The immune privilege of testis and gravid uterus: Same difference?

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 509-520

  Arck, Petra ^a   Solano, María Emilia ^a   Walecki, Magdalena ^b   Meinhardt, Andreas ^b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Gravid uterus; Immune privilege; Progesterone; Testis; Testosterone; Tolerance

Indexed keywords

ANDROGEN; ANTIGEN; NEOANTIGEN; PROGESTERONE; TESTOSTERONE; UNCLASSIFIED DRUG;

BLOOD EPIDIDYMIS BARRIER; CELL FUNCTION; CELL INTERACTION; DECIDUA; DENDRITIC CELL; FETUS; GERM CELL; GRAVID UTERUS; HOST; HUMAN; IMMUNE PRIVILEGE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; LEUKOCYTE; LEYDIG CELL; LYMPHOCYTE; MACROPHAGE; NATURAL KILLER CELL; NONHUMAN; PERITUBULAR CELL; PERMEABILITY BARRIER; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; REVIEW; SERTOLI CELL; SPERMATOCYTE; STROMA CELL; T LYMPHOCYTE SUBPOPULATION; TESTIS; UTERUS;

GRAVID UTERUS; IMMUNE PRIVILEGE; PROGESTERONE; TESTIS; TESTOSTERONE; TOLERANCE;

FEMALE; GERM CELLS; HUMANS; IMMUNE TOLERANCE; MALE; MATERNAL-FETAL EXCHANGE; PREGNANCY; PREGNANCY COMPLICATIONS; TESTIS; UTERUS;

EID: 84888307806     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.09.022     Document Type: Review

References (197)

1. Adam M., Urbanski H.F., Garyfallou V.T., Welsch U., Kohn F.M., Ullrich Schwarzer J., Strauss L., Poutanen M., Mayerhofer A. High levels of the extracellular matrix proteoglycan decorin are associated with inhibition of testicular function. Int. J. Androl. 2012, 35:550-561.
2. Aisemberg J., Vercelli C.A., Bariani M.V., Billi S.C., Wolfson M.L., Franchi A.M. Progesterone is essential for protecting against LPS-induced pregnancy loss. LIF as a potential mediator of the anti-inflammatory effect of progesterone. PLoS One 2013, 8:e56161.
3. Ait-Azzouzene D., Caucheteux S., Tchang F., Wantyghem J., Moutier R., Langkopf A., Gendron M.C., Kanellopoulos-Langevin C. Transgenic major histocompatibility complex class I antigen expressed in mouse trophoblast affects maternal immature B cells. Biol. Reprod. 2001, 65:337-344.
4. Aluvihare V.R., Kallikourdis M., Betz A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 2004, 5:266-271.
5. Andre S., Tough D.F., Lacroix-Desmazes S., Kaveri S.V., Bayry J. Surveillance of antigen-presenting cells by CD4+ CD25+ regulatory T cells in autoimmunity: immunopathogenesis and therapeutic implications. Am. J. Pathol. 2009, 174:1575-1587.
6. Apps R., Murphy S.P., Fernando R., Gardner L., Ahad T., Moffett A. Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies. Immunology 2009, 127:26-39.
7. Arck P.C., Gilhar A., Bienenstock J., Paus R. The alchemy of immune privilege explored from a neuroimmunological perspective. Curr. Opin. Pharmacol. 2008, 8:480-489.
8. Arck P.C., Rucke M., Rose M., Szekeres-Bartho J., Douglas A.J., Pritsch M., Blois S.M., Pincus M.K., Barenstrauch N., Dudenhausen J.W., Nakamura K., Sheps S., Klapp B.F. Early risk factors for miscarriage: a prospective cohort study in pregnant women. Reprod. Biomed. Online 2008, 17:101-113.
9. Arck P.C., Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat Med. 2013, 19(5):548-556.
10. Arruvito L., Giulianelli S., Flores A.C., Paladino N., Barboza M., Lanari C., Fainboim L. NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J. Immunol. 2008, 180:5746-5753.
11. Baban B., Chandler P., McCool D., Marshall B., Munn D.H., Mellor A.L. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J. Reprod. Immunol. 2004, 61:67-77.
12. Bagavant H., Thompson C., Ohno K., Setiady Y., Tung K.S. Differential effect of neonatal thymectomy on systemic and organ-specific autoimmune disease. Int. Immunol. 2002, 14:1397-1406.
13. Bai X., Williams J.L., Greenwood S.L., Baker P.N., Aplin J.D., Crocker I.P. A placental protective role for trophoblast-derived TNF-related apoptosis-inducing ligand (TRAIL). Placenta 2009, 30:855-860.
14. Bain J. The many faces of testosterone. Clin. Interv. Aging 2007, 2:567-576.
15. Bhushan S., Hossain H., Lu Y., Geisler A., Tchatalbachev S., Mikulski Z., Schuler G., Klug J., Pilatz A., Wagenlehner F., Chakraborty T., Meinhardt A. Uropathogenic E. coli induce different immune response in testicular and peritoneal macrophages: implications for testicular immune privilege. PLoS One 2011, 6:e28452.
16. Bhushan S., Tchatalbachev S., Klug J., Fijak M., Pineau C., Chakraborty T., Meinhardt A. Uropathogenic Escherichia coli block MyD88-dependent and activate MyD88-independent signaling pathways in rat testicular cells. J. Immunol. 2008, 180:5537-5547.
