Mechanisms of testicular immune privilege

Frontiers of Biology in China

Volumn 6, Issue 1, 2011, Pages 19-30

  Wang, Tao ^a   Feng, Xueying ^a   Han, Daishu ^a  

^a PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

immune privilege; immunoregulation; spermatogenesis; testis

Indexed keywords

EID: 79251628627     PISSN: 16733509     EISSN: 16733622     Source Type: Journal    
DOI: 10.1007/s11515-011-1010-4     Document Type: Review

References (119)

1. Aberts B JA, Lewis J, Ratt M, Roberts K, Walter P (2001). Molecular Biology of the Cells, 4th. New York: Garland Science.
2. Aguilar R, Antón F, Bellido C, Aguilar E, Gaytan F (1995). Testicular serotonin is related to mast cells but not to Leydig cells in the rat. J Endocrinol, 146(1): 15-21.
3. Aubry F, Habasque C, Satie A P, Jégou B, Samson M (2000). Expression and regulation of the CXC-chemokines, GRO/KC and IP-10/mob-1 in rat seminiferous tubules. Eur Cytokine Netw, 11(4): 690-698.
4. Avallet O, Vigier M, Leduque P, Dubois P M, Saez J M (1994). Expression and regulation of transforming growth factor-beta 1 messenger ribonucleic acid and protein in cultured porcine Leydig and Sertoli cells. Endocrinology, 134(5): 2079-2087.
5. Banchereau J, Steinman R M (1998). Dendritic cells and the control of immunity. Nature, 392(6673): 245-252.
6. Bebo B F Jr, Yong T, Orr E L, Linthicum D S (1996). Hypothesis: a possible role for mast cells and their inflammatory mediators in the pathogenesis of autoimmune encephalomyelitis. J Neurosci Res, 45(4): 340-348.
7. Bellgrau D, Gold D, Selawry H, Moore J, Franzusoff A, Duke R C (1995). A role for CD95 ligand in preventing graft rejection. Nature, 377(6550): 630-632.
8. Benoist C, Mathis D (2002). Mast cells in autoimmune disease. Nature, 420(6917): 875-878.
9. Bhushan S, Tchatalbachev S, Klug J, Fijak M, Pineau C, Chakraborty T, Meinhardt A (2008). Uropathogenic Escherichia coli block MyD88-dependent and activate MyD88-independent signaling pathways in rat testicular cells. J Immunol, 180(8): 5537-5547.
10. Breucker H (1978). Macrophages, a normal component in seasonally involuting testes of the swan, Cygnus olor. Cell Tissue Res, 193(3): 463-471.
11. Brinster R L (2002). Germline stem cell transplantation and transgenesis. Science, 296(5576): 2174-2176.
12. Buzzard J J, Loveland K L, O'Bryan M K, O'Connor A E, Bakker M, Hayashi T, Wreford N G, Morrison J R, de Kretser D M (2004). Changes in circulating and testicular levels of inhibin A and B and activin A during postnatal development in the rat. Endocrinology, 145(7): 3532-3541.
13. Cameron D F, Whittington K, Schultz R E, Selawry H P (1990). Successful islet/abdominal testis transplantation does not require Leydig cells. Transplantation, 50(4): 649-653.
14. Chen Y, Wang H, Qi N, Wu H, Xiong W, Ma J, Lu Q, Han D (2009). Functions of TAM RTKs in regulating spermatogenesis and male fertility in mice. Reproduction, 138(4): 655-666.
15. Cheng X, Dai H, Wan N, Moore Y, Vankayalapati R, Dai Z (2009). Interaction of programmed death-1 and programmed death-1 ligand-1 contributes to testicular immune privilege. Transplantation, 87(12): 1778-1786.
16. Com E, Bourgeon F, Evrard B, Ganz T, Colleu D, Jégou B, Pineau C (2003). Expression of antimicrobial defensins in the male reproductive tract of rats, mice, and humans. Biol Reprod, 68(1): 95-104.
17. Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, Straub R H (2004). Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus, 13(9): 635-638.
18. Dai Z, Nasr I W, Reel M, Deng S, Diggs L, Larsen C P, Rothstein D M, Lakkis F G (2005). Impaired recall of CD8 memory T cells in immunologically privileged tissue. J Immunol, 174(3): 1165-1170.
19. Dal Secco V, Riccioli A, Padula F, Ziparo E, Filippini A (2008). Mouse Sertoli cells display phenotypical and functional traits of antigenpresenting cells in response to interferon gamma. Biol Reprod, 78(2): 234-242.
