Received date: 23 Aug 2010
Accepted date: 02 Nov 2010
Published date: 01 Feb 2011
Copyright
The testis exhibits a distinctive form of immune privilege to protect the germ cells from the host immune attack. The property of testicular immune privilege was originally attributed to the blood-testis barrier in the seminiferous epithelium, which sequesters antigens. Recent studies have uncovered several levels of immune control besides the blood-testis barrier involved in the privilege of the testis, including the mechanisms of immune tolerance, reduced immune activation, localized active immunosuppression and antigen-specific immunoregulation. The somatic cells of the testis, especially Sertoli cells, play a key role in regulating the testicular immune privileged status. The constitutive expression of anti-inflammatory factors in the testis by somatic cells is essential for local immunosuppression. Growing evidence shows that androgens orchestrate the inhibition of proinflammatory factors and shift cytokine balance toward a tolerogenic environment. Disruption of these protective mechanisms, which may be caused by trauma, infection and genetic factors, can lead to orchitis and infertility. This review article highlights the unique immune environment of the testis, particularly focuses on the regulation of testicular immune privilege.
Key words： immune privilege; testis; immunoregulation; spermatogenesis
Tao WANG , Xueying FENG , Daishu HAN . Mechanisms of testicular immune privilege[J]. Frontiers in Biology, 2011 , 06(01) : 19 -30 . DOI: 10.1007/s11515-011-1010-4
| 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 antigen-presenting 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 M K, 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 M P (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 |
Jacobo P, Guazzone V A, Jarazo-Dietrich S, Theas M S, Lustig L (2009). Differential changes in CD4+ and CD8+ 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): 444–448PMID:7530337
|
| 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 M P, 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 M O, 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 I W, 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 M A, 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). Testis-derived 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 cell-initiated 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 virus-mediated 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 T-lymphocyte 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
|
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