New insights into the role of mast cells in autoimmunity: Evidence for a common mechanism of action?

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 1, 2012, Pages 57-65

  Walker, Margaret E ^a   Hatfield, Julianne K ^a   Brown, Melissa A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Autoimmunity; Inflammation; Mast cells; Neutrophils; TNF

Indexed keywords

ARGINASE 1; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 33; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPONTIN; SUBSTANCE P; TUMOR NECROSIS FACTOR;

ASTROCYTE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; BULLOUS PEMPHIGOID; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; ENDOCRINE OPHTHALMOPATHY; GUILLAIN BARRE SYNDROME; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE PROLIFERATION; MAST CELL; MULTIPLE SCLEROSIS; NONHUMAN; PEMPHIGUS VULGARIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SJOEGREN SYNDROME; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION; TH17 CELL;

ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; B-LYMPHOCYTES; CENTRAL NERVOUS SYSTEM; HUMANS; HYPERSENSITIVITY; IMMUNOMODULATION; INFLAMMATION; INFLAMMATION MEDIATORS; MAST CELLS; T-LYMPHOCYTES;

MURINAE;

EID: 82955198480     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.02.009     Document Type: Review

References (96)

1. Okayama Y., Kawakami T. Development, migration, and survival of mast cells. Immunol. Res. 2006, 34:97-115.
2. Rao K.N., Brown M.A. Mast cells: multifaceted immune cells with diverse roles in health and disease. Ann. NY Acad. Sci. 2008, 1143:83-104.
3. Metz M., Maurer M. Mast cells-key effector cells in immune responses. Trends Immunol. 2007, 28:234-241.
4. Kneilling M., Rocken M. Mast cells: novel clinical perspectives from recent insights. Exp. Dermatol. 2009, 18:488-496.
5. Kalesnikoff J., Galli S.J. New developments in mast cell biology. Nat. Immunol. 2008, 9:1215-1223.
6. Sayed B.A., Christy A., Quirion M.R., Brown M.A. The master switch: the role of mast cells in autoimmunity and tolerance. Annu. Rev. Immunol. 2008, 26:705-739.
7. Wei O.L., Hilliard A., Kalman D., Sherman M. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect. Immun. 2005, 73:1978-1985.
8. Velin D., Bachmann D., Bouzourene H., Michetti P. Mast cells are critical mediators of vaccine-induced Helicobacter clearance in the mouse model. Gastroenterology 2005, 129:142-155.
9. Lawrence C.E., Paterson Y.Y., Wright S.H., Knight P.A., Miller H.R. Mouse mast cell protease-1 is required for the enteropathy induced by gastrointestinal helminth infection in the mouse. Gastroenterology 2004, 127:155-165.
10. Anthony R.M., Rutitzky L.I., Urban J.F., Stadecker M.J., Gause W.C. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 2007, 7:975-987.
11. Sundstrom J.B., Hair G.A., Ansari A.A., Secor W.E., Gilfillan A.M., Metcalfe D.D., Kirshenbaum A.S. IgE-FcepsilonRI interactions determine HIV coreceptor usage and susceptibility to infection during ontogeny of mast cells. J. Immunol. 2009, 182:6401-6409.
12. Taub D.D., Mikovits J.A., Nilsson G., Schaffer E.M., Key M.L., Petrow-Sadowski C., Ruscetti F.W. Alterations in mast cell function and survival following in vitro infection with human immunodeficiency viruses-1 through CXCR4. Cell. Immunol. 2004, 230:65-80.
13. Becker Y. HIV-1 induced AIDS is an allergy and the allergen is the Shed gp120-a review, hypothesis, and implications. Virus Genes 2004, 28:319-331.
14. Kitamura Y., Go S., Hatanaka K. Decrease of mast cells in W/Wv mice and their increase by bone marrow transplantation. Blood 1978, 52:447-452.
