The osteopontin transgenic mouse is a new model for Sjögren's syndrome

Clinical Immunology

Volumn 157, Issue 1, 2015, Pages 30-42

  Husain Krautter, Sehba ^a,b   Kramer, Jill M ^b,c,d,e   Li, Wentian ^b   Guo, Benchang ^b   Rothstein, Thomas L ^a,b,d  

^a Elmezzi Graduate School of Molecular Medicine   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c LONG ISLAND JEWISH MEDICAL CENTER   (United States)

^d DONALD AND BARBARA ZUCKER SCHOOL OF MEDICINE AT HOFSTRA NORTHWELL   (United States)

^e UNIVERSITY AT BUFFALO   (United States)

Author keywords

B cell; Osteopontin; Sialadenitis; Sjogren's syndrome

Indexed keywords

AUTOANTIBODY; OSTEOPONTIN; SJOEGREN SYNDROME AUTOANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; IMMUNOPATHOGENESIS; LACRIMAL GLAND; LYMPHOCYTIC INFILTRATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALIVARY GLAND; SALIVATION; SERUM; SEX DIFFERENCE; SJOEGREN SYNDROME; T LYMPHOCYTE; TRANSGENIC MOUSE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CELL SURVIVAL; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOPHYSIOLOGY; UPREGULATION;

ANIMALS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; OSTEOPONTIN; SEX FACTORS; SJOGREN'S SYNDROME; UP-REGULATION;

EID: 84921490784     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2014.12.010     Document Type: Article

References (80)

