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Sertoli Cell Proteins in Testicular Paracriny

  • D. D. Mruk
  • C. Yan Cheng
Conference paper
Part of the Ernst Schering Research Foundation Workshop book series (SCHERING FOUND, volume 6)

Abstract

Sertoli cells are the irregular-shaped columnar cells in the testis which occupy about 17–19% of the total volume of the seminiferous epithelium in the rat. They extend from the basal to the adluminal compartment of the seminiferous epithelium covering an enormous surface area (for reviews, see Bardin et al., 1988; de Kretser and Kerr, 1988; Jégou, 1993). Due to this unique morphological feature, a single Sertoli cell in the adult rat testis has direct contact with approximately 30–50 germ cells in different stages of development (Russell et al., 1983; Weber et al.,1983; Wong and Russell, 1983) via either anchoring junctions (AJ), communicating gap junctions (GJ) or other cellular modifications such as ectoplasmic specializations, an anchoring-like junction, present between elongate spermatids and Sertoli cells. They are also the only somatic cell type in the testis having direct physical contacts and interactions with developing germ cells behind the blood-testis barrier formed by adjacent inter-Sertoli tight junctions (TJ) (except spermatogonia residing outside of the blood-testis barrier in the rat) (for reviews, see de Kretser and Kerr, 1988; Jégou, 1993; Bardin et al., 1988) (Fig. 1). In addition, this barrier also creates a unique microenvironment in which spermatogenesis takes place since virtually all stages of germ cell development, except the mitotic division of spermatogonia and differentiation of type B spermatogonia into preleptotene spermatocytes, are segregated from the systemic circulation. At the basal compartment of the seminiferous epithelium, Sertoli cells also have physical contacts with peritubular myoid cells and have indirect access to cells in the interstitium such as Leydig cells with which interactions occur via paracrine factors. As such, Sertoli cells interact with germ, Leydig, and peritubular myoid cells biochemically via paracrine factors produced by Sertoli cells in addition to the physical contacts between these cells. Moreover, recent studies have demonstrated that paracrine factors released by germ or peritubular myoid cells can also regulate Sertoli cell and testicular functions illustrating the existence of a two-way trafficking between these cells. Since several reviews can be found in the literature dealing with this subject area (see Skinner, 1991; Skinner, 1993; Griswold, 1993; Jégou and Sharpe, 1993), we will limit our discussion in this mini-review on the recent advancements in studying the paracrine regulation of testicular functions via factors produced by Sertoli cells in particular their roles in regulating the turnover of TJ, AJ, and GJ during the process of germ cell movement throughout spermatogenesis.

Fig. 1

Fig. 1. Cross-section of a seminiferous tubule from an adult rat showing the intimate morphological relationships between Sertoli cells and germ cells at different stages of their development. S, Sertoli cell nucleus; sg, spermatogonium; sp, spermatocyte; rs, round spermatid; es, elongate spermatid. (Courtesy of Dr. Li-ji Zhu)

Keywords

Germ Cell Sertoli Cell Leydig Cell Seminiferous Epithelium Inducible cAMP Early Repressor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Ailenberg M, Stetler-Stevenson WG, Fritz IB (1991) Secretion of latent type IV procollagenase and active type IV collagenase by testicular cells in culture. Biochem J 279: 75–80PubMedGoogle Scholar
  2. Anderson RA, Evans LW, Irvine DS, McIntyre MA, Groome NP, Riley SC (1998) Follistatin and activin A production by the male reproductive tract. Human Reprod 13: 3319–3325CrossRefGoogle Scholar
  3. Armstrong DT, Moon YS, Fritz IB, Dorrington JH (1975) Synthesis of estradiol-1713 by Sertoli cells in culture: stimulation by FSH and dibutryl cyclic AMP. Curr Top Mol Endocrinol 2: 85–96PubMedGoogle Scholar
  4. Avallet O, Vigier M, Leduque P, Dubois PM, Saez JM (1994) Expression and regulation of transforming growth factor-131 messenger ribonucleic acid and protein in cultured porcine Leydig and Sertoli cells. Endocrinology 134: 2079–2087PubMedCrossRefGoogle Scholar
  5. Avallet D, Vigier M, Perrard-Sapori MH, Saez JM (1987) Transforming growth factor beta inhibits Leydig cell functions. Biochem Biophys Res Commun 146: 575–581PubMedCrossRefGoogle Scholar
  6. Balda MS, Gonzalez-Mariscal L, Contreras RG, Macias-Silva M, Tones-Marquez ME, Garcia Sainz JA, Cereijido M (1991) Assembly and sealing of tight junctions: possible participation of G-proteins, phospholipase C, protein kinase C and calmodulin. J Membrane Biol 122: 193–202CrossRefGoogle Scholar
  7. Bardin CW, Cheng CY, Musto NA, Gunsalus GL (1988) The Sertoli cell. In: The Physiology of Reproduction. Vol 1. Eds. Knobil E, Neill JD, Ewing LL, Greenwald GS, Markert CL and Pfaff DW. New York, Raven Press, pp. 933–974Google Scholar
  8. Besset V, Le Magueresse-Battistoni B, Collette J, Benahmed M (1996) Tumor necrosis factor-oc stimulates insulin-like growth factor binding protein 3 expression in cultured porcine Sertoli cells. Endocrinology 137: 296–303PubMedCrossRefGoogle Scholar
  9. Beumer TL, Kiyokawa H, Roepers-Gajadien HL, Van der Bos LA, Lock TM, Gademan IS, Rutgers DH, Koof A, De Rooij DG (1999) Regulatory role of p27kipl in the mouse and human testis. Endocrinology 140: 1834–1840PubMedCrossRefGoogle Scholar
  10. Bhat KG, Malhotra P, Karande AA, Adiga PR (1995) Immunohistochemical localization of riboflavin carrier protein in testicular cells of mammals. Indian J Exp Biol 33: 12–16PubMedGoogle Scholar
  11. Blok LJ, Hoogerbrugge JW, Themmen AP, Baarends WM, Post M, Grootegoed JA (1992) Transient down-regulation of androgen receptor messenger ribonucleic acid (mRNA) expression in Sertoli cells by follicle stimulating hormone is followed by up-regulation of androgen receptor mRNA and protein. Endocrinology 131: 1343–1349PubMedCrossRefGoogle Scholar
  12. Blok LJ, Mackenbach P, Trapman J, Themmen AP, Brinkmann AO, Grootegoed JA (1989) Follicle stimulating hormone regulates androgen receptor mRNA in Sertoli cells. Mol Cell Endocrinol 63: 267–271PubMedCrossRefGoogle Scholar
  13. Boockfor FR, Morris RA, De Simone DC, Hunt DM, Walsh KB (1998) Sertoli cell expression of the cystic fibrosis transmembrane conductance regulator. Am J Physiol 274: C922–930PubMedGoogle Scholar
  14. Boujrad N, Ogwuegbu SO, Gamier M, Lee CH, Martin BM, Papadopoulos V (1995) Identification of a stimulator of steroid hormone synthesis isolated from testis. Science 268: 1609–1612PubMedCrossRefGoogle Scholar
