Skip to main content
SpringerLink
Log in

Blood-Tissue Barriers

Morphofunctional and Immunological Aspects of the Blood-Testis and Blood-Epididymal Barriers

  • Chapter
  • First Online:
Biology and Regulation of Blood-Tissue Barriers

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 763))

Abstract

The blood-testis barrier (BTB) is known for its ability to create an immune privilege site in the seminiferous epithelium, but less is known of the blood-epididymal barrier (BEB). It is already established that the fully functional BTB and BEB are much more complex and consist of anatomical/physical (tight junctions, basolateral and apical membranes), physiological and immunological components, which are all necessary to make a functioning barrier in the testis and epididymis. However, comparative data for metazoans suggest that an effective Sertoli cell barrier is not entirely necessary for the development of germ cells during spermatogenesis or that our knowledge about the barrier structure/function in metazoans is still immature. This chapter compares the unique barrier formed by the Sertoli cells of the testis to that formed by the apical junctional complexes of the epididymal epithelium.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Davson H, Zlokovic B, Rakic L et al. An introduction to the blood-brain barrier. London: Mcmillan 1993; 1–335.

    Book  Google Scholar 

  2. Rubin LL, Staddon JM. The cell biology of the blood brain barrier. Annu Rev Neurosci 1999; 22:11–28.

    Article  CAS  PubMed  Google Scholar 

  3. O’Rand MG, Romrell LJ. Appearance of cell surface auto-and isoantigens during spermatogenesis in the rabbit. Dev Biol 1977; 55:347–358.

    Article  CAS  Google Scholar 

  4. Tung PS, Fritz IB. Specific surface antigens on rat pachytene spermatocytes and successive classes of germinal cells. Dev Biol 1978; 64:297–315.

    Article  CAS  PubMed  Google Scholar 

  5. Wong EW, Cheng CY. Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol Biol 2009; 278:309–353.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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.

    Google Scholar 

  7. Setchell BP, Voglmary JK, Waites GMH. A blood-testis barrier restricting passage from blood into rete testis fluid but not into lymph. J Physiol 1969; 200:73–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kormano M. Penetration of intravenous trypan blue into the rat testis and epididymis. Acta Histochem 1968; 30:133–136.

    CAS  PubMed  Google Scholar 

  9. Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 1970; 3:308–326.

    Article  CAS  PubMed  Google Scholar 

  10. Flickinger C, Fawcett DW. The junctional specializations of Sertoli cells in the seminiferous epithelium. Anat Record 1967; 158:207–221.

    Article  CAS  Google Scholar 

  11. Hoffer AP, Hinton BT. Morphological evidence for a blood-epididymis barrier and the effects of gossypol on its integrity. Biol Reprod 1984; 30:991–1004.

    Article  CAS  PubMed  Google Scholar 

  12. Ribbert H. Die Abscheidung intravenous injizierten gelosten Karminis in der Geweben. Z Allgem Physiol 1904; 4:201:214.

    Google Scholar 

  13. Bouffard G. Injection des couleurs de benzidine aux animaux normaux. Ann Inst Pasteur, Paris 1906; 20:539–546.

    CAS  Google Scholar 

  14. Chiquoine D. Observations on the early events of cadmium necrosis of the testis. Anat Rec 1964; 149:23–36.

    Article  CAS  PubMed  Google Scholar 

  15. Nicander L. An electron microscopical study of cell contacts in the seminiferous tubules of some mammals. Z Zellforsch Mikrosk Anat 1967; 83:375–397.

    Article  CAS  PubMed  Google Scholar 

  16. Setchell BP. The blood-testicular fluid barrier in sheep. J Physiol 1967; 189:63–65.

    Article  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. Fawcett DW, Leak LV, Heidger PM Jr. Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil Suppl 1970; 10:105–122.

    CAS  PubMed  Google Scholar 

  19. Abraham M. The male germ cell protective barrier along phylogenesis. Int Rev Cytol 1991; 130:111–190.

    Article  CAS  PubMed  Google Scholar 

  20. Russell LD, Peterson RN. Sertoli cell junctions: morphological and function correlates. Int Rev Cyt 1985; 94:177–211.

