Innate Immune Signaling Induces Interleukin-7 Production from Salivary Gland Cells and Accelerates the Development of Primary Sjögren's Syndrome in a Mouse Model

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Jin, Jun O ^a   Shinohara, Yoshinori ^b   Yu, Qing ^a  

^a FORSYTH INSTITUTE   (United States)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CXCL9 CHEMOKINE; CYTOKINE ANTIBODY; GAMMA INTERFERON; INTERFERON; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA ANTIBODY; POLYINOSINIC POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; EPITHELIUM CELL; EX VIVO STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SALIVARY GLAND; SIGNAL TRANSDUCTION; SJOEGREN SYNDROME; T LYMPHOCYTE; UPREGULATION;

ANIMALS; CHEMOKINE CXCL9; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; INTERFERON-GAMMA; INTERLEUKIN-7; KILLER CELLS, NATURAL; LIGANDS; MICE; MICE, KNOCKOUT; POLY I-C; RECEPTORS, CXCR3; SALIVARY GLANDS; SIGNAL TRANSDUCTION; SJOGREN'S SYNDROME; T-LYMPHOCYTE SUBSETS; TH1 CELLS;

EID: 84885747649     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077605     Document Type: Article

References (51)

1. Segal B, Bowman SJ, Fox PC, Vivino FB, Murukutla N, et al. (2009) Primary Sjogren's Syndrome: health experiences and predictors of health quality among patients in the United States. Health Qual Life Outcomes 7: 46. doi:10.1186/1477-7525-7-46. PubMed: 19473510.
2. Voulgarelis M, Tzioufas AG, (2010) Pathogenetic mechanisms in the initiation and perpetuation of Sjogren's syndrome. Nat Rev Rheumatol 6: 529-537. doi:10.1038/nrrheum.2010.118. PubMed: 20683439.
3. Theander E, Manthorpe R, Jacobsson LT, (2004) Mortality and causes of death in primary Sjogren's syndrome: a prospective cohort study. Arthritis Rheum 50: 1262-1269. doi:10.1002/art.20176. PubMed: 15077310.
4. Katsifis GE, Moutsopoulos NM, Wahl SM, (2007) T lymphocytes in Sjogren's syndrome: contributors to and regulators of pathophysiology. Clin Rev Allergy Immunol 32: 252-264. doi:10.1007/s12016-007-8011-8. PubMed: 17992592.
5. Lee BH, Tudares MA, Nguyen CQ, (2009) Sjogren's syndrome: an old tale with a new twist. Arch Immunol Ther Exp (Warsz) 57: 57-66. doi:10.1007/s00005-009-0002-4.
6. Nikolov NP, Illei GG, (2009) Pathogenesis of Sjogren's syndrome. Curr Opin Rheumatol 21: 465-470. doi:10.1097/BOR.0b013e32832eba21. PubMed: 19568172.
7. Nguyen CQ, Kim H, Cornelius JG, Peck AB, (2007) Development of Sjogren's syndrome in nonobese diabetic-derived autoimmune-prone C57BL/6.NOD-Aec1Aec2 mice is dependent on complement component-3. J Immunol 179: 2318-2329. PubMed: 17675493.
8. Hayakawa I, Tedder TF, Zhuang Y, (2007) B-lymphocyte depletion ameliorates Sjogren's syndrome in Id3 knockout mice. Immunology 122: 73-79. doi:10.1111/j.1365-2567.2007.02614.x. PubMed: 17472721.
9. Vosters JL, Landek-Salgado MA, Yin H, Swaim WD, Kimura H, et al. (2009) Interleukin-12 induces salivary gland dysfunction in transgenic mice, providing a new model of Sjogren's syndrome. Arthritis Rheum 60: 3633-3641. doi:10.1002/art.24980. PubMed: 19950301.
10. Yin H, Vosters JL, Roescher N, D'Souza A, Kurien BT, et al. (2011) Location of immunization and interferon-gamma are central to induction of salivary gland dysfunction in Ro60 peptide immunized model of Sjogren's syndrome. PLOS ONE 6: e18003. doi:10.1371/journal.pone.0018003. PubMed: 21464925.
11. Roescher N, Tak PP, Illei GG, (2010) Cytokines in Sjogren's syndrome: potential therapeutic targets. Ann Rheum Dis 69: 945-948. doi:10.1136/ard.2009.115378. PubMed: 20410069.
12. Cha S, Brayer J, Gao J, Brown V, Killedar S, et al. (2004) A dual role for interferon-gamma in the pathogenesis of Sjogren's syndrome-like autoimmune exocrinopathy in the nonobese diabetic mouse. Scand J Immunol 60: 552-565. doi:10.1111/j.0300-9475.2004.01508.x. PubMed: 15584966.
13. Nguyen CQ, Hu MH, Li Y, Stewart C, Peck AB, (2008) Salivary gland tissue expression of interleukin-23 and interleukin-17 in Sjogren's syndrome: findings in humans and mice. Arthritis Rheum 58: 734-743. doi:10.1002/art.23214. PubMed: 18311793.