  15. Bourdon V, Defamie N, Fenichel P, Pointis G (1999) Regulation of tissue-type plasminogen activator and its inhibitor (PAI-1) by lipopolysaccharide-induced phagocytosis in a Sertoli cell line. Exp Cell Res 247: 367–372PubMedCrossRefGoogle Scholar
  16. Bourdon V, Lablack A, Abbe P, Segretain D, Pointis G (1998) Characterization of a clonal Sertoli cell line using adult PyLT transgenic mice. Biol Reprod 58: 591–599PubMedCrossRefGoogle Scholar
  17. Boussouar F, Grataroli R, Ji J, Benahmed M (1999) Tumor necrosis factor-y stimulates lactate dehydrogenase A expression in porcine cultured Sertoli cells: mechanisms of action. Endocrinology 140: 3054–3062PubMedCrossRefGoogle Scholar
  18. Braghiroli L, Silvestrini B, Sorrentino C, Grima J, Mruk D, Cheng CY (1998) Regulation of a2-macroglobulin expression in rat Sertoli cells and hepatocytes by germ cells in vitro. Biol Reprod 59: 111–123PubMedCrossRefGoogle Scholar
  19. Byers S, Graham R, Dai HN, Hoxter B (1991) Development of Sertoli cell junctional specializations and the distribution of the tight-junction associated protein ZO-1 in the mouse testis. Am J Anat 191: 35–47PubMedCrossRefGoogle Scholar
  20. Byers SW, Sujarit S, Jégou B, Butz S, Hoschutzky H, Herrenknecht K, MacCalman C, Blaschuk OW (1994) Cadherins and cadherin-associated molecules in the developing and maturing rat testis. Endocrinology 134: 630–639PubMedCrossRefGoogle Scholar
  21. Cameron DF, Muffly KE (1991) Hormonal regulation of spermatid binding. J Cell Sci 100: 623–633PubMedGoogle Scholar
  22. Cancilla B, Risbridger GP (1998) Differential localization of fibroblast growth factor receptor-1, -2, -3, and —4 in fetal, immature, and adult rat testes. Biol Reprod 58: 1138–1145PubMedCrossRefGoogle Scholar
  23. Carreau S, Genissel C, Bilinska B, Levallet J (1999) Sources of oestrogen in the testis and reproductive tract of the male. Int J Androl 22: 211–223PubMedCrossRefGoogle Scholar
  24. Castellon EA (1999) Influence of age, hormones, and germ cells on glutathione S-transferase activity in cultured Sertoli cells. Int J Androl 22: 49–55PubMedCrossRefGoogle Scholar
  25. Chaudhary J, Skinner MK (1999) E-box and cyclic adenosine monophosphate response elements are both required for follicle stimulating hormone-induced transferrin promoter activation in Sertoli cells. Endocrinology 140: 1262–1271PubMedCrossRefGoogle Scholar
  26. Chen Y, Dicou E, Djakiew D (1997) Characterization of nerve growth factor precursor protein expression in rat round spermatids and the trophic effects of nerve growth factor in the maintenance of Sertoli cell viability. Mol Cell Endocrinol 127: 129–136PubMedCrossRefGoogle Scholar
  27. Cheng CY, Bardin CW (1986) Rat testicular testibumin is a protein responsive to follicle stimulating hormone and testosterone that shares immunodeterminants with albumin. Biochemistry 25: 5276–5288PubMedCrossRefGoogle Scholar
  28. Cheng CY, Grima J, Stahler MS, Guglielmotti A, Silvestrini B, Bardin CW (1990) Sertoli cell synthesizes and secretes a protease inhibitor, a2-macroglobulin. Biochemistry 29: 1063–1068PubMedCrossRefGoogle Scholar
  29. Cheng CY, Grima J, Stahler MS, Lockshin RA, Bardin CW (1989) Testins are structurally related Sertoli cell proteins whose secretion is tightly coupled to the presence of germ cells. J Biol Chem 264: 21386–21393PubMedGoogle Scholar
  30. Cheng CY, Mathur PP, Grima J (1988) Structural analysis of clusterin and its subunits in ram rete testis fluid. Biochemistry 27: 4079–4088PubMedCrossRefGoogle Scholar
  31. Cheng CY, Morris PL, Mathur PP, Marshall A, Grima J, Turner TT, Carreau S, Tung KSK, Bardin CW (1988) Identification of a factor in fractions of Sertoli cell enriched culture medium containing CMB-21 that stimulates androgen production by Leydig cells. In: Nonsteroidal Gonadal Factors: Physiological Roles and Possibilities in Contraceptive Development. Eds. Hodgen G, Rosenwachs Z, Speiler J. Norfolk, Jones Institute Press, pp. 192–201Google Scholar
  32. Cheng CY, Morris PL, Zwain I, Carreau S, Drosdowsky MA, Bardin CW (1993) A Leydig cell stimulator from Sertoli cells. In: Sexual Precocity. Etiology, Diagnosis, and Management. Eds. Grave GD, Cutler GB. New York, Raven Press, pp. 221–227Google Scholar
  33. Chung SSW, Lee WM, Cheng CY (1999b) A study on the formation of spe- cialized inter-Sertoli cell junctions in vitro. J Cell Physiol 181: 258–272PubMedCrossRefGoogle Scholar
  34. Chung SSW, Mo MY, Silvestrini B, Lee WM, Cheng CY (1998a) Rat testicular N-cadherin: its complementary deoxyribonucleic acid cloning and regulation. Endocrinology 139: 1853–1862PubMedCrossRefGoogle Scholar
  35. Chung SSW, Mruk D, Lee WM, Cheng CY (1999a) Identification and purification of proteins from germ cell-conditioned medium. Biochem Mol Biol Int 47: 479–491PubMedGoogle Scholar
  36. Chung SSW, Zhu L-J, Mo MY, Silvestrini B, Lee WM, Cheng CY (1998b) Evidence for cross-talk between Sertoli and germ cells using selected cathepsins as markers. J Androl 19: 686–703PubMedGoogle Scholar
  37. Collard MW, Day R, Akil H, Uhler MD, Douglass JO (1990) Sertoli cells are the primary site of prodynorphin gene expression in rat testis: regulation of mRNA and secreted peptide levels by cyclic adenosine 3’,5’-monophosphate analogs in cultured cells. Mol Endocrinol Metab 72: 1332–1339Google Scholar
  38. Cunningham DB, Segretain D, Arnaud D, Rogner UC, Avner P (1998) The mouse Tsx gene is expressed in Sertoli cells of the adult testis and transiently in premeiotic germ cells during puberty. Dev Biol 15: 345–360CrossRefGoogle Scholar
  39. Cyr DG, Hermo L, Egenberger N, Mertineit C, Trasler JM, Laird DW (1999) Cellular immunolocalization of occludin during embryonic and postnatal development of the mouse testis and epididymis. Endocrinology 140: 3815–3825PubMedCrossRefGoogle Scholar
  40. Davidoff MS, Middendorff R, Pusch W, Muller D, Wichers S, Holstein AF (1999) Sertoli and Leydig cells of the human testis express neurofilament triplet proteins. Histochem Cell Biol 111: 173–187PubMedCrossRefGoogle Scholar
  41. De Cesaris P, Starace D, Ricciolo A, Padula F, Filippini A, Ziparo E (1998) Tumor necrosis factor-a induces interleukin-6 production and integrin expression by distinct transduction pathways. J Biol Chem 273: 7566–7571PubMedCrossRefGoogle Scholar
  42. Dejucq N, Dugast I, Ruffault A, Van der Meide PH, Jégou B (1995) Interferon-a and -y expression in the rat testis. Endocrinology 136: 4925–4931PubMedCrossRefGoogle Scholar
  43. Dejucq N, Lienard MO, Guillaume E, Dorval I, Jégou B (1998) Expression of interferons-a and -y in testicular interstitial tissue and spermatogonia of the rat. Endocrinology 139: 3081–3087PubMedCrossRefGoogle Scholar