20. De S K, Chen H L, Pace J L, Hunt J S, Terranova P F, Enders G C (1993). Expression of tumor necrosis factor-alpha in mouse spermatogenic cells. Endocrinology, 133(1): 389-396.
21. De Cesaris P, Filippini A, Cervelli C, Riccioli A, Muci S, Starace G, Stefanini M, Ziparo E (1992). Immunosuppressive molecules produced by Sertoli cells cultured in vitro: biological effects on lymphocytes. Biochem Biophys Res Commun, 186(3): 1639-1646.
22. Dejucq N, Lienard M O, Guillaume E, Dorval I, Jégou B (1998). Expression of interferons-alpha and-gamma in testicular interstitial tissue and spermatogonia of the rat. Endocrinology, 139(7): 3081-3087.
23. Diemer T, Hales D B, Weidner W (2003). Immune-endocrine interactions and Leydig cell function: the role of cytokines. Andrologia, 35(1): 55-63.
24. Dobrinski I (2005). Germ cell transplantation and testis tissue xenografting in domestic animals. Anim Reprod Sci, 89(1-4): 137-145.
25. Duckett R J, Hedger M P, McLachlan R I, Wreford N G (1997). The effects of gonadotropin-releasing hormone immunization and recombinant follicle-stimulating hormone on the Leydig cell and macrophage populations of the adult rat testis. J Androl, 18(4): 417-423.
26. Dym M (1994). Basement membrane regulation of Sertoli cells. Endocr Rev, 15(1): 102-115.
27. Dym M, Romrell L J (1975). Intraepithelial lymphocytes in the male reproductive tract of rats and rhesus monkeys. J Reprod Fertil, 42(1): 1-7.
28. Fallarino F, Luca G, Calvitti M, Mancuso F, Nastruzzi C, Fioretti M C, Grohmann U, Becchetti E, Burgevin A, Kratzer R, van Endert P, Boon L, Puccetti P, Calafiore R (2009). Therapy of experimental type 1 diabetes by isolated Sertoli cell xenografts alone. J Exp Med, 206(11): 2511-2526.
29. Fijak M, Iosub R, Schneider E, Linder M, Respondek K, Klug J, Meinhardt A (2005). Identification of immunodominant autoantigens in rat autoimmune orchitis. J Pathol, 207(2): 127-138.
30. Fijak M, Meinhardt A (2006). The testis in immune privilege. Immunol Rev, 213(1): 66-81.
31. Filippini A, Riccioli A, Padula F, Lauretti P, D'Alessio A, De Cesaris P, Gandini L, Lenzi A, Ziparo E (2001). Control and impairment of immune privilege in the testis and in semen. Hum Reprod Update, 7(5): 444-449.
32. Foulds L M, Boysen R I, Crane M, Yang Y, Muir J A, Smith A I, de Kretser D M, Hearn M T, Hedger M P (2008). Molecular identification of lyso-glycerophosphocholines as endogenous immunosuppressives in bovine and rat gonadal fluids. Biol Reprod, 79(3): 525-536.
33. Gerdprasert O, O'Bryan M K, Muir J A, Caldwell A M, Schlatt S, de Kretser D M, Hedger M P (2002a). The response of testicular leukocytes to lipopolysaccharide-induced inflammation: further evidence for heterogeneity of the testicular macrophage population. Cell Tissue Res, 308(2): 277-285.
34. Gerdprasert O, O'Bryan MK, Nikolic-Paterson D J, Sebire K, de Kretser D M, Hedger M P (2002b). Expression of monocyte chemoattractant protein-1 and macrophage colony-stimulating factor in normal and inflamed rat testis. Mol Hum Reprod, 8(6): 518-524.
35. Guazzone V A, Jacobo P, Theas M S, Lustig L (2009). Cytokines and chemokines in testicular inflammation: A brief review. Microsc Res Tech, 72(8): 620-628.
36. Guazzone V A, Rival C, Denduchis B, Lustig L (2003). Monocyte chemoattractant protein-1 (MCP-1/CCL2) in experimental autoimmune orchitis. J Reprod Immunol, 60(2): 143-157.
37. Haas G G Jr, D'Cruz O J, De Bault L E (1988). Distribution of human leukocyte antigen-ABC and -D/DR antigens in the unfixed human testis. Am J Reprod Immunol Microbiol, 18(2): 47-51.
