Androgen initiates sertoli cell tight junction formation in the hypogonadal (hpg) mouse

Biology of Reproduction

Volumn 87, Issue 2, 2012, Pages

  McCabe, Mark J ^a,b   Allan, Charles M ^c   Foo, Caroline F H ^a   Nicholls, Peter K ^a,d   McTavish, Kirsten J ^c   Stanton, Peter G ^a,d  

^a MONASH MEDICAL CENTRE   (Australia)

^b RMIT UNIVERSITY   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d MONASH UNIVERSITY   (Australia)

Author keywords

Blood testis barrier; Claudin 11; Claudin 3; Gonadotropins; Sertoli cells; Spermatogenesis; Tight junctions

Indexed keywords

ANDROSTANOLONE; CLAUDIN 11; CLAUDIN 3; FOLLITROPIN; GONADOTROPIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; HORMONAL REGULATION; IMMUNOLOCALIZATION; IN VIVO STUDY; MALE; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOGENESIS; TESTIS; TIGHT JUNCTION;

ANDROGENS; ANIMALS; CONNEXINS; DIHYDROTESTOSTERONE; DISEASE MODELS, ANIMAL; FOLLICLE STIMULATING HORMONE; HUMANS; HYPOGONADISM; MALE; MICE; MICE, TRANSGENIC; ORGAN SIZE; RATS; RNA, MESSENGER; SERTOLI CELLS; TIGHT JUNCTIONS;

MUS;

EID: 84869450857     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.094318     Document Type: Article

References (53)

