NOD.H-2h4 mice: An important and underutilized animal model of autoimmune thyroiditis and sjogren's syndrome

Advances in Immunology

Volumn 126, Issue , 2015, Pages 1-43

  Braley Mullen, Helen ^a   Yu, Shiguang ^b  

^a University of Missouri   (United States)

^b ARKANSAS STATE UNIVERSITY   (United States)

Author keywords

Autoimmunity; Mouse models; Sjogren's syndrome; Thyroiditis

Indexed keywords

AUTOANTIBODY; CD28 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; IMMUNOGLOBULIN G2A; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; THYROGLOBULIN; THYROGLOBULIN ANTIBODY; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNE THYROIDITIS; AUTOIMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; HAPLOTYPE; HASHIMOTO DISEASE; HISTOLOGY; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNIZATION; MALE; MOUSE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SJOEGREN SYNDROME; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYROID FUNCTION; THYROID NODULE; ANIMAL; DISEASE MODEL; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE; NONOBESE DIABETIC MOUSE;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INTERFERON-GAMMA; LYMPHOCYTES; MALE; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; SJOGREN'S SYNDROME; THYROIDITIS, AUTOIMMUNE;

EID: 84923291062     PISSN: 00652776     EISSN: 15578445     Source Type: Book Series    
DOI: 10.1016/bs.ai.2014.11.001     Document Type: Chapter

References (109)

