Blood-tissue barriers morphofunctional and immunological aspects of the blood-testis and blood-epididymal barriers

Advances in Experimental Medicine and Biology

Volumn 763, Issue , 2013, Pages 237-259

  França, Luiz R ^a   Auharek, Sarah A ^a   Hess, Rex A ^b   Dufour, Jannette M ^c   Hinton, Barry T ^d  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; CLAUDIN 5; CYCLOSPORIN; FOLLITROPIN; LEUKEMIA INHIBITORY FACTOR; MULTIDRUG RESISTANCE PROTEIN 1; THYROID HORMONE; TRANSFORMING GROWTH FACTOR BETA;

ANATOMICAL CONCEPTS; APOPTOSIS; ARTICLE; AUTOIMMUNITY; BASOLATERAL MEMBRANE; BLOOD EPIDIDYMAL BARRIER; BLOOD TESTIS BARRIER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; DESMOSOME; DIABETES MELLITUS; ELECTRON MICROSCOPY; EPIDIDYMIS; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; ION TRANSPORT; LEYDIG CELL; LYMPHOCYTE; MEIOSIS; MORPHOLOGY; NONHUMAN; PERMEABILITY BARRIER; PHYLOGENY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOCYTE; SPERMATOGENESIS; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84934435062     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-4711-5_12     Document Type: Article

References (177)

1. Davson H, Zlokovic B, Rakic L, et al. An introduction to the blood-brain barrier. London: Mcmillan 1993; 1-335
2. Rubin LL, Staddon JM. Thc ccll biology ofthc blood brain barricr. Annu Rev Neurosci 1999; 22:11-28
3. O'Rand MG, Romrell LJ. Appearance of cell surface auto-And isoantigens during spermatogenesis in the rabbit. Dev BioI 1977; 55:347-358
4. Tung PS, Fritz lB. Specific surface antigens on rat pachytene spermatocytes and successive classes of germinal cells. Dev BioI 1978; 64:297-315
5. Wong EW, Cheng CY. Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol BioI 2009; 278:309-353
6. Robaire B, Hinton, BT, Orgebin-Crist MC. The epididymis. In: Neill JD, ed. Physiology of Reproduction, 3rd ed. New York: Elsevier Press, 2006:1071-1148
7. Setchell BP, Voglmary JK, Waites GMH. A blood-Testis barrier restricting passage from blood into rete testis fluid but not into lymph. J Physiol1969; 200:73-85
8. Kormano M. Penetration of intravenous trypan blue into the rat testis and epididymis. Acta Histochem 1968; 30: 133-136
9. Dym M, Fawcett DW. The blood-Testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. BioI Reprod 1970; 3:308-326
10. Flickinger C, Fawcett DW. The junctional specializations of Sertoli cells in the seminiferous epithelium. Anat Record 1967; 158:207-221
11. Hoffer AP, Hinton BT. Morphological evidence for a blood-epididymis barrier and the effects of gossypol on its integrity. BioI Reprod 1984; 30:991-1004
12. Mital P, Hinton BT, Dufour JM. The blood-Testis and blood-epididymis barriers are more than just their tight junctions doi: 10. 1095/biolreprod. 1 10.087452
13. Ribbert H. Die Abscheidung intravenous injizierten gelosten Karminis in Der Geweben. Z Allgem Physiol 1904; 4:201:214
14. Bouffard G. Injection des couleurs De benzidine aux animaux normaux. Ann Inst Pasteur, Paris 1906; 20:539-546
15. Chiquoine D. Observations on the early events of cadmium necrosis ofthe testis. AnatRec 1964; 149:23-36
16. Nicander L. An electron microscopical study of cell contacts in the seminiferous tubules of some mammals. Z Zellforsch Mikrosk Anat 1967; 83:375-397
17. Setchell BP. The blood-Testicular fluid barrier in sheep. J Physiol1967; 189:63-65
18. Dym M. The fine structure of the monkey (Macaca) Sertoli cell and its role in maintaining the blood-Testis barrier. Anat Rec 1973; 175:639-656
19. Fawcett DW, Leak LV, Heidger PM Jr. Electron microscopic observations on the structural components of the blood-Testis barrier. J Reprod Fertil Supp11970; 10:105-122