1. Oldberg A., Franzen A., Heinegard D. Cloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:8819-8823.
2. Brown L.F., Berse B., Van de Water L., Papadopoulos-Sergiou A., Perruzzi C.A., Manseau E.J., et al. Expression and distribution of osteopontin in human tissues: widespread association with luminal epithelial surfaces. Mol. Biol. Cell 1992, 3:1169-1180.
3. McKee M.D., Nanci A. Secretion of Osteopontin by macrophages and its accumulation at tissue surfaces during wound healing in mineralized tissues: a potential requirement for macrophage adhesion and phagocytosis. Anat. Rec. 1996, 245:394-409.
4. Kourepini E., Aggelakopoulou M., Alissafi T., Paschalidis N., Simoes D.C., Panoutsakopoulou V. Osteopontin expression by CD103- dendritic cells drives intestinal inflammation. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:E856-E865.
5. O'Regan A.W., Chupp G.L., Lowry J.A., Goetschkes M., Mulligan N., Berman J.S. Osteopontin is associated with T cells in sarcoid granulomas and has T cell adhesive and cytokine-like properties in vitro. J. Immunol. 1999, 162:1024-1031.
6. Guo B., Tumang J.R., Rothstein T.L. B cell receptor crosstalk: B cells express osteopontin through the combined action of the alternate and classical BCR signaling pathways. Mol. Immunol. 2009, 46:587-591.
7. Keszei M., Detre C., Castro W., Magelky E., O'Keeffe M., Kis-Toth K., et al. Expansion of an osteopontin-expressing T follicular helper cell subset correlates with autoimmunity in B6.Sle1b mice and is suppressed by the H1-isoform of the Slamf6 receptor. FASEB journal: official publication of the Federation of American Societies for. Exp. Biol. 2013, 27:3123-3131.
8. D'Alfonso S., Barizzone N., Giordano M., Chiocchetti A., Magnani C., Castelli L., et al. Two single-nucleotide polymorphisms in the 5' and 3' ends of the osteopontin gene contribute to susceptibility to systemic lupus erythematosus. Arthritis Rheum. 2005, 52:539-547.
9. Xu G., Nie H., Li N., Zheng W., Zhang D., Feng G., et al. Role of osteopontin in amplification and perpetuation of rheumatoid synovitis. J. Clin. Invest. 2005, 115:1060-1067.
10. Shimizu Y., Ota K., Ikeguchi R., Kubo S., Kabasawa C., Uchiyama S. Plasma osteopontin levels are associated with disease activity in the patients with multiple sclerosis and neuromyelitis optica. J. Neuroimmunol. 2013, 263:148-151.
11. Chiocchetti A., Orilieri E., Cappellano G., Barizzone N., DA S., DA G., et al. The osteopontin gene +1239A/C single nucleotide polymorphism is associated with type 1 diabetes mellitus in the Italian population. Int. J. Immunopathol. Pharmacol. 2010, 23:263-269.
12. Karamizadeh Z., Kamali Sarvestani E., Saki F., Karamifar H., Amirhakimi G.H., Namavar Shooshtarian M.H., et al. Investigation of osteopontin levels and genomic variation of osteopontin and its receptors in Type 1 diabetes mellitus. J. Endocrinol. Investig. 2013, 36:1090-1093.
13. Marciano R., D'Annunzio G., Minuto N., Pasquali L., Santamaria A., Di Duca M., et al. Association of alleles at polymorphic sites in the Osteopontin encoding gene in young type 1 diabetic patients. Clin. Immunol. 2009, 131:84-91.
14. Gazal S., Sacre K., Allanore Y., Teruel M., Goodall A.H., Tohma S., et al. Identification of secreted phosphoprotein 1 gene as a new rheumatoid arthritis susceptibility gene. Ann. Rheum. Dis. 2014, 0:1-8.
15. Wang Y.H., Zhao M.S., Zhao Y. Expression of osteopontin in labial glands of patients with primary Sjogren's syndrome. Beijing Da Xue Xue Bao 2012, 44:236-239.
16. Wu G.L., Li T.Y., Fan Y.S., Yu G.Y. Therapeutic effect of Chinese herbal medicine for strengthening qi, nourishing yin, and removing stasis on serum osteopontin and quality of life of patients with primary Sjogren's syndrome. Chin. J. Integr. Med. 2011, 17:710-714.
17. Vitali C., Bombardieri S., Jonsson R., Moutsopoulos H.M., Alexander E.L., Carsons S.E., et al. Classification criteria for Sjogren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann. Rheum. Dis. 2002, 61:554-558.
18. Shiboski S.C., Shiboski C.H., Criswell L., Baer A., Challacombe S., Lanfranchi H., et al. American College of Rheumatology classification criteria for Sjogren's syndrome: a data-driven, expert consensus approach in the Sjogren's International Collaborative Clinical Alliance cohort. Arthritis Care Res. 2012, 64:475-487.