1. Abdulahad W.H., Kroese F., Vissink A., Bootsma H. Immune regulation and B-cell depletion therapy in patients with primary Sjogren's syndrome. Journal of Autoimmunity 2012, 39:103-111.
2. Allen E.M., Appel M.C., Braverman L.E. The effect of iodide ingestion on the development of spontaneous lymphocytic thyroiditis in the diabetes-prone BB.W rat. Endocrinology 1986, 118:1977-1981.
3. Ansari M.J., Salama A.D., Chitnis T., Smith R.N., Yagita H., Akiba H., et al. The programmed death-1 pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. The Journal of Experimental Medicine 2003, 198:63-69.
4. Asa S.L., Mete O. Thyroid neoplasms of follicular cell derivation: A simplified approach. Seminars in Diagnostic Pathology 2013, 30:178-185.
5. Bagchi N., Brown T.R., Sundick R.S. Thyroid cell injury is an initial event in the induction of autoimmune thyroiditis by iodine in obese strain chickens. Endocrinology 1995, 136:5054-5060.
6. Bagchi N., Brown T.R., Urdanivia L., Sundick R.S. Induction of autoimmune thyroiditis in chickens by dietary iodine. Science 1985, 230:325-327.
7. Barin J.G., Talor M.V., Sharma R.B., Rose N.R., Burek C.L. Iodination of murine thyroglobulin enhances autoimmune reactivity in the NOD.H-2h4 mouse. Clinical and Experimental Immunology 2005, 142:251-259.
8. Blank C., Gajewski T.F., Mackensen A. Interaction of PDL-1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: Implications for tumor immunotherapy. Cancer Immunology, Immunotherapy 2005, 54:307-314.
9. Blaydes J.P., Wynford-Thomas D. Loss of responsiveness to TGF-β is tightly linked to tumorigenicity in a model of thyroid tumor progression. International Journal of Cancer 1996, 65:525-530.
10. Boehm U., Klamp T., Groot M., Howard J.C. Cellular responses to interferon-γ. Annual Review of Immunology 1997, 15:749-795.
11. Bonita R.E., Rose N.R., Rasooly L., Caturegli P., Burek C.L. Adhesion molecules as susceptibility factors in spontaneous autoimmune thyroiditis in the NOD-H2h4 mouse. Experimental and Molecular Pathology 2002, 73:155-163.
12. Bonita R.E., Rose N.R., Rasooly L., Caturegli P., Burek C.L. Kinetics of mononuclear cell infiltration and cytokine expression in iodine-induced thyroiditis in the NOD-H2h4 mouse. Experimental and Molecular Pathology 2003, 74:1-12.
13. Bour-Jordan H., Bluestone J.A. Regulating the regulators: Costimulatory signals control the homeostasis and function of regulatory T cells. Immunological Reviews 2009, 229:41-66.
14. Bour-Jordan H., Esensten J.H., Martinez-Llordella M., Penaranda C., Stumpf M., Bluestone J.A. Intrinsic and extrinsic control of peripheral T-cell tolerance by costimulatory molecules of the CD28/B7 family. Immunological Reviews 2011, 241:180-205.
15. Braley-Mullen H., Chen K., Wei Y., Yu S. Role of TGFbeta in development of spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. Journal of Immunology 2001, 167:7111-7118.
16. Braley-Mullen H., Sharp G.C., Medling B., Tang H. Spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. Journal of Autoimmunity 1999, 12:157-165.
17. Braley-Mullen H., Yu S. Early requirement for B cells for development of spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. Journal of Immunology 2000, 165:7262-7269.
18. Bravo S.B., Pampin S., Cameselle-Teijeiro J., Carneiro C., Dominguez F., Barreiro F., et al. TGF-β induced apoptosis in human thyrocytes is mediated by p27kip1 reduction and is overridden in neoplastic thyrocytes by NF-κB activation. Oncogene 2003, 22:7819-7830.
19. Burek C.L., Rose N.R. Autoimmune thyroiditis and ROS. Autoimmunity Reviews 2008, 7:530-537.
20. Burek C.L., Sharma R.B., Rose N.R. NKT cell regulation of autoimmune thyroiditis. Autoimmunity 2003, 36:405-408.
21. Burek C.L., Talor M.V. Environmental triggers of autoimmune thyroiditis. Journal of Autoimmunity 2009, 33:183-189.
22. Burek C.L., Talor M., Santana C., Rose N.R. Thyroiditis in NOD.H-2h4 mice born and reared in conventional housing and ingesting different doses of iodine. FASEB Journal 1998, 12:A1097.
23. Carayanniotis G. Recognition of thyroglobulin by T cells: The role of iodine. Thyroid 2007, 17:963-973.