15. Nakano T., Sonoda T., Hayashi C., Yamatodani A., Kanayama Y., Yamamura T., Asai H., Yonezawa T., Kitamura Y., Galli S.J. Fate of bone marrow-derived cultured mast cells after intracutaneous, intraperitoneal, and intravenous transfer into genetically mast cell-deficient W/Wv mice. Evidence that cultured mast cells can give rise to both connective tissue type and mucosal mast cells. J Exp Med 1985, 162:1025-1043.
16. Galli S.J., Kitamura Y. Genetically mast-cell-deficient W/Wv and Sl/Sld mice. Their value for the analysis of the roles of mast cells in biologic responses in vivo. Am J Pathol 1987, 127:191-198.
17. Grimbaldeston M.A., Chen C.C., Piliponsky A.M., Tsai M., Tam S.Y., Galli S.J. Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am. J. Pathol. 2005, 167:835-848.
18. Nautiyal K.M., Ribeiro A.C., Pfaff D.W., Silver R. Brain mast cells link the immune system to anxiety-like behavior. Proc. Natl Acad. Sci. USA 2008, 105:18053-18057.
19. Tanzola M.B., Robbie-Ryan M., Gutekunst C.A., Brown M.A. Mast cells exert effects outside the central nervous system to influence experimental allergic encephalomyelitis disease course. J. Immunol. 2003, 171:4385-4391.
20. Sayed B.A., Christy A.L., Walker M.E., Brown M.A. Meningeal mast cells affect early T cell central nervous system infiltration and blood-brain barrier integrity through TNF: a role for neutrophil recruitment?. J. Immunol. 2010, 184:6891-6900.
21. Chiaravalloti N.D., DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008, 7:1139-1151.
22. F.D. Lublin, Clinical features and diagnosis of multiple sclerosis, Neurol Clin 23 (2005) 1-15, v.
23. Olitsky P.K., Yager R.H. Experimental disseminated encephalomyelitis in white mice. J. Exp. Med. 1949, 90:213-224.
24. Wekerle H. Lessons from multiple sclerosis: models, concepts, observations. Ann. Rheum. Dis. 2008, 67(Suppl 3):iii56-iii60.
25. Kermode A.G., Thompson A.J., Tofts P., MacManus D.G., Kendall B.E., Kingsley D.P., Moseley I.F., Rudge P., McDonald W.I. Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenet Clin Implicat, Brain 1990, 113(Pt 5):1477-1489.
26. Steinman L. Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system. Cell 1996, 85:299-302.
27. Jager A., Kuchroo V.K. Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand. J. Immunol. 2010, 72:173-184.
28. Fletcher J.M., Lalor S.J., Sweeney C.M., Tubridy N., Mills K.H. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 2010, 162:1-11.
29. Neuman J. Ueber das Vorkommen der sogneannten "Mastzellen" bei pathologischen Veraenderungen des Gehirns. Arch. Pathol Anat. Physiol. Virchows 1890, 122:378-381.
30. Bebo B.F., Yong T., Orr E.L., Linthicum D.S. Hypothesis: a possible role for mast cells and their inflammatory mediators in the pathogenesis of autoimmune encephalomyelitis. J. Neurosci. Res. 1996, 45:340-348.
31. Ibrahim M.Z., Reder A.T., Lawand R., Takash W., Sallouh-Khatib S. The mast cells of the multiple sclerosis brain. J. Neuroimmunol. 1996, 70:131-138.
32. Rozniecki J.J., Hauser S.L., Stein M., Lincoln R., Theoharides T.C. Elevated mast cell tryptase in cerebrospinal fluid of multiple sclerosis patients. Ann. Neurol. 1995, 37:63-66.
33. Lock C., Hermans G., Pedotti R., Brendolan A., Schadt E., Garren H., Langer-Gould A., Strober S., Cannella B., Allard J., Klonowski P., Austin A., Lad N., Kaminski N., Galli S.J., Oksenberg J.R., Raine C.S., Heller R., Steinman L. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 2002, 8:500-508.