17. Billingham R.E., Brent L., Medawar P.B. Actively acquired tolerance of foreign cells. Nature 1953, 172:603-606.
18. Blois S.M., Alba Soto C.D., Tometten M., Klapp B.F., Margni R.A., Arck P.C. Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biol. Reprod. 2004, 70:1018-1023.
19. Blois S.M., Joachim R., Kandil J., Margni R., Tometten M., Klapp B.F., Arck P.C. Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J. Immunol. 2004, 172:5893-5899.
20. Blois S.M., Ilarregui J.M., Tometten M., Garcia M., Orsal A.S., Cordo-Russo R., Toscano M.A., Bianco G.A., Kobelt P., Handjiski B., Tirado I., Markert U.R., Klapp B.F., Poirier F., Szekeres-Bartho J., Rabinovich G.A., Arck P.C. A pivotal role for galectin-1 in fetomaternal tolerance. Nat. Med. 2007, 13:1450-1457.
21. Blois S.M., Barrientos G., Garcia M.G., Orsal A.S., Tometten M., Cordo-Russo R.I., Klapp B.F., Santoni A., Fernandez N., Terness P., Arck P.C. Interaction between dendritic cells and natural killer cells during pregnancy in mice. J. Mol. Med. (Berl.) 2008, 86:837-852.
22. Boockfor F.R., Wang D., Lin T., Nagpal M.L., Spangelo B.L. Interleukin-6 Secretion from rat Leydig cells in culture. Endocrinology 1994, 134:2150-2155.
23. Carayannopoulos L.N., Barks J.L., Yokoyama W.M., Riley J.K. Murine trophoblast cells induce NK cell interferon-gamma production through KLRK1. Biol. Reprod. 2010, 83:404-414.
24. Chaouat G., Clark D.A. FAS/FAS ligand interaction at the placental interface is not required for the success of allogeneic pregnancy in anti-paternal MHC preimmunized mice. Am. J. Reprod. Immunol. 2001, 45:108-115.
25. Chazara O., Xiong S., Moffett A. Maternal KIR and fetal HLA-C: a fine balance. J. Leukoc. Biol. 2011, 90:703-716.
26. Cheng C.Y., Mruk D.D. The blood-testis barrier and its implications for male contraception. Pharmacol. Rev. 2012, 64:16-64.
27. Cheng C.Y., Wong E.W., Lie P.P., Li M.W., Mruk D.D., Yan H.H., Mok K.W., Mannu J., Mathur P.P., Lui W.Y., Lee W.M., Bonanomi M., Silvestrini B. Regulation of blood-testis barrier dynamics by desmosome, gap junction, hemidesmosome and polarity proteins: an unexpected turn of events. Spermatogenesis 2011, 1:105-115.
28. Chien C.H., Lai J.N., Liao C.F., Wang O.Y., Lu L.M., Huang M.I., Lee W.F., Shie M.C., Chien E.J. Mifepristone acts as progesterone antagonist of non-genomic responses but inhibits phytohemagglutinin-induced proliferation in human T cells. Hum. Reprod. 2009, 24:1968-1975.
29. Clark D.A. Immunological factors in pregnancy wastage: fact or fiction. Am. J. Reprod. Immunol. 2008, 59:277-300.
30. Clark D.A., Chaouat G., Arck P.C., Mittruecker H.W., Levy G.A. Cytokine-dependent abortion in CBA×DBA/2 mice is mediated by the procoagulant fgl2 prothrombinase [correction of prothombinase]. J. Immunol. 1998, 160:545-549.
31. Collins M.K., Tay C.S., Erlebacher A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J. Clin. Invest. 2009, 119:2062-2073.
32. Condon J.C., Jeyasuria P., Faust J.M., Wilson J.W., Mendelson C.R. A decline in the levels of progesterone receptor coactivators in the pregnant uterus at term may antagonize progesterone receptor function and contribute to the initiation of parturition. Proc. Natl. Acad. Sci. USA 2003, 100:9518-9523.
33. Corcoran M.P., Meydani M., Lichtenstein A.H., Schaefer E.J., Dillard A., Lamon-Fava S. Sex hormone modulation of proinflammatory cytokine and C-reactive protein expression in macrophages from older men and postmenopausal women. J. Endocrinol. 2010, 206:217-224.
34. Cush J.J. Biological drug use: US perspectives on indications and monitoring. Ann. Rheum. Dis. 2005, 64(Suppl. 4):18-23.
35. Cyr D.G., Gregory M., Dube E., Dufresne J., Chan P.T., Hermo L. Orchestration of occludins, claudins, catenins and cadherins as players involved in maintenance of the blood-epididymal barrier in animals and humans. Asian J. Androl. 2007, 9:463-475.
36. Dalal M., Kim S., Voskuhl R.R. Testosterone therapy ameliorates experimental autoimmune encephalomyelitis and induces a T helper 2 bias in the autoantigen-specific T lymphocyte response. J. Immunol. 1997, 159:3-6.
37. Diemer T., Huwe P., Ludwig M., Hauck E.W., Weidner W. Urogenital infection and sperm motility. Andrologia 2003, 35:283-287.
38. Doyle T.J., Kaur G., Putrevu S.M., Dyson E.L., Dyson M., McCunniff W.T., Pasham M.R., Kim K.H., Dufour J.M. Immunoprotective properties of primary Sertoli cells in mice: potential functional pathways that confer immune privilege. Biol. Reprod. 2012, 86:1-14.
39. Dunn C.L., Kelly R.W., Critchley H.O. Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod. Biomed. Online 2003, 7:151-161.