20. Abraham M. The male germ cell protective barrier along phylogenesis. Int Rev Cytol 1991; 130: 111-190
21. Russell LD, Peterson RN. Sertoli cell junctions: Morphological and function correlates. lnt Rev Cyt 1985; 94: 177-211
22. Neaves WB. Permeability ofSertoli cell tight junctions to lanthanum after ligation of ductus deferens and ductuli efferentes. J Cell BioI 1973; 59:559-572
23. Russell L. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1978; 148:313-328
24. Bart J, Groen HJ, van Der GraafWT, et al. An oncological view on the blood-Testis barrier. Lancet Oncol 2002; 3:357-363
25. DiNapoli L, Capel B. SRY and the standoff in sex determination. Mol Endocrinol2008; 22:1-9
26. Sharpe RM, Millar MR, Mckinnell C. Relative roles of testosterone and the germ cell complement in detrmining stage-dependent changes in protein secretion by isolated ret seminiferous tubules. lnt J Androl 1993; 16:71-81
27. Cooke PS, Holsberger DR, Franya LR. Thyroid hormone regulation of Sertoli Cell Development. In: Skinner MK, Griswold MD eds. The Sertoli Cell Biology. San Diego: Elsevier Science, 2005:217-226
28. Russell LD, Ren HP, Sinha Hikim I, et al. A comparative study in 12 mammalian species of volume densities, volumes, and numerical densities of selected testis components emphasizing those related to the Sertoli cell. AmJ Anat 1989; 188:21-30
29. Gondos B, Berndston WE. Postnatal and pubertal development. In: Russell LD, Griswold MD eds. The Sertoli Cell. Clearwater: Cache River Press, 1993: 115-154
30. Franya LR, Silva VAJ, Chiarini-Garcia H, et al. Cell proliferation and hormonal changes during postnatal development of the testis in the pig. BioI Reprod 2000; 63: 1629-1636
31. Morrow CM, Tyagi G, Simon L, et al. Claudin 5 expression in mouse seminiferous epithelium is dependent upon the transcription factor Ets variant 5 and contributes to blood-Testis barrier function. BioI Reprod 2009; 81 :871-879
32. Morrow CM, Mruk D, Cheng CY, et al. Claudin and oeeludin expression and function in the seminiferous epithelium. Philos Trans R Soc Lond B BioI Sci 2010; 365: 1679-1696
33. Setehell BP. Blood-Testis barrier, junctional and transport proteins and spermatogenesis. In: Cheng CY ed. Molecular Mechanisms in Spermatogenesis. Austin: Landes Bioscience, 2007:212-233
34. Ross AJ, Amy SP, Mahar PL, et al. BCL W mediates survival of postmitotie Sertoli cells by regulating BAX activity. Dev BioI 2001; 239:295-308
35. Russell LD, Warren J, Debeljuk L, et al. Spermatogenesis in Belw-defieient mice. Bioi Reprod 2001; 65:318-332
36. Russell LD, Ettlin RA, Sinha HAP, et al. Histological and histopatologieal evaluation ofthe testis. Clearwater: Cache River Press 1990; 286
37. Chaudhary J, Sadler-Riggleman I, Ague JM, et al. The helix-loop-helix inhibitor of differentiation (ID roteins induce postmitotie terminally differentiated Sertoli cells to re-enter the cell cycle and proliferate. BioI Reprod 2005 72 1205-1217
38. Tarulli GA, Stanton PG, Lerehl A, et al. Adult Sertoli cells arc not terminally differentiated in the Djungarian hamster: Effect ofFSH on proliferation and junction protein organization. Bioi Reprod 2006; 74:798-806
39. Johnson L, Thompson DL Jr, Varner DD. Role of Sertoli cell number and function on regulation of spermatogenesis. Anim Reprod Sci 2008; 105:23-51
40. Ahmed EA, Barten-van Rijbroek AD, Kal HB, et al. Proliferative activity in vitro and DNA repair indicate that adult mouse and human Sertoli cells are not terminally differentiated, quiescent cells. BioI Reprod 2009; 80:1084-1091
41. Chui K, Trivedi A, Cheng CY, et al. Characterization and Functionality of Proliferative Human Sertoli Cells. Cell Transplant 2010 doi: 1O.3727/0963689IOx536563