34. Brenner T., Soffer D., Shalit M., Levi-Schaffer F. Mast cells in experimental allergic encephalomyelitis: characterization, distribution in the CNS and in vitro activation by myelin basic protein and neuropeptides. J. Neurol. Sci. 1994, 122:210-213.
35. Dietsch G.N., Hinrichs D.J. Mast cell proteases liberate stable encephalitogenic fragments from intact myelin. Cell. Immunol. 1991, 135:541-548.
36. Johnson D., Seeldrayers P.A., Weiner H.L. The role of mast cells in demyelination. 1. Myelin proteins are degraded by mast cell proteases and myelin basic protein and P2 can stimulate mast cell degranulation. Brain Res. 1988, 444:195-198.
37. Dimitriadou V., Pang X., Theoharides T.C. Hydroxyzine inhibits experimental allergic encephalomyelitis (EAE) and associated brain mast cell activation. Int. J. Immunopharmacol. 2000, 22:673-684.
38. Dietsch G.N., Hinrichs D.J. The role of mast cells in the elicitation of experimental allergic encephalomyelitis. J. Immunol. 1989, 142:1476-1481.
39. Secor V.H., Secor W.E., Gutekunst C.A., Brown M.A. Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis. J. Exp. Med. 2000, 191:813-822.
40. Trotter J.L., Clark H.B., Collins K.G., Wegeschiede C.L., Scarpellini J.D. Myelin proteolipid protein induces demyelinating disease in mice. J. Neurol. Sci. 1987, 79:173-188.
41. Tuohy V.K., Lu Z., Sobel R.A., Laursen R.A., Lees M.B. Identification of an encephalitogenic determinant of myelin proteolipid protein for SJL mice. J. Immunol. 1989, 142:1523-1527.
42. Sayed B., Walker M., Brown M. Mast cells regulate disease severity in a relasping remitting model of multiple sclerosis. Cutting Edge: Immunol. 2011, 186:3294-3298.
43. Carlson T., Kroenke M., Rao P., Lane T.E., Segal B. The Th17-ELR+ CXC chemokine pathway is essential for the development of central nervous system autoimmune disease. J. Exp. Med. 2008, 205:811-823.
44. Kannan K., Ortmann R.A., Kimpel D. Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology 2005, 12:167-181.
45. Lee D.M., Friend D.S., Gurish M.F., Benoist C., Mathis D., Brenner M.B. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 2002, 297:1689-1692.
46. Hueber A.J., Asquith D.L., Miller A.M., Reilly J., Kerr S., Leipe J., Melendez A.J., McInnes I.B. Mast cells express IL-17A in rheumatoid arthritis synovium. J. Immunol. 2010, 184:3336-3340.
47. Sandler C., Lindstedt K.A., Joutsiniemi S., Lappalainen J., Juutilainen T., Kolah J., Kovanen P.T., Eklund K.K. Selective activation of mast cells in rheumatoid synovial tissue results in production of TNF-alpha, IL-1beta and IL-1Ra. Inflamm. Res. 2007, 56:230-239.
48. Shin K., Nigrovic P.A., Crish J., Boilard E., McNeil H.P., Larabee K.S., Adachi R., Gurish M.F., Gobezie R., Stevens R.L., Lee D.M. Mast cells contribute to autoimmune inflammatory arthritis via their tryptase/heparin complexes. J. Immunol. 2009, 182:647-656.
49. Sawamukai N., Yukawa S., Saito K., Nakayamada S., Kambayashi T., Tanaka Y. Mast cell-derived tryptase inhibits apoptosis of human rheumatoid synovial fibroblasts via rho-mediated signaling. Arthritis Rheum. 2010, 62:952-959.