  44. de Kretser DM, Kerr JB (1988) The cytology of the testis. In: The Physiology of Reproduction. Vol 1. Eds. Knobil E and Neill J. New York, Raven Press, pp. 837–932Google Scholar
  45. Delfino F, Walker WH (1998) Stage-specific nuclear expression of NF-13 in mammalian testis. Mol Endocrinol 12: 1696–1707PubMedCrossRefGoogle Scholar
  46. Dorrington JH, Armstrong DT (1975) Follicle-stimulating hormone stimulates estradiol-143 synthesis in cultured Sertoli cells. Proc Natl Acad Sci USA 72: 2677–2681PubMedCrossRefGoogle Scholar
  47. Dutertre M, Rey R, Porteu A, Josso N, Picard JY (1997) A mouse Sertoli cell line expressing anti-Mullerian hormone and its type II receptor. Mol Cell Endocrinol 136: 57–65PubMedCrossRefGoogle Scholar
  48. Dym M, Lamsam-Casalotti S, Jia MC, Kelinman HK, Padadopoulos V (1991) Basement membrane increases G-protein levels and follicle stimulating hormone responsiveness of Sertoli cell adenylyl cyclase activity. Endocrinology 128: 1167–1176PubMedCrossRefGoogle Scholar
  49. Eikvar L, Levy FO, Attramadal H, Jutte NH, Froysa A, Tvermyr SM, Hansson V (1985) Glucagon-stimulated cyclic AMP production and formation of estradiol in Sertoli cell cultures from immature rats. Mol Cell Endocrinol 39: 107–113PubMedCrossRefGoogle Scholar
  50. Enders GC, Millette CF (1988) Pachytene spermatocyte and round spermatid binding to Sertoli cells in vitro. J Cell Sci 90: 105–114PubMedGoogle Scholar
  51. Ergun S, Harneit S, Paust HJ, Mukhopadhyay AK, Holstein AF (1998) Endothelin and endothelin receptors A and B in the human testis. Anat Embryo] (Berl) 199: 207–214Google Scholar
  52. Eskild W, Ree AH, Levy FO, Jahnsen T, Hansson V (1991) Cellular localization of mRNAs for retinoic acid receptor-a, cellular retinol-binding protein, and cellular retinoic acid-binding protein in rat testis: evidence for germ cell-specific mRNA. Biol Reprod 44: 53–61PubMedCrossRefGoogle Scholar
  53. Esnard A, Esnard F, Guillou F, Gauthier F (1992) Production of the cysteine proteinase inhibitor cystatin C by rat Sertoli cells. FEBS Lett 300: 131–135PubMedCrossRefGoogle Scholar
  54. Feig LA, Bellve AR, Erickson NH, Klagsbrun M (1980) Mitogenic polypeptide of the mammalian seminiferous epithelium: biology of the seminiferous growth factor ( SGF ). Proc Natl Acad Sci USA 77: 4774–4778Google Scholar
  55. Feig LA, Klagsbrun M, Bellve AR (1983) Sertoli cells contain a mitogenic polypeptide. J Cell Biol 97: 1435–1443PubMedCrossRefGoogle Scholar
  56. Frayne J, Nicholson HD (1998) Localization of oxytocin receptors in the human and macaque monkey male reproductive tracts: evidence for a physiological role of oxytocin in the male. Mol Hum Reprod 4: 527–532PubMedCrossRefGoogle Scholar
  57. Fujisawa M, Bardin CW, Morris PL (1992) A germ cell factor(s) modulates preproenkephalin gene expression in rat Sertoli cells. Mol Cell Endocrinol 84: 79–88PubMedCrossRefGoogle Scholar
  58. Gaemers IC, Van Pelt AM, Van der Saag PT, Hoogerbrugge JW, Themmen AP, De Rooij DG (1998) Differential expression pattern of retinoid X receptors in adult murine testicular cells implies varying roles for these receptors in spermatogenesis. Biol Reprod 58: 1351–1356PubMedCrossRefGoogle Scholar
  59. Gérard N, Corlu A, Kneip B, Kercret H, Rissel M, Guguen-Guillouzo C, Jégou B (1995) Liver-regulating protein ( LRP) is a plasma membrane protein involved in cell contact mediated regulation of Sertoli cell function by primary spermatocytes. J Cell Sci 108: 917–925Google Scholar
  60. Grima J, Calcagno K, Cheng CY (1996) Purification, cDNA cloning, and developmental stages in the steady-state mRNA level of rat testicular tissue inhibitor of metalloproteases-2 (TIMP-2). J Androl 17: 263–275PubMedGoogle Scholar
  61. Grima J, Wong CCS, Zhu LJ, Zong SD, Cheng CY (1998) Testin secreted by Sertoli cells is associated with the cell surface, and its expression correlates with the disruption of Sertoli-germ cell junctions but not the inter-Sertoli cell junction. J Biol Chem 273: 21040–21053PubMedCrossRefGoogle Scholar
  62. Griswold MD (1993) Protein secretion by Sertoli cells: general considerations. In: The Sertoli Cell. Eds. Russell LD, Griswold MD. Clearwater, Cache River Press, pp 195–200Google Scholar
  63. Griswold MD (1995) Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 52: 211–216PubMedCrossRefGoogle Scholar
  64. Guillaumot P, Benahmed M (1999) Prolactin receptors are expressed and hor- monally regulated in rat Sertoli cells. Mol Cell Endocrinol 149: 163–168PubMedCrossRefGoogle Scholar
  65. Gustafsson K, Söder O, Pollanen P, Ritzén EM (1985) Isolation and partial characterization of an interleukin- 1-like factor from rat testis interstitial fluid. J Reprod Immunol 14: 139–150CrossRefGoogle Scholar
  66. Guttman JA, Mulholland DJ, Vogl AW (1999) Plectin is a concentrated at intercellular junctions and at the nuclear surface in morphologically differentiated rat Sertoli cells. Anat Rec 254: 418–428PubMedCrossRefGoogle Scholar
  67. Hadley MA, Weeks BS, Kleinman HK, Dym M (1990) Laminin promotes formation of cord-like structures by Sertoli cells in vitro. Dev Biol 140: 318–327PubMedCrossRefGoogle Scholar
  68. Hagenäs L, Ritzén EM, Ploön L, Hansson V, French FS, Nayfeh SN (1975) Sertoli cell origin of testicular androgen binding protein ( ABP ). Mol Cell Endocrinol 2: 339–350Google Scholar
  69. Hakovirta H, Yan W, Kaleva M, Zhang F, Vanttinen K, Morris PL, Söder M, Parvinen M, Toppari J. (1999) Function of stem cell factor as a survival factor of spermatogonia and localization of messenger ribonucleic acid in the rat seminiferous epithelium. Endocrinology 140: 1492–1498PubMedCrossRefGoogle Scholar
  70. Hall PF (1988) Testicular steroid synthesis: organization and regulation. In: The Physiology of Reproduction. Vol I. Eds. Knobil E, Neil JD. New York, Raven Press, pp 975–998Google Scholar
  71. Hall SH, Conti M, French FS, Joseph DR (1990) Follicle-stimulating hormone regulation of androgen-binding protein messenger RNA in Sertoli cell cultures. Mol Endocrinol 4: 349–355PubMedCrossRefGoogle Scholar
  72. Howe CC, Overton GC, Sawicki J, Softer D, Stein P, Strickland S (1988) Expression of SPARC/osteonectin transcript in murine embryos and gonads. Differentiation 37: 20–25PubMedCrossRefGoogle Scholar
  73. Huggenvik J, Griswold MD (1981) Retinol binding protein in rat testicular cells. J Reprod Fertil 61: 403–408PubMedCrossRefGoogle Scholar
  74. Igdoura SA, Rasky A, Morales CR (1996) Trafficking of sulfated glycoprotein-1 (prosaposin) to lysosomes or to the extracellular space in rat Sertoli cells. Cell Tissue Res 283: 385–394PubMedCrossRefGoogle Scholar
  75. Ito E, Toki T, Ishihara H, Ohtani H, Gu L, Yokoyama M, Engel JD, Yamamoto M (1993) Erythroid transcription factor GATA-1 is abundantly transcribed in mouse testis. Nature 362: 466–468PubMedCrossRefGoogle Scholar