    Article  CAS  Google Scholar 

  21. Neaves WB. Permeability of Sertoli cell tight junctions to lanthanum after ligation of ductus deferens and ductuli efferentes. J Cell Biol 1973; 59:559–572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Russell L. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1978; 148:313–328.

    Article  Google Scholar 

  23. Bart J, Groen HJ, van der Graaf WT et al. An oncological view on the blood-testis barrier. Lancet Oncol 2002; 3:357–363.

    Article  PubMed  Google Scholar 

  24. DiNapoli L, Capel B. SRY and the standoff in sex determination. Mol Endocrinol 2008; 22:1–9.

    Article  CAS  PubMed  Google Scholar 

  25. 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. Int J Androl 1993; 16:71–81.

    Article  CAS  PubMed  Google Scholar 

  26. Cooke PS, Holsberger DR, França 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.

    Chapter  Google Scholar 

  27. 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. Am J Anat 1989; 188:21–30.

    Article  Google Scholar 

  28. Gondos B, Berndston WE. Postnatal and pubertal development. In: Russell LD, Griswold MD eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:115–154.

    Google Scholar 

  29. França LR, Silva VAJ, Chiarini-Garcia H et al. Cell proliferation and hormonal changes during postnatal development of the testis in the pig. Biol Reprod 2000; 63:1629–1636.

    Article  PubMed  Google Scholar 

  30. 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. Biol Reprod 2009; 81:871–879.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Morrow CM, Mruk D, Cheng CY et al. Claudin and occludin expression and function in the seminiferous epithelium. Philos Trans R Soc Lond B Biol Sci 2010; 365:1679–1696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Setchell BP. Blood-testis barrier, junctional and transport proteins and spermatogenesis. In: Cheng CY ed. Molecular Mechanisms in Spermatogenesis. Austin: Landes Bioscience, 2007:212–233.

    Google Scholar 

  33. Ross AJ, Amy SP, Mahar PL et al. BCLW mediates survival of postmitotic Sertoli cells by regulating BAX activity. Dev Biol 2001; 239:295–308.

    Article  CAS  PubMed  Google Scholar 

  34. Russell LD, Warren J, Debeljuk L et al. Spermatogenesis in Bclw-deficient mice. Biol Reprod 2001; 65:318–332.

    Article  CAS  PubMed  Google Scholar 

  35. Russell LD, Ettlin RA, Sinha HAP et al. Histological and histopatological evaluation of the testis. Clearwater: Cache River Press 1990; 286.

    Google Scholar 

  36. Chaudhary J, Sadler-Riggleman I, Ague JM et al. The helix-loop-helix inhibitor of differentiation (ID) proteins induce postmitotic terminally differentiated Sertoli cells to re-enter the cell cycle and proliferate. Biol Reprod 2005; 72:1205–1217.

    Article  CAS  PubMed  Google Scholar 

  37. Tarulli GA, Stanton PG, Lerchl A et al. Adult Sertoli cells are not terminally differentiated in the Djungarian hamster: effect of FSH on proliferation and junction protein organization. Biol Reprod 2006; 74:798–806.

    Article  CAS  PubMed  Google Scholar 

  38. 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.

    Article  CAS  PubMed  Google Scholar 

  39. 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. Biol Reprod 2009; 80:1084–1091.

    Article  CAS  PubMed  Google Scholar 

  40. Chui K, Trivedi A, Cheng CY et al. Characterization and Functionality of Proliferative Human Sertoli Cells. Cell Transplant 2010 doi: 10.3727/096368910x536563.

    Article  PubMed  Google Scholar 

  41. Pelletier RM. Cyclic modulation of Sertoli cell junctional complexes in a seasonal breeder: the mink (Mustela vison). Am J Anat 1988; 183:68–102.

    Article  CAS  PubMed  Google Scholar 

  42. 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.

    Article  CAS  Google Scholar 

  43. Sharpe RM, Mckinnell C, Kivlin C et al. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reprod 2003; 125:769–784.