42. Pelletier RM. Cyclic modulation of Sertoli cell junctional complexes in a seasonal breeder: The mink (Mustela vison). Am J Anat 1988; 183:68-102
43. Hutchison GR, Scott HM, Walker M, et al. Sertoli cell development and function in an animal model of testicular dysgenesis syndrome. Bio Reprod 2008; 78:352-360
44. Sharpe RM, Mekinnell C, Kivlin C, et al. Proliferation and functional maturation ofSertoli cells, and their relevance to disorders of testis function in adulthood. Reprod 2003; 125:769-784
45. Willems A, Batlouni SR, Esnal A, et al. Selective ablation of the androgen receptor in mouse sertoli cells affects sertoli cell maturation, barrier formation and eytoskel, et al development. PLoS One 2010; 5 :c14168
46. Hikim APS, Bartke A, Russell LD. The seasonal breeding hamster as a model to study structure-function relationships in the testis. Tiss Cell 1988; 20:63-78
47. Komljenovie D, SandhoffR, Teigler A, et al. Disruption ofblood-Testis barrier dynamics in ether-lipid-deficient mice. Cell Tissue Res 2009; 337:281-299
48. Grier HJ, Taylor RG. Testieularmaturationandregression in the common snook. JFish Bioi 1998; 53:521-542
49. Cinquetti R, Dramis L. Histological, histochemical, enzyme histochemical and ultrastructural investigations of the testis ofPadogobius martensi between annual breeding seasons. J Fish BioI 2003; 63: 1402-1428
50. Batlouni SR, Romagosa E, Borella Ml. The reproductive eyele of male catfish Pseudoplatystoma faseiatum (Teleostei, Pimelodidae) revealed by changes of the germinal epithelium. An approach addressed to aquaculture. Anim Reprod Sci 2006; 96:116-132
51. Batlouni SR, Carreno FR, Romagosa E. Cell junctions in the germinal epithelium may play an important role in spermatogenesis of the catfish P. faseiatum (Pisces, Siluriformes). J Mol Histo12005; 36:97-110
52. De Montgolfier B, Dufresne J, Letourneau M, et al. The expression of multiple eonnexins throughout spermatogenesis in the rainbow trout testis suggests a role for complex intercellular communication. BioI Reprod 2007; 76:2-8
53. Bergmann M, Sehindelmeiser J, Greven H. The blood-Testis barrier in vertebrates having different testicular organization. Cell Tissue Res 1984; 238: 145-150
54. Grier HP. Comparative organization of Sertoli cells ineluding the Sertoli cell barrier. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:704-739
55. Pudney J. Comparative cytology ofthe nonmammalian vertebrate Sertoli cell. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:612-657
56. McClusky LM. Stage-dependency of apoptosis and blood-Testis barrier in the dogfish shark (Squalus aeanthias): Cadmium-induced changes as assessed by vital fluorescence techniques. Cell Tissue Res 2006; 325:541-553
57. Leal MC, Cardoso ER, Nobrega RH, et al. Histological and stereologieal evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. BioI Reprod 2009; 81: 177-187
58. Batlouni SR, Nobrega RH, Franya LR. Cell junctions in fish seminiferous epithelium. Fish Physiol Bioehem 2009; 35:207-217
59. Schulz RW, Menting S, Bogerd J, et al. Sertoli cell proliferation in the adult testis: Evidence from two fish species belonging to different orders. BioI Reprod 2005; 73:891-898
60. Howards SS, Jessee SJ, Johnson AL. Micropuncture studies of the blood-seminiferous tubule barrier. Bioi Reprod 1976; 14:264-269
61. Turner TT, D' Addario DA, Howards SS. [3H]3-0-methyl-D-glucose transport from blood into the lumina of the seminiferous and epididymal tubules in intact and vasectomized hamsters. J Reprod Fertil 1980; 60:285-289
62. Hinton BT, Howards SS. Permeability characteristics of the epithelium in the rat caput epididymidis. J Reprod Fertil 1981; 63:95-99
