Interleukin-33 Primes Mast Cells for Activation by IgG Immune Complexes

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Kaieda, Shinjiro ^a   Wang, Jun Xia ^a   Shnayder, Ruslan ^a   Fishgal, Nadia ^a   Hei, Hillary ^a   Lee, Richard T ^a   Stevens, Richard L ^a   Nigrovic, Peter A ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CXCL2 CHEMOKINE; IMMUNOGLOBULIN G; INTERLEUKIN 1BETA; INTERLEUKIN 33; INTERLEUKIN 33 RECEPTOR; INTERLEUKIN RECEPTOR; MESSENGER RNA; PROTEIN ST2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY COMPLEX; ARTHRITIS; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FIBROBLAST; IMMUNOREGULATION; MAST CELL; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION;

ANIMALS; ANTIGEN-ANTIBODY COMPLEX; FEEDBACK, PHYSIOLOGICAL; INTERLEUKINS; MAST CELLS; MICE; MICE, TRANSGENIC; RECEPTORS, IGG; RECEPTORS, INTERLEUKIN; RNA, MESSENGER;

EID: 84867426868     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047252     Document Type: Article

References (53)

1. Nakano T, Sonoda T, Hayashi C, Yamatodani A, Kanayama Y, et al. (1985) 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 162: 1025-1043.
2. Sonoda S, Sonoda T, Nakano T, Kanayama Y, Kanakura Y, et al. (1986) Development of mucosal mast cells after injection of a single connective tissue-type mast cell in the stomach mucosa of genetically mast cell-deficient W/Wv mice. J Immunol 137: 1319-1322.
3. Gurish MF, Pear WS, Stevens RL, Scott ML, Sokol K, et al. (1995) Tissue-regulated differentiation and maturation of a v-abl-immortalized mast cell-committed progenitor. Immunity 3: 175-186.
4. Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, et al. (2005) Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu Rev Immunol 23: 749-786.
5. Levi-Schaffer F, Austen KF, Gravallese PM, Stevens RL, (1986) Coculture of interleukin 3-dependent mouse mast cells with fibroblasts results in a phenotypic change of the mast cells. Proc Natl Acad Sci U S A 83: 6485-6488.
6. Levi-Schaffer F, Austen KF, Caulfield JP, Hein A, Gravallese PM, et al. (1987) Co-culture of human lung-derived mast cells with mouse 3T3 fibroblasts: morphology and IgE-mediated release of histamine, prostaglandin D2, and leukotrienes. J Immunol 139: 494-500.
7. Koma Y, Ito A, Watabe K, Hirata T, Mizuki M, et al. (2005) Distinct role for c-kit receptor tyrosine kinase and SgIGSF adhesion molecule in attachment of mast cells to fibroblasts. Lab Invest 85: 426-435.
8. Anderson DM, Lyman SD, Baird A, Wignall JM, Eisenman J, et al. (1990) Molecular cloning of mast cell growth factor, a hematopoietin that is active in both membrane bound and soluble forms. Cell 63: 235-243.
9. Flanagan JG, Chan DC, Leder P, (1991) Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the Sld mutant. Cell 64: 1025-1035.
10. Dayton ET, Caulfield JP, Hein A, Austen KF, Stevens RL, (1989) Regulation of the growth rate of mouse fibroblasts by IL-3-activated mouse bone marrow-derived mast cells. J Immunol 142: 4307-4313.
11. Nigrovic PA, Lee DM, (2007) Synovial mast cells: role in acute and chronic arthritis. Immunol Rev 217: 19-37.
12. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, et al. (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23: 479-490.
13. Lunderius-Andersson C, Enoksson M, Nilsson G, (2012) Mast Cells Respond to Cell Injury through the Recognition of IL-33. Front Immunol 3: 82.
14. Liew FY, Pitman NI, McInnes IB, (2010) Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol 10: 103-110.