24. Carayanniotis G. Molecular parameters linking thyroglobulin iodination with autoimmune thyroiditis. Hormones (Athens, Greece) 2011, 10:27-35.
25. Caturegli P., Hejazi M., Suzuki K., Dohan O., Carrasco N., Kohn L.D., et al. Hypothyroidism in transgenic mice expressing IFN-gamma in the thyroid. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:1719-1724.
26. Chen C.R., Hamidi S., Braley-Mullen H., Nagayama Y., Bresee C., Aliesky H.A., et al. Antibodies to thyroid peroxidase arise spontaneously with age in NOD.H-2h4 mice and appear after thyroglobulin antibodies. Endocrinology 2010, 151:4583-4593.
27. Chen K., Wei Y., Sharp G.C., Braley-Mullen H. Mechanisms of spontaneous resolution versus fibrosis in granulomatous experimental autoimmune thyroiditis. Journal of Immunology 2003, 171:6236-6243.
28. Chen K., Wei Y., Sharp G.C., Braley-Mullen H. Balance of proliferation and cell death between thyrocytes and myofibroblasts regulates thyroid fibrosis in granulomatous experimental autoimmune thyroiditis (G-EAT). Journal of Leukocyte Biology 2005, 77:166-172.
29. Chiorini J.A., Cihakova D., Ouellette C.E., Caturegli P. Sjogren syndrome: Advances in the pathogenesis from animal models. Journal of Autoimmunity 2009, 33:190-196.
30. Cihakova D., Talor M.V., Barin J.G., Baldeviano G.C., Fairweather D., Rose N.R., et al. Sex differences in a murine model of Sjogren's syndrome. Annals of the New York Academy of Sciences 2009, 1173:378-383.
31. Delaleu N., Nguyen C.Q., Peck A.B., Jansson R. Sjogren's syndrome: Studying the disease in mice. Arthritis Research & Therapy 2011, 13:217-223.
32. DeMay R.M. Follicular lesions of the thyroid. W(h)ither follicular carcinoma?. American Journal of Clinical Pathology 2000, 114:681-683.
33. Derwahl M., Studer H. Hyperplasia versus adenoma in endocrine tissues: Are they different?. Trends in Endocrinology and Metabolism 2002, 13:23-28.
34. Ellis J.S., Braley-Mullen H. Regulatory T cells in B cell-deficient and WT mice differ functionally and in expression of cell surface markers. Immunology 2014, in press.
35. Ellis J.S., Hong S.H., Zaghouani H., Braley-Mullen H. Reduced effectiveness of CD4+Foxp3+ regulatory T cells in CD28-deficient NOD.H-2h4 mice leads to increased severity of spontaneous autoimmune thyroiditis. Journal of Immunology 2013, 191:4940-4949.
36. Ellis J.S., Wan X., Braley-Mullen H. Transient depletion of CD4+ CD25+ regulatory T cells results in multiple autoimmune diseases in wild-type and B-cell-deficient NOD mice. Immunology 2013, 139:179-186.
37. Fang Y., Yu S., Braley-Mullen H. Contrasting roles of IFN-gamma in murine models of autoimmune thyroid diseases. Thyroid 2007, 17:989-994.
38. Fang Y., Yu S., Braley-Mullen H. TGF-beta promotes proliferation of thyroid epithelial cells in IFN-gamma(-/-) mice by down-regulation of p21 and p27 via AKT pathway. The American Journal of Pathology 2012, 180:650-660.
39. Good-Jacobson K.I., Szumilas C.G., Chen L., Sharpe A.H., Tomayko M.M., Shlomchik M.J. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nature Immunology 2010, 11:535-542.
40. Hamel K.M., Cao Y., Ashaye S., Wang Y., Dunn R., Kehry M.R., et al. B cell depletion enhances T regulatory cell activity essential in the suppression of arthritis. Journal of Immunology 2011, 187:4900-4906.
41. Hayakawa I., Tedder T.F., Zhuang Y. B-lymphocyte depletion ameliorates Sjogren's syndrome in Id3 knockout mice. Immunology 2007, 122:73-79.
42. + T cells indicate Tfh cell activity and promote antibody responses upon antigen re-exposure. Immunity 2013, 39:770-781.
43. Hong S.H., Braley-Mullen H. Follicular B cells in thyroids of mice with spontaneous autoimmune thyroiditis contribute to disease pathogenesis and are targets of anti-CD20 antibody therapy. Journal of Immunology 2014, 192:897-905.
44. Horie I., Abiru N., Nagayama Y., Kuriya G., Saitoh O., Ichikawa T., et al. T helper type 17 immune response plays an indispensable role for development of iodine-induced autoimmune thyroiditis in nonobese diabetic-H2h4 mice. Endocrinology 2009, 150:5135-5142.
45. Horie I., Abiru N., Sakamoto H., Iwakura Y., Nagayama Y. Induction of autoimmune thyroiditis by depletion of CD4+CD25+ regulatory T cells in thyroiditis-resistant IL-17, but not interferon-{gamma} receptor, knockout nonobese diabetic-H2h4 mice. Endocrinology 2011, 152:4448-4454.