19. Lavoie T.N., Lee B.H., Nguyen C.Q. Current concepts: mouse models of Sjogren's syndrome. J. Biomed. Biotechnol. 2011, 2011:549107.
20. Cha S., Peck A.B., Humphreys-Beher M.G. Progress in understanding autoimmune exocrinopathy using the non-obese diabetic mouse: an update. Crit. Rev. Oral Biol. Med. 2002, 13:5-16.
21. Iizuka J., Katagiri Y., Tada N., Murakami M., Ikeda T., Sato M., et al. Introduction of an osteopontin gene confers the increase in B1 cell population and the production of anti-DNA autoantibodies. Lab. Invest. 1998, 78:1523-1533.
22. Zhong X., Tumang J.R., Gao W., Bai C., Rothstein T.L. PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for V(H)11/V(H)12 and phosphatidylcholine binding. Eur. J. Immunol. 2007, 37:2405-2410.
23. Schneider T.J., Grillot D., Foote L.C., Nunez G.E., Rothstein T.L. Bcl-x protects primary B cells against Fas-mediated apoptosis. J. Immunol. 1997, 159:4834-4839.
24. Obermuller N., Gassler N., Gretz N., Kranzlin B., Hoffmann S., Geiger H., et al. Distinct immunohistochemical expression of osteopontin in the adult rat major salivary glands. J. Mol. Histol. 2006, 37:53-60.
25. Ogbureke K.U., Fisher L.W. Expression of SIBLINGs and their partner MMPs in salivary glands. J. Dent. Res. 2004, 83:664-670.
26. Delaleu N., Nguyen C.Q., Peck A.B., Jonsson R. Sjogren's syndrome: studying the disease in mice. Arthritis Res. Ther. 2011, 13:217.
27. Daniels T.E., Cox D., Shiboski C.H., Schiodt M., Wu A., Lanfranchi H., et al. Associations between salivary gland histopathologic diagnoses and phenotypic features of Sjogren's syndrome among 1,726 registry participants. Arthritis Rheum. 2011, 63:2021-2030.
28. Robinson C.P., Brayer J., Yamachika S., Esch T.R., Peck A.B., Stewart C.A., et al. Transfer of human serum IgG to nonobese diabetic Igmu null mice reveals a role for autoantibodies in the loss of secretory function of exocrine tissues in Sjogren's syndrome. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7538-7543.
29. Okuma A., Hoshino K., Ohba T., Fukushi S., Aiba S., Akira S., et al. Enhanced apoptosis by disruption of the STAT3-IkappaB-zeta signaling pathway in epithelial cells induces Sjogren's syndrome-like autoimmune disease. Immunity 2013, 38:450-460.
30. Mongini P.K., Kramer J.M., Ishikawa T.O., Herschman H., Esposito D. Candidate chromosome 1 disease susceptibility genes for Sjogren's syndrome xerostomia are narrowed by novel NOD.B10 congenic mice. Clin. Immunol. 2014, 153:79-90.
31. Szodoray P., Alex P., Jonsson M.V., Knowlton N., Dozmorov I., Nakken B., et al. Distinct profiles of Sjogren's syndrome patients with ectopic salivary gland germinal centers revealed by serum cytokines and BAFF. Clin. Immunol. 2005, 117:168-176.
32. Katsifis G.E., Rekka S., Moutsopoulos N.M., Pillemer S., Wahl S.M. Systemic and local interleukin-17 and linked cytokines associated with Sjogren's syndrome immunopathogenesis. Am. J. Pathol. 2009, 175:1167-1177.
33. Szodoray P., Alex P., Brun J.G., Centola M., Jonsson R. Circulating cytokines in primary Sjogren's syndrome determined by a multiplex cytokine array system. Scand. J. Immunol. 2004, 59:592-599.
34. Li H., Dai M., Zhuang Y. A T cell intrinsic role of Id3 in a mouse model for primary Sjogren's syndrome. Immunity 2004, 21:551-560.
35. Li J., Maruyama T., Zhang P., Konkel J.E., Hoffman V., Zamarron B., et al. Mutation of inhibitory helix-loop-helix protein Id3 causes γδ T-cell lymphoma in mice. Blood 2010, 116:5615-5621.
36. Sapone A., de Magistris L., Pietzak M., Clemente M.G., Tripathi A., Cucca F., et al. Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 2006, 55:1443-1449.
37. Watts T., Berti I., Sapone A., Gerarduzzi T., Not T., Zielke R., et al. Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2916-2921.
38. Eerola E., Mottonen T., Hannonen P., Luukkainen R., Kantola I., Vuori K., et al. Intestinal flora in early rheumatoid arthritis. Br. J. Rheumatol. 1994, 33:1030-1038.
39. Szymula A., Rosenthal J., Szczerba B.M., Bagavant H., Fu S.M., Deshmukh U.S. T cell epitope mimicry between Sjogren's syndrome Antigen A (SSA)/Ro60 and oral, gut, skin and vaginal bacteria. Clin. Immunol. 2014, 152:1-9.