  76. Ivell R, Balvers M, Rust W, Bathgate R, Einspanier A (1997) Oxytocin and male reproductive function. Adv Exp Med Biol 424: 253–264PubMedCrossRefGoogle Scholar
  77. Jaillard C, Chatelain PG, Saez JM (1987) In vitro regulation of pig Sertoli cell growth and function: effects of fibroblast growth factors and somatomedinc. Biol Reprod 37: 665–674PubMedCrossRefGoogle Scholar
  78. Jégou B (1993) The Sertoli-germ cell communication network in mammals. Int Rev Cytol 147: 25–96PubMedCrossRefGoogle Scholar
  79. Jégou B, Sharpe RM (1993) Paracrine mechanisms in testicular control. In: Molecular Biology of the Male Reproductive System. Eds. de Kretser DM. New York, Academic Press, pp 274–322Google Scholar
  80. Jenab S, Morris PL (1996) Differential activation of signal transducer and activator of transcription (STAT)-3 and STAT-1 transcription factors and c-fos messenger ribonucleic acid by interleukin-6 and interferon-yin Sertoli cells. Endocrinology 137: 4738–4743PubMedCrossRefGoogle Scholar
  81. Jenab S, Morris PL (1997) Transcriptional regulation of Sertoli cell immediate early genes by interleukin-6 and interferon-g is mediated through phosphorylation of STAT-3 and STAT-1 proteins. Endocrinology 138: 2740–2746PubMedCrossRefGoogle Scholar
  82. Jenab S, Morris PL (1998) Testicular and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells. Endocrinology 139: 1883–1890.PubMedCrossRefGoogle Scholar
  83. Jiang C, Hall SJ, Boekelheide K (1997) Cloning and characterization of the 5’ flanking region of the stem cell factor gene in rat Sertoli cells. Gene 185: 285–290PubMedCrossRefGoogle Scholar
  84. Jonsson CK, Zetterstrom RH, Holst M, Parvinen M, Söder 0 (1999) Constitutive expression of interleukin-la messenger ribonucleic acid in rat Sertoli cells is dependent upon interaction with germ cells. Endocrinology 140: 3755–3761Google Scholar
  85. Kaipia A, Penttila TL, Shimasaki S, Ling N, Parvinen M, Toppari J (1992) Expression of inhibin (3A and 13a, follistatin, and activin A receptor messenger ribonucleic acids in the rat seminiferous epithelium. Endocrinology 131: 2703–2710PubMedCrossRefGoogle Scholar
  86. Kanzaki M, Fujisawa M, Okuda Y, Okada H, Arakawa S, Kamidono S (1996) Expression and regulation of neuropeptide Y messenger ribonucleic acid in cultured immature rat Leydig and Sertoli cells. Endocrinology 137: 1249–1257PubMedCrossRefGoogle Scholar
  87. Kanzaki M, Morris PL (1998) Identification and regulation of testicular interferon-y (INF-y) receptor subunits: INF-y enhances interferon regulatory factor-1 and interleukin-1(3 converting enzyme expression. Endocrinology 139: 2636–2644PubMedCrossRefGoogle Scholar
  88. Kent J, Wheatley SC, Andrews JE, Sinclair AH, Koopman P (1996) A male-specific role for SOX9 in vertebrate sex determination. Development 122: 2813–2822PubMedGoogle Scholar
  89. Keon BH, Schafer S, Kuhn C, Grund C, Franke WW (1996) Symplekin, a novel type of tight junction plaque protein. J Cell Biol 134: 1003–1018PubMedCrossRefGoogle Scholar
  90. Khan SA, Mirsafian M, Howdeshell K, Dorrington JH (1999) Transforming growth factor-beta inhibits DNA synthesis in immature rat Leydig cells in vitro. Mol Cell Endocrinol 148: 21–28PubMedCrossRefGoogle Scholar
  91. Khan SA, Schmidt K, Hallin P, DiPauli R, DeGeyter C, Nieschlag E (1988) Human testis cytosol and ovarian follicular fluid contain high amounts of interleukin-1-like factor(s). Mol Cell Endocrinol 58: 221–230PubMedCrossRefGoogle Scholar
  92. Kierszenbaum AL, Feldman M, Lea 0, Spruill WA, Tres LL, Petrusz P, French FS (1980) Localization of androgen-binding protein in proliferating Sertoli cells in culture. Proc Natl Acad Sci USA 77: 5322–5326PubMedCrossRefGoogle Scholar
  93. Kim KH, Wright WW (1997) A comparison of the effects of testicular maturation and aging on the stage-specific expression of CP-2/cathepsin L messenger ribonucleic acid by Sertoli cells of the Brown Norway rat. Biol Re-prod 57: 167–1477Google Scholar
  94. Kissell K, Hamm S, Schulz M, Vecchi A, Garlanda C, Engelhardt B (1998) Immunohistochemical localization of the murine transferrin receptor ( TfR) on blood-tissue barriers using a novel anti-TfR monoclonal antibody. Histochem Cell Biol 110: 63–72Google Scholar
  95. Klaij IA, Timmerman MA, Blok LJ, Grootegoed JA, De Jong FH (1992) Regulation of inhibin-(3B subunit mRNA expression in rat Sertoli cells: consequences for the production of bioactive and immunoreactive inhibin. Mol Cell Endocrinol 85: 237–246PubMedCrossRefGoogle Scholar
  96. Klaij IA, Tosbosch AM, Themmen AP, Shimasaki S, De Jong FH, Grootegoed JA (1990) Regulation of inhibin-a and -f3 B subunit mRNA levels in rat Sertoli cells. Mol Cell Endocrinol 68: 45–52PubMedCrossRefGoogle Scholar
  97. Lacroix M, Fritz IB. (1982) The control of the synthesis and secretion of plasminogen activator by rat Sertoli cells in culture. Mol Cell Endocrinol 26: 247–258PubMedCrossRefGoogle Scholar
  98. Lamb DJ (1993) Growth factors and testicular development. J Urol 150: 583–592PubMedGoogle Scholar
  99. Lamb DJ, Spotts GS, Shubhada S, Baker KR (1991) Partial characterization of a unique mitogenic activity secreted by rat Sertoli cells. Mol Cell Endocrinol 79: 1–12PubMedCrossRefGoogle Scholar
  100. Lee J, Richburg JH, Shipp EB, Meistrich ML, Boekelheide K (1999) The Fas system, a regulator of testicular germ cell apoptosis, is differentially up-regulated in Sertoli cell versus gem cell injury of the testis. Endocrinology 140: 852–858PubMedCrossRefGoogle Scholar
  101. Le Magueresse-Battistoni B, Morera AM, Goddard I, Benahmed M (1995) Expression of mRNAs for transforming growth factor-(3 receptors in the rat testis. Endocrinology 136: 2788–2791PubMedCrossRefGoogle Scholar
  102. Le Magueresse-Battistoni B, Pernod G, Sigillo F, Kolodie L, Benahmed M (1998) Plasminogen activator inhibitor-1 is expressed in cultured rat Sertoli cells. Biol Reprod 59: 591–598PubMedCrossRefGoogle Scholar
  103. Le Magueresse-Battistoni B, Wolff J, Morera AM, Benahmed M (1994) Fibroblast growth factor receptor type 1 expression during rat testicular development and its regulation in cultured Sertoli cells. Endocrinology 135: 2404–2411PubMedCrossRefGoogle Scholar
  104. Li LY, Seddon AP, Meister A, Risley MS (1989) Spermatogenic cell-somatic cell interactions are required for maintenance of spermatogenic cell glutathione. Biol Reprod 40: 317–331PubMedCrossRefGoogle Scholar
  105. Lim K, Hwang BD (1995) Follicle stimulating hormone transiently induces expression of proto-oncogene c-myc expression in primary Sertoli cell cultures from early pubertal and prepubertal rat. Mol Cell Endocrinol 28: 51–56CrossRefGoogle Scholar