15. Hsu CL, Neilsen CV, Bryce PJ, (2010) IL-33 is produced by mast cells and regulates IgE-dependent inflammation. PLoS One 5: e11944.
16. Tominaga S, (1989) A putative protein of a growth specific cDNA from BALB/c-3T3 cells is highly similar to the extracellular portion of mouse interleukin 1 receptor. FEBS Lett 258: 301-304.
17. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G, (2007) Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol 179: 2051-2054.
18. Ho LH, Ohno T, Oboki K, Kajiwara N, Suto H, et al. (2007) IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcepsilonRI signals. J Leukoc Biol 82: 1481-1490.
19. Iikura M, Suto H, Kajiwara N, Oboki K, Ohno T, et al. (2007) IL-33 can promote survival, adhesion and cytokine production in human mast cells. Lab Invest 87: 971-978.
20. Moulin D, Donze O, Talabot-Ayer D, Mezin F, Palmer G, et al. (2007) Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells. Cytokine 40: 216-225.
21. Xu D, Jiang HR, Kewin P, Li Y, Mu R, et al. (2008) IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc Natl Acad Sci U S A 105: 10913-10918.
22. Enoksson M, Lyberg K, Moller-Westerberg C, Fallon PG, Nilsson G, et al. (2011) Mast cells as sensors of cell injury through IL-33 recognition. J Immunol 186: 2523-2528.
23. Pushparaj PN, Tay HK, H'Ng SC, Pitman N, Xu D, et al. (2009) The cytokine interleukin-33 mediates anaphylactic shock. Proc Natl Acad Sci U S A 106: 9773-9778.
24. Silver MR, Margulis A, Wood N, Goldman SJ, Kasaian M, et al. (2009) IL-33 synergizes with IgE-dependent and IgE-independent agents to promote mast cell and basophil activation. Inflamm Res 59: 207-218.
25. Andrade MV, Iwaki S, Ropert C, Gazzinelli RT, Cunha-Melo JR, et al. (2010) Amplification of cytokine production through synergistic activation of NFAT and AP-1 following stimulation of mast cells with antigen and IL-33. Eur J Immunol 41: 760-772.
26. Kaieda S, Shin K, Nigrovic PA, Seki K, Lee RT, et al. (2010) Synovial fibroblasts promote the expression and granule accumulation of tryptase via interleukin-33 and its receptor ST-2 (IL1RL1). J Biol Chem 285: 21478-21486.
27. Thakurdas SM, Melicoff E, Sansores-Garcia L, Moreira DC, Petrova Y, et al. (2007) The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections. J Biol Chem 282: 20809-20815.
28. McNeil HP, Shin K, Campbell IK, Wicks IP, Adachi R, et al. (2008) The mouse mast cell-restricted tetramer-forming tryptases mouse mast cell protease 6 and mouse mast cell protease 7 are critical mediators in inflammatory arthritis. Arthritis Rheum 58: 2338-2346.
29. Shin K, Nigrovic PA, Crish J, Boilard E, McNeil HP, et al. (2009) Mast cells contribute to autoimmune inflammatory arthritis via their tryptase/heparin complexes. J Immunol 182: 647-656.
30. Palmer G, Talabot-Ayer D, Lamacchia C, Toy D, Seemayer CA, et al. (2009) Inhibition of interleukin-33 signaling attenuates the severity of experimental arthritis. Arthritis Rheum 60: 738-749.
31. Xu D, Jiang HR, Li Y, Pushparaj PN, Kurowska-Stolarska M, et al. (2010) IL-33 exacerbates autoantibody-induced arthritis. J Immunol 184: 2620-2626.
32. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM, et al. (2006) Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol 7: 284-292.
33. Nigrovic PA, Malbec O, Lu B, Markiewski MM, Kepley C, et al. (2010) C5a receptor enables participation of mast cells in immune complex arthritis independently of Fcgamma receptor modulation. Arthritis Rheum 62: 3322-3333.