63. Turner TT, Cochran RC, Howards SS. Transfer of steroids across the hamster blood testis and blood epididymal barriers. Bioi Reprod 1981; 25:342-348
64. Turner TT, D'Addario DA, Howards SS. The blood epididymal barrier to [3H]-inulin in intact and vasectomized hamsters. Invest Urol 1981; 19:89-91
65. Hinton BT, Howards SS. Rat testis and epididymis can transport [3H]3-0-methyl-D-glucose, [3H] inositol and [3H] alpha-Aminoisobutyric acid across its epithelia in vivo. Bioi Reprod 1982; 27:1181-1189
66. Hinton BT, Hernandez H. Neutral amino acid absorption by the rat epididymis. BioI Reprod 1987; 37:288-292
67. Brooks DE, Hamilton DW. Mallek AH. The uptake of L-(methyl-3H) carnitine by the rat epididymis. Biochem. Biophys Res Commun 1973; 52:1354-1360
68. Hinton BT, Setchell BP. Concentration and uptake of carnitine in the rat epididymis. A micropuncture study. In: Carnitine, Biosynthesis, Metabolism and Functions. Frenkel RA, McGarry JD, eds. New York: Academic Press, 1980:237-250
69. Hinton BT, Hernandez H. Selective luminal absorption of L-carnitine from the proximal regions of the rat epididymis. Possible relationships to development of sperm motility. J Andro11985; 6:300-305
70. Obermann H, W ingbermuhler A, Munz S, et al. A putative 12-Transmembrane domain cotransporter associated with apical membranes of the epididymal duct. J AndroI2003; 24:542-556
71. Pastor-Soler N, Bagnis C, Sabolic I, et al. Aquaporin 9 expression along the male reproductive tract. BioI Reprod2001; 65:384-393
72. Da Silva N, Pietrement C, Brown D, et al. Segmental and cellular expression of aquaporins in the male excurrent duct. Biochim Biophys Acta 2006; 1758: 1025-1033
73. Hermo L, Schellenberg M, LiuL Y, et al. Membrane domain specificity in the spatial distribution of aquaporins 5,7,9 and II in efferent ducts and epididymis of rats. J Histochem Cytochem 2008; 56:1121-1135
74. Domeniconi RF, Orsi AM, Justulin Jr, et al. Immunolocalization of aquaporins 1,2 and 7 in rete testis, efferent ducts, epididymis and vas deferens of adult dog. Cell Tissue Res 2008; 332:329-335
75. Setchell BP, Brooks DE. Anatomy, vasculature, innervation and fluids of the male reproductive tract. In: Knobil E, Neill ro, eds. The Physiology of Reproduction. New York: Raven Press, 1988:753-836
76. Hinton BT, Setchell BP. Fluid secretion and movement. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993 :249-267
77. Setchell BP. Blood-Testis barrier, junctional and transport proteins and spermatogenesis. Adv Exp Med Bioi 2008; 636:212-233
78. Pastor-Soler N, Pietrement C, Breton S. Role of acid/base transporters in the male reproductive tract and potential consequences of their malfunction. Physiology 2005; 20:417-428
79. Da Silva N, Shum WW, Breton S. Regulation of vacuolar proton pumping ATPase-dependent luminal acidification in the epididymis. Asian J Androl 2007; 9:476-482
80. Shum WW, Da Silva N, Brown D, et al. Regulation ofluminal acidification in the male reproductive tract via cell-cell crosstalk. J Exp BioI 2009; 212: 1753-1761
81. Shum WW, Da Silva N, McKee M, et al. Transepithelial projections from basal cells arc luminal sensors in pseudostratified epithelia. Ce112008; 135:1108-1117
82. Blomqvist SR, Vidarsson H, Soder 0, et al. Epididymal expression of the forkhead transcription factor Foxi I is required for male fertility. EMBO J 2006; 25:4131-4141
83. Sonnenberg-Riethmacher E, Walter B, Riethmacher D, et al. The c-ros tyrosine kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis. Genes Dev 1996; 10: 1184-1193
84. Yeung CH, Sonnenberg-Riethmacher E, Cooper TG. Infertile spermatozoa of c-ros tyrosine kinase receptor knockout mice show flagellar angulation and maturational defects in cell volume regulatory mechanisms. BioI Reprod 1999; 61:1062-1069