  106. Lim K, Yoo JH, Kim KY, Kweon GR, Kwak ST, Hwang BD (1994) Testosterone regulation of proto-oncogene c-myc expression in primary Sertoli cell cultures from prepubertal rats. J Androl 15: 543–550PubMedGoogle Scholar
  107. Lin ML, DePhillip RM (1996) Sex-dependent expression of placental ( P)-cadherin during mouse gonadogenesis. Anat Rec 246: 535–544Google Scholar
  108. Lindsey JS, Wilkinson MF (1996) PEM: a testosterone-and LH regulated homeobox gene expressed in mouse Sertoli cells and epididymis. Dev Biol 179: 471–484PubMedCrossRefGoogle Scholar
  109. Loganzo F Jr, Fletcher PW (1992) Follicle stimulating hormone increases guanine nucleotide-binding regulatory protein subunit oti-3 mRNA but decreases ai-1 and a;-2 mRNA in Sertoli cells. Mol Endocrinol 6: 1259–1267PubMedCrossRefGoogle Scholar
  110. Madhubala R, Shubhada S, Steinberger A, Tsai YH (1987) Inhibition of orni-thine decarboxylase activity by follicle stimulating hormone in primary culture of rat Sertoli cells. J Androl 8: 383–387PubMedGoogle Scholar
  111. Maeda S, Nam SY, Fujisawa M, Nakamuta N, Ogawa K, Kurohmaru M, Hayashi Y (1998) Localization of cytoplasmic dynein light-intermediate chain mRNA in the rat testis using in situ hybridization. Cell Struct Funct 23: 9–15PubMedCrossRefGoogle Scholar
  112. Maguire SM, Tribley WA, Griswold MD (1997) Follicle stimulating hormone ( FSH) regulates the expression of FSH receptor messenger ribonucleic acid in cultured Sertoli cells and in hypophysectomized rat testis. Biol Reprod 56: 1106–1111Google Scholar
  113. Mathur PP, Grima J, Mo MY, Zhu Li, Aravindan GR, Calcagno K, O’Bryan M, Chung S, Mruk D, Lee WM, Silvestrini B, Cheng CY (1997) Differential expression of multiple cathepsin mRNAs in the rat testis during maturation and following lonidamine induced tissue restructuring. Biochem Mol Biol Int 42: 217–233PubMedGoogle Scholar
  114. McClure RF, Heppelmann CJ, Paya CV (1999) Constitutive Fas ligand gene transcription in Sertoli cells is regulated by Sp l. J Biol Chem 274: 7756–7762PubMedCrossRefGoogle Scholar
  115. Mead R, Hinchliffe SJ, Morgan BP (1999) Molecular cloning, expression and characterization of the rat analogue of human membrane cofactor protein. Immunology 98: 137–143PubMedCrossRefGoogle Scholar
  116. Means AR, Huckins C (1974) Coupled events in the early biochemical actions of FSH on the Sertoli cells of the testis. Curr Top Mol Endocrinol 1: 145–165PubMedGoogle Scholar
  117. Miller MG, Mulholland DJ, Vogl AW (1999) Rat testis motor proteins associated with spermatid translocation (dynein) and spermatid flagella (kinesin II). Biol Reprod 60: 1047–1056PubMedCrossRefGoogle Scholar
  118. Mita M, Hall PF (1982) Metabolism of round spermatids from rats: lactate as the preferred substrate. Biol Reprod 26: 445–455PubMedCrossRefGoogle Scholar
  119. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R (1996) SOX9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 14: 62–68CrossRefGoogle Scholar
  120. Morena AR, Boitani C, De Grossi S, Stefanini M, Conti M (1995) Stage and cell-specific expression of the adenosine 3’,5’-monophosphate-phosphodiesterase genes in the rat seminiferous epithelium. Endocrinology 136: 687–695PubMedCrossRefGoogle Scholar
  121. Morita K, Sasaki H, Fujimoto K, Furuse M, Tsukita S (1999) Claudin 11/OSPbased tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 145: 579–588PubMedCrossRefGoogle Scholar
  122. Mruk D, Cheng CY (1999) Sertolin is a novel testicular gene in studying Ser- toli-germ cell interactions in the rat testis. J Biol Chem 274: 27056–27068PubMedCrossRefGoogle Scholar
  123. Mruk D, Cheng CH, Cheng YH, Mo MY, Grima J, Silvestrini B, Lee WM, Cheng CY (1998) Rat testicular extracellular superoxide dismutase: its purification, cellular distribution, and regulation. Biol Reprod 59: 298–308PubMedCrossRefGoogle Scholar
  124. Mruk D, Zhu LJ, Silvestrini B, Lee WM, Cheng CY (1997) Interactions of proteases and protease inhibitors in Sertoli-germ cell cocultures preceding the formation of specialized Sertoli-germ cell junctions in vitro. J Androl 8: 612–622.Google Scholar
  125. Mullaney BP, Skinner MK (1992) Basic fibroblast growth factor (bFGF) gene expression and protein production during pubertal development of the seminiferous tubule: follicle stimulating hormone-induced Sertoli cell bFGF expression. Endocrinology 131: 2928–2934PubMedCrossRefGoogle Scholar
  126. Mullaney BP, Skinner MK (1993) Transforming growth factor-13 (131, (32, 133) gene expression and action during pubertal development of the seminiferous tubules: potential role at the onset of spermatogenesis. Mol Endocrinol 7: 67–76Google Scholar
  127. Muller D, Paust HJ, Middendorff R, Davidoff MS (1997) Nerve growth factor ( NGF) receptors in male reproductive organs. Adv Exp Med Biol 424: 157–158Google Scholar
  128. Nargolwalla C, McCabe D, Fritz IB (1990) Modulation of levels of messenger RNA for tissue-type plasminogen activator in rat Sertoli cells, and levels of messenger RNA for plasminogen activator inhibitor in testis peritubular cells. Mol Cell Endocrinol 70: 73–80PubMedCrossRefGoogle Scholar
  129. O’Bryan MK, Cheng CY (1997) Purification and cellular localization of 132microglobulin in the testis. Life Sci 61: 487–494PubMedCrossRefGoogle Scholar
  130. O’Bryan MK, Grima J, Mruk D, Cheng CY (1997) Haptoglobin is a Sertoli cell product in the rat seminiferous epithelium: its purification and regulation. J Androl 18: 637–645PubMedGoogle Scholar
  131. Olaso R, Pairault C, Habert R (1998) Expression of type I and II receptors for transforming growth factor -(3 in the adult rat testis. Histochem Cell Biol 110: 613–618PubMedCrossRefGoogle Scholar
  132. Ong DE, Chytil F (1978) Cellular retinoic acid-binding protein from rat testis. J Biol Chem 253: 4551–4554PubMedGoogle Scholar
  133. Orth JM, Christensen AK (1979) Localization of 125I-labelled FSH in the testes of hypophysectomized rats by autoradiography at the light and electron microscope levels. Endocrinology 101: 262–278CrossRefGoogle Scholar
  134. Oyen O, Sandberg M, Levy FO, Tasken K, Beebe S, Hansson V, Jahnsen T (1988) Molecular cloning and cell-specific expression of newly discovered subunits of cAMP-dependent protein kinases: implications for different cellular responses to cAMP. APMIS Suppl 2: 238–250PubMedGoogle Scholar
  135. Papadopoulos V (1991) Identification and purification of a human Sertoli cell-secreted protein (hSCSP-80) stimulating Leydig cell steroid biosynthesis. J Clin Endocrinol Metab 72: 1332–1339PubMedCrossRefGoogle Scholar
  136. Papadopoulos V, Jia MC, Culty M, Hall PF, Dym M (1993) Rat Sertoli cell aromatase cytochrome P450: regulation by cell culture conditions and relationship to the state of cell differentiation. In Vitro Cell Dev Biol Anim 29: 943–949Google Scholar