46. Hutchings P.R., Cooke A., Dawe K., Champion B.R., Geysen M., Valerio R., et al. A thyroxine-containing peptide can induce murine experimental autoimmune thyroiditis. The Journal of Experimental Medicine 1992, 175:869-872.
47. Hutchings P.R., Verma S., Phillips J.M., Harach S.Z., Howlett S., Cooke A. Both CD4(+) T cells and CD8(+) T cells are required for iodine accelerated thyroiditis in NOD mice. Cellular Immunology 1999, 192:113-121.
48. Ishida Y., Kondo T., Takyasu T., Iwakura Y., Mukaida N. The essential involvement of cross-talk between IFN-γ and TGF-β in the skin wound healing process. Journal of Immunology 2004, 172:1848-1855.
49. Jasani B., Wyllie F.S., Wright P.A., Lemoine N.R., Williams E.D., Wynford-Thomas D. Immunocytochemically detectable TGF-β associated with malignancy in thyroid epithelial neoplasia. Growth Factors 1990, 2:149-155.
50. Karnell J.L., Mahmoud T.I., Herbst R., Ettinger R. Discerning the kinetics of autoimmune manifestations in a model of Sjogren's syndrome. Molecular Immunology 2014, 62(2):277-282.
51. Kayes T.D., Braley-Mullen H. Culture promotes transfer of thyroid epithelial cell hyperplasia and proliferation by reducing regulatory T cell numbers. Cellular Immunology 2013, 285:84-91.
52. Kayes T., Fang Y., Yu S., Downey E., Wang S., Braley-Mullen H. Agonistic anti-CD40 induces thyrocyte proliferation and promotes thyroid autoimmunity by increasing CD40 expression on thyroid epithelial cells. Journal of Immunology 2013, 190:3928-3938.
53. Keir M.E., Butte M.J., Freeman G.J., Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annual Review of Immunology 2008, 26:677-704.
54. Kimura E.T., Kopp P., Zbaeren J., Asmis L.M., Ruchti C., Maciel R.M., et al. Expression of transforming growth factor -β1, β2, and β3 in multinodular goiters and differentially thyroid carcinomas: A comparative study. Thyroid 1999, 9:119-125.
55. Kolypetri P., Carayanniotis G. Apoptosis of NOD.H2h4 thyrocytes by low concentrations of iodide is associated with impaired control of oxidative stress. Thyroid 2014, 24:1170-1178.
56. Kolypetri P., Carayanniotis K., Rahman S., Georghiou P.E., Magafa V., Cordopatis P., et al. The thyroxine-containing thyroglobulin peptide (aa 2549-2560) is a target epitope in iodide-accelerated spontaneous autoimmune thyroiditis. Journal of Immunology 2014, 193:96-101.
57. Kolypetri P., Noel N.A., Carayanniotis K.A., Carayanniotis G. Iodine content of thyroglobulin in NOD.H2-h4 mice developing iodine-accelerated autoimmune thyroiditis. Hormones (Athens, Greece) 2010, 9:151-160.
58. Kondo T., Ezzat S., Asa S.L. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nature Reviews. Cancer 2006, 6:292-306.
59. Kong Y. Experimental autoimmune thyroiditis in the mouse. Current Protocols in Immunology 2007, (Unit 15.7). Chapter 15.
60. Kong Y., Flynn J.C. Opportunistic autoimmune disorders potentiated by immune-checkpoint inhibitors anti-CTLA-4 and anti-PD-1. Frontiers in Immunology 2014, 5:1-8.
61. Kyriakidis N.C., Kapsogeorgou E.K., Tzioufas A.G. A comprehensive review of autoantibodies in primary Sjogren's syndrome: Clinical phenotypes and regulatory mechanisms. Journal of Autoimmunity 2014, 51:67-74.
62. Li H.S., Carayanniotis G. Iodination of tyrosyls in thyroglobulin generates neoantigenic determinants that cause thyroiditis. Journal of Immunology 2006, 176:4479-4483.
63. Li H.S., Jiang H.Y., Carayanniotis G. Modifying effects of iodine on the immunogenicity of thyroglobulin peptides. Journal of Autoimmunity 2007, 28:171-176.
64. Li M., Wan Y.Y., Sanjabi S., Robertson A.K., Flavell R.A. Transforming growth factor-β regulation of immune response. Annual Review of Immunology 2006, 24:99-146.
65. Logan A., Smith C., Becks G.P., Gonzale A.M., Phillips I.D., Hill D.J. Enhanced expression of transforming growth factor-β1 during thyroid hyperplasia in rats. Journal of Endocrinology 1994, 141:45-57.
66. Lund F.E., Randall T.D. Effector and regulatory B cells: Modulators of CD4+ T cell immunity. Nature Reviews. Immunology 2010, 10:236-247.