50. Palmer H.S., Kelso E.B., Lockhart J.C., Sommerhoff C.P., Plevin R., Goh F.G., Ferrell W.R. Protease-activated receptor 2 mediates the proinflammatory effects of synovial mast cells. Arthritis Rheum. 2007, 56:3532-3540.
51. Xu D., Jiang H.R., Kewin P., Li Y., Mu R., Fraser A.R., Pitman N., Kurowska-Stolarska M., McKenzie A.N., McInnes I.B., Liew F.Y. IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc. Natl Acad. Sci. USA 2008, 105:10913-10918.
52. Xu D., Jiang H.R., Li Y., Pushparaj P.N., Kurowska-Stolarska M., Leung B.P., Mu R., Tay H.K., McKenzie A.N., McInnes I.B., Melendez A.J., Liew F.Y. IL-33 exacerbates autoantibody-induced arthritis. J. Immunol. 2010, 184:2620-2626.
53. Navi D., Saegusa J., Liu F.T. Mast cells and immunological skin diseases. Clin. Rev. Allergy Immunol. 2007, 33:144-155.
54. Chen R., Ning G., Zhao M.L., Fleming M.G., Diaz L.A., Werb Z., Liu Z. Mast cells play a key role in neutrophil recruitment in experimental bullous pemphigoid. J. Clin. Invest. 2001, 108:1151-1158.
55. Liu Z., Diaz L.A., Troy J.L., Taylor A.F., Emery D.J., Fairley J.A., Giudice G.J. A passive transfer model of the organ-specific autoimmune disease, bullous pemphigoid, using antibodies generated against the hemidesmosomal antigen, BP180. J. Clin. Invest. 1993, 92:2480-2488.
56. Dvorak A.M., Mihm M.C., Osage J.E., Kwan T.H., Austen K.F., Wintroub B.U. Bullous pemphigoid, an ultrastructural study of the inflammatory response: eosinophil, basophil and mast cell granule changes in multiple biopsies from one patient. J. Invest. Dermatol. 1982, 78:91-101.
57. Baba T., Sonozaki H., Seki K., Uchiyama M., Ikesawa Y., Toriisu M. An eosinophil chemotactic factor present in blister fluids of bullous pemphigoid patients. J. Immunol. 1976, 116:112-116.
58. Katayama I., Doi T., Nishioka K. High histamine level in the blister fluid of bullous pemphigoid. Arch. Dermatol. Res. 1984, 276:126-127.
59. D'Auria L., Pietravalle M., Cordiali-Fei P., Ameglio F. Increased tryptase and myeloperoxidase levels in blister fluids of patients with bullous pemphigoid: correlations with cytokines, adhesion molecules and anti-basement membrane zone antibodies. Exp. Dermatol. 2000, 9:131-137.
60. Brockow K., Abeck D., Hermann K., Ring J. Tryptase concentration in skin blister fluid from patients with bullous skin conditions. Arch. Dermatol. Res. 1996, 288:771-773.
61. Bluestone J.A., Herold K., Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 2010, 464:1293-1300.
62. Geoffrey R., Jia S., Kwitek A.E., Woodliff J., Ghosh S., Lernmark A., Wang X., Hessner M.J. Evidence of a functional role for mast cells in the development of type 1 diabetes mellitus in the BioBreeding rat. J. Immunol. 2006, 177:7275-7286.
63. Louvet C., Szot G.L., Lang J., Lee M.R., Martinier N., Bollag G., Zhu S., Weiss A., Bluestone J.A. Tyrosine kinase inhibitors reverse type 1 diabetes in nonobese diabetic mice. Proc. Natl Acad. Sci. USA 2008, 105:18895-18900.
64. Liu J., Divoux A., Sun J., Zhang J., Clement K., Glickman J.N., Sukhova G.K., Wolters P.J., Du J., Gorgun C.Z., Doria A., Libby P., Blumberg R.S., Kahn B.B., Hotamisligil G.S., Shi G.P. Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat. Med. 2009, 15:940-945.