  137. Palombi F, Farini D, Salanova M, De Grossi S, Stefanini M (1992) Development and cyto-differentiation of peritubular myoid cells in rat testis. Anat Rec 233: 32–40PubMedCrossRefGoogle Scholar
  138. Pelletier RM (1995) The distribution of connexin 43 is associated with the germ cell differentiation and with the modulation of the Sertoli cell junctional barrier in continual (guinea pig) and seasonal breeders’ (mink) testes. J Androl 16: 400–409PubMedGoogle Scholar
  139. Pelletier RM, Okawara Y, Vitale ML, Anderson JM (1997) Differential distribution of the tight-junction-associated protein ZO-I isoforms a+ and a in guinea pig Sertoli cells: a possible association with F-actin and G-actin. Biol Reprod 57: 367–376PubMedCrossRefGoogle Scholar
  140. Pelletier R, Trifaro JM, Carbajal ME, Okawara Y, Vitale ML (1999) Calcium-dependent actin-filament-severing protein scinderin levels and localization in bovine testis, epididymis, and spermatozoa. Biol Reprod 60: 1128–1136PubMedCrossRefGoogle Scholar
  141. Persson H, Ayer-Lievre C, Söder O, Villar MJ, Metsis M, Olson L, Ritzén M, Hokfelt T (1990) Expression of (3-nerve growth factor receptor mRNA in Sertoli cells down-regulated by testosterone. Science 247: 704–707PubMedCrossRefGoogle Scholar
  142. Phamantu NT, Bonnamy PJ, Bouakka M, Bocquet J (1995) Inhibition of proteoglycan synthesis induces an increase in follicle stimulating hormone ( FSH)-stimulated estradiol production by immature rat Sertoli cells. Mol Cell Endocrinol 109: 37–45Google Scholar
  143. Pineau C, Sharpe RM, Saunders PT, Gérard N, Jégou B (1990) Regulation of Sertoli cell inhibin production and of inhibin-a subunit mRNA levels by specific germ cell types. Mol Cell Endocrinol 72: 13–22PubMedCrossRefGoogle Scholar
  144. Pollack SE, Furth EE, Kallen CB, Arakane F, Kiriakidou M, Kozarsky KF, Strauss JF III (1997) Localization of the steroidogenic acute regulatory protein in human tissues. J Clin Endocrinol Metab 82: 4243–4251PubMedCrossRefGoogle Scholar
  145. Pöllanen P, Söder O, Parvinen M (1989) Interleukin-1-alpha stimulation of spermatogonial proliferation in vivo. Reprod Fertil Develop 1: 85–87CrossRefGoogle Scholar
  146. Ratcliffe MJ, Rubin LL, Staddon JM (1997) Dephosphorylation of the cadherin-associated p100/p120 proteins in response to activation of protein kinase C in epithelial cells. J Biol Chem 272: 1–8CrossRefGoogle Scholar
  147. Reader SC, Foster PM (1990) The in vitro effects of four isomers of dinitrotoluene on rat Sertoli and Sertoli-germ cell cocultures: germ cell detachment and lactate and pyruvate production. Toxicol Appl Pharmacol 106: 287–294PubMedCrossRefGoogle Scholar
  148. Ree AH, Hansson V, Walaas SI, Eskild W, Tasken KA (1999) Calcium/phospholipid-dependent protein kinases in rat Sertoli cells: regulation of androgen receptor messenger ribonucleic acid. Biol Reprod 60: 1257–1262PubMedCrossRefGoogle Scholar
  149. Rees JL, Daly AK, Redfern CPF (1989) Differential expression of the a and b retinoic acid receptors in tissues of the rat. Biochem J 259: 917–919PubMedGoogle Scholar
  150. Reynolds AB, Daniel J, McCrea P, Wheelock MJ, Wu J, Zhang Z (1994) Identification of a new catenin: The tyrosine kinase substrate p120cdS associates with E-cadherin complexes. Mol Cell Biol 14: 8333–8342PubMedGoogle Scholar
  151. Rhee K, Wolgemuth DJ (1995) Cdk family genes are expressed not only in dividing but also in terminally differentiated mouse germ cells, suggesting their possible function during both cell division and differentiation. Dev Dyn 204: 406–420PubMedCrossRefGoogle Scholar
  152. Risley MS, Tan IP, Roy C, Saez JC (1992) Cell-, age-, and stage-dependent distribution of connexin 43 gap junctions in testes. J Cell Sci 103: 81–96PubMedGoogle Scholar
  153. Rivarola MA, Sanchez P, Saez JM (1985) Stimulation of ribonucleic acid and deoxyribonucleic acid synthesis in spermatogenic cells by their coculture with Sertoli cells. Endocrinology 117: 1796–1802PubMedCrossRefGoogle Scholar
  154. Roberts KP, Griswold MD (1990) Characterization of rat transferrin receptor cDNA: the regulation of transferrin receptor mRNA in testes and in Sertoli cells in culture. Mol Endocrinol 4: 531–542PubMedCrossRefGoogle Scholar
  155. Rubin LL, Staddon JM (1999) The cell biology of the blood-brain barrier. Annu Rev Neurosci 22: 11–28PubMedCrossRefGoogle Scholar
  156. Russell LD, Tallon DM, Weber JE, Wong V, Peterson RN (1983) Three-dimensional reconstruction of a rat stage V Sertoli cell: III. A study of specific cellular relationships. Am J Anat 167: 181–192Google Scholar
  157. Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, Inazawa J, Fujimoto K, Tsukita S (1997) Mammalian occludin in epithelial cells: its expression and subcellular distribution. Eur J Cell Biol 73: 222–231PubMedGoogle Scholar
  158. Salanova M, Ricci G, Boitani C, Stefanini M, De Grossi S, Palombi F (1998) Junctional contacts between Sertoli cells in normal and aspermatogenic rat seminiferous epitheliu contain a6ß1 integrins, and their formation is controlled by follicle stimulating hormone. Biol Reprod 58: 371–378PubMedCrossRefGoogle Scholar
  159. Salanova M, Stefanini M, De Curtis I, Palombi F (1995) Integrin receptor a6ß I is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol Reprod 52: 79–87PubMedCrossRefGoogle Scholar
  160. Salas-Cortes L, Jaubert F, Barbaux S, Nessmann C, Bono MR, Fellous M, McElreavey K, Rosemblatt M (1999) The human SRY protein is present in fetal and adult Sertoli cells and germ cells. Int J Dev Biol 43: 135–140PubMedGoogle Scholar
  161. Samy ET, Li JCH, Grima J, Lee WM, Silvestrini B, Cheng CY (2000) Sertoli cell prostaglandin D2 synthetase (PGD-S) is a multi-functional molecule: its expression and regulation. Endocrinology 141: 710–721PubMedCrossRefGoogle Scholar
  162. Sanchez A, Jimenez R, Burgos M, Diaz De la Guardia R (1994) A substance secreted by rat Sertoli cells indices feminization of embryonic chick testes in vitro. Anat Embryo] (Berl) 189: 531–537Google Scholar
  163. Santiemma V, Salfi V, Casasanta N, Fabbrini A (1987) Lactate dehydrogenase and malate dehydrogenase of Sertoli cells in rats. Arch Androl 19: 59–64PubMedCrossRefGoogle Scholar
  164. Saunders PT, Fisher JS, Sharpe RM, Millar MR (1998) Expression of oestrogen receptor-(3 (ER-(3) occurs in multiple cell types, including some germ cells, in the rat testis. J Endocrinol 156: R13–17PubMedCrossRefGoogle Scholar
  165. Sharpe RM, Fraser HM, Cooper I, Rommerts FF (1981) Sertoli-Leydig cell communication via an LHRH-like factor. Nature 290: 785–787PubMedCrossRefGoogle Scholar