    Article  CAS  Google Scholar 

  44. 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 cytoskeletal development. PLoS One 2010; 5:e14168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 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.

    Article  CAS  Google Scholar 

  46. Komljenovic D, Sandhoff R, Teigler A et al. Disruption of blood-testis barrier dynamics in ether-lipid-deficient mice. Cell Tissue Res 2009; 337:281–299.

    Article  CAS  PubMed  Google Scholar 

  47. Grier HJ, Taylor RG. Testicular maturation and regression in the common snook. J Fish Biol 1998; 53:521–542.

    Article  Google Scholar 

  48. Cinquetti R, Dramis L. Histological, histochemical, enzyme histochemical and ultrastructural investigations of the testis of Padogobius martensi between annual breeding seasons. J Fish Biol 2003; 63:1402–1428.

    Article  CAS  Google Scholar 

  49. Batlouni SR, Romagosa E, Borella MI. The reproductive cycle of male catfish Pseudoplatystoma fasciatum (Teleostei, Pimelodidae) revealed by changes of the germinal epithelium. An approach addressed to aquaculture. Anim Reprod Sci 2006; 96:116–132.

    Article  CAS  PubMed  Google Scholar 

  50. Batlouni SR, Carreño FR, Romagosa E. Cell junctions in the germinal epithelium may play an important role in spermatogenesis of the catfish P. fasciatum (Pisces, Siluriformes). J Mol Histol 2005; 36:97–110.

    Article  CAS  PubMed  Google Scholar 

  51. De Montgolfier B, Dufresne J, Letourneau M et al. The expression of multiple connexins throughout spermatogenesis in the rainbow trout testis suggests a role for complex intercellular communication. Biol Reprod 2007; 76:2–8.

    Article  PubMed  CAS  Google Scholar 

  52. Bergmann M, Schindelmeiser J, Greven H. The blood-testis barrier in vertebrates having different testicular organization. Cell Tissue Res 1984; 238:145–150.

    Article  Google Scholar 

  53. Grier HP. Comparative organization of Sertoli cells including the Sertoli cell barrier. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:704–739.

    Google Scholar 

  54. Pudney J. Comparative cytology of the nonmammalian vertebrate Sertoli cell. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:612–657.

    Google Scholar 

  55. McClusky LM. Stage-dependency of apoptosis and blood-testis barrier in the dogfish shark (Squalus acanthias): cadmium-induced changes as assessed by vital fluorescence techniques. Cell Tissue Res 2006; 325:541–553.

    Article  CAS  PubMed  Google Scholar 

  56. Leal MC, Cardoso ER, Nóbrega RH et al. Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol Reprod 2009; 81:177–187.

    Article  CAS  PubMed  Google Scholar 

  57. Batlouni SR, Nóbrega RH, França LR. Cell junctions in fish seminiferous epithelium. Fish Physiol Biochem 2009; 35:207–217.

    Article  CAS  PubMed  Google Scholar 

  58. Schulz RW, Menting S, Bogerd J et al. Sertoli cell proliferation in the adult testis: evidence from two fish species belonging to different orders. Biol Reprod 2005; 73:891–898.

    Article  CAS  PubMed  Google Scholar 

  59. Howards SS, Jessee SJ, Johnson AL. Micropuncture studies of the blood-seminiferous tubule barrier. Biol Reprod 1976; 14:264–269.

    Article  CAS  PubMed  Google Scholar 

  60. Turner TT, D’Addario DA, Howards SS. [3H]3-O-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.

    Article  CAS  PubMed  Google Scholar 

  61. Hinton BT, Howards SS. Permeability characteristics of the epithelium in the rat caput epididymidis. J Reprod Fertil 1981; 63:95–99.

    Article  CAS  PubMed  Google Scholar 

  62. Turner TT, Cochran RC, Howards SS. Transfer of steroids across the hamster blood testis and blood epididymal barriers. Biol Reprod 1981; 25:342–348.

    Article  CAS  PubMed  Google Scholar 

  63. 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.