38. Hafizi S, Dahlbäck B (2006a). Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev, 17(4): 295-304.
39. Hafizi S, Dahlbäck B (2006b). Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J, 273(23): 5231-5244.
40. Head J R, Billingham R E (1985). Immune privilege in the testis. II. Evaluation of potential local factors. Transplantation, 40(3): 269-275.
41. Head J R, Neaves W B, Billingham R E (1983). Immune privilege in the testis. I. Basic parameters of allograft survival. Transplantation, 36(4): 423-431.
42. Hedger M P (1997). Testicular leukocytes: what are they doing? Rev Reprod, 2(1): 38-47.
43. Hedger MP (2002). Macrophages and the immune responsiveness of the testis. J Reprod Immunol, 57(1-2): 19-34.
44. Hedger M P, Meinhardt A (2000). Local regulation of T cell numbers and lymphocyte-inhibiting activity in the interstitial tissue of the adult rat testis. J Reprod Immunol, 48(2): 69-80.
45. Hedger M P, Meinhardt A (2003). Cytokines and the immune-testicular axis. J Reprod Immunol, 58(1): 1-26.
46. Hu J, You S, Li W, Wang D, Nagpal M L, Mi Y, Liang P, Lin T (1998). Expression and regulation of interferon-gamma-inducible protein 10 gene in rat Leydig cells. Endocrinology, 139(8): 3637-3645.
47. Huleihel M, Lunenfeld E (2004). Regulation of spermatogenesis by paracrine/autocrine testicular factors. Asian J Androl, 6(3): 259-268.
48. Hussein M R, Abou-Deif E S, Bedaiwy M A, Said T M, Mustafa M G, Nada E, Ezat A, Agarwal A (2005). Phenotypic characterization of the immune and mast cell infiltrates in the human testis shows normal and abnormal spermatogenesis. Fertil Steril, 83(5): 1447-1453.
49. Hutson J C (1994). Testicular macrophages. Int Rev Cytol, 149: 99-143.
50. Itoh M, Terayama H, Naito M, Ogawa Y, Tainosho S (2005). Tissue microcircumstances for leukocytic infiltration into the testis and epididymis in mice. J Reprod Immunol, 67(1-2): 57-67.
51. + effector and regulatory T lymphocyte subsets in the testis of rats undergoing autoimmune orchitis. J Reprod Immunol, 81(1): 44-54.
52. Jarow J P, Wright W W, Brown T R, Yan X, Zirkin B R (2005). Bioactivity of androgens within the testes and serum of normal men. J Androl, 26(3): 343-348.
53. Ju S T, Panka D J, Cui H, Ettinger R, el-Khatib M, Sherr D H, Stanger B Z, Marshak-Rothstein A (1995). Fas(CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature, 373(6513): 444-448.
54. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Ogura A, Toyokuni S, Honjo T, Shinohara T (2003). Allogeneic offspring produced by male germ line stem cell transplantation into infertile mouse testis. Biol Reprod, 68(1): 167-173.
55. Keir M E, Liang S C, Guleria I, Latchman Y E, Qipo A, Albacker L A, Koulmanda M, Freeman G J, Sayegh M H, Sharpe A H (2006). Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med, 203(4): 883-895.
56. Kern S, Maddocks S (1995). Indomethacin blocks the immunosuppressive activity of rat testicular macrophages cultured in vitro. J Reprod Immunol, 28(3): 189-201.
57. Kern S, Robertson S A, Mau V J, Maddocks S (1995). Cytokine secretion by macrophages in the rat testis. Biol Reprod, 53(6): 1407-1416.
58. Kim Y, Turner D, Nelson J, Dobrinski I, McEntee M, Travis A J (2008). Production of donor-derived sperm after spermatogonial stem cell transplantation in the dog. Reproduction, 136(6): 823-831.
59. Krieger J N (1984). Epididymitis, orchitis, and related conditions. Sex Transm Dis, 11(3): 173-181.
60. Kuopio T, Savouras P O, Pelliniemi L J, Huhtaniemi I T (1989). Transplantation of newborn rat testis under the kidney capsule of adult host as a model to study the structure and function of Leydig cells. J Androl, 10(5): 335-345.
61. Le Tortorec A, Denis H, Satie A P, Patard J J, Ruffault A, Jégou B, Dejucq-Rainsford N (2008). Antiviral responses of human Leydig cells to mumps virus infection or poly I: C stimulation. Hum Reprod, 23(9): 2095-2103.