14. Nguyen CQ, Sharma A, Lee BH, She JX, McIndoe RA, et al. (2009) Differential gene expression in the salivary gland during development and onset of xerostomia in Sjogren's syndrome-like disease of the C57BL/6.NOD-Aec1Aec2 mouse. Arthritis Res Ther 11: R56. doi:10.1186/ar2676. PubMed: 19379516.
15. Park JH, Adoro S, Guinter T, Erman B, Alag AS, et al. (2010) Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat Immunol 11: 257-264. doi:10.1038/ni.1840. PubMed: 20118929.
16. Sprent J, Surh CD, (2011) Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat Immunol 12: 478-484. PubMed: 21739670.
17. Calzascia T, Pellegrini M, Lin A, Garza KM, Elford AR, et al. (2008) CD4 T cells, lymphopenia, and IL-7 in a multistep pathway to autoimmunity. Proc Natl Acad Sci U S A 105: 2999-3004. doi:10.1073/pnas.0712135105. PubMed: 18287017.
18. Lee LF, Axtell R, Tu GH, Logronio K, Dilley J, et al. (2011) IL-7 promotes T(H)1 development and serum IL-7 predicts clinical response to interferon-beta in multiple sclerosis. Sci Transl Med 3: 93ra68.
19. Pellegrini M, Calzascia T, Toe JG, Preston SP, Lin AE, et al. (2011) IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144: 601-613. doi:10.1016/j.cell.2011.01.011. PubMed: 21295337.
20. Hartgring SA, Bijlsma JW, Lafeber FP, van Roon JA, (2006) Interleukin-7 induced immunopathology in arthritis. Ann Rheum Dis 65 (Suppl 3):: iii69-iii74. doi:10.1136/ard.2006.058479. PubMed: 17038478.
21. Hartgring SA, Willis CR, Alcorn D, Nelson LJ, Bijlsma JW, et al. (2010) Blockade of the interleukin-7 receptor inhibits collagen-induced arthritis and is associated with reduction of T cell activity and proinflammatory mediators. Arthritis Rheum 62: 2716-2725. doi:10.1002/art.27578. PubMed: 20499386.
22. Gonzalez-Quintial R, Lawson BR, Scatizzi JC, Craft J, Kono DH, et al. (2011) Systemic autoimmunity and lymphoproliferation are associated with excess IL-7 and inhibited by IL-7Ralpha blockade. PLOS ONE 6: e27528. doi:10.1371/journal.pone.0027528. PubMed: 22102903.
23. Shinohara T, Nemoto Y, Kanai T, Kameyama K, Okamoto R, et al. (2011) Upregulated IL-7 receptor alpha expression on colitogenic memory CD4+ T cells may participate in the development and persistence of chronic colitis. J Immunol 186: 2623-2632. doi:10.4049/jimmunol.1000057. PubMed: 21217010.
24. Totsuka T, Kanai T, Nemoto Y, Makita S, Okamoto R, et al. (2007) IL-7 Is essential for the development and the persistence of chronic colitis. J Immunol 178: 4737-4748. PubMed: 17404253.
25. Yamazaki M, Yajima T, Tanabe M, Fukui K, Okada E, et al. (2003) Mucosal T cells expressing high levels of IL-7 receptor are potential targets for treatment of chronic colitis. J Immunol 171: 1556-1563. PubMed: 12874249.
26. Lee LF, Logronio K, Tu GH, Zhai W, Ni I, et al. (2012) Anti-IL-7 receptor-alpha reverses established type 1 diabetes in nonobese diabetic mice by modulating effector T-cell function. Proc Natl Acad Sci U S A 109: 12674-12679. doi:10.1073/pnas.1203795109. PubMed: 22733769.
27. Bikker A, van Woerkom JM, Kruize AA, Wenting-van Wijk M, de Jager W, et al. (2010) Increased expression of interleukin-7 in labial salivary glands of patients with primary Sjogren's syndrome correlates with increased inflammation. Arthritis Rheum 62: 969-977. doi:10.1002/art.27318. PubMed: 20131250.
28. Jin JO, Kawai T, Cha S, Yu Q, (2013) Interleukin-7 enhances Th1 response to promote the development of Sjogren's Syndrome-Like autoimmune exocrinopathy. Arthritis Rheum.
29. Cha S, Nagashima H, Brown VB, Peck AB, Humphreys-Beher MG, (2002) Two NOD Idd-associated intervals contribute synergistically to the development of autoimmune exocrinopathy (Sjogren's syndrome) on a healthy murine background. Arthritis Rheum 46: 1390-1398. doi:10.1002/art.10258. PubMed: 12115247.
30. Cha S, Nagashima H, Peck AB, Humphreys-Beher MG, (2002) IDD3 and IDD5 alleles from nod mice mediate Sjogren's syndrome-like autoimmunity. Adv Exp Med Biol 506: 1035-1039. doi:10.1007/978-1-4615-0717-8_44. PubMed: 12614028.
31. Sawa Y, Arima Y, Ogura H, Kitabayashi C, Jiang JJ, et al. (2009) Hepatic interleukin-7 expression regulates T cell responses. Immunity 30: 447-457. doi:10.1016/j.immuni.2009.01.007. PubMed: 19285437.