    CAS  PubMed  Google Scholar 

  64. Hinton BT, Howards SS. Rat testis and epididymis can transport [3H] 3-O-methyl-D-glucose, [3H] inositol and [3H] alpha-aminoisobutyric acid across its epithelia in vivo. Biol Reprod 1982; 27:1181–1189.

    Article  CAS  PubMed  Google Scholar 

  65. Hinton BT, Hernandez H. Neutral amino acid absorption by the rat epididymis. Biol Reprod 1987; 37:288–292.

    Article  CAS  PubMed  Google Scholar 

  66. 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.

    Article  CAS  Google Scholar 

  67. 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.

    Chapter  Google Scholar 

  68. 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 Androl 1985; 6:300–305.

    Article  CAS  PubMed  Google Scholar 

  69. Obermann H, Wingbermuhler A, Munz S et al. A putative 12-transmembrane domain cotransporter associated with apical membranes of the epididymal duct. J Androl 2003; 24:542–556.

    Article  CAS  PubMed  Google Scholar 

  70. Pastor-Soler N, Bagnis C, Sabolic I et al. Aquaporin 9 expression along the male reproductive tract. Biol Reprod 2001; 65:384–393.

    Article  CAS  PubMed  Google Scholar 

  71. 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.

    Article  PubMed  CAS  Google Scholar 

  72. Hermo L, Schellenberg M, Liu LY et al. Membrane domain specificity in the spatial distribution of aquaporins 5, 7, 9 and 11 in efferent ducts and epididymis of rats. J Histochem Cytochem 2008; 56:1121–1135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 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.

    Article  CAS  PubMed  Google Scholar 

  74. Setchell BP, Brooks DE. Anatomy, vasculature, innervation and fluids of the male reproductive tract. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. New York: Raven Press, 1988:753–836.

    Google Scholar 

  75. Hinton BT, Setchell BP. Fluid secretion and movement. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:249–267.

    Google Scholar 

  76. Setchell BP. Blood-testis barrier, junctional and transport proteins and spermatogenesis. Adv Exp Med Biol 2008; 636:212–233.

    Article  CAS  PubMed  Google Scholar 

  77. 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.

    Article  CAS  PubMed  Google Scholar 

  78. 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.

    Article  PubMed  CAS  Google Scholar 

  79. Shum WW, Da Silva N, Brown D et al. Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk. J Exp Biol 2009; 212:1753–1761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Shum WW, Da Silva N, McKee M et al. Transepithelial projections from basal cells are luminal sensors in pseudostratified epithelia. Cell 2008; 135:1108–1117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Blomqvist SR, Vidarsson H, Soder O et al. Epididymal expression of the forkhead transcription factor Foxi1 is required for male fertility. EMBO J 2006; 25:4131–4141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 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.

    Article  CAS  PubMed  Google Scholar 

  83. 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. Biol Reprod 1999; 61:1062–1069.

    Article  CAS  PubMed  Google Scholar 

  84. Yeung CH, Wagenfeld A, Nieschlag E et al. The cause of infertility of male c-ros tyrosine receptor knockout mice. Biol Reprod 2000; 63:612–618.

    Article  CAS  PubMed  Google Scholar 

  85. Wagenfeld A, Yeung CH, Lehnert W et al. Lack of glutamate transporter EAAC1 in the epididymis of infertile c-ros receptor-kinase deficient mice. J Androl 2002; 23:772–782.

    CAS  PubMed  Google Scholar 

  86. Xu Y, Yeung CH, Setiawan I et al. Sodium-inorganic phosphate cotransporter NaPi-IIb in the epididymis and its potential role in male fertility studied in a transgenic mouse model. Biol Reprod 2003; 69:1135–1141.

    Article  CAS  PubMed  Google Scholar 

  87. 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.

    Article  CAS  PubMed  Google Scholar 

  88. 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.

    Article  CAS  PubMed  Google Scholar 

  89. Hausman RH. Biology of Hydra. In: Burnett AL, ed. New York: Academic Press, 1973:393–453.

    Chapter  Google Scholar 

  90. Wood RL, Kuda AM. Formation of junctions in regenerating hydra: septate junctions. J Ultrastruct Res 1980; 70:104–117.