40. Elliot M.G., Crespi B.J. Placental invasiveness mediates the evolution of hybrid inviability in mammals. Am. Nat. 2006, 168:114-120.
41. Erlebacher A., Zhang D., Parlow A.F., Glimcher L.H. Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system. J. Clin. Invest. 2004, 114:39-48.
42. Erlebacher A., Vencato D., Price K.A., Zhang D., Glimcher L.H. Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Invest. 2007, 117:1399-1411.
43. Fijak M., Meinhardt A. The testis in immune privilege. Immunol. Rev. 2006, 213:66-81.
44. Fijak M., Iosub R., Schneider E., Linder M., Respondek K., Klug J., Meinhardt A. Identification of immunodominant autoantigens in rat autoimmune orchitis. J. Pathol. 2005, 207:127-138.
45. Fijak M., Schneider E., Klug J., Bhushan S., Hackstein H., Schuler G., Wygrecka M., Gromoll J., Meinhardt A. 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.
46. 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. Molecular identification of lyso-glycerophosphocholines as endogenous immunosuppressives in bovine and rat gonadal fluids. Biol. Reprod. 2008, 79:525-536.
47. Friebe A., Douglas A.J., Solano E., Blois S.M., Hagen E., Klapp B.F., Clark D.A., Arck P.C. Neutralization of LPS or blockage of TLR4 signaling prevents stress-triggered fetal loss in murine pregnancy. J. Mol. Med. (Berl.) 2011, 89:689-699.
48. Frungieri M.B., Weidinger S., Meineke V., Kohn F.M., Mayerhofer A. Proliferative action of mast-cell tryptase is mediated by PAR2, COX2, prostaglandins, and PPARgamma: possible relevance to human fibrotic disorders. Proc. Natl. Acad. Sci. USA 2002, 99:15072-15077.
49. Fujisaki J., Wu J., Carlson A.L., Silberstein L., Putheti P., Larocca R., Gao W., Saito T.I., Lo Celso C., Tsuyuzaki H., Sato T., Cote D., Sykes M., Strom T.B., Scadden D.T., Lin C.P. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 2011, 474:216-219.
50. Gerdprasert O., O'Bryan M.K., Muir J.A., Caldwell A.M., Schlatt S., de Kretser D.M., Hedger M.P. The response of testicular leukocytes to lipopolysaccharide-induced inflammation: further evidence for heterogeneity of the testicular macrophage population. Cell Tissue Res. 2002, 308:277-285.
51. Gow A., Southwood C.M., Li J.S., Pariali M., Riordan G.P., Brodie S.E., Danias J., Bronstein J.M., Kachar B., Lazzarini R.A. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell 1999, 99:649-659.
52. Gregory M., Cyr D.G. Identification of multiple claudins in the rat epididymis. Mol. Reprod. Dev. 2006, 73:580-588.
53. Grimaldi C.M., Cleary J., Dagtas A.S., Moussai D., Diamond B. Estrogen alters thresholds for B cell apoptosis and activation. J. Clin. Invest. 2002, 109:1625-1633.
54. Guazzone V.A., Hollwegs S., Mardirosian M., Jacobo P., Hackstein H., Wygrecka M., Schneider E., Meinhardt A., Lustig L., Fijak M. Characterization of dendritic cells in testicular draining lymph nodes in a rat model of experimental autoimmune orchitis. Int. J. Androl. 2011, 34:276-289.
55. Guleria I., Khosroshahi A., Ansari M.J., Habicht A., Azuma M., Yagita H., Noelle R.J., Coyle A., Mellor A.L., Khoury S.J., Sayegh M.H. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J. Exp. Med. 2005, 202:231-237.
56. Haddad Kashani H., Moshkdanian G., Atlasi M.A., Taherian A.A., Naderian H., Nikzad H. Expression of galectin-3 as a testis inflammatory marker in vasectomised mice. Cell J. 2013, 15:11-18.
57. Haidl G., Duan Y.G., Chen S.J., Kohn F.M., Schuppe H.C., Allam J.P. The role of mast cells in male infertility. Expert Rev. Clin. Immunol. 2011, 7:627-634.
58. Hales D.B. Testicular macrophage modulation of Leydig cell steroidogenesis. J. Reprod. Immunol. 2002, 57:3-18.
59. Hayes R., Chalmers S.A., Nikolic-Paterson D.J., Atkins R.C., Hedger M.P. Secretion of bioactive interleukin 1 by rat testicular macrophages in vitro. J. Androl. 1996, 17:41-49.
60. Head J.R., Neaves W.B., Billingham R.E. Immune privilege in the testis. I. Basic parameters of allograft survival. Transplantation 1983, 36:423-431.
61. Hedger M.P. Macrophages and the immune responsiveness of the testis. J. Reprod. Immunol. 2002, 57:19-34.
62. Hedger M.P., Meinhardt A. Local regulation of T cell numbers and lymphocyte-inhibiting activity in the interstitial tissue of the adult rat testis. J. Reprod. Immunol. 2000, 48:69-80.
63. Hedger M.P., Winnall W.R. Regulation of activin and inhibin in the adult testis and the evidence for functional roles in spermatogenesis and immunoregulation. Mol. Cell. Endocrinol. 2012, 359:30-42.
64. Hendry W.F. Male infertility. Br. J. Hosp. Med. 1979, 22:47-60.
65. Hiby S.E., Regan L., Lo W., Farrell L., Carrington M., Moffett A. Association of maternal killer-cell immunoglobulin-like receptors and parental HLA-C genotypes with recurrent miscarriage. Hum. Reprod. 2008, 23:972-976.