62. Lemke G, Rothlin C V (2008). Immunobiology of the TAM receptors. Nat Rev Immunol, 8(5): 327-336.
63. Li H, Ren J, Dhabuwala C B, Shichi H (1997). Immunotolerance induced by intratesticular antigen priming: expression of TGF-beta, Fas and Fas ligand. Ocul Immunol Inflamm, 5(2): 75-84.
64. Lu Q, Gore M, Zhang Q, Camenisch T, Boast S, Casagranda F, Lai C, Skinner M K, Klein R, Matsushima G K, Earp H S, Goff S P, Lemke G (1999). Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature, 398(6729): 723-728.
65. Lu Q, Lemke G (2001). Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science, 293(5528): 306-311.
66. Lui W Y, Wong C H, Mruk D D, Cheng C Y (2003). TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology, 144(4): 1139-1142.
67. Ma P, Ge Y, Wang S, Ma J, Xue S, Han D (2004). Spermatogenesis following syngeneic testicular transplantation in Balb/c mice. Reproduction, 128(2): 163-170.
68. McLachlan R I (2002). Basis, diagnosis and treatment of immunological infertility in men. J Reprod Immunol, 57(1-2): 35-45.
69. Meinhardt A, Bacher M, McFarlane J R, Metz C N, Seitz J, Hedger MP, de Kretser D M, Bucala R (1996). Macrophage migration inhibitory factor production by Leydig cells: evidence for a role in the regulation of testicular function. Endocrinology, 137(11): 5090-5095.
70. Meinhardt A, Bacher M, Metz C, Bucala R, Wreford N, Lan H, Atkins R, Hedger M (1998). Local regulation of macrophage subsets in the adult rat testis: examination of the roles of the seminiferous tubules, testosterone, and macrophage-migration inhibitory factor. Biol Reprod, 59(2): 371-378.
71. Meinhardt A, Bacher M, Wennemuth G, Eickhoff R, Hedger M (2000). Macrophage migration inhibitory factor (MIF) as a paracrine mediator in the interaction of testicular somatic cells. Andrologia, 32(1): 46-48.
72. Meinhardt A, Hedger M P. Immunological, paracrine and endocrine aspects of testicular immune privilege. Mol Cell Endocrinol. doi: 10. 1016/j. mce. 2010. 03. 022.
73. Melaine N, Liénard MO, Guillaume E, Ruffault A, Dejucq-Rainsford N, Jégou B (2003). Production of the antiviral proteins 2′5′oligoadenylate synthetase, PKR and Mx in interstitial cells and spermatogonia. J Reprod Immunol, 59(1): 53-60.
74. Mellor A L, Munn D H (2004). IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol, 4(10): 762-774.
75. Mellor A L, Sivakumar J, Chandler P, Smith K, Molina H, Mao D, Munn D H (2001). Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol, 2(1): 64-68.
76. Millar D G, Garza K M, Odermatt B, Elford A R, Ono N, Li Z, Ohashi P S (2003). Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat Med, 9(12): 1469-1476.
77. Nasr IW, Wang Y, Gao G, Deng S, Diggs L, Rothstein D M, Tellides G, Lakkis F G, Dai Z (2005). Testicular immune privilege promotes transplantation tolerance by altering the balance between memory and regulatory T cells. J Immunol, 174(10): 6161-6168.
78. O'Bryan M K, Gerdprasert O, Nikolic-Paterson D J, Meinhardt A, Muir J A, Foulds L M, Phillips D J, de Kretser D M, Hedger M P (2005). Cytokine profiles in the testes of rats treated with lipopolysaccharide reveal localized suppression of inflammatory responses. Am J Physiol Regul Integr Comp Physiol, 288(6): R1744-R1755.
79. Okuma Y, Saito K, O'Connor A E, Phillips D J, de Kretser D M, Hedger M P (2005). Reciprocal regulation of activin A and inhibin B by interleukin-1 (IL-1) and follicle-stimulating hormone (FSH) in rat Sertoli cells in vitro. J Endocrinol, 185(1): 99-110.
80. Pelletier R M, Yoon S R, Akpovi C D, Silvas E, Vitale M L (2009). Defects in the regulatory clearance mechanisms favor the breakdown of self-tolerance during spontaneous autoimmune orchitis. Am J Physiol Regul Integr Comp Physiol, 296(3): R743-R762.