65. Pilartz M., Jess T., Indefrei D., Schroder J.M. Adoptive transfer-experimental allergic neuritis in newborn Lewis rats results in inflammatory infiltrates, mast cell activation, and increased Ia expression with only minor nerve fiber degeneration. Acta Neuropathol. 2002, 104:513-524.
66. Buckner J.H. Mechanisms of impaired regulation by CD4(+)CD25(+)FOXP3(+) regulatory T cells in human autoimmune diseases. Nat. Rev. Immunol. 2010, 10:849-859.
67. Gri G., Piconese S., Frossi B., Manfroi V., Merluzzi S., Tripodo C., Viola A., Odom S., Rivera J., Colombo M.P., Pucillo C.E. CD4+CD25+ regulatory T cells suppress mast cell degranulation and allergic responses through OX40-OX40L interaction. Immunity 2008, 29:771-781.
68. Kashyap M., Thornton A.M., Norton S.K., Barnstein B., Macey M., Brenzovich J., Shevach E., Leonard W.J., Ryan J.J. Cutting edge: CD4 T cell-mast cell interactions alter IgE receptor expression and signaling. J. Immunol. 2008, 180:2039-2043.
69. Piconese S., Gri G., Tripodo C., Musio S., Gorzanelli A., Frossi B., Pedotti R., Pucillo C.E., Colombo M.P. Mast cells counteract regulatory T-cell suppression through interleukin-6 and OX40/OX40L axis toward Th17-cell differentiation. Blood 2009, 114:2639-2648.
70. de Vries V.C., Wasiuk A., Bennett K.A., Benson M.J., Elgueta R., Waldschmidt T.J., Noelle R.J. Mast cell degranulation breaks peripheral tolerance. Am. J. Transplant. 2009, 9:2270-2280.
71. Forward N.A., Furlong S.J., Yang Y., Lin T.J., Hoskin D.W. Mast cells down-regulate CD4+CD25+ T regulatory cell suppressor function via histamine H1 receptor interaction. J. Immunol. 2009, 183:3014-3022.
72. Hemdan N.Y., Birkenmeier G., Wichmann G., Abu El-Saad A.M., Krieger T., Conrad K., Sack U. Interleukin-17-producing T helper cells in autoimmunity. Autoimmun. Rev. 2010, 9:785-792.
73. Zhu J., Paul W.E. Heterogeneity and plasticity of T helper cells. Cell Res. 2010, 20:4-12.
74. Tripodo C., Gri G., Piccaluga P.P., Frossi B., Guarnotta C., Piconese S., Franco G., Vetri V., Pucillo C.E., Florena A.M., Colombo M.P., Pileri S.A. Mast cells and Th17 cells contribute to the lymphoma-associated pro-inflammatory microenvironment of angioimmunoblastic T-cell lymphoma. Am. J. Pathol. 2010, 177:792-802.
75. Kawakami T., Kitaura J., Xiao W., Kawakami Y. IgE regulation of mast cell survival and function. Novartis Found. Symp. 2005, 271:100-107. discussion 108-114, 145-151.
76. Malbec O., Daeron M. The mast cell IgG receptors and their roles in tissue inflammation. Immunol. Rev. 2007, 217:206-221.
77. Merluzzi S., Frossi B., Gri G., Parusso S., Tripodo C., Pucillo C. Mast cells enhance proliferation of B lymphocytes and drive their differentiation toward IgA-secreting plasma cells. Blood 2010, 115:2810-2817.
78. Minagar A., Shapshak P., Fujimura R., Ownby R., Heyes M., Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 2002, 202:13-23.
79. Kim D.Y., Jeoung D., Ro J.Y. Signaling pathways in the activation of mast cells cocultured with astrocytes and colocalization of both cells in experimental allergic encephalomyelitis. J. Immunol. 2010, 185:273-283.