66. Hoffer P., Hinton T. Morphological evidence for a blood-epididymis barrier and the effects of gossypol on its integrity. Biol. Reprod. 1984, 30:991-1004.
67. Hofmann N., Kuwert E. Chronic, nonpathogen-related orchitis. Z. Hautkr. 1979, 54:173-180.
68. Honaramooz A., Yang Y. Recent advances in application of male germ cell transplantation in farm animals. Vet. Med. Int. 2010, 2011.
69. Hughes G.C., Clark E.A., Wong A.H. The intracellular progesterone receptor regulates CD4+ T cells and T cell-dependent antibody responses. J. Leukoc. Biol. 2013, 93:369-375.
70. Hunt J.S., Vassmer D., Ferguson T.A., Miller L. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J. Immunol. 1997, 158:4122-4128.
71. Hutson J.C. Development of cytoplasmic digitations between Leydig cells and testicular macrophages of the rat. Cell Tissue Res. 1992, 267:385-389.
72. Hutson J.C. Physiologic interactions between macrophages and Leydig cells. Exp. Biol. Med. (Maywood) 2006, 231:1-7.
73. Iosub R., Klug J., Fijak M., Schneider E., Frohlich S., Blumbach K., Wennemuth G., Sommerhoff C., Steinhoff M., Meinhardt A. Development of testicular inflammation in the rat involves activation of proteinase-activated receptor-2. J. Pathol. 2006, 208:686-698.
74. Jacobo P., Guazzone V.A., Jarazo-Dietrich S., Theas M.S., 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.
75. Jarow J.P., Wright W.W., Brown T.R., Yan X., Zirkin B.R. Bioactivity of androgens within the testes and serum of normal men. J. Androl. 2005, 26:343-348.
76. Joachim R., Zenclussen A.C., Polgar B., Douglas A.J., Fest S., Knackstedt M., Klapp B.F., Arck P.C. The progesterone derivative dydrogesterone abrogates murine stress-triggered abortion by inducing a Th2 biased local immune response. Steroids 2003, 68:931-940.
77. Kalkunte S.S., Mselle T.F., Norris W.E., Wira C.R., Sentman C.L., Sharma S. Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J. Immunol. 2009, 182:4085-4092.
78. Kallikourdis M., Andersen K.G., Welch K.A., Betz A.G. Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc. Natl. Acad. Sci. USA 2007, 104:594-599.
79. Kaufmann P., Black S., Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 2003, 69:1-7.
80. Kern S., Robertson S.A., Mau V.J., Maddocks S. Cytokine secretion by macrophages in the rat testis. Biol. Reprod. 1995, 53:1407-1416.
81. Kim M.R., Park D.W., Lee J.H., Choi D.S., Hwang K.J., Ryu H.S., Min C.K. Progesterone-dependent release of transforming growth factor-beta1 from epithelial cells enhances the endometrial decidualization by turning on the Smad signalling in stromal cells. Mol. Hum. Reprod. 2005, 11:801-808.
82. King A., Allan D.S., Bowen M., Powis S.J., Joseph S., Verma S., Hiby S.E., McMichael A.J., Loke Y.W., Braud V.M. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 2000, 30:1623-1631.
83. King A., Burrows T.D., Hiby S.E., Bowen J.M., Joseph S., Verma S., Lim P.B., Gardner L., Le Bouteiller P., Ziegler A., Uchanska-Ziegler B., Loke Y.W. Surface expression of HLA-C antigen by human extravillous trophoblast. Placenta 2000, 21:376-387.
84. Kopcow H.D., Rosetti F., Leung Y., Allan D.S., Kutok J.L., Strominger J.L. T cell apoptosis at the maternal-fetal interface in early human pregnancy, involvement of galectin-1. Proc. Natl. Acad. Sci. USA 2008, 105:18472-18477.
85. Korbutt G.S., Elliott J.F., Rajotte R.V. Cotransplantation of allogeneic islets with allogeneic testicular cell aggregates allows long-term graft survival without systemic immunosuppression. Diabetes 1997, 46:317-322.
86. Koubovec D., Ronacher K., Stubsrud E., Louw A., Hapgood J.P. Synthetic progestins used in HRT have different glucocorticoid agonist properties. Mol. Cell. Endocrinol. 2005, 242:23-32.
87. Kovats S., Main E.K., Librach C., Stubblebine M., Fisher S.J., DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990, 248:220-223.
88. Krey G., Frank P., Shaikly V., Barrientos G., Cordo-Russo R., Ringel F., Moschansky P., Chernukhin I.V., Metodiev M., Fernandez N., Klapp B.F., Arck P.C., Blois S.M. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J. Mol. Med. (Berl.) 2008, 86:999-1011.
89. Lewis K.L., Reizis B. Dendritic cells: arbiters of immunity and immunological tolerance. Cold Spring Harb. Perspect. Biol. 2012, 4:a007401.
90. Li C., Houser B.L., Nicotra M.L., Strominger J.L. HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc. Natl. Acad. Sci. USA 2009, 106:5767-5772.
91. Lim H.G., Lee H.M., Oh B.C., Lee J.R. Cell-mediated immunomodulation of chemokine receptor 7-expressing porcine sertoli cells in murine heterotopic heart transplantation. J. Heart Lung Transplant. 2009, 28:72-78.
92. Liva S.M., Voskuhl R.R. Testosterone acts directly on CD4+ T lymphocytes to increase IL-10 production. J. Immunol. 2001, 167:2060-2067.