85. Yeung CH, Wagenfeld A, Nieschlag E, et al. The cause of infertility of male c-ros tyrosine receptor knockout mice. BioI Reprod 2000; 63:612-618
86. Wagenfeld A, Yeung CH, Lehnert W, et al. Lack of glutamate transporter EAACI in the epididymis of infertile c-ros receptor-kinase deficient mice. J Androl 2002; 23 :772-782
87. Xu Y, Yeung CH, Setiawan I, et al. Sodium-inorganic phosphate cotransporter NaPi-JIb in the epididymis and its potential role in male fertility studied in a transgenic mouse model. BioI Reprod 2003; 69: 1135-1141
88. Yeung CH, Breton S, Setiawan I, et al. Increased luminal pH in the epididymis of infertile c-ros knockout mice and the expression of sodium-hydrogen exchangers and vacuolar proton pump. Mol Reprod Dev 2004; 68: 159-168
89. Wong V, Russell LD. Three-dimensional reconstruction of a rat stage V Sertoli cell: I. Methods, basic configuration and dimensions. Am J Anat 1983; 167:143-161
90. Hausman RH. Biology of Hydra. In: Burnett AL, ed. New York: Academic Press, 1973:393-453
91. Wood RL, Kuda AM. Formation of junctions in regenerating hydra: Septate junctions. J Ultrastruct Res 1980; 70:104-117
92. Favard P. Evolution des ultrastructures cellulaires au cours De la spermatogenese De 1'. Ascaris. Ann Sci Nat Zool 1961; 21 :53-152
93. O'Donovan P, Abraham M. Somatic tissue-male germ cell barrier in three hermaphrodite invertebrates: Dugesia bib lica (Platyhelminthes), Placobdella costata (Annelida) and Levantina hierosolyma (Mollusca J Morpho11987; 192:217-227
94. Koulish S, Kramer CR. An electron microscopic study of a 'Sertoli-like' cell in the testis of a barnacle, Balanus. Tissue Cell 1986; 18:383-393
95. De Jong-Brink M, De With ND, Hurkmans PJ. A morphological, enzyme-cytochemical and physiological study of the blood-gonad barrier in the hermaphroditic snail Lymnaea stagnalis. Cell Tissue Res 1984; 235:593-600
96. Gilula NB, Fawcett DW, Aoki A. The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Dev BioI 1976; 50: 142-168
97. Franchi E, Camatini M, DeCurtis I. Morphological evidence of a permeability barrier in urodele testis. J Ultrastruct Res 1982; 80:253-263
98. Bergmann M, Greven H, Schindelmeiser J. Observations on the blood-Testis barrier in a frog and a salamander. Cell Tissue Res 1983; 232: 189-200
99. Cavicchia JC, Moviglia GA. The blood-Testis barrier in the toad (Bufo arenarum Hensel): A freeze fracture and lanthanum tracer study. Anat Rec 1983; 205:387-396
100. Baccetti B, Bigliardi E, Talluri MV, et al. The Sertoli cell in lizards. J Ultrastruct Res 1983; 85:11-23
101. Cooksey EJ, Rothwell B. The ultrastructure of the Sertoli cell and its differentiation in the domestic fowl (Gallus domesticus). J Anat 1973; 114:329-345
102. Osman DI, Elwall H, PIõen L. Specialized cell contacts and the blood-Testis barrier in the seminiferous tubules of the domestic fowl (Gallus domesticus).Int J Andro11980; 3:553-562
103. Dym M, Cavicchia Je. Further observations on the blood testis barrier in monkeys. BioI Reprod 1977; 17:390-403
104. Dym M, Cavicchia JC. Functional morphology of the testis. BioI Reprod 1978; 18: 1-5
105. Johnson MH, Setchell BP. Protein and immunoglobulin content of rete testis fluid of rams. J Reprod Fertil 1968; 17:403-406
106. Johnson MH. The distribution of immunoglobulin and spermatozoalautoantigen in the genital tract of the male guinea pig: Its relationship to autoallergicorchitis. Fertil Steril 1972; 23:383-392
107. Dym M, Romrell LJ . Intraepitheliallymphocytes in the male reproductive tract of rats and rhesus monkeys. JReprod Ferti11975; 42:1-7
