Mice lacking Axl and Mer tyrosine kinase receptors are susceptible to experimental autoimmune orchitis induction

Immunology and Cell Biology

Volumn 93, Issue 3, 2015, Pages 311-320

  Li, Nan ^a,b   Liu, Zhenghui ^a   Zhang, Yue ^a   Chen, Qiaoyuan ^a   Liu, Peng ^a   Cheng, C Yan ^b   Lee, Will M ^c   Chen, Yongmei ^a   Han, Daishu ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b POPULATION COUNCIL   (United States)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

FREUND ADJUVANT; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE AXL; PROTEIN TYROSINE KINASE MER; UNCLASSIFIED DRUG; AUTOANTIBODY; AUTOANTIGEN; AXL RECEPTOR TYROSINE KINASE; MERTK PROTEIN, MOUSE; ONCOPROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD TESTIS BARRIER; CELL FREE SYSTEM; CONTROLLED STUDY; EXPERIMENTAL AUTOIMMUNE DISEASE; EXPERIMENTAL AUTOIMMUNE ORCHITIS; GERM CELL; MACROPHAGE; MOUSE; NONHUMAN; ORCHITIS; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE EPITHELIUM; T LYMPHOCYTE; UPREGULATION; ANIMAL; AUTOIMMUNE DISEASE; C57BL MOUSE; DISEASE MODEL; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; TESTIS;

MAMMALIA; MUS;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNE DISEASES; BLOOD-TESTIS BARRIER; DISEASE MODELS, ANIMAL; HUMANS; IMMUNE TOLERANCE; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORCHITIS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; T-LYMPHOCYTES; TESTIS;

EID: 84925152495     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.97     Document Type: Article

References (46)