93. Lyall F., Bulmer J.N., Kelly H., Duffie E., Robson S.C. Human trophoblast invasion and spiral artery transformation: the role of nitric oxide. Am. J. Pathol. 1999, 154:1105-1114.
94. Madeja Z., Yadi H., Apps R., Boulenouar S., Roper S.J., Gardner L., Moffett A., Colucci F., Hemberger M. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl. Acad. Sci. USA 2011, 108:4012-4017.
95. Maekawa M., Kamimura K., Nagano T. Peritubular myoid cells in the testis: their structure and function. Arch. Histol. Cytol. 1996, 59:1-13.
96. Mahi-Brown C.A., Yule T.D., Tung K.S. Adoptive transfer of murine autoimmune orchitis to naive recipients with immune lymphocytes. Cell. Immunol. 1987, 106:408-419.
97. Malkin C.J., Pugh P.J., Jones R.D., Kapoor D., Channer K.S., Jones T.H. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J. Clin. Endocrinol. Metab. 2004, 89:3313-3318.
98. Mao G., Wang J., Kang Y., Tai P., Wen J., Zou Q., Li G., Ouyang H., Xia G., Wang B. Progesterone increases systemic and local uterine proportions of CD4+CD25+ Treg cells during midterm pregnancy in mice. Endocrinology 2010, 151:5477-5488.
99. Martin-Du Pan R., Bischof P., de Boccard G., Campana A. Is diclofenac helpful in the diagnosis of partial epididymal obstruction?. Hum. Reprod. 1997, 12:396-397.
100. Mayerhofer A. Human testicular peritubular cells - more than meets the eye. Reproduction 2013.
101. McCabe M.J., Tarulli G.A., Meachem S.J., Robertson D.M., Smooker P.M., Stanton P.G. Gonadotropins regulate rat testicular tight junctions in vivo. Endocrinology 2010, 151:2911-2922.
102. Medawar P.B. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates. Symp. Soc. Exp. Biol. 1953, 320-338.
103. Medina K.L., Kincade P.W. Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc. Natl. Acad. Sci. USA 1994, 91:5382-5386.
104. Medina K.L., Smithson G., Kincade P.W. Suppression of B lymphopoiesis during normal pregnancy. J. Exp. Med. 1993, 178:1507-1515.
105. Meinhardt A., Hedger M.P. Immunological, paracrine and endocrine aspects of testicular immune privilege. Mol. Cell. Endocrinol. 2011, 335:60-68.
106. Meinhardt A., Bacher M., McFarlane J.R., Metz C.N., Seitz J., Hedger M.P., de Kretser D.M., Bucala R. Macrophage migration inhibitory factor production by Leydig cells: evidence for a role in the regulation of testicular function. Endocrinology 1996, 137:5090-5095.
107. Meinhardt A., Bacher M., Metz C., Bucala R., Wreford N., Lan H., Atkins R., Hedger M. 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. 1998, 59:371-378.
108. Meng J., Holdcraft R.W., Shima J.E., Griswold M.D., Braun R.E. Androgens regulate the permeability of the blood-testis barrier. Proc. Natl. Acad. Sci. USA 2005, 102:16696-16700.
109. Meng J., Greenlee A.R., Taub C.J., Braun R.E. Sertoli cell-specific deletion of the androgen receptor compromises testicular immune privilege in mice. Biol. Reprod. 2011, 85:254-260.
110. Millar D.G., Garza K.M., Odermatt B., Elford A.R., Ono N., Li Z., Ohashi P.S. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat. Med. 2003, 9:1469-1476.
111. Mital P., Kaur G., Dufour J.M. Immunoprotective sertoli cells: making allogeneic and xenogeneic transplantation feasible. Reproduction 2010, 139:495-504.
112. Mital P., Hinton B.T., Dufour J.M. The blood-testis and blood-epididymis barriers are more than just their tight junctions. Biol. Reprod. 2011, 84:851-858.
113. Mjosberg J., Svensson J., Johansson E., Hellstrom L., Casas R., Jenmalm M.C., Boij R., Matthiesen L., Jonsson J.I., Berg G., Ernerudh J. Systemic reduction of functionally suppressive CD4dimCD25highFoxp3+ Tregs in human second trimester pregnancy is induced by progesterone and 17beta-estradiol. J. Immunol. 2009, 183:759-769.
114. Moffett A., Loke C. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 2006, 6:584-594.
115. Moffett-King A. Natural killer cells and pregnancy. Nat. Rev. Immunol. 2002, 2:656-663.
116. Moldenhauer L.M., Hayball J.D., Robertson S.A. Utilising T cell receptor transgenic mice to define mechanisms of maternal T cell tolerance in pregnancy. J. Reprod. Immunol. 2010, 87:1-13.
117. Moldenhauer L.M., Keenihan S.N., Hayball J.D., Robertson S.A. GM-CSF is an essential regulator of T cell activation competence in uterine dendritic cells during early pregnancy in mice. J. Immunol. 2010, 185:7085-7096.
118. Mruk D.D., Cheng C.Y. Drug transporters in spermatogenesis: a re-evaluation of recent data on P-glycoprotein. Spermatogenesis 2012, 2:70-72.
119. Munoz-Cruz S., Togno-Pierce C., Morales-Montor J. Non-reproductive effects of sex steroids: their immunoregulatory role. Curr. Top. Med. Chem. 2011, 11:1714-1727.
120. Nagamatsu T., Schust D.J., Sugimoto J., Barrier B.F. Human decidual stromal cells suppress cytokine secretion by allogenic CD4+ T cells via PD-1 ligand interactions. Hum. Reprod. 2009, 24:3160-3171.