40. Brayer J.B., Cha S., Nagashima H., Yasunari U., Lindberg A., Diggs S., et al. IL-4-dependent effector phase in autoimmune exocrinopathy as defined by the NOD.IL-4-gene knockout mouse model of Sjogren's syndrome. Scand. J. Immunol. 2001, 54:133-140.
41. Gao J., Killedar S., Cornelius J.G., Nguyen C., Cha S., Peck A.B. Sjogren's syndrome in the NOD mouse model is an interleukin-4 time-dependent, antibody isotype-specific autoimmune disease. J. Autoimmun. 2006, 26:90-103.
42. Nguyen C.Q., Gao J.H., Kim H., Saban D.R., Cornelius J.G., Peck A.B. IL-4-STAT6 signal transduction-dependent induction of the clinical phase of Sjogren's syndrome-like disease of the nonobese diabetic mouse. J. Immunol. 2007, 179:382-390.
43. Ashkar S., Weber G.F., Panoutsakopoulou V., Sanchirico M.E., Jansson M., Zawaideh S., et al. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 2000, 287:860-864.
44. Chen G., Zhang X., Li R., Fang L., Niu X., Zheng Y., et al. Role of osteopontin in synovial Th17 differentiation in rheumatoid arthritis. Arthritis Rheum. 2010, 62:2900-2908.
45. Yang M., Ma C., Liu S., Sun J., Shao Q., Gao W., et al. Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopontin. Immunology 2009, 128:e237-e249.
46. Mitsias D.I., Tzioufas A.G., Veiopoulou C., Zintzaras E., Tassios I.K., Kogopoulou O., et al. The Th1/Th2 cytokine balance changes with the progress of the immunopathological lesion of Sjogren's syndrome. Clin. Exp. Immunol. 2002, 128:562-568.
47. Nguyen C.Q., Yin H., Lee B.H., Carcamo W.C., Chiorini J.A., Peck A.B. Pathogenic effect of interleukin-17A in induction of Sjogren's syndrome-like disease using adenovirus-mediated gene transfer. Arthritis Res. Ther. 2010, 12:R220.
48. Cornec D., Devauchelle-Pensec V., Tobon G.J., Pers J.O., Jousse-Joulin S., Saraux A. B cells in Sjogren's syndrome: from pathophysiology to diagnosis and treatment. J. Autoimmun. 2012, 39:161-167.
49. Pers J.O., Youinou P. Are the B cells cast with the leading part in the Sjogren's syndrome scenario?. Oral Dis. 2013, 20(6):529-537.
50. Lampe M.A., Patarca R., Iregui M.V., Cantor H. Polyclonal B cell activation by the Eta-1 cytokine and the development of systemic autoimmune disease. J. Immunol. 1991, 147:2902-2906.
51. Denhardt D.T., Guo X. Osteopontin: a protein with diverse functions. FASEB J. 1993, 7:1475-1482.
52. Patarca R., Wei F.Y., Singh P., Morasso M.I., Cantor H. Dysregulated expression of the T cell cytokine Eta-1 in CD4-8- lymphocytes during the development of murine autoimmune disease. J. Exp. Med. 1990, 172:1177-1183.
53. Take Y., Nakata K., Hashimoto J., Tsuboi H., Nishimoto N., Ochi T., et al. Specifically modified osteopontin in rheumatoid arthritis fibroblast-like synoviocytes supports interaction with B cells and enhances production of interleukin-6. Arthritis Rheum. 2009, 60:3591-3601.
54. Agnholt J., Kelsen J., Schack L., Hvas C.L., Dahlerup J.F., Sørensen E.S. Osteopontin, a protein with cytokine-like properties, is associated with inflammation in Crohn's disease. Scand. J. Immunol. 2007, 65:453-460.
55. Nakama K., Miyazaki Y., Nasu M. Immunophenotyping of lymphocytes in the lung interstitium and expression of osteopontin and interleukin-2 mRNAs in two different murine models of pulmonary fibrosis. Exp. Lung Res. 1998, 24:57-70.
56. Whitington P.F., Malladi P., Melin-Aldana H., Azzam R., Mack C.L., Sahai A. Expression of osteopontin correlates with portal biliary proliferation and fibrosis in biliary atresia. Pediatr. Res. 2005, 57:837-844.
57. Wiwanitkit V. Effect of interleukin-2 and tumor necrosis factor-alpha on osteopontin: molecular function and biological process. Pediatr. Int. 2008, 50:213-215.
58. Luo X.Y., Takahara T., Kawai K., Fujino M., Sugiyama T., Tsuneyama K., et al. IFN-gamma deficiency attenuates hepatic inflammation and fibrosis in a steatohepatitis model induced by a methionine- and choline-deficient high-fat diet. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 305:G891-G899.
59. Karcher E.L., Hill T.M., Bateman H.G., Schlotterbeck R.L., Vito N., Sordillo L.M., et al. Comparison of supplementation of n-3 fatty acids from fish and flax oil on cytokine gene expression and growth of milk-fed Holstein calves. J. Dairy Sci. 2014, 97:2329-2337.
60. Diao H., Iwabuchi K., Li L., Onoe K., Van Kaer L., Kon S., et al. Osteopontin regulates development and function of invariant natural killer T cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15884-15889.