1. Yule TD, Montoya GD, Russell LD, Williams TM, Tung KS. Autoantigenic germ cells exist outside the blood testis barrier. J Immunol 1988; 141: 1161-1167
2. Jacobo P, Guazzone VA, Theas MS, Lustig L. Testicular autoimmunity. Autoimmun Rev 2011; 10: 201-204
3. Naito M, Terayama H, Hirai S, Qu N, Lustig L, Itoh M. Experimental autoimmune orchitis as a model of immunological male infertility. Med Mol Morphol 2012; 45: 185-189
4. Rival C, Theas MS, Suescun MO, Jacobo P, Guazzone V, van Rooijen N et al. Functional and phenotypic characteristics of testicular macrophages in experimental autoimmune orchitis. J Pathol 2008; 215: 108-117
5. Jacobo P, Guazzone VA, Jarazo-Dietrich S, Theas MS, Lustig L. Differential changes in CD4+ and CD8+ effector and regulatory T lymphocyte subsets in the testis of rats undergoing autoimmune orchitis. J Reprod Immunol 2009; 81: 44-54
6. Rival C, Lustig L, Iosub R, Guazzone VA, Schneider E, Meinhardt A et al. Identification of a dendritic cell population in normal testis and in chronically inflamed testis of rats with autoimmune orchitis. Cell Tissue Res 2006; 324: 311-318
7. Mahi-Brown CA, Tung KS. Activation requirements of donor T cells and host T cell recruitment in adoptive transfer of murine experimental autoimmune orchitis (EAO). Cell Immunol 1989; 124: 368-379
8. Guazzone VA, Jacobo P, Theas MS, Lustig L. Cytokines and chemokines in testicular inflammation: a brief review. Microsc Res Tech 2009; 72: 620-628
9. Hafizi S, Dahlback B. Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev 2006; 17: 295-304
10. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C et al. The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 1995; 80: 661-670
11. Godowski PJ, Mark MR, Chen J, Sadick MD, Raab H, Hammonds RG. Reevaluation of the roles of protein S and Gas6 as ligands for the receptor tyrosine kinase Rse/Tyro 3. Cell 1995; 82: 355-358
12. Lu Q, Gore M, Zhang Q, Camenisch T, Boast S, Casagranda F et al. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 1999; 398: 723-728
13. Lu Q, Lemke G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 2001; 293: 306-311
14. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 2007; 131: 1124-1136
15. Lemke G, Burstyn-Cohen T. TAM receptors and the clearance of apoptotic cells. Ann N Y Acad Sci 2010; 1209: 23-29
16. Rothlin CV, Lemke G. TAM receptor signaling and autoimmune disease. Curr Opin Immunol 2010; 22: 740-746
17. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol 2008; 8: 327-336
18. Fijak M, Bhushan S, Meinhardt A. Immunoprivileged sites: the testis. Methods Mol Biol 2011; 677: 459-470
19. Li N, Wang T, Han D. Structural, cellular and molecular aspects of immune privilege in the testis. Front Immunol 2012; 3: 152
20. Wang H, Chen Y, Ge Y, Ma P, Ma Q, Ma J et al. Immunoexpression of Tyro 3 family receptors-Tyro 3, Axl, and Mer-And their ligand Gas6 in postnatal developing mouse testis. J Histochem Cytochem 2005; 53: 1355-1364
21. Xiong W, Chen Y, Wang H, Wu H, Lu Q, Han D. Gas6 and the Tyro 3 receptor tyrosine kinase subfamily regulate the phagocytic function of Sertoli cells. Reproduction 2008; 135: 77-87
22. Zhang Y, Li N, Chen Q, Yan K, Liu Z, Zhang X et al. Breakdown of immune homeostasis in the testis of mice lacking Tyro3, Axl and Mer receptor tyrosine kinases. Immunol Cell Biol 2013; 91: 416-426
23. Chen Y, Wang H, Qi N, Wu H, Xiong W, Ma J et al. Functions of TAM RTKs in regulating spermatogenesis and male fertility in mice. Reproduction 2009; 138: 655-666
24. Itoh M, De-Rooij D, Takeuchi Y. Mode of inflammatory cell infiltration in testes of mice injected with syngeneic testicular germ cells without adjuvant. J Anat 1995; 187 (Pt 3): 671-679
25. Rival C, Guazzone VA, Theas MS, Lustig L. Pathomechanism of autoimmune orchitis. Andrologia 2005; 37: 226-227
26. Doncel GF, Di Paola JA, Lustig L. Sequential study of the histopathology and cellular and humoral immune response during the development of an autoimmune orchitis in Wistar rats. Am J Reprod Immunol 1989; 20: 44-51
27. Fijak M, Schneider E, Klug J, Bhushan S, Hackstein H, Schuler G et al. Testosterone replacement effectively inhibits the development of experimental autoimmune orchitis in rats: evidence for a direct role of testosterone on regulatory T cell expansion. J Immunol 2011; 186: 5162-5172
28. Ye F, Li Q, Ke Y, Lu Q, Han L, Kaplan HJ et al. TAM receptor knockout mice are susceptible to retinal autoimmune induction. Invest Ophthalmol Vis Sci 2011; 52: 4239-4246
29. Ye F, Han L, Lu Q, Dong W, Chen Z, Shao H et al. Retinal self-Antigen induces a predominantly Th1 effector response in Axl and Mertk double-knockout mice. J Immunol 2011; 187: 4178-4186
30. Shang T, Zhang X, Wang T, Sun B, Deng T, Han D. Toll-like receptor-initiated testicular innate immune responses in mouse Leydig cells. Endocrinology 2011; 152: 2827-2836
31. Sun B, Qi N, Shang T, Wu H, Deng T, Han D. Sertoli cell-initiated testicular innate immune response through toll-like receptor-3 activation is negatively regulated by Tyro3, Axl, and mer receptors. Endocrinology 2010; 151: 2886-2897
32. Schenten D, Medzhitov R. The control of adaptive immune responses by the innate immune system. Adv Immunol 2011; 109: 87-124
33. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11: 373-384
34. Li M, Zhou Y, Feng G, Su SB. The critical role of Toll-like receptor signaling pathways in the induction and progression of autoimmune diseases. Curr Mol Med 2009; 9: 365-374
35. Zetterstrom CK, Strand ML, Soder O. The high mobility group box chromosomal protein 1 is expressed in the human and rat testis where it may function as an antibacterial factor. Hum Reprod 2006; 21: 2801-2809
36. Biggiogera M, Tanguay RM, Marin R, Wu Y, Martin TE, Fakan S. Localization of heat shock proteins in mouse male germ cells: an immunoelectron microscopical study. Exp Cell Res 1996; 229: 77-85
37. Reiling N, Holscher C, Fehrenbach A, Kroger S, Kirschning CJ, Goyert S et al. Cutting edge: toll-like receptor (TLR)2- And TLR4-mediated pathogen recognition in resistance to airborne infection with Mycobacterium tuberculosis. J Immunol 2002; 169: 3480-3484
38. Drennan MB, Nicolle D, Quesniaux VJ, Jacobs M, Allie N, Mpagi J et al. Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am J Pathol 2004; 164: 49-57
39. Suescun MO, Rival C, Theas MS, Calandra RS, Lustig L. Involvement of tumor necrosis factor-Alpha in the pathogenesis of autoimmune orchitis in rats. Biol Reprod 2003; 68: 2114-2121
40. Rival C, Theas MS, Guazzone VA, Lustig L. Interleukin-6 and IL-6 receptor cell expression in testis of rats with autoimmune orchitis. J Reprod Immunol 2006; 70: 43-58
41. Theas MS, Rival C, Jarazo-Dietrich S, Jacobo P, Guazzone VA, Lustig L. Tumour necrosis factor-Alpha released by testicular macrophages induces apoptosis of germ cells in autoimmune orchitis. Hum Reprod 2008; 23: 1865-1872
42. Tung KS, Unanue ER, Dixon FJ. Pathogenesis of experimental allergic orchitis II The role of antibody. J Immunol 1971; 106: 1463-1472
43. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science 2010; 327: 291-295
44. Siu MK, Lee WM, Cheng CY. The interplay of collagen IV, tumor necrosis factor-Alpha, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell-Tight junction dynamics in the rat testis. Endocrinology 2003; 144: 371-387
45. Jacobo P, Perez CV, Theas MS, Guazzone VA, Lustig L. CD4+ and CD8+ T cells producing Th1 and Th17 cytokines are involved in the pathogenesis of autoimmune orchitis. Reproduction 2011; 141: 249-258
46. Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE. Androgens regulate the permeability of the blood-Testis barrier. Proc Natl Acad Sci USA 2005; 102: 16696-16700