108. Wang J, Wreford NG, Lan HY, et al. Leukocyte populations of the adult rat testis following removal of the Leydig cells by treatment with ethane dimethanesulfonate and subcutaneous testosterone implants. BioI Reprod 1994; 51:551-561
109. Rival C, Lustig L, Iosub R, et al. Identification ofadendritic cell population in normal testis and in chronically inflamed testis of rats with autoimmune orchitis. Cell Tissue Res 2006; 324:311-318
110. Koskimies AI, Kormano M, Lahti A. A difference in the immunoglobulin content of seminiferous tubule fluid and rete testis fluid of the rat. J Reprod Fert 1971; 27:463-465
111. Tung KSK, Unanue ER, Dixon FJ. Pathogenesis of experimental allergic orchitis. n. The role of antibody. J Immuno11971; 106:1463-1472
112. Yule TD, Montoya GD, Russell LD, et al. Autoantigenic germ cells exist outside the blood-Testis barrier. J Immuno11988; 141:1161-1167
113. Samy ET, Setiady YY, Ohno K, et al. The role of physiological self-Antigen in the acquisition and maintenance of regulatory T-cell function. Immunol Rev 2006; 212: 170-184
114. Marsh JA, O'Hem P, Goldberg E. The role of an X-linked gene in the regulation of secondary humoral response kinetics to sperm-specific LDH-C4 antigens. J Immuno11981; 126: 100-106
115. Yule TD, Mahi-Brown CA, Tung KS. Role of testicular autoantigens and influence of Iymphokines in testicular autoimmune disease. J Reprod Immuno11990; 18:89-103
116. Barker CF, Billingham RE. Immunologically privileged sites. Adv ImmunoI1977; 25:1-54
117. Setchell BP. The testis and tissue transplantation: Historical aspects. J Reprod Immunol 1990; 18: 1-8
118. Selawry HP. Islet Transplantation to immunoprivileged sites. In: Lanza RP, Chick WL, eds. Pancreatic Islet Transplantation, vol 2, Immunomodulation of Pancreatic Islets. Austin:Landes/CRC Press, 1994:75-86
119. Head JR, Neaves WB, Billingham RE. Immune privilege in the testis. I. Basic parameters of allograft survival. Transplantation 1983; 36:423-431
120. Dufour JM, Rajotte RV, Korbutt GS, et al. Harnessing the innnunomodulatory properties of Sertoli cells to enable xenotransplantation in type I diabetes. Immunol Invest 2003; 32:275-297
121. Bobzien B, Yasunami Y, Majercik M, et al.lntratesticular transplants of islet xenografts (rat to mouse Diabetes 1983; 32:213-216
122. Dobrinski 1. Male germ cell transplantation. Reprod Dom Anim 2008; 43:288-294
123. Honaramooz A, Yang Y. Recent advances in applications of male genn cell transplantation in farm animals. Vet Med Int 2010; epub
124. Brinster RL, Zimmerman JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 1994; 91:11298-11302
125. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 1994; 91: 11303-11307
126. Ogawa T, Dobrinski I, Brinster RL. Recipient preparation is critical for spennatogonial transplantation in the rat. Tissue Cell 1999; 31:461-471
127. Kanatsu-Shinohara M, Ogonuki N, Inoue K, et al. Allogeneic offspring produced by male germ line stem cell transplantation into infertile mouse testis. BioI Reprod 2003; 68: 167-173
128. Zhang Z, Renfree MB, Short RV. Successful intra-And interspecific male germ cell transplantation in the rat. BioI Reprod 2003; 68:961-967
129. Honaramooz A, Megee SO, Dobrinski 1. Genn cell transplantation in pigs. Bioi Reprod 2002; 66:21-28
130. Mikkolal M, Sironen A, Kopp C, et al. Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-Tail spenn defect. Reprod Dom Anim 2006; 41:124-128
131. Honaramooz A, Behboodi E, Blash S, et al. Germ cell transplantation in goats. Mol Reprod Dev 2003; 64:422-428
132. Honaramooz A, Behboodi E, Megee SO, et al. Fertility and gennline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. BioI Reprod 2003; 69:1260-1264