61. Sabo-Attwood T., Ramos-Nino M.E., Eugenia-Ariza M., Macpherson M.B., Butnor K.J., Vacek P.C., et al. Osteopontin modulates inflammation, mucin production, and gene expression signatures after inhalation of asbestos in a murine model of fibrosis. Am. J. Pathol. 2011, 178:1975-1985.
62. Persy V.P., Verhulst A., Ysebaert D.K., De Greef K.E., De Broe M.E. Reduced postischemic macrophage infiltration and interstitial fibrosis in osteopontin knockout mice. Kidney Int. 2003, 63:543-553.
63. Zhang Z.X., Shek K., Wang S., Huang X., Lau A., Yin Z., et al. Osteopontin expressed in tubular epithelial cells regulates NK cell-mediated kidney ischemia reperfusion injury. J. Immunol. 2010, 185:967-973.
64. Rusakiewicz S., Nocturne G., Lazure T., Semeraro M., Flament C., Caillat-Zucman S., et al. NCR3/NKp30 contributes to pathogenesis in primary Sjogren's syndrome. Sci. Transl. Med. 2013, 5:195ra96.
65. Chung J.W., Kim M.S., Piao Z.H., Jeong M., Yoon S.R., Shin N., et al. Osteopontin promotes the development of natural killer cells from hematopoietic stem cells. Stem Cells 2008, 26:2114-2123.
66. Sato K., Iwai A., Nakayama Y., Morimoto J., Takada A., Maruyama M., et al. Osteopontin is critical to determine symptom severity of influenza through the regulation of NK cell population. Biochem. Biophys. Res. Commun. 2012, 417:274-279.
67. Wang K.X., Denhardt D.T. Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev. 2008, 19:333-345.
68. Hur E.M., Youssef S., Haws M.E., Zhang S.Y., Sobel R.A., Steinman L. Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nat. Immunol. 2007, 8:74-83.
69. Kawamura K., Iyonaga K., Ichiyasu H., Nagano J., Suga M., Sasaki Y. Differentiation, maturation, and survival of dendritic cells by osteopontin regulation. Clin. Diagn. Lab. Immunol. 2005, 12:206-212.
70. Burdo T.H., Wood M.R., Fox H.S. Osteopontin prevents monocyte recirculation and apoptosis. J. Leukoc. Biol. 2007, 81:1504-1511.
71. Ma N., He Y., Xiao H., Han G., Chen G., Wang Y., et al. BAFF maintains T-cell survival by inducing OPN expression in B cells. Mol. Immunol. 2014, 57:129-137.
72. Daridon C., Devauchelle V., Hutin P., Le Berre R., Martins-Carvalho C., Bendaoud B., et al. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjogren's syndrome. Arthritis Rheum. 2007, 56:1134-1144.
73. Lavie F., Miceli-Richard C., Quillard J., Roux S., Leclerc P., Mariette X. Expression of BAFF (BLyS) in T cells infiltrating labial salivary glands from patients with Sjogren's syndrome. J. Pathol. 2004, 202:496-502.
74. Groom J., Kalled S.L., Cutler A.H., Olson C., Woodcock S.A., Schneider P., et al. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. J. Clin. Invest. 2002, 109:59-68.
75. Hansen A., Lipsky P.E., Dorner T. B cells in Sjogren's syndrome: indications for disturbed selection and differentiation in ectopic lymphoid tissue. Arthritis Res. Ther. 2007, 9:218.
76. Carubbi F., Cipriani P., Marrelli A., Benedetto P., Ruscitti P., Berardicurti O., et al. Efficacy and safety of rituximab treatment in early primary Sjogren's syndrome: a prospective, multi-center, follow-up study. Arthritis Res. Ther. 2013, 15:R172.
77. Dass S., Bowman S.J., Vital E.M., Ikeda K., Pease C.T., Hamburger J., et al. Reduction of fatigue in Sjogren syndrome with rituximab: results of a randomised, double-blind, placebo-controlled pilot study. Ann. Rheum. Dis. 2008, 67:1541-1544.
78. Toussirot E., Bereau M. The risk of progressive multifocal leukoencephalopathy under biological agents used in the treatment of chronic inflammatory diseases. Inflamm. Allergy Drug Targets 2014, 13(2):121-127.
79. Fan K., Dai J., Wang H., Wei H., Cao Z., Hou S., et al. Treatment of collagen-induced arthritis with an anti-osteopontin monoclonal antibody through promotion of apoptosis of both murine and human activated T cells. Arthritis Rheum. 2008, 58:2041-2052.
80. Boumans M.J., Houbiers J.G., Verschueren P., Ishikura H., Westhovens R., Brouwer E., et al. Safety, tolerability, pharmacokinetics, pharmacodynamics and efficacy of the monoclonal antibody ASK8007 blocking osteopontin in patients with rheumatoid arthritis: a randomised, placebo controlled, proof-of-concept study. Ann. Rheum. Dis. 2012, 71:180-185.