67. Marino E., Villanueva J., Walters S., Liuwantara D., Mackay F., Grey S.T. CD4(+)CD25(+) T-cells control autoimmunity in the absence of B-cells. Diabetes 2009, 58:1568-1577.
68. Massague J., Blain S.W., Lo R.S. TGF-β signaling in growth control, cancer, and heritable disorders. Cell 2000, 103:295-309.
69. Mete O., Asa S.L. Pitfalls in the diagnosis of follicular epithelial proliferations of the thyroid. Advances in Anatomic Pathology 2012, 19:363-373.
70. Nagayama Y., Horie I., Saitoh O., Nakahara M., Abiru N. CD4+CD25+ naturally occurring regulatory T cells and not lymphopenia play a role in the pathogenesis of iodide-induced autoimmune thyroiditis in NOD-H2h4 mice. Journal of Autoimmunity 2007, 29:195-202.
71. Nishimura H., Minato N., Nakano T., Honjo T. Immunological studies on PD-1-deficient mice: Implication of PD-1 as a negative regulator for B cell responses. International Immunology 1998, 10:1563-1572.
72. Pardoll D.M. The blockade of immune checkpoints in cancer immunotherapy. Nature Reviews. Cancer 2012, 12:252-264.
73. Podolin P.L., Pressey A., DeLarato N.H., Fischer P.A., Peterson L.B., Wicker L.S. I-E+nonobese diabetic mice develop insulitis and diabetes. The Journal of Experimental Medicine 1993, 178:793-803.
74. Prins J., Todd J.A., Rodrigues N.R., Ghosh S., Hogarth P.M., Wicker L.S., et al. Linkage on chromosome 3 of autoimmune diabetes and defective Fc receptor for IgG in NOD mice. Science 1993, 260:695-698.
75. Rasooly L., Burek C.L., Rose N.R. Iodine-induced autoimmune thyroiditis in NOD-H-2h4 mice. Clinical Immunology and Immunopathology 1996, 81:287-292.
76. Rose N.R., Bonita R., Burek C.L. Iodine: An environmental trigger of thyroidits. Autoimmunity Reviews 1992, 1:97-103.
77. Russo M.A., Antico Arciuch V.G., Di Cristofano A. Mouse models of follicular and papillary thyroid cancer progression. Frontiers in Endocrinology 2012, 2:1-9.
78. Sakuishi K., Apetoh L., Sullivan J.M., Blazar B.M., Kuchroo V.K., Anderson A.C. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. The Journal of Experimental Medicine 2010, 207:2187-2194.
79. Salomon B., Lenschow D.J., Rhee L., Ashourian N., Singh B., Sharpe A., et al. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000, 12:431-440.
80. Saxena V., Lienesch D.W., Zhou M., Bommireddy R., Azhar M., Doetschman T., et al. Dual roles of immunoregulatory cytokines TGF-β in the pathogenesis of autoimmune-mediated organ damage. Journal of Immunology 2008, 180:1903-1912.
81. Serreze D.V., Chapman H.D., Niens M., Dunn R., Kehry M.R., Driver J.P., et al. Loss of intra-islet CD20 expression may complicate efficacy of B-cell-directed type 1 diabetes therapies. Diabetes 2011, 60:2914-2921.
82. Sharma R.B., Alegria J.D., Talor M.V., Rose N.R., Caturegli P., Burek C.L. Iodine and IFN-gamma synergistically enhance intercellular adhesion molecule 1 expression on NOD.H2h4 mouse thyrocytes. Journal of Immunology 2005, 174:7740-7745.
83. Sharma R.B., Fan X., Caturegli P., Rose N.R., Burek C.L. Invariant NKT cell lines derived from the NOD.H2 mouse enhance autoimmune thyroiditis. Journal of Thyroid Research 2011, 2011:895-923.
84. Sharma R., Traore K., Trush M.A., Rose N.R., Burek C.L. Intracellular adhesion molecule-1 up-regulation on thyrocytes by iodine of non-obese diabetic.H2(h4) mice is reactive oxygen species-dependent. Clinical and Experimental Immunology 2008, 152:13-20.
85. Sharpe A.H., Freeman G.J. The B7-CD28 superfamily. Nature Reviews. Immunology 2002, 2:116-126.
86. Sharpe A.H., Wherry E.J., Ahmed R., Freeman G.J. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nature Immunology 2007, 8:239-245.
87. Shi L., Bi M., Yang R., Zhou J., Zhao S., Fan C., et al. Defective expression of regulatory B cells in iodine-induced autoimmune thyroiditis in non-obese diabetic H-2(h4) mice. Journal of Endocrinological Investigation 2014, 37:43-50.
88. Sullivan D.E., Ferris M., Nguyen H., Abboud E., Brody A.R. TNF-α induces TGF-β1 expression in lung fibroblasts at the transcriptional level via AP-1 activation. Journal of Cellular and Molecular Medicine 2009, 13:1866-1876.
89. Tang H., Sharp G.C., Peterson K.E., Braley-Mullen H. IFN-γ-deficient mice develop severe granulomatous experimental autoimmune thyroiditis with eosinophil infiltration in thyroids. Journal of Immunology 1998, 160:5105-5112.