81. Pöllänen P, von Euler M, Jahnukainen K, Saari T, Parvinen M, Sainio-Pöllänen S, Söder O (1993). Role of transforming growth factor beta in testicular immunosuppression. J Reprod Immunol, 24(2): 123-137.
82. Potashnik H, Elhija MA, Lunenfeld E, Potashnik G, Schlatt S, Nieschlag E, Huleihel M (2005). Interleukin-6 expression during normal maturation of the mouse testis. Eur Cytokine Netw, 16(2): 161-165.
83. Raburn D J, Coquelin A, Reinhart A J, Hutson J C (1993). Regulation of the macrophage population in postnatal rat testis. J Reprod Immunol, 24(2): 139-151.
84. Riccioli A, Starace D, Galli R, Fuso A, Scarpa S, Palombi F, De Cesaris P, Ziparo E, Filippini A (2006). Sertoli cells initiate testicular innate immune responses through TLR activation. J Immunol, 177(10): 7122-7130.
85. Rival C, Theas M S, Guazzone V A, Lustig L (2006). Interleukin-6 and IL-6 receptor cell expression in testis of rats with autoimmune orchitis. J Reprod Immunol, 70(1-2): 43-58.
86. Rival C, Theas M S, Suescun M O, Jacobo P, Guazzone V, van Rooijen N, Lustig L (2008). Functional and phenotypic characteristics of testicular macrophages in experimental autoimmune orchitis. J Pathol, 215(2): 108-117.
87. Rothlin C V, Ghosh S, Zuniga E I, Oldstone M B, Lemke G (2007). TAM receptors are pleiotropic inhibitors of the innate immune response. Cell, 131(6): 1124-1136.
88. Saari T, Jahnukainen K, Pöllänen P (1996). Autoantigenicity of the basal compartment of seminiferous tubules in the rat. J Reprod Immunol, 31(1-2): 65-79.
89. Sanberg P R, Borlongan C V, Saporta S, Cameron D F (1996). Testisderived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain. Nat Biotechnol, 14(13): 1692-1695.
90. Sanchez J F, Crooks D R, Lee C T, Schoen C J, Amable R, Zeng X, Florival-Victor T, Morales N, Truckenmiller M E, Smith D R, Freed W J (2006). GABAergic lineage differentiation of AF5 neural progenitor cells in vitro. Cell Tissue Res, 324(1): 1-8.
91. Sarkar O, Mathur P P, Cheng C Y, Mruk D D (2008). Interleukin 1 alpha (IL1A) is a novel regulator of the blood-testis barrier in the rat. Biol Reprod, 78(3): 445-454.
92. Schlatt S, Meinhardt A, Nieschlag E (1997). Paracrine regulation of cellular interactions in the testis: factors in search of a function. Eur J Endocrinol, 137(2): 107-117.
93. Selawry H P, Cameron D F (1993). Sertoli cell-enriched fractions in successful islet cell transplantation. Cell Transplant, 2(2): 123-129.
94. Selawry H P, Whittington K (1984). Extended allograft survival of islets grafted into intra-abdominally placed testis. Diabetes, 33(4): 405-406.
95. Selawry H P, Whittington K B (1988). Prolonged intratesticular islet allograft survival is not dependent on local steroidogenesis. Horm Metab Res, 20(9): 562-565.
96. Selsted M E, Ouellette A J (2005). Mammalian defensins in the antimicrobial immune response. Nat Immunol, 6(6): 551-557.
97. Setchell B P, Granholm T, Ritzén E M (1995). Failure of thyroid allografts to function in the testes of cynomolgous monkeys. J Reprod Immunol, 28(1): 75-80.
98. Sharpe R M, Donachie K, Cooper I (1988). Re-evaluation of the intratesticular level of testosterone required for quantitative maintenance of spermatogenesis in the rat. J Endocrinol, 117(1): 19-26, NP.
99. Sipione S, Simmen K C, Lord S J, Motyka B, Ewen C, Shostak I, Rayat G R, Dufour J M, Korbutt G S, Rajotte R V, Bleackley R C (2006). Identification of a novel human granzyme B inhibitor secreted by cultured sertoli cells. J Immunol, 177(8): 5051-5058.
100. Siu M K, Lee W M, Cheng C Y (2003). 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, 144(1): 371-387.
101. Statter M B, Foglia R P, Parks D E, Donahoe P K (1988). Fetal and postnatal testis shows immunoprivilege as donor tissue. J Urol, 139(1): 204-210.