  166. Shibamoto S, Hayakawa M, Takeuchi K, Hari T, Miyazawa K, Kitamura N, Johnson KR, Wheelock MJ, Matsuyoshi N, Takeichi, Ito F (1995) Association of p120, a tyrosine kinases substrate, with E-cadherin/catenin complexes. J Cell Biol 128: 949–957PubMedCrossRefGoogle Scholar
  167. Shibayama-Imazu T, Ogane K, Hasegawa Y, Nakajo S, Shioda S, Ochiai H, Nakai Y, Nakaya K (1998) Distribution of PNP-14 ((3-synuclein) in neuroendocrine tissues: localization in Sertoli cells. Mol Reprod Dev 50: 163–169PubMedCrossRefGoogle Scholar
  168. Shubhada S, Baker K, Baker S, Lamb DJ (1996) Sertoli cell secreted growth factor: cellular origin, endocrine, and paracrine regulation of secretion. J Androl 15: 128–135Google Scholar
  169. Shubhada S, Lin SN, Qian ZY, Steinberger A, Tsai YH (1989) Polyamine profiles in rat testis, germ cells, and Sertoli cells during testicular maturation. J Androl 10: 145–151PubMedGoogle Scholar
  170. Sigillo F, Guillou F, Fontaine I, Benahmed M, Le Magueresse-Battistoni B (1999) In vitro regulation of rat Sertoli cell transferrin expression by tumor necrosis factor-a and retinoic acid. Mol Cell Endocrinol 148: 163–170PubMedCrossRefGoogle Scholar
  171. Skinner MK (1991) Cell-cell interactions in the testis. Endocr Rev 12: 45–77PubMedCrossRefGoogle Scholar
  172. Skinner MK (1993) Secretion of growth factors and other regulatory factors. In: The Sertoli Cell, Eds. Russell LD and Griswold MD. Clearwater, Cache River Press, pp. 237–247Google Scholar
  173. Skinner MK, Fritz IB (1985) Structural characterization of proteoglycans produced by testicular peritubular cells and Sertoli cells. J Biol Chem 260: 11874–11883PubMedGoogle Scholar
  174. Skinner MK, Griswold MD (1980) Sertoli cells synthesize and secrete transfen-in-like protein. J Biol Chem 255: 9523–9525PubMedGoogle Scholar
  175. Skinner MK, Griswold MD (1983) Sertoli cells synthesize and secrete a ceruloplasmin-like protein. Biol Reprod 28: 1225–1229PubMedCrossRefGoogle Scholar
  176. Skinner MK, Moses HL (1989) Transforming growth factor beta gene expression and action in the seminiferous tubule: peritubular cell-Sertoli cell interactions. Mol Endocrinol 3: 625–634PubMedCrossRefGoogle Scholar
  177. Skinner MK, Takacs K, Coffey RJ (1989) Transforming growth factor-alpha gene expression and action in the seminiferous tubule: peritubular cell-Sertoli cell interactions. Endocrinology 124: 845–854PubMedCrossRefGoogle Scholar
  178. Skinner MK, Tung PS, Fritz IB (1985) Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J Cell Biol 100: 1941–1947PubMedCrossRefGoogle Scholar
  179. Slegtenhorst-Eegdeman KE, Post M, Baarends WM, Themmen AP, Grootegoed JA (1995) Regulation of gene expression in Sertoli cells by follicle stimulating hormone (FSH): cloning and characterization of LRPR 1, a primary response gene encoding a leucine-rich protein. Mol Cell Endocrinol 108: 115–124PubMedCrossRefGoogle Scholar
  180. Slegtenhorst-Eegdeman KE, Verhoef-Post M, Parvinen M, Grootegoed JA, Themmen AP (1998) Differential regulation of leucine-rich primary response gene 1 (LRPR1) mRNA expression in rat testis and ovary. Mol Hum Reprod 4: 649–656PubMedCrossRefGoogle Scholar
  181. Smith EP, Hall SH, Monaco L, French FS, Wilson MW, Conti M (1989) A rat Sertoli cell factor similar to basic fibroblast growth factor increases c-fos messenger ribonucleic acid in cultured Sertoli cells. Mol Endocrinol 3: 954–961PubMedCrossRefGoogle Scholar
  182. Sorrentino C, Silvestrini B, Braghiroli L, Chung SS, Giacomelli S. Leone MG, Xie Y, Sui Y, Mo M, Cheng CY (1998) Rat prostaglandin D2 synthetase: its tissue distribution, changes during maturation, and regulation in the testis and epididymis. Biol Reprod 59: 843–853PubMedCrossRefGoogle Scholar
  183. Staddon JM, Herrenknecht K, Smales C, Rubin LL (1995) Evidence that tyrosine phosphorylation may increase tight junction permeability. J Cell Sci 108: 609–619PubMedGoogle Scholar
  184. Stahler MS, Schlegel C, Bardin CW, Silvestrini B, Cheng CY (1991) Œ2Macroglobulin is not an acute-phase protein in the rat testis. Endocrinology 128: 2805–2814Google Scholar
  185. Stephan JP, Syed V, Jégou B (1997) Regulation of Sertoli cell IL-1 and IL-6 production in vitro. Mol Cell Endocrinol 134: 109–118PubMedCrossRefGoogle Scholar
  186. Suarez-Quian CA, Dai MZ, Onoda M, Kriss RM, Dym M (1989) Epidermal growth factor receptor localization in the rat and monkey testes. Biol Re-prod 41: 921–932CrossRefGoogle Scholar
  187. Subramanian S, Adiga PR (1996) Hormonal modulation of riboflavin carrier protein secretion by immature rat Sertoli cells in culture. Mol Cell Endocrinol 120: 41–50PubMedCrossRefGoogle Scholar
  188. Subramanian S, Adiga PR (1999) Characterization and hormonal modulation of immunoreactive thiamin carrier protein in immature rat Sertoli cells in culture. J Steroid Biochem Mol Biol 68: 23–30PubMedCrossRefGoogle Scholar
  189. Swift TA, Dias JA (1988) Testosterone suppression of ornithine decarboxylase activity in rat Sertoli cells. Endocrinology 123: 687–693PubMedCrossRefGoogle Scholar
  190. Syed V, Söder 0, Arver S, Lindh M, Khan S, Ritzen EM (1988) Ontogeny and cellular origin of an interleukin- 1-like factor in the reproductive tract of the male rat. Int J Androl 11: 437–447PubMedCrossRefGoogle Scholar
  191. Sylvester SR, Morales C, Oko R, Griswold MD (1991) Localization of sulfated glycoprotein-2 (clusterin) on spermatozoa and in the reproductive tract of the male rat. Biol Reprod 45: 195–207PubMedCrossRefGoogle Scholar
  192. Sylvester SR, Skinner MK, Griswold MD (1984) A sulfated glycoprotein synthesized by Sertoli cells and by epididymal cells is a component of the sperm membrane. Biol Reprod 31: 1087–1101PubMedCrossRefGoogle Scholar
  193. Tan IP, Roy C, Saez JC, Saez CG, Paul DL, Risley MS (1996) Regulated assembly of connexin 33 and connexin 43 into rat Sertoli cell gap junctions. Biol Reprod 54: 1300–1310PubMedCrossRefGoogle Scholar
  194. Tohonen V, Osterlund C, Nordqvist K (1998) Testatin: a cystatin-related gene expressed during early testis development. Proc Natl Acad Sci USA 95: 14208–14213PubMedCrossRefGoogle Scholar
  195. Tres LL, Smith EP, Van Wyk JJ, Kierszenbaum AL (1986) Immunoreactive sites and accumulation of somatomedin-C in rat Sertoli-spermatogenic cell co-cultures. Exp Cell Res 162: 33–50PubMedCrossRefGoogle Scholar
  196. Tryggvason K (1993) The laminin family. Curr Opin Cell Biol 5: 877–882PubMedCrossRefGoogle Scholar
  197. Tsai YN, Lin SN (1985) Differential release of polyamines by cultured rat Sertoli cells. J Androl 6: 348–352PubMedGoogle Scholar
  198. Tsuruta JK, O’Brien DA, Griswold MD (1993) Sertoli cell and germ cell cystatin C: stage-dependent expression of two distinct messenger ribonucleic acid transcripts in rat testis. Biol Reprod 49: 1045–1054PubMedCrossRefGoogle Scholar