121. Nakanishi Y., Shiratsuchi A. Phagocytic removal of apoptotic spermatogenic cells by Sertoli cells: mechanisms and consequences. Biol. Pharm. Bull. 2004, 27:13-16.
122. Nancy P., Tagliani E., Tay C.S., Asp P., Levy D.E., Erlebacher A. Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science 2012, 336:1317-1321.
123. Neaves W.B. The effect of vasectomy on the testes of inbred Lewis rats. J. Reprod. Fertil. 1978, 54:405-411.
124. Norton M.T., Fortner K.A., Oppenheimer K.H., Bonney E.A. Evidence that CD8 T-cell homeostasis and function remain intact during murine pregnancy. Immunology 2010, 131:426-437.
125. Norwitz E.R., Schust D.J., Fisher S.J. Implantation and the survival of early pregnancy. N. Engl. J. Med. 2001, 345:1400-1408.
126. O'Bryan M.K., Hedger M.P. Inflammatory networks in the control of spermatogenesis: chronic inflammation in an immunologically privileged tissue?. Adv. Exp. Med. Biol. 2009, 636:92-114.
127. 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. Cytokine profiles in the testes of rats treated with lipopolysaccharide reveal localized suppression of inflammatory responses. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288:R1744-1755.
128. O'Rand M.G., Romrell L.J. Appearance of cell surface auto- and isoantigens during spermatogenesis in the rabbit. Dev. Biol. 1977, 55:347-358.
129. Owen R.D. Immunogenetic consequences of vascular anastomoses between bovine twins. Science 1945, 102:400-401.
130. Page E.K., Dar W.A., Knechtle S.J. Tolerogenic therapies in transplantation. Front. Immunol. 2012, 3:198.
131. Pelletier R.M. Cyclic formation and decay of the blood-testis barrier in the mink (Mustela vison), a seasonal breeder. Am. J. Anat. 1986, 175:91-117.
132. Pelletier R.M., Yoon S.R., Akpovi C.D., Silvas E., Vitale M.L. Defects in the regulatory clearance mechanisms favor the breakdown of self-tolerance during spontaneous autoimmune orchitis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296:R743-762.
133. Perez C.V., Sobarzo C.M., Jacobo P.V., Pellizzari E.H., Cigorraga S.B., Denduchis B., Lustig L. Loss of occludin expression and impairment of blood-testis barrier permeability in rats with autoimmune orchitis: effect of interleukin 6 on Sertoli cell tight junctions. Biol. Reprod. 2012, 87:122.
134. Petroff M.G., Kharatyan E., Torry D.S., Holets L. The immunomodulatory proteins B7-DC, B7-H2, and B7-H3 are differentially expressed across gestation in the human placenta. Am. J. Pathol. 2005, 167:465-473.
135. Piccinini A.M., Midwood K.S. DAMPening inflammation by modulating TLR signalling. Mediators Inflamm. 2010, 2010.
136. Pijnenborg R., Vercruysse L., Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006, 27:939-958.
137. Plaks V., Birnberg T., Berkutzki T., Sela S., BenYashar A., Kalchenko V., Mor G., Keshet E., Dekel N., Neeman M., Jung S. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 2008, 118:3954-3965.
138. Polgar B., Kispal G., Lachmann M., Paar C., Nagy E., Csere P., Miko E., Szereday L., Varga P., Szekeres-Bartho J. Molecular cloning and immunologic characterization of a novel cDNA coding for progesterone-induced blocking factor. J. Immunol. 2003, 171:5956-5963.
139. Qu N., Terayama H., Naito M., Ogawa Y., Hirai S., Kitaoka M., Yi S.Q., Itoh M. Caput epididymitis but not orchitis was induced by vasectomy in a murine model of experimental autoimmune orchitis. Reproduction 2008, 135:859-866.
140. Redman C.W., Sargent I.L. Latest advances in understanding preeclampsia. Science 2005, 308:1592-1594.
141. Rettew J.A., Huet-Hudson Y.M., Marriott I. Testosterone reduces macrophage expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol. Reprod. 2008, 78:432-437.
142. Rival C., Lustig L., Iosub R., Guazzone V.A., Schneider E., Meinhardt A., Fijak M. 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.
143. Rival C., Theas M.S., Suescun M.O., Jacobo P., Guazzone V., van Rooijen N., Lustig L. Functional and phenotypic characteristics of testicular macrophages in experimental autoimmune orchitis. J. Pathol. 2008, 215:108-117.
144. Robertson S.A., Guerin L.R., Moldenhauer L.M., Hayball J.D. Activating T regulatory cells for tolerance in early pregnancy - the contribution of seminal fluid. J. Reprod. Immunol. 2009, 83:109-116.
145. Rowe J.H., Ertelt J.M., Xin L., Way S.S. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 2012, 490:102-106.
146. Samstein R.M., Josefowicz S.Z., Arvey A., Treuting P.M., Rudensky A.Y. Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict. Cell 2012, 150:29-38.
147. Samuel T., Kolk A.H., Rumke P., Van Lis J.M. Autoimmunity to sperm antigens in vasectomized men. Clin. Exp. Immunol. 1975, 21:65-74.
148. Sanberg P.R., Borlongan C.V., Saporta S., Cameron D.F. Testis-derived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain. Nat. Biotechnol. 1996, 14:1692-1695.
149. Sand K. Experiments on the internal secretion of the sexual glands, especially on experimental hermaphroditism. J. Physiol. 1919, 53:257-263.