    Article  CAS  PubMed  Google Scholar 

  91. Favard P. Evolution des ultrastructures cellulaires au cours de la spermatogenese de l’. Ascaris. Ann Sci Nat Zool 1961; 21:53–152.

    Google Scholar 

  92. O’ Donovan P, Abraham M. Somatic tissue-male germ cell barrier in three hermaphrodite invertebrates: Dugesia biblica (Platyhelminthes), Placobdella costata (Annelida) and Levantina hierosolyma (Mollusca). J Morphol 1987; 192:217–227.

    Article  CAS  Google Scholar 

  93. 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.

    Article  CAS  PubMed  Google Scholar 

  94. 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.

    Article  PubMed  Google Scholar 

  95. Gilula NB, Fawcett DW, Aoki A. The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Dev Biol 1976; 50:142–168.

    Article  CAS  PubMed  Google Scholar 

  96. Franchi E, Camatini M, DeCurtis I. Morphological evidence of a permeability barrier in urodele testis. J Ultrastruct Res 1982; 80:253–263.

    Article  CAS  PubMed  Google Scholar 

  97. 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.

    Article  CAS  PubMed  Google Scholar 

  98. 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.

    Article  CAS  PubMed  Google Scholar 

  99. Baccetti B, Bigliardi E, Talluri MV et al. The Sertoli cell in lizards. J Ultrastruct Res 1983; 85:11–23.

    Article  CAS  PubMed  Google Scholar 

  100. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Osman DI, Elwall H, Plõen L. Specialized cell contacts and the blood-testis barrier in the seminiferous tubules of the domestic fowl (Gallus domesticus). Int J Androl 1980; 3:553–562.

    Article  CAS  PubMed  Google Scholar 

  102. Dym M, Cavicchia JC. Further observations on the blood testis barrier in monkeys. Biol Reprod 1977; 17:390–403.

    Article  CAS  PubMed  Google Scholar 

  103. Dym M, Cavicchia JC. Functional morphology of the testis. Biol Reprod 1978; 18:1–5.

    Article  CAS  PubMed  Google Scholar 

  104. Johnson MH, Setchell BP. Protein and immunoglobulin content of rete testis fluid of rams. J Reprod Fertil 1968; 17:403–406.

    Article  PubMed  Google Scholar 

  105. 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.

    Article  CAS  PubMed  Google Scholar 

  106. Dym M, Romrell LJ. Intraepithelial lymphocytes in the male reproductive tract of rats and rhesus monkeys. J Reprod Fertil 1975; 42:1–7.

    Article  CAS  PubMed  Google Scholar 

  107. 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. Biol Reprod 1994; 51:551–561.

    Article  CAS  PubMed  Google Scholar 

  108. Rival C, Lustig L, Iosub R et al. Identification of a dendritic cell population in normal testis and in chronically inflamed testis of rats with autoimmune orchitis. Cell Tissue Res 2006; 324:311–318.

    Article  PubMed  Google Scholar 

  109. 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.

    Article  CAS  Google Scholar 

  110. Tung KSK, Unanue ER, Dixon FJ. Pathogenesis of experimental allergic orchitis. II. The role of antibody. J Immunol 1971; 106:1463–1472.

    CAS  PubMed  Google Scholar 

  111. Yule TD, Montoya GD, Russell LD et al. Autoantigenic germ cells exist outside the blood-testis barrier. J Immunol 1988; 141:1161–1167.

    CAS  PubMed  Google Scholar 

  112. 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.

    Article  CAS  PubMed  Google Scholar 

  113. Marsh JA, O’Hern 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 Immunol 1981; 126:100–106.

    CAS  PubMed  Google Scholar 

  114. Yule TD, Mahi-Brown CA, Tung KS. Role of testicular autoantigens and influence of lymphokines in testicular autoimmune disease. J Reprod Immunol 1990; 18:89–103.

    Article  CAS  PubMed  Google Scholar 

  115. Barker CF, Billingham RE. Immunologically privileged sites. Adv Immunol 1977; 25:1–54.

    CAS  PubMed  Google Scholar 

  116. Setchell BP. The testis and tissue transplantation: historical aspects. J Reprod Immunol 1990; 18:1–8.

    Article  CAS  PubMed  Google Scholar 

  117. 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.