80. Bulanova E., Bulfone-Paus S. P2 receptor-mediated signaling in mast cell biology. Purinergic Signal 2010, 6:3-17.
81. Hudson C.A., Christophi G.P., Gruber R.C., Wilmore J.R., Lawrence D.A., Massa P.T. Induction of IL-33 expression and activity in central nervous system glia. J. Leukoc. Biol. 2008, 84:631-643.
82. Steinman L. A molecular trio in relapse and remission in multiple sclerosis. Nat. Rev. Immunol. 2009, 9:440-447.
83. Rangaswami H., Bulbule A., Kundu G.C. Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol. 2006, 16:79-87.
84. Denhardt D.T., Burger E.H., Kazanecki C., Krishna S., Semeins C.M., Klein-Nulend J. Osteopontin-deficient bone cells are defective in their ability to produce NO in response to pulsatile fluid flow. Biochem. Biophys. Res. Commun. 2001, 288:448-453.
85. O'Regan A.W., Hayden J.M., Berman J.S. Osteopontin augments CD3-mediated interferon-gamma and CD40 ligand expression by T cells, which results in IL-12 production from peripheral blood mononuclear cells. J. Leukoc. Biol. 2000, 68:495-502.
86. Renkl A.C., Wussler J., Ahrens T., Thoma K., Kon S., Uede T., Martin S.F., Simon J.C., Weiss J.M. Osteopontin functionally activates dendritic cells and induces their differentiation toward a Th1-polarizing phenotype. Blood 2005, 106:946-955.
87. Shinohara M.L., Lu L., Bu J., Werneck M.B., Kobayashi K.S., Glimcher L.H., Cantor H. Osteopontin expression is essential for interferon-alpha production by plasmacytoid dendritic cells. Nat. Immunol. 2006, 7:498-506.
88. Diao H., Kon S., Iwabuchi K., Kimura C., Morimoto J., Ito D., Segawa T., Maeda M., Hamuro J., Nakayama T., Taniguchi M., Yagita H., Van Kaer L., Onoe K., Denhardt D., Rittling S., Uede T. Osteopontin as a mediator of NKT cell function in T cell-mediated liver diseases. Immunity 2004, 21:539-550.
89. Nagasaka A., Matsue H., Matsushima H., Aoki R., Nakamura Y., Kambe N., Kon S., Uede T., Shimada S. Osteopontin is produced by mast cells and affects IgE-mediated degranulation and migration of mast cells. Eur. J. Immunol. 2008, 38:489-499.
90. O'Connor T.M., O'Connell J., O'Brien D.I., Goode T., Bredin C.P., Shanahan F. The role of substance P in inflammatory disease. J. Cell. Physiol. 2004, 201:167-180.
91. Reinke E., Fabry Z. Breaking or making immunological privilege in the central nervous system: the regulation of immunity by neuropeptides. Immunol. Lett. 2006, 104:102-109.
92. Theoharides T.C., Donelan J.M., Papadopoulou N., Cao J., Kempuraj D., Conti P. Mast cells as targets of corticotropin-releasing factor and related peptides. Trends Pharmacol. Sci. 2004, 25:563-568.
93. Ansel J.C., Brown J.R., Payan D.G., Brown M.A. Substance P selectively activates TNF-alpha gene expression in murine mast cells. J. Immunol. 1993, 150:4478-4485.
94. Oboki K., Ohno T., Kajiwara N., Saito H., Nakae S. IL-33 and IL-33 receptors in host defense and diseases. Allergol. Int. 2010, 59:143-160.
95. Roussel L., Erard M., Cayrol C., Girard J.P. Molecular mimicry between IL-33 and KSHV for attachment to chromatin through the H2A-H2B acidic pocket. EMBO Rep 2008, 9:1006-1012.
96. Liew F.Y., Pitman N.I., McInnes I.B. Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol 2010, 10:103-110.