A Novel Interleukin 33/ST2 Signaling Regulates Inflammatory Response in Human Corneal Epithelium

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Lin, Jing ^a,b   Zhang, Lili ^a,b   Zhao, Guiqiu ^a   Su, Zhitao ^b,c   Deng, Ruzhi ^b,c   Pflugfelder, Stephen C ^b   Li, De Quan ^b  

^a QINGDAO UNIVERSITY MEDICAL COLLEGE   (China)

^b CULLEN EYE INSTITUTE   (United States)

^c WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; CELL PROTEIN; INTERLEUKIN 33; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; PROTEIN ST2; QUINAZOLINE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION (PARAMETERS); CORNEA CELL; CORNEA EPITHELIUM; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERLEUKIN 33 GENE; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ADULT; AGED; ANTIBODIES, NEUTRALIZING; CYTOKINES; EPITHELIAL CELLS; EPITHELIUM, CORNEAL; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKINS; MIDDLE AGED; NF-KAPPA B; NITRILES; PRIMARY CELL CULTURE; QUINAZOLINES; RECEPTORS, CELL SURFACE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SULFONES;

EID: 84876069196     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060963     Document Type: Article

References (50)

1. 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.
2. 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.
3. 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.
4. Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, et al. (2008) IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol 20: 1019-1030.
5. Carriere V, Roussel L, Ortega N, Lacorre DA, Americh L, et al. (2007) IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc Natl Acad Sci U S A 104: 282-287.
6. Moussion C, Ortega N, Girard JP, (2008) The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'? PLoS One 3: e3331.
7. Sanada S, Hakuno D, Higgins LJ, Schreiter ER, McKenzie AN, et al. (2007) IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system. J Clin Invest 117: 1538-1549.
8. Prefontaine D, Lajoie-Kadoch S, Foley S, Audusseau S, Olivenstein R, et al. (2009) Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J Immunol 183: 5094-5103.
9. Saenz SA, Taylor BC, Artis D, (2008) Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol Rev 226: 172-190.
10. Matsuda A, Okayama Y, Terai N, Yokoi N, Ebihara N, et al. (2009) The role of interleukin-33 in chronic allergic conjunctivitis. Invest Ophthalmol Vis Sci 50: 4646-4652.
11. Kobori A, Yagi Y, Imaeda H, Ban H, Bamba S, et al. (2010) Interleukin-33 expression is specifically enhanced in inflamed mucosa of ulcerative colitis. J Gastroenterol 45: 999-1007.
12. 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.
13. Tominaga S, Jenkins NA, Gilbert DJ, Copeland NG, Tetsuka T, (1991) Molecular cloning of the murine ST2 gene. Characterization and chromosomal mapping. Biochim Biophys Acta 1090: 1-8.
14. 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.
15. Tominaga S, Kuroiwa K, Tago K, Iwahana H, Yanagisawa K, et al. (1999) Presence and expression of a novel variant form of ST2 gene product in human leukemic cell line UT-7/GM. Biochem Biophys Res Commun 264: 14-18.
16. 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.
17. Kearley J, Buckland KF, Mathie SA, Lloyd CM, (2009) Resolution of allergic inflammation and airway hyperreactivity is dependent upon disruption of the T1/ST2-IL-33 pathway. Am J Respir Crit Care Med 179: 772-781.
18. Kurokawa M, Matsukura S, Kawaguchi M, Ieki K, Suzuki S, et al. (2011) Expression and effects of IL-33 and ST2 in allergic bronchial asthma: IL-33 induces eotaxin production in lung fibroblasts. Int Arch Allergy Immunol 155 (Suppl 1): 12-20.
19. Liu XC, Liu XF, Jian CX, Li CJ, He SZ, (2012) IL-33 is induced by amyloid-beta stimulation and regulates inflammatory cytokine production in retinal pigment epithelium cells. Inflammation 35: 776-784.
20. Pastorelli L, Garg RR, Hoang SB, Spina L, Mattioli B, et al. (2010) Epithelial-derived IL-33 and its receptor ST2 are dysregulated in ulcerative colitis and in experimental Th1/Th2 driven enteritis. Proc Natl Acad Sci U S A 107: 8017-8022.
21. Lohning M, Stroehmann A, Coyle AJ, Grogan JL, Lin S, et al. (1998) T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc Natl Acad Sci U S A 95: 6930-6935.
22. Moritz DR, Rodewald HR, Gheyselinck J, Klemenz R, (1998) The IL-1 receptor-related T1 antigen is expressed on immature and mature mast cells and on fetal blood mast cell progenitors. J Immunol 161: 4866-4874.
23. Cherry WB, Yoon J, Bartemes KR, Iijima K, Kita H, (2008) A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J Allergy Clin Immunol 121: 1484-1490.