    Google Scholar 

  118. Head JR, Neaves WB, Billingham RE. Immune privilege in the testis. I. Basic parameters of allograft survival. Transplantation 1983; 36:423–431.

    Article  CAS  PubMed  Google Scholar 

  119. Dufour JM, Rajotte RV, Korbutt GS et al. Harnessing the immunomodulatory properties of Sertoli cells to enable xenotransplantation in type I diabetes. Immunol Invest 2003; 32:275–297.

    Article  CAS  PubMed  Google Scholar 

  120. Bobzien B, Yasunami Y, Majercik M et al. Intratesticular transplants of islet xenografts (rat to mouse). Diabetes 1983; 32:213–216.

    Article  CAS  PubMed  Google Scholar 

  121. Dobrinski I. Male germ cell transplantation. Reprod Dom Anim 2008; 43:288–294.

    Article  Google Scholar 

  122. Honaramooz A, Yang Y. Recent advances in applications of male germ cell transplantation in farm animals. Vet Med Int 2010; epub.

    Google Scholar 

  123. Brinster RL, Zimmerman JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 1994; 91:11298–11302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A 1994; 91:11303–11307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Ogawa T, Dobrinski I, Brinster RL. Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 1999; 31:461–471.

    Article  CAS  PubMed  Google Scholar 

  126. Kanatsu-Shinohara M, Ogonuki N, Inoue K et al. Allogeneic offspring produced by male germ line stem cell transplantation into infertile mouse testis. Biol Reprod 2003; 68:167–173.

    Article  CAS  PubMed  Google Scholar 

  127. Zhang Z, Renfree MB, Short RV. Successful intra-and interspecific male germ cell transplantation in the rat. Biol Reprod 2003; 68:961–967.

    Article  CAS  PubMed  Google Scholar 

  128. Honaramooz A, Megee SO, Dobrinski I. Germ cell transplantation in pigs. Biol Reprod 2002; 66:21–28.

    Article  CAS  PubMed  Google Scholar 

  129. 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 sperm defect. Reprod Dom Anim 2006; 41:124–128.

    Article  Google Scholar 

  130. Honaramooz A, Behboodi E, Blash S et al. Germ cell transplantation in goats. Mol Reprod Dev 2003; 64:422–428.

    Article  CAS  PubMed  Google Scholar 

  131. Honaramooz A, Behboodi E, Megee SO et al. Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. Biol Reprod 2003; 69:1260–1264.

    Article  CAS  PubMed  Google Scholar 

  132. Herrid M, Vignarajan S, Davey R et al. Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 2006; 132:617–624.

    Article  CAS  PubMed  Google Scholar 

  133. Kim Y, Turner D, Nelson J et al. Production of donor-derived sperm after spermatogonial stem cell transplantation in the dog. Reproduction 2008; 136:823–831.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Rodriguez-Sosa JR, Silvertown JD, Foster RA et al. Transduction and transplantation of spermatogonia into the testis of ram lambs through the extra-testicular rete. Reprod Dom Anim 2009; 44:612–620.

    Article  CAS  Google Scholar 

  135. Herrid M, Olejnik J, Jackson M et al. Irradiation enhances the efficiency of testicular germ cell transplantation in sheep. Biol Reprod 2009; 81:898–905.

    Article  CAS  PubMed  Google Scholar 

  136. Pollanen P, Soder O, Uksila J. Testicular immunosuppressive protein. J Reprod Immunol 1988; 14:125–138.

    Article  CAS  PubMed  Google Scholar 

  137. Pollanen P, von Euler M, Sainio-Pollanen S et al. Immunosuppressive activity in the rat seminiferous tubules. J Reprod Immunol 1992; 22:117–126.

    Article  CAS  PubMed  Google Scholar 

  138. 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.

    Article  CAS  PubMed  Google Scholar 

  139. De Cesaris P, Filippini A, Cervelli C et al. Immunosuppressive molecules produced by Sertoli cells cultured in vitro: biological effects on lymphocytes. Biochem Biophys Res Commun 1992; 186:1639–1646.