133. Herrid M, Vignarajan S, Davey R, et al. Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 2006; 132:617-624
134. Kim Y, Turner D, Nelson J, et al. Production of donor-derived spenn after spennatogonial stem cell transplantation in the dog. Reproduction 2008; 136:823-831
135. Rodriguez-Sosa JR, Silvertown m, Foster RA, et al. Transduction and transplantation of spennatogonia into the testis ofram lambs through the extra-Testicular rete. Reprod Dom Anim 2009; 44:612-620
136. Herrid M, Olejnik J, Jackson M, et al. Irradiation enhances the efficiency oftesticular germ cell transplantation in sheep. BioI Reprod 2009; 81 :898-905
137. Pollanen P, Soder O, Uksila J. Testicularimmunosuppressiveprotein. JReprodImmunol1988; 14: 125-138
138. Pollanen P, von Euler M, Sainio-Pollanen S, et al. Immunosuppressive activity in the rat seminiferous tubules. J Reprod Immunol 1992; 22: 117-126
139. Selawry HP, Kotb M, Herrod HG, et al. Production of a factor, or factors, suppressing IL-2 production and T-cell proliferation by Sertoli cell-enriched preparations. A potential role for islet transplantation in an immunologically privileged site. Transplantation 1991; 52:846-850
140. De Cesaris P, Filippini A, Cervelli C, et al. Immunosuppressive molecules producedby Sertoli cells cultured in vitro: Biological effects on lymphocytes. Biochem Biophys Res Commun 1992; 186: 1639-1646
141. Wyatt CR, Law L, Magnuson JA, et al. Suppression of lymphocyte proliferation by proteins secreted by cultured Sertoli cells. J Reprod Immuno11988; 14:27-40
142. Hedger MP, Qin JX, Robertson DM, et al. Intragonadal regulation of immune system functions. Reprod Fertil Dev 1990; 2:263-280
143. Hurtenbach U, Shearer GM. Germ cell-induced immune suppression in mice. Effect of inoculation of syngeneic spennatozoa on sell-mediated innnune responses. J Exp Med 1982; 155: 1719-1729
144. Bryniarski K, Szczepanik M, Maresz K, et al. Subpopulations of mouse testicular macrophages and their immunoregulatory function. Am J Reprod Immuno12004; 52:27-35
145. Mital P, Kaur G, Dufour 1M. Immunoprotectivesertoli cells: Making allogeneic and xenogeneic transplantation feasible. Reproduction 2010; 139:495-504
146. Meinhardt A, Hedger MP. Immunological, paracrine and endocrine aspects oftesticular immune privilege. Mol Cell Endocrinol published 2010; PMLD:20363290
147. Guazzone VA, Jacobo P, Theas MS, et al. Cytokines and chemokines in testicular inflammation: A brief review 2009; 72:620-628
148. Hedger MP, Meinhardt A. Cytokines and the immune-Testicular axis. J Reprod Immunol2003; 58: 1-26
149. Dai Z, Nasr IW, Reel M, et al. Impaired recall of CD8 memory T-cells in immunologically privileged tissue. J Immunol 2005; 174: 1165-1170
150. Nasr IW, Wang Y, Gao G, et al. Testicular immune privilege promotes transplantation tolerance by altering the balance between memory and regulatory T-cells. lImmunol 2005; 174:6161-6168
151. Hedger MP. Macrophages and the immune responsiveness ofthe testis. J Reprodlmmunol2002; 57: 19-34
152. Rival C, Guazzone VA, von Wulffen W et al. Expression of costimulatory molecules, chemokine receptors and pro inflammatory cytokincs in dcndritic cells from normal and chronically inflamed rat testis. Mol Hum Reprod 2007; 13:853-861
153. Selawry HP, Whittington K. Extended allograft survival of islets grafted into intra-Abdominally placed testis. Diabetes 1984; 33:405-406
154. Selawry HP, Whittington KB. Prolonged intratesticular islet graft survival is not dependent on local steriodogenesis. Horm Metab Res 1988; 20:562-565
155. Cameron DF, Whittington K, Schultz RE et al. Successful islet/abdominal testis transplantation docs not require Leydig cells. Transplantation 1990; 50:649-653