90. Tang B., Vu M., Booker T., Santner S.J., Miller F.R., Anver M.R., et al. TGF-β switches from tumor suppressor to prometastatic factor in a model of breast cancer progression. The Journal of Clinical Investigation 2003, 112:1116-1124.
91. Turco A., Coppa A., Aloe S., Baccheschi G., Morrone S., Zupi G., et al. Overexpression of TGF-β-type II receptor reduces tumorigenicity and metastatic potential of K-ras-transformed thyroid cells. International Journal of Cancer 1999, 80:85-91.
92. Tzioufas A.G., Kapsogeorgou E.K., Moutsopoulos H.M. Pathogenesis of Sjogren's syndrome: What we know and what we should learn. Journal of Autoimmunity 2012, 39:4-8.
93. Ulloa L., Doody J., Massague J. Inhibition of transforming growth factor-β/SMAD signaling by interferon-γ/STAT pathway. Nature 1999, 387:710-713.
94. Verma S., Hutchings P., Guo J., McLachlan S., Rapoport B., Cooke A. Role of MHC class I expression and CD8(+) T cells in the evolution of iodine-induced thyroiditis in NOD-H2(h4) and NOD mice. European Journal of Immunology 2000, 30:1191-1202.
95. Vladutiu A.O., Rose N.R. Autoimmune murine thyroiditis: Relation to histocompatibility (H-2) complex. Science 1971, 174:1137-1139.
96. Wei Y., Chen K., Sharp G.C., Braley-Mullen H. FLIP and FasL expression by inflammatory cells vs thyrocytes can be predictive of chronic inflammation or resolution of autoimmune thyroiditis. Clinical Immunology 2003, 108:221-233.
97. Wicker L.S., Todd J.A., Peterson L.B. Genetic control of autoimmune diabetes in the NOD mouse. Annual Review of Immunology 1995, 13:179-200.
98. Yip I., Pang X.P., Berg L., Hershman J.M. Antitumor actions of interferon-gamma and interleukin-1 beta on human papillary thyroid carcinoma cell lines. The Journal of Clinical Endocrinology and Metabolism 1995, 80:1664-1669.
99. Yu S., Downey E.F., Braley-Mullen H. Agonistic anti-CD40 promotes early development and increases the incidence of severe thyroid epithelial cell hyperplasia (TEC H/P) in CD4-/- mice. Immunity, Inflammation and Disease 2013, 1:14-25.
100. Yu S., Dunn R., Kehry M.R., Braley-Mullen H. B cell depletion inhibits spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. Journal of Immunology 2008, 180:7706-7713.
101. Yu S., Ellis J.S., Dunn R., Kehry M.R., Braley-Mullen H. Transient depletion of B cells in young mice results in activation of regulatory T cells that inhibit development of autoimmune disease in adults. International Immunology 2012, 24:233-242.
102. Yu S., Fang Y., Sharav T., Sharp G.C., Braley-Mullen H. CD8+ T cells induce thyroid epithelial cell hyperplasia and fibrosis. Journal of Immunology 2011, 186:2655-2662.
103. Yu S., Fang Y., Sharp G.C., Braley-Mullen H. Transgenic expression of TGF-beta on thyrocytes inhibits development of spontaneous autoimmune thyroiditis and increases regulatory T cells in thyroids of NOD.H-2h4 mice. Journal of Immunology 2010, 184:5352-5359.
104. Yu S., Maiti P.K., Dyson M., Jain R., Braley-Mullen H. B cell-deficient NOD.H-2h4 mice have CD4+CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. The Journal of Experimental Medicine 2006, 203:349-358.
105. Yu S., Medling B., Yagita H., Braley-Mullen H. Characteristics of inflammatory cells in spontaneous autoimmune thyroiditis of NOD.H-2h4 mice. Journal of Autoimmunity 2001, 16:37-46.
106. Yu S., Sharp G.C., Braley-Mullen H. Dual roles for IFN-gamma, but not for IL-4, in spontaneous autoimmune thyroiditis in NOD.H-2h4 mice. Journal of Immunology 2002, 169:3999-4007.
107. Yu S., Sharp G.C., Braley-Mullen H. Thyroid epithelial cell hyperplasia in IFN-gamma deficient NOD.H-2h4 mice. Clinical Immunology 2006, 118:92-100.
108. Yu S., Sharp G.C., Braley-Mullen H. Thyrocytes responding to IFN-gamma are essential for development of lymphocytic spontaneous autoimmune thyroiditis and inhibition of thyrocyte hyperplasia. Journal of Immunology 2006, 176:1259-1265.
109. Yu S., Sharp G.C., Braley-Mullen H. TGF-beta promotes thyroid epithelial cell hyperplasia and fibrosis in IFN-gamma-deficient NOD.H-2h4 mice. Journal of Immunology 2008, 181:2238-2245.