1. Aravindan GR, Mruk D, Lee WM, Cheng CY. Identification, isolation, and characterization of a 41-kilodalton protein from rat germ cellconditioned medium exhibiting concentration-dependent dual biological activities. Endocrinology 1997; 138:3259-3268.
2. Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82:825-874.
3. Griswold MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol 1998; 9:411-416.
4. Setchell BP. Hormones: what the testis really sees. Reprod Fertil Dev 2004; 16:535-545.
5. Chung NP, Cheng CY. Is cadmium chloride-induced inter-sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? Endocrinology 2001; 142:1878-1888.
6. Chung NP, Mruk D, Mo MY, Lee WM, Cheng CYA. 22-amino acid synthetic peptide corresponding to the second extracellular loop of rat occludin perturbs the blood-testis barrier and disrupts spermatogenesis reversibly in vivo. Biol Reprod 2001; 65:1340-1351.
7. Russell LD, Peterson RN. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 1985; 94:177-211.
8. Vitale R, Fawcett DW, Dym M. The normal development of the bloodtestis barrier and the effects of clomiphene and estrogen treatment. Anat Rec 1973; 176:331-344.
9. Pelletier RM. Cyclic formation and decay of the blood-testis barrier in the mink (Mustela vison), a seasonal breeder. Am J Anat 1986; 175:91-117.
10. Pelletier RM. Cyclic modulation of Sertoli cell junctional complexes in a seasonal breeder: the mink (Mustela vison). Am J Anat 1988; 183:68-102.
11. Morita K, Sasaki H, Fujimoto K, Furuse M, Tsukita S. Claudin-11/OSPbased tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol 1999; 145:579-588.
12. Gliki G, Ebnet K, Aurrand-Lions M, Imhof BA, Adams RH. Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 2004; 431: 320-324.
13. Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T, Tsukita S. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 2000; 11:4131-4142.
14. Wong CH, Cheng CY. The blood-testis barrier: its biology, regulation, and physiological role in spermatogenesis. Curr Top Dev Biol 2005; 71: 263-296.
15. Pelletier RM. The blood-testis barrier: the junctional permeability, the proteins and the lipids. Prog Histochem Cytochem 2011; 46:49-127.
16. Kaitu'u-Lino TJ, Sluka P, Foo CF, Stanton PG. Claudin-11 expression and localisation is regulated by androgens in rat Sertoli cells in vitro. Reproduction 2007; 133:1169-1179.
17. Su L, Mruk DD, Lee WM, Cheng CY. Differential effects of testosterone and TGF-beta3 on endocytic vesicle-mediated protein trafficking events at the blood-testis barrier. Exp Cell Res 2010; 316:2945-2960.
18. Florin A, Maire M, Bozec A, Hellani A, Chater S, Bars R, Chuzel F, Benahmed M. Androgens and postmeiotic germ cells regulate claudin-11 expression in rat Sertoli cells. Endocrinology 2005; 146:1532-1540.
19. Tarulli GA, Stanton PG, Lerchl A, Meachem SJ. 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.
20. McCabe MJ, Tarulli GA, Meachem SJ, Robertson DM, Smooker PM, Stanton PG. Gonadotropins regulate rat testicular tight junctions in vivo. Endocrinology 2010; 151:2911-2922.
21. Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE. Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci U S A 2005; 102:16696-16700.
22. Tarulli GA, Meachem SJ, Schlatt S, Stanton PG. Regulation of testicular tight junctions by gonadotrophins in the adult Djungarian hamster in vivo. Reproduction 2008; 135:867-877.
23. Komljenovic D, Sandhoff R, Teigler A, Heid H, Just WW, Gorgas K. Disruption of blood-testis barrier dynamics in ether-lipid-deficient mice. Cell Tissue Res 2009; 337:281-299.
24. Chihara M, Otsuka S, Ichii O, Hashimoto Y, Kon Y. Molecular dynamics of the blood-testis barrier components during murine spermatogenesis. Mol Reprod Dev 2010; 77:630-639.
25. Allan CM, Haywood M, Swaraj S, Spaliviero J, Koch A, Jimenez M, Poutanen M, Levallet J, Huhtaniemi I, Illingworth P, Handelsman DJ. A novel transgenic model to characterize the specific effects of folliclestimulating hormone on gonadal physiology in the absence of luteinizing hormone actions. Endocrinology 2001; 142:2213-2220.
26. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G. Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature 1977; 269:338-340.
27. Charlton HM, Halpin DM, Iddon C, Rosie R, Levy G, McDowell IF, Megson A, Morris JF, Bramwell A, Speight A, Ward BJ, Broadhead J, et al. The effects of daily administration of single and multiple injections of gonadotropin-releasing hormone on pituitary and gonadal function in the hypogonadal (hpg) mouse. Endocrinology 1983; 113:535-544.
28. Huang HF, Marshall GR, Rosenberg R, Nieschlag E. Restoration of spermatogenesis by high levels of testosterone in hypophysectomized rats after long-term regression. Acta Endocrinol (Copenh) 1987; 116:433-444.
29. Mason AJ, Hayflick JS, Zoeller RT, Young WS III, Phillips HS, Nikolics K, Seeburg PH. A deletion truncating the gonadotropin-releasing hormone gene is responsible for hypogonadism in the hpg mouse. Science 1986; 234:1366-1371.
30. Jimenez M, Spaliviero JA, Grootenhuis AJ, Verhagen J, Allan CM, Handelsman DJ. Validation of an ultrasensitive and specific immunofluorometric assay for mouse follicle-stimulating hormone. Biol Reprod 2005; 72:78-85.
31. Ebling FJ, Brooks AN, Cronin AS, Ford H, Kerr JB. Estrogenic induction of spermatogenesis in the hypogonadal mouse. Endocrinology 2000; 141: 2861-2869.
32. Myers M, Ebling FJ, Nwagwu M, Boulton R, Wadhwa K, Stewart J, Kerr JB. Atypical development of Sertoli cells and impairment of spermatogenesis in the hypogonadal (hpg) mouse. J Anat 2005; 207:797-811.
33. Singh J, O'Neill C, Handelsman DJ. Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology 1995; 136:5311-5321.
34