34. Smith DE, (2011) The biological paths of IL-1 family members IL-18 and IL-33. J Leukoc Biol 89: 383-392.
35. Nigrovic PA, Binstadt BA, Monach PA, Johnsen A, Gurish M, et al. (2007) Mast cells contribute to initiation of autoantibody-mediated arthritis via IL-1. Proc Natl Acad Sci U S A 104: 2325-2330.
36. Townsend MJ, Fallon PG, Matthews DJ, Jolin HE, McKenzie AN, (2000) T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J Exp Med 191: 1069-1076.
37. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, et al. (2002) Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 297: 1689-1692.
38. Lee DM, Kiener HP, Agarwal SK, Noss EH, Watts GF, et al. (2007) Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315: 1006-1010.
39. Razin E, Ihle JN, Seldin D, Mencia-Huerta JM, Katz HR, et al. (1984) Interleukin 3: A differentiation and growth factor for the mouse mast cell that contains chondroitin sulfate E proteoglycan. J Immunol 132: 1479-1486.
40. Kim ND, Chou RC, Seung E, Tager AM, Luster AD, (2006) A unique requirement for the leukotriene B4 receptor BLT1 for neutrophil recruitment in inflammatory arthritis. J Exp Med 203: 829-835.
41. Alves-Filho JC, Sonego F, Souto FO, Freitas A, Verri WA Jr, et al. (2010) Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med 16: 708-712.
42. Wipke BT, Allen PM, (2001) Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 167: 1601-1608.
43. Jacobs JP, Ortiz-Lopez A, Campbell JJ, Gerard CJ, Mathis D, et al. (2010) Deficiency of CXCR2, but not other chemokine receptors, attenuates autoantibody-mediated arthritis in a murine model. Arthritis Rheum 62: 1921-1932.
44. Shushakova N, Skokowa J, Schulman J, Baumann U, Zwirner J, et al. (2002) C5a anaphylatoxin is a major regulator of activating versus inhibitory FcgammaRs in immune complex-induced lung disease. J Clin Invest 110: 1823-1830.
45. Ohno T, Oboki K, Morita H, Kajiwara N, Arae K, et al. (2011) Paracrine IL-33 stimulation enhances lipopolysaccharide-mediated macrophage activation. PLoS One 6: e18404.
46. Galli SJ, Maurer M, Lantz CS, (1999) Mast cells as sentinels of innate immunity. Curr Opin Immunol 11: 53-59.
47. Chou RC, Kim ND, Sadik CD, Seung E, Lan Y, et al. (2010) Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 33: 266-278.
48. Blatner NR, Bonertz A, Beckhove P, Cheon EC, Krantz SB, et al. (2010) In colorectal cancer mast cells contribute to systemic regulatory T-cell dysfunction. Proc Natl Acad Sci U S A 107: 6430-6435.
49. Komai-Koma M, Brombacher F, Pushparaj PN, Arendse B, McSharry C, et al. (2012) Interleukin-33 amplifies IgE synthesis and triggers mast cell degranulation via interleukin-4 in naive mice. Allergy.
50. Wang JX, Bair AM, King SL, Shnayder R, Huang YF, et al. (2012) Ly6G ligation blocks recruitment of neutrophils via a beta 2 integrin-dependent mechanism. Blood 120: 1489-98.
51. Luthi AU, Cullen SP, McNeela EA, Duriez PJ, Afonina IS, et al. (2009) Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity 31: 84-98.
52. Kakkar R, Hei H, Dobner S, Lee RT, (2012) Interleukin 33 as a mechanically responsive cytokine secreted by living cells. J Biol Chem 287: 6941-8.
53. Nigrovic PA, Lee DM (2006) Immune complexes and innate immunity in rheumatoid arthritis. In: Firestein GS, Panayi GS, Wollheim FA, editors. Rheumatoid Arthritis: new frontiers in pathogenesis and treatment. 2nd ed. Oxford: Oxford University Press. 135-156.