    Article  PubMed  Google Scholar 

  140. Wyatt CR, Law L, Magnuson JA et al. Suppression of lymphocyte proliferation by proteins secreted by cultured Sertoli cells. J Reprod Immunol 1988; 14:27–40.

    Article  CAS  PubMed  Google Scholar 

  141. Hedger MP, Qin JX, Robertson DM et al. Intragonadal regulation of immune system functions. Reprod Fertil Dev 1990; 2:263–280.

    Article  CAS  PubMed  Google Scholar 

  142. Hurtenbach U, Shearer GM. Germ cell-induced immune suppression in mice. Effect of inoculation of syngeneic spermatozoa on sell-mediated immune responses. J Exp Med 1982; 155:1719–1729.

    Article  CAS  PubMed  Google Scholar 

  143. Bryniarski K, Szczepanik M, Maresz K et al. Subpopulations of mouse testicular macrophages and their immunoregulatory function. Am J Reprod Immunol 2004; 52:27–35.

    Article  PubMed  Google Scholar 

  144. Mital P, Kaur G, Dufour JM. Immunoprotectivesertoli cells: making allogeneic and xenogeneic transplantation feasible. Reproduction 2010; 139:495–504.

    Article  CAS  PubMed  Google Scholar 

  145. Meinhardt A, Hedger MP. Immunological, paracrine and endocrine aspects of testicular immune privilege. Mol Cell Endocrinol published 2010; PMID:20363290.

    Google Scholar 

  146. Guazzone VA, Jacobo P, Theas MS et al. Cytokines and chemokines in testicular inflammation: A brief review 2009; 72:620–628.

    CAS  Google Scholar 

  147. Hedger MP, Meinhardt A. Cytokines and the immune-testicular axis. J Reprod Immunol 2003; 58:1–26.

    Article  CAS  PubMed  Google Scholar 

  148. 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.

    Article  CAS  PubMed  Google Scholar 

  149. Nasr IW, Wang Y, Gao G et al. Testicular immune privilege promotes transplantation tolerance by altering the balance between memory and regulatory T-cells. J Immunol 2005; 174:6161–6168.

    Article  CAS  PubMed  Google Scholar 

  150. Hedger MP. Macrophages and the immune responsiveness of the testis. J Reprod Immunol 2002; 57:19–34.

    Article  CAS  PubMed  Google Scholar 

  151. Rival C, Guazzone VA, von Wulffen W et al. Expression of costimulatory molecules, chemokine receptors and proinflammatory cytokines in dendritic cells from normal and chronically inflamed rat testis. Mol Hum Reprod 2007; 13:853–861.

    Article  CAS  PubMed  Google Scholar 

  152. Selawry HP, Whittington K. Extended allograft survival of islets grafted into intra-abdominally placed testis. Diabetes 1984; 33:405–406.

    Article  CAS  PubMed  Google Scholar 

  153. Selawry HP, Whittington KB. Prolonged intratesticular islet graft survival is not dependent on local steriodogenesis. Horm Metab Res 1988; 20:562–565.

    Article  CAS  PubMed  Google Scholar 

  154. Cameron DF, Whittington K, Schultz RE et al. Successful islet/abdominal testis transplantation does not require Leydig cells. Transplantation 1990; 50:649–653.

    Article  CAS  PubMed  Google Scholar 

  155. 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.

    Article  PubMed  Google Scholar 

  156. Whitmore WF 3rd, Gittes RF. Intratesticular grafts: the testis as an exceptional immunologically privileged site. Trans Am Assoc Genitourin Surg 1978; 70:76–80.

    CAS  PubMed  Google Scholar 

  157. Head JR, Billingham RE. Immune privilege in the testis. II. Evaluation of potential local factors. Transplantation 1985; 40:269–275.

    Article  CAS  PubMed  Google Scholar 

  158. Selawry HP, Cameron DF. Sertoli cell-enriched fractions in successful islet celltransplantation. Cell Transplant 1993; 2:123–129.