150. Sasaki Y., Sakai M., Miyazaki S., Higuma S., Shiozaki A., Saito S. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 2004, 10:347-353.
151. Scarpellini F., Sbracia M. Use of granulocyte colony-stimulating factor for the treatment of unexplained recurrent miscarriage: a randomised controlled trial. Hum. Reprod. 2009, 24:2703-2708.
152. Schatz F., Krikun G., Caze R., Rahman M., Lockwood C.J. Progestin-regulated expression of tissue factor in decidual cells: implications in endometrial hemostasis, menstruation and angiogenesis. Steroids 2003, 68:849-860.
153. Schell C., Albrecht M., Mayer C., Schwarzer J.U., Frungieri M.B., Mayerhofer A. Exploring human testicular peritubular cells: identification of secretory products and regulation by TNFalpha. Endocrinology 2008.
154. Schill W.B., Schneider J., Ring J. The use of ketotifen, a mast cell blocker, for treatment of oligo- and asthenozoospermia. Andrologia 1986, 18:570-573.
155. Schnitzler F., Fidder H., Ferrante M., Ballet V., Noman M., Van Assche G., Spitz B., Hoffman I., Van Steen K., Vermeire S., Rutgeerts P. Outcome of pregnancy in women with inflammatory bowel disease treated with antitumor necrosis factor therapy. Inflamm. Bowel Dis. 2011, 17:1846-1854.
156. Schuppe H.C., Meinhardt A. Immune privilege and inflammation of the testis. Chem. Immunol. Allergy 2005, 88:1-14.
157. Schuppe H.C., Meinhardt A., Allam J.P., Bergmann M., Weidner W., Haidl G. Chronic orchitis: a neglected cause of male infertility?. Andrologia 2008, 40:84-91.
158. Segerer S.E., Rieger L., Kapp M., Dombrowski Y., Muller N., Dietl J., Kammerer U. MIC-1 (a multifunctional modulator of dendritic cell phenotype and function) is produced by decidual stromal cells and trophoblasts. Hum. Reprod. 2012, 27:200-209.
159. Selawry H.P., Cameron D.F. Sertoli cell-enriched fractions in successful islet cell transplantation. Cell Transplant. 1993, 2:123-129.
160. Seppanen E., Fisk N.M., Khosrotehrani K. Pregnancy-acquired fetal progenitor cells. J. Reprod. Immunol. 2013, 97:27-35.
161. Setchell B.P. The testis and tissue transplantation: historical aspects. J. Reprod. Immunol. 1990, 18:1-8.
162. Sharkey A.M., Gardner L., Hiby S., Farrell L., Apps R., Masters L., Goodridge J., Lathbury L., Stewart C.A., Verma S., Moffett A. Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J. Immunol. 2008, 181:39-46.
163. Shechter R., London A., Schwartz M. Orchestrated leukocyte recruitment to immune-privileged sites: absolute barriers versus educational gates. Nat. Rev. Immunol. 2013, 13:206-218.
164. Shimada S., Nishida R., Takeda M., Iwabuchi K., Kishi R., Onoe K., Minakami H., Yamada H. Natural killer, natural killer T, helper and cytotoxic T cells in the decidua from sporadic miscarriage. Am. J. Reprod. Immunol. 2006, 56:193-200.
165. Skomsvoll J.F., Wallenius M., Koksvik H.S., Rodevand E., Salvesen K.A., Spigset O., Kvien T.K. Drug insight: anti-tumor necrosis factor therapy for inflammatory arthropathies during reproduction, pregnancy and lactation. Nat. Clin. Pract. Rheumatol. 2007, 3:156-164.
166. Smith B.E., Braun R.E. Germ cell migration across Sertoli cell tight junctions. Science 2012, 338:798-802.
167. Su L., Mruk D.D., Cheng C.Y. Drug transporters, the blood-testis barrier, and spermatogenesis. J. Endocrinol. 2011, 208:207-223.
168. Suominen J.S., Wang Y., Kaipia A., Toppari J. Tumor necrosis factor-alpha (TNF-alpha) promotes cell survival during spermatogenesis, and this effect can be blocked by infliximab, a TNF-alpha antagonist. Eur. J. Endocrinol. 2004, 151:629-640.
169. Szekeres-Bartho J., Reznikoff-Etievant M.F., Varga P., Pichon M.F., Varga Z., Chaouat G. Lymphocytic progesterone receptors in normal and pathological human pregnancy. J. Reprod. Immunol. 1989, 16:239-247.
170. Szekeres-Bartho J., Szekeres G., Debre P., Autran B., Chaouat G. Reactivity of lymphocytes to a progesterone receptor-specific monoclonal antibody. Cell. Immunol. 1990, 125:273-283.
171. Taglauer E.S., Yankee T.M., Petroff M.G. Maternal PD-1 regulates accumulation of fetal antigen-specific CD8+ T cells in pregnancy. J. Reprod. Immunol. 2009, 80:12-21.
172. Tangri S., Raghupathy R. Expression of cytokines in placentas of mice undergoing immunologically mediated spontaneous fetal resorptions. Biol. Reprod. 1993, 49:850-856.
173. Thuere C., Zenclussen M.L., Schumacher A., Langwisch S., Schulte-Wrede U., Teles A., Paeschke S., Volk H.D., Zenclussen A.C. Kinetics of regulatory T cells during murine pregnancy. Am. J. Reprod. Immunol. 2007, 58:514-523.