  199. Ueno N, Baird A, Esch F, Ling N, Guillemin R (1987) Isolation and partial characterization of basic fibroblast growth factor from bovine testis. Mol Cell Endocrinol 49: 189–194PubMedCrossRefGoogle Scholar
  200. Ulisse S, Rucci N, Persanti D, Carosa E, Graziano FM, Pavan A, Ceddia P, Arizzi M, Muzi P, Cironi L, Gnessi L, D’Armiento M, Jannini EA (1998) Regulation by thyroid hormone of the expression of basement membrane components in rat prepubertal Sertoli cells. Endocrinology 139: 741–747PubMedCrossRefGoogle Scholar
  201. van der Donk JA, de Ruiter-Bootsma AL, Ultee-van Gessel AM, Wauben-Penris PJ (1986) Cell-cell interaction between rat Sertoli cells and mouse germ cells in vitro. Expt Cell Res 164: 191–198CrossRefGoogle Scholar
  202. Vannelli BG, Barni T, Orlando C, Natali A, Serio M, Balboni GC (1988) Insulin-like growth factor-I (IGF-I) and IGF-I receptor in human testis: an immunohistochemical study. Fertil Steril 49: 666–669PubMedGoogle Scholar
  203. Vigier B, Picard JY, Campargue J, Forest MG, Heyman Y, Josso N (1985) Secretion of anti-Mullerian hormone by immature bovine Sertoli cells in primary culture, studies by a competition-type radioimmunoassay: lack of modulation by either FSH or testosterone. Mol Cell Endocrinol 43: 141–150PubMedCrossRefGoogle Scholar
  204. Wada M, Shintani Y, Kosaka M, Sano T, Hizawa K, Saito S (1996) Immunohistochemical localization of activin A and follistatin in human tissues. Endocr J 43: 375–385PubMedCrossRefGoogle Scholar
  205. Waeber G, Meyer TE, LeSieur M, Hermann HL, Gérard N, Habener JF (1991) Developmental stage-specific expression of cyclic adenosine 3’,5’ mono-phosphate response element-binding protein CREB during spermatogenesis involves alternative exon splicing. Mol Endocrinol 5: 1418–1430PubMedCrossRefGoogle Scholar
  206. Walker WH, Daniel PB, Habener JF (1998) Inducible cAMP early repressor ICER down-regulation of CREB gene expression in Sertoli cells. Mol Cell Endocrinol 143: 167–178PubMedCrossRefGoogle Scholar
  207. Wang JE, Josefsen GM, Hansson V, Haugen TB (1998) Residual bodies and IL-la stimulate expression of mRNA for IL-la and IL-1 receptor type I in cultured rat Sertoli cells. Mol Cell Endocrinol 137: 139–144PubMedCrossRefGoogle Scholar
  208. Weber JE, Russell LD, Wong V, Peterson RN (1983) Three-dimensional reconstruction of a rat stage V Sertoli cell: II. Morphometry of Sertoli-Sertoli and Sertoli-germ-cell relationships. Am J Anat 167: 163–179Google Scholar
  209. Weiner KX, Dias JA (1990) Protein synthesis is required for testosterone to decrease ornithine decarboxylase messenger RNA levels in rat Sertoli cells. Mol Endocrinol 4: 1791–1798PubMedCrossRefGoogle Scholar
  210. Wells A, Ware MF, Allen FD, Lauffenburger DA (1999) Shaping up for shipping out: PLCy signaling of morphology changes in EGF-stimulated fibroblast migration. Cell Mot Cytoskeleton 44: 227–233Google Scholar
  211. Welsh MJ, Gaestel M (1998) Small heat-shock protein family: function in health and disease. Ann NY Acad Sci 851: 28–35PubMedCrossRefGoogle Scholar
  212. Welsh MJ, Wu W, Parvinen M, Gilmont RR (1996) Variation in expression of hsp27 messenger ribonucleic acid during the cycle of the seminiferous epithelium and co-localization of hsp27 and microfilaments in Sertoli cells of the rat. Biol Reprod 55: 141–151PubMedCrossRefGoogle Scholar
  213. Wilkinson MF, Kleeman J, Richards J, MacLeod CL (1990) A novel oncofetal gene is expressed in a stage-specific manner in murine embryonic development. Dev Biol 141: 451–455PubMedCrossRefGoogle Scholar
  214. Williams J, Foster PM (1988) The production of lactate and pyruvate as sensitive indices of altered rat Sertoli cell function in vitro following the addition of various testicular toxicants. Toxicol Appl Pharmacol 94: 160–170PubMedCrossRefGoogle Scholar
  215. Wissenbach U, Schroth G, Philipp S, Flockerzi V (1998) Structure and mRNA expression of a bovine trp homologue related to mammalian trp2 transcripts. FEBS Lett 429: 61–66PubMedCrossRefGoogle Scholar
  216. Wolf KW, Winking H (1996) The organization of microtubules and filamentous actin in cytospin preparations of Sertoli cells from w/wwei mutant mice devoid of germ cells. Anat Embryol (Berl) 193: 413–417Google Scholar
  217. Wong CCS, Chung SSW, Zhu LJ, Mruk D, Lee WM, Cheng CY (2000) Changes in the expression of junctional and nonjunctional complex component genes when inter-Sertoli tight junctions are formed in vitro. J Androl (in press)Google Scholar
  218. Wong V, Russell LD (1983) Three-dimensional reconstruction of a rat stage V Sertoli cell: I. Methods, basic configuration, and dimensions. Am J Anat 167: 143–161Google Scholar
  219. Wright WW, Musto NA, Mather JP, Bardin CW (1981) Sertoli cells secrete both testis-specific and serum proteins. Proc Natl Acad Sci USA 78: 7565–7569PubMedCrossRefGoogle Scholar
  220. Wrobel KH, Bickel D, Kujat R (1995) Distribution pattern of F-actin, vimentin, and a-tubulin in the bovine testis during postnatal development. Acta Anat (Basel) 153: 263–272CrossRefGoogle Scholar
  221. Wrobel KH, Bickel D, Schimmel M, Kujat R (1996) Immunohistochemical demonstration of nerve growth factor receptor in bovine testis. Cell Tissue Res 285: 189–197PubMedCrossRefGoogle Scholar
  222. Yan W, West A, Toppari J, Landetie J (1997) Stage-specific expression and phosphorylation of retinoblastoma protein (pRb) in the rat seminiferous epithelium. Mol Cell Endocrinol 132: 137–148PubMedCrossRefGoogle Scholar
  223. Yomogida K, Ohtani H, Harigae H, Ito E, Nishimune Y, Engel JD, Yamamoto M (1994) Developmental stage-and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells. Development 120: 1759–1766PubMedGoogle Scholar
  224. Yoshikawa K, Aizawa T (1988) Expression of the enkephalin precursor gene in rat Sertoli cells: regulation by follicle stimulating hormone. FEBS Lett 237: 183–186PubMedCrossRefGoogle Scholar
  225. Zhai Y, Higgins D, Napoli JL (1997) Coexpression of the mRNAs encoding retinol dehydrogenase isoenzymes and cellular retinol-binding protein. J Cell Physiol 173 36 13Google Scholar
  226. Zhu LJ, Krempels K, Bardin CW, O’Carroll AM, Mezey E (1998) The localization of messenger ribonucleic acids for somatostatin receptors 1, 2, and 3 in rat testis. Endocrinology 139: 350–357Google Scholar
  227. Zwain IH, Cheng CY (1994) Rat seminiferous tubular culture medium contains a biological factor that inhibits Leydig cell steroidogenesis: its purification and mechanism of action. Mol Cell Endocrinol 104: 213–227PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2000

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  • D. D. Mruk
  • C. Yan Cheng

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