    Article  CAS  PubMed  Google Scholar 

  159. 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.

    Article  CAS  PubMed  Google Scholar 

  160. 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.

    Article  PubMed  Google Scholar 

  161. 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.

    Article  PubMed  Google Scholar 

  162. Fijak M, Meinhardt A. The testis in immune privilege. Immunol Rev 2006; 213:66–81.

    Article  CAS  PubMed  Google Scholar 

  163. Skinner MK. Sertoli cell-somatic cell interactions. In: Skinner MK, Griswold MD, eds. Sertoli cell biology. San Diego: 6Elsevier Academic Press, 2005:317–328.

    Chapter  Google Scholar 

  164. Shamekh R, El-Badri NS, Saporta S et al. Sertoli cells induce systemic donor-specific tolerance in xenogenic transplantation model. Cell Transplant 2006; 15:45–53.

    Article  CAS  PubMed  Google Scholar 

  165. Dym M, Romrell LJ. Intraepithelial lymphocytes in the male reproductive tract of rats and rhesus monkeys. J Reprod Fertil 1975; 42:1–7.

    Article  CAS  PubMed  Google Scholar 

  166. 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. Biol Reprod 1999; 61:705–714.

    Article  CAS  PubMed  Google Scholar 

  167. 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.

    Article  CAS  PubMed  Google Scholar 

  168. Yeung CH, Bergmann M, Cooper TG. Non-specific uptake of IgG by rat epididymal tubules in vitro. Int J Androl 1991; 14:364–373.

    Article  CAS  PubMed  Google Scholar 

  169. Knee RA, Hickey DK, Beagley KW et al. Transport of IgG 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. Biol Reprod 2005; 73:688–694.

    Article  CAS  PubMed  Google Scholar 

  170. Beagley KW, Wu ZL, Pomering M et al. Immune responses in the epididymis: implications for immunocontraception. J Reprod Fertil Suppl 1998; 53:235–245.

    CAS  PubMed  Google Scholar 

  171. Itoh 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.

    Article  CAS  PubMed  Google Scholar 

  172. Itoh 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 Cytol 1995; 58:575–579.

    Article  CAS  PubMed  Google Scholar 

  173. Kazeem AA. A critical consideration of the rat epididymis as an immunologically privileged site. Scand J Immunol 1988; 27:149–156.

    Article  CAS  PubMed  Google Scholar 

  174. Pollanen P, Cooper TG. Immunology of the testicular excurrent ducts. J Reprod Immunol 1994; 26:167–216.

    Article  CAS  PubMed  Google Scholar 

  175. Da Silva N, Cortez-Retamozo V, Reinecker HC et al. A dense network of dendritic cells populates the murine epididymis. Reproduction 2011; in press.

    Google Scholar 

  176. Wheeler K, Tardiff S, Rival C et al. Regulatory T cells determine tolerogenic versus autoimmune response to sperm in vasectomized mice. PNAS 2011; in press.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Morphology, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil

    Luiz R. França & Sarah A. Auharek

  2. Department of Comparative Biosciences, University of Illinois, Urbana, Illinois, USA

    Rex A. Hess

  3. Department of Cell Biology and Biochemistry, Texas Tech University Health Sciences Center, Lubbock, Texas, USA

    Jannette M. Dufour

  4. Department of Cell Biology, University of Virginia School of Medicine, Charlottesville, Virginia, USA

    Barry T. Hinton

Authors
  1. Luiz R. França
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah A. Auharek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rex A. Hess
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jannette M. Dufour
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Barry T. Hinton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luiz R. França .

Editor information

Editors and Affiliations

  1. Center for Biomedical Research, Population Council, New York, New York, USA

    C. Yan Cheng PhD

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

França, L.R., Auharek, S.A., Hess, R.A., Dufour, J.M., Hinton, B.T. (2013). Blood-Tissue Barriers. In: Cheng, C.Y. (eds) Biology and Regulation of Blood-Tissue Barriers. Advances in Experimental Medicine and Biology, vol 763. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4711-5_12

Download citation

Publish with us

Policies and ethics

Search

Navigation