32. Jin JO, Yu Q, (2012) Systemic administration of TLR3 agonist induces IL-7 expression and IL-7-dependent CXCR3 ligand production in the lung. J Leukoc Biol, 93: 413-25. PubMed: 23271706.
33. Mariette X, Gottenberg JE, (2010) Pathogenesis of Sjogren's syndrome and therapeutic consequences. Curr Opin Rheumatol 22: 471-477. doi:10.1097/BOR.0b013e32833c36c5. PubMed: 20671520.
34. Sharma R, Deshmukh US, Zheng L, Fu SM, Ju ST, (2009) X-linked Foxp3 (Scurfy) mutation dominantly inhibits submandibular gland development and inflammation respectively through adaptive and innate immune mechanisms. J Immunol 183: 3212-3218. doi:10.4049/jimmunol.0804355. PubMed: 19648271.
35. Deshmukh US, Nandula SR, Thimmalapura PR, Scindia YM, Bagavant H, (2009) Activation of innate immune responses through Toll-like receptor 3 causes a rapid loss of salivary gland function. J Oral Pathol Med 38: 42-47. PubMed: 19192049.
36. Nandula SR, Scindia YM, Dey P, Bagavant H, Deshmukh US, (2011) Activation of innate immunity accelerates sialoadenitis in a mouse model for Sjogren's syndrome-like disease. Oral Dis 17: 801-807. doi:10.1111/j.1601-0825.2011.01839.x. PubMed: 21815968.
37. Ittah M, Miceli-Richard C, Gottenberg JE, Sellam J, Eid P, et al. (2008) Viruses induce high expression of BAFF by salivary gland epithelial cells through TLR- and type-I IFN-dependent and-independent pathways. Eur J Immunol 38: 1058-1064. doi:10.1002/eji.200738013. PubMed: 18350548.
38. Li J, Jeong MY, Bae JH, Shin YH, Jin M, et al. (2010) Toll-like Receptor3-mediated Induction of Chemokines in Salivary Epithelial Cells. Korean J Physiol Pharmacol 14: 235-240. doi:10.4196/kjpp.2010.14.4.235. PubMed: 20827338.
39. Kawakami A, Nakashima K, Tamai M, Nakamura H, Iwanaga N, et al. (2007) Toll-like receptor in salivary glands from patients with Sjogren's syndrome: functional analysis by human salivary gland cell line. J Rheumatol 34: 1019-1026. PubMed: 17407216.
40. Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN, (2007) TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med 13: 543-551. doi:10.1038/nm1590. PubMed: 17479100.
41. Takeuchi O, Akira S, (2008) MDA5/RIG-I and virus recognition. Curr Opin Immunol 20: 17-22. doi:10.1016/j.coi.2008.01.002. PubMed: 18272355.
42. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105. doi:10.1038/nature04734. PubMed: 16625202.
43. Wang Q, Miller DJ, Bowman ER, Nagarkar DR, Schneider D, et al. (2011) MDA5 and TLR3 initiate pro-inflammatory signaling pathways leading to rhinovirus-induced airways inflammation and hyperresponsiveness. PLOS Pathog 7: e1002070. PubMed: 21637773.
44. Ittah M, Miceli-Richard C, Gottenberg JE, Sellam J, Lepajolec C, et al. (2009) B-cell-activating factor expressions in salivary epithelial cells after dsRNA virus infection depends on RNA-activated protein kinase activation. Eur J Immunol 39: 1271-1279. doi:10.1002/eji.200839086. PubMed: 19337998.
45. Matsumoto M, Oshiumi H, Seya T, (2011) Antiviral responses induced by the TLR3 pathway. Rev Med Virol. PubMed: 21312311.
46. McCartney S, Vermi W, Gilfillan S, Cella M, Murphy TL, et al. (2009) Distinct and complementary functions of MDA5 and TLR3 in poly(I:C)-mediated activation of mouse NK cells. J Exp Med 206: 2967-2976. doi:10.1084/jem.20091181. PubMed: 19995959.
47. Kim KD, Zhao J, Auh S, Yang X, Du P, et al. (2007) Adaptive immune cells temper initial innate responses. Nat Med 13: 1248-1252. doi:10.1038/nm1633. PubMed: 17891146.
48. Schmidt KN, Leung B, Kwong M, Zarember KA, Satyal S, et al. (2004) APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J Immunol 172: 138-143. PubMed: 14688319.
49. Lauzon NM, Mian F, MacKenzie R, Ashkar AA, (2006) The direct effects of Toll-like receptor ligands on human NK cell cytokine production and cytotoxicity. Cell Immunol 241: 102-112. doi:10.1016/j.cellimm.2006.08.004. PubMed: 17049504.
50. Groom JR, Luster AD, (2011) CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 89: 207-215. doi:10.1038/icb.2010.158. PubMed: 21221121.
51. Groom JR, Luster AD, (2011) CXCR3 in T cell function. Exp Cell Res 317: 620-631. doi:10.1016/j.yexcr.2010.12.017. PubMed: 21376175.