156. Whitmore WF 3rd, Karsh L, Gittes RF. The role of germinal epithelium and spermatogenesis in the privileged survival of intratesticular grafts. J Urol 1985; 134:782-786
157. Whitmore WF 3rd, Gittes RF . Intratesticular grafts: The testis as an exceptional immunologically privileged site. Trans Am Assoc Genitourin Surg 1978; 70:76-80
158. Head JR, Billingham RE. Immune privilege in the testis. II. Evaluation of potential local factors. Transplantation 1985; 40:269-275
159. Selawry HP, Cameron DF. Sertoli cell-enriched fractions in successful islet celltransplantation. Cell Transplant 1993; 2: 123-129
160. Korbutt GS, Elliott JF, Rajotte RV. Cotransplantation of allogeneic islets with allogeneic testicular cell aggregates allows long-Term graft survival without systemic immunosuppression. Diabetes 1997; 46:317-322
161. Dufour JM, Lord SJ, Kin T, et al. Comparison of successful and unsuccessful islet/Sertoli cell cotransplant grafts in streptozotocin induced diabetic mice. Cell Transplant 2008; 16:1029-1038
162. Dufour JM, Dass B, Halley K et al. Sertoli cell line lacks the immunoprotective properties associated with primary Sertoli cells. Cell Transplant 2008; 17:525-534
163. Fijak M, Meinhardt A. The testis in immune privilege. Immunol Rev 2006; 213:66-81
164. Skinner MK. Sertoli cell-somatic cell interactions. In: Skinner MK, GriswoldMD, eds. Sertoli cell biology. San Diego: Elsevier Academic Press, 2005:317-328
165. Shamekh R, EI-Badri NS, Saporta S, et al. Sertoli cells induce systemic donor-specific tolerance inxenogenic transplantation model. Cell Transplant 2006; 15:45-53
166. Dym M, Romrell LJ . Intraepitheliallymphocytes in the male reproductive tract of rats and rhesus monkeys. J Reprod Fertil 1975; 42: 1-7
167. Serre V, Robaire B. Distribution of immune cells in the epididymis of the aging Brown Norway rat is segment-specific and related to the luminal content. BioI Reprod 1999; 61 :705-714
168. Wong PY, Tsang AY, Fu WO et al. Restricted entry of an anti-rat epididymal protein IgG into the rat epididymis. Int J Androl 1983; 6:275-282
169. Yeung CH, Bergmann M, Cooper TG. Non-specific uptake of IgG by rat epididymal tubules in vitro. Int J Androl 1991; 14:364-373
170. Knee RA, Hickey DK, Beagley KW et al. Transport oflgG across the blood-luminal barrier of the male reproductive tract of the rat and the effect of estradiol administration on reabsorption of fluid and IgG by the epididymal ducts. BioI Reprod 2005; 73:688-694
171. Beagley KW, Wu ZL, Pomering M, et al. Immune responses in the epididymis: Implications for immunocontraception. J Reprod Fertil Supp11998; 53:235-245
172. Hoh M, Xie Q, Miyamoto K, et al. Major differences between the testis and epididymis in the induction of granulomas in response to extravasated germ cells. I. A light microscopical study in mice. Int J Androl 1999; 22:316-323
173. ltoh M, Chen XH, Takeuchi Y et al. Morphological demonstration of the immune privilege in the testis using adjuvants: Tissue responses of male reproductive organs in mice injected with Bordetellapertussigens. Arch Histol Cyto11995; 58:575-579
174. Kazeem AA. A critical consideration of the rat epididymis as an immunologically privileged site. Scand J Immunol1988; 27: 149-156
175. Pollanen P, CooperTG. Immunology ofthe testicular excurrent ducts. JReprod Immunol1994; 26: 167-216
176. Da Silva N, Cortez-Retamozo V, Reinecker HC et al. A dense network of dendritic cells populates the murine epididymis. Reproduction 20 II; in press
177. Wheeler K, Tardiff S, Rival C et al. Regulatory T cells determine tolerogenic versus autoimmune response to sperm in vasectomized mice. PNAS 20 II; in press