174. Tilburgs T., Roelen D.L., van der Mast B.J., van Schip J.J., Kleijburg C., de Groot-Swings G.M., Kanhai H.H., Claas F.H., Scherjon S.A. Differential distribution of CD4(+)CD25(bright) and CD8(+)CD28(-) T-cells in decidua and maternal blood during human pregnancy. Placenta 2006, 27(Suppl. A):S47-S53.
175. Tung K.S. Human sperm antigens and antisperm antibodies I. Studies on vasectomy patients. Clin. Exp. Immunol. 1975, 20:93-104.
176. Tung P.S., Fritz I.B. Specific surface antigens on rat pachytene spermatocytes and successive classes of germinal cells. Dev. Biol. 1978, 64:297-315.
177. Tung K.S., Teuscher C. Mechanisms of autoimmune disease in the testis and ovary. Hum. Reprod. Update 1995, 1:35-50.
178. Tung K.S., Teuscher C., Meng A.L. Autoimmunity to spermatozoa and the testis. Immunol. Rev. 1981, 55:217-255.
179. Turner T.T., D'Addario D.A., Howards S.S. Effects of vasectomy on the blood-testis barrier of the hamster. J. Reprod. Fertil. 1979, 55:323-328.
180. Vacca P., Cantoni C., Vitale M., Prato C., Canegallo F., Fenoglio D., Ragni N., Moretta L., Mingari M.C. Crosstalk between decidual NK and CD14+ myelomonocytic cells results in induction of Tregs and immunosuppression. Proc. Natl. Acad. Sci. USA 2010, 107:11918-11923.
181. Vacca P., Vitale C., Montaldo E., Conte R., Cantoni C., Fulcheri E., Darretta V., Moretta L., Mingari M.C. CD34+ hematopoietic precursors are present in human decidua and differentiate into natural killer cells upon interaction with stromal cells. Proc. Natl. Acad. Sci. USA 2011, 108:2402-2407.
182. van der Meer A., Lukassen H.G., van Lierop M.J., Wijnands F., Mosselman S., Braat D.D., Joosten I. Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells. Mol. Hum. Reprod. 2004, 10:189-195.
183. Van Rood J.J., Eernisse J.G., Van Leeuwen A. Leucocyte antibodies in sera from pregnant women. Nature 1958, 181:1735-1736.
184. Vornberger W., Prins G., Musto N.A., Suarez-quian C.A. Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology 1994, 134.
185. Wahabi, H.A., Abed Althagafi, N.F., Elawad, M., Al Zeidan, R.A., 2011. Progestogen for treating threatened miscarriage. Cochrane Database Syst. Rev. CD005943.
186. Wang J., Wreford N.G., Lan H.Y., Atkins R., Hedger M.P. 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. 1994, 51:551-561.
187. Wang R.S., Yeh S., Chen L.M., Lin H.Y., Zhang C., Ni J., Wu C.C., di Sant'Agnese P.A., deMesy-Bentley K.L., Tzeng C.R., Chang C. Androgen receptor in sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes. Endocrinology 2006, 147:5624-5633.
188. Welter H., Kohn F.M., Mayerhofer A. Mast cells in human testicular biopsies from patients with mixed atrophy: increased numbers, heterogeneity, and expression of cyclooxygenase 2 and prostaglandin D2 synthase. Fertil. Steril. 2011, 96:309-313.
189. Wheeler K., Tardif S., Rival C., Luu B., Bui E., Del Rio R., Teuscher C., Sparwasser T., Hardy D., Tung K.S. Regulatory T cells control tolerogenic versus autoimmune response to sperm in vasectomy. Proc. Natl. Acad. Sci. USA 2011, 108:7511-7516.
190. Winger E.E., Reed J.L. Treatment with tumor necrosis factor inhibitors and intravenous immunoglobulin improves live birth rates in women with recurrent spontaneous abortion. Am. J. Reprod. Immunol. 2008, 60:8-16.
191. Winnall W.R., Muir J.A., Hedger M.P. Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro. J. Leukoc. Biol. 2011, 90:133-143.
192. Wurfel, W., Santjohanser, C., Hirv, K., Buhl, M., Meri, O., Laubert, I., von Hertwig, I., Fiedler, K., Krusmann, J., Krusmann, G., 2010. High pregnancy rates with administration of granulocyte colony-stimulating factor in ART-patients with repetitive implantation failure and lacking killer-cell immunglobulin-like receptors. Hum. Reprod. 25, 2151-2152; author reply 2152.
193. Yao M.W., Lim H., Schust D.J., Choe S.E., Farago A., Ding Y., Michaud S., Church G.M., Maas R.L. Gene expression profiling reveals progesterone-mediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. Mol. Endocrinol. 2003, 17:610-627.
194. Yule T.D., Montoya G.D., Russell L.D., Williams T.M., Tung K.S. Autoantigenic germ cells exist outside the blood testis barrier. J. Immunol. 1988, 141:1161-1167.
195. Zhao J.X., Zeng Y.Y., Liu Y. Fetal alloantigen is responsible for the expansion of the CD4(+)CD25(+) regulatory T cell pool during pregnancy. J. Reprod. Immunol. 2007, 75:71-81.
196. Zhu Y., Hanna R.N., Schaaf M.J., Spaink H.P., Thomas P. Candidates for membrane progestin receptors-past approaches and future challenges. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2008, 148:381-389.
197. Zinaman M.J., Clegg E.D., Brown C.C., O'Connor J., Selevan S.G. Estimates of human fertility and pregnancy loss. Fertil. Steril. 1996, 65:503-509.