the Th1 immune response to Helicobacter. J. Immunol. 2003. 170: 3782-3789.
84. Pils,M. C., Pisano, F., Fasnacht, N., Heinrich, J.M., Groebe, L., Schippers, A., Rozell, B., Jack, R. S. and Muller, W., Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur. J. Immunol. 2010. 40: 443-448.
85. Zhang, X., Majlessi, L., Deriaud, E., Leclerc, C. and Lo-Man, R., Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 2009. 31: 761-771.