24. Suzukawa M, Iikura M, Koketsu R, Nagase H, Tamura C, et al. (2008) An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J Immunol 181: 5981-5989.
25. Kumar S, Minnich MD, Young PR, (1995) ST2/T1 protein functionally binds to two secreted proteins from Balb/c 3T3 and human umbilical vein endothelial cells but does not bind interleukin 1. J Biol Chem 270: 27905-27913.
26. Tajima S, Bando M, Ohno S, Sugiyama Y, Oshikawa K, et al. (2007) ST2 gene induced by type 2 helper T cell (Th2) and proinflammatory cytokine stimuli may modulate lung injury and fibrosis. Exp Lung Res 33: 81-97.
27. Oshikawa K, Yanagisawa K, Tominaga S, Sugiyama Y, (2002) Expression and function of the ST2 gene in a murine model of allergic airway inflammation. Clin Exp Allergy 32: 1520-1526.
28. Leung BP, Xu D, Culshaw S, McInnes IB, Liew FY, (2004) A novel therapy of murine collagen-induced arthritis with soluble T1/ST2. J Immunol 173: 145-150.
29. Miller AM, Xu D, Asquith DL, Denby L, Li Y, et al. (2008) IL-33 reduces the development of atherosclerosis. J Exp Med 205: 339-346.
30. Szerafin T, Niederpold T, Mangold A, Hoetzenecker K, Hacker S, et al. (2009) Secretion of soluble ST2- possible explanation for systemic immunosuppression after heart surgery. Thorac Cardiovasc Surg 57: 25-29.
31. Hayakawa H, Hayakawa M, Kume A, Tominaga S, (2007) Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J Biol Chem 282: 26369-26380.
32. Yin H, Huang BJ, Yang H, Huang YF, Xiong P, et al. (2006) Pretreatment with soluble ST2 reduces warm hepatic ischemia/reperfusion injury. Biochem Biophys Res Commun 351: 940-946.
33. Oshikawa K, Kuroiwa K, Tago K, Iwahana H, Yanagisawa K, et al. (2001) Elevated soluble ST2 protein levels in sera of patients with asthma with an acute exacerbation. Am J Respir Crit Care Med 164: 277-281.
34. Komai-Koma M, Xu D, Li Y, McKenzie AN, McInnes IB, et al. (2007) IL-33 is a chemoattractant for human Th2 cells. Eur J Immunol 37: 2779-2786.
35. 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.
36. Pecaric-Petkovic T, Didichenko SA, Kaempfer S, Spiegl N, Dahinden CA, (2009) Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 113: 1526-1534.
37. Choi YS, Choi HJ, Min JK, Pyun BJ, Maeng YS, et al. (2009) Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production. Blood 114: 3117-3126.
38. Bourgeois E, Van LP, Samson M, Diem S, Barra A, et al. (2009) The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 39: 1046-1055.
39. 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.
40. 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.
41. Jones LA, Roberts F, Nickdel MB, Brombacher F, McKenzie AN, et al. (2010) IL-33 receptor (T1/ST2) signalling is necessary to prevent the development of encephalitis in mice infected with Toxoplasma gondii. Eur J Immunol 40: 426-436.
42. Becerra A, Warke RV, de BN, Rothman AL, Bosch I, (2008) Elevated levels of soluble ST2 protein in dengue virus infected patients. Cytokine 41: 114-120.
43. Li DQ, Zhou N, Zhang L, Ma P, Pflugfelder SC, (2010) Suppressive effects of azithromycin on zymosan-induced production of proinflammatory mediators by human corneal epithelial cells. Invest Ophthalmol Vis Sci 51: 5623-5629.
44. Bian F, Qi H, Ma P, Zhang L, Yoon KC, et al. (2010) An immunoprotective privilege of corneal epithelial stem cells against Th17 inflammatory stress by producing glial cell-derived neurotrophic factor. Stem Cells 28: 2172-2181.
45. Bonanno JA, Polse KA, (1987) Effect of rigid contact lens oxygen transmissibility on stromal pH in the living human eye. Ophthalmology 94: 1305-1309.
46. Ma P, Wang Z, Pflugfelder SC, Li DQ, (2010) Toll-like receptors mediate induction of peptidoglycan recognition proteins in human corneal epithelial cells. Exp Eye Res 90: 130-136.
47. Kim HS, Jun S, de Paiva CS, Chen Z, Pflugfelder SC, et al. (2004) Phenotypic characterization of human corneal epithelial cells expanded ex vivo from limbal explant and single cell cultures. Exp Eye Res 79: 41-49.
48. Zhang L, Lu R, Zhao G, Pflugfelder SC, Li DQ, (2011) TLR-mediated induction of pro-allergic cytokine IL-33 in ocular mucosal epithelium. Int J Biochem Cell Biol 43: 1383-1391.
49. Luo L, Li D-Q, Doshi A, Farley W, Corrales RM, et al. (2004) Experimental dry eye stimulates production of inflammatory cytokines and MMP-9 and activates MAPK signaling pathways on the ocular surface. Invest Ophthalmol Vis Sci 45: 4293-4301.
50. de Paiva CS, Corrales RM, Villarreal AL, Farley WJ, Li D-Q, et al. (2006) Corticosteroid and doxycycline suppress MMP-9 and inflammatory cytokine expression, MAPK activation in the corneal epithelium in experimental dry eye. Exp Eye Res 83: 526-535.