102. Suarez-Pinzon W, Korbutt G S, Power R, Hooton J, Rajotte R V, Rabinovitch A (2000). Testicular sertoli cells protect islet beta-cells from autoimmune destruction in NOD mice by a transforming growth factor-beta1-dependent mechanism. Diabetes, 49(11): 1810-1818.
103. Sun B, Qi N, Shang T, Wu H, Deng T, Han D (2010). Sertoli cellinitiated testicular innate immune response through toll-like receptor-3 activation is negatively regulated by Tyro3, Axl, and mer receptors. Endocrinology, 151(6): 2886-2897.
104. Takeda K, Akira S (2005). Toll-like receptors in innate immunity. Int Immunol, 17(1): 1-14.
105. Teuscher C, Blankenhorn E P, Hickey W F (1987). Differential susceptibility to actively induced experimental allergic encephalomyelitis and experimental allergic orchitis among BALB/c substrains. Cell Immunol, 110(2): 294-304.
106. Theas M S, Rival C, Jarazo-Dietrich S, Jacobo P, Guazzone V A, Lustig L (2008). Tumour necrosis factor-alpha released by testicular macrophages induces apoptosis of germ cells in autoimmune orchitis. Hum Reprod, 23(8): 1865-1872.
107. Theas S, Rival C, Lustig L (2003). Germ cell apoptosis in autoimmune orchitis: involvement of the Fas-FasL system. Am J Reprod Immunol, 50(2): 166-176.
108. Tung K S, Teuscher C, Meng A L (1981). Autoimmunity to spermatozoa and the testis. Immunol Rev, 55(1): 217-255.
109. Wahlsten J L, Gitchell H L, Chan C C, Wiggert B, Caspi R R (2000). Fas and Fas ligand expressed on cells of the immune system, not on the target tissue, control induction of experimental autoimmune uveitis. J Immunol, 165(10): 5480-5486.
110. Wang H, Chen Y, Ge Y, Ma P, Ma Q, Ma J, Wang H, Xue S, Han D (2005). Immunoexpression of Tyro 3 family receptors-Tyro 3, Axl, and Mer-and their ligand Gas6 in postnatal developing mouse testis. J Histochem Cytochem, 53(11): 1355-1364.
111. Wang J, Wreford N G, Lan H Y, Atkins R, Hedger M P (1994). Leukocyte populations of the adult rat testis following removal of the Leydig cells by treatment with ethane dimethane sulfonate and subcutaneous testosterone implants. Biol Reprod, 51(3): 551-561.
112. Watanabe M, Kashiwakura Y, Kusumi N, Tamayose K, Nasu Y, Nagai A, Shimada T, Daida H, Kumon H (2005). Adeno-associated virusmediated human IL-10 gene transfer suppresses the development of experimental autoimmune orchitis. Gene Ther, 12(14): 1126-1132.
113. Wekerle H, Sun D, Oropeza-Wekerle R L, Meyermann R (1987). Immune reactivity in the nervous system: modulation of Tlymphocyte activation by glial cells. J Exp Biol, 132: 43-57.
114. Winnall W R, Muir J A, Hedger M P (2009). Differential responses of epithelial Sertoli cells of the rat testis to Toll-Like receptor 2 and 4 ligands: implications for studies of testicular inflammation using bacterial lipopolysaccharides. Innate Immun. doi: 10. 1177/1753425909354764. (in press).
115. Wu H, Wang H, Xiong W, Chen S, Tang H, Han D (2008). Expression patterns and functions of toll-like receptors in mouse sertoli cells. Endocrinology, 149(9): 4402-4412.
116. Wyatt C R, Law L, Magnuson J A, Griswold M D, Magnuson N S (1988). Suppression of lymphocyte proliferation by proteins secreted by cultured Sertoli cells. J Reprod Immunol, 14(1): 27-40.
117. Xerri L, Devilard E, Hassoun J, Mawas C, Birg F (1997). Fas ligand is not only expressed in immune privileged human organs but is also coexpressed with Fas in various epithelial tissues. Mol Pathol, 50(2): 87-91.
118. Xiong Y, Hales D B (1993). Expression, regulation, and production of tumor necrosis factor-alpha in mouse testicular interstitial macrophages in vitro. Endocrinology, 133(6): 2568-2573.
119. Zeyse D, Lunenfeld E, Beck M, Prinsloo I, Huleihel M (2000). Induction of interleukin-1alpha production in murine Sertoli cells by interleukin-1. Biol Reprod, 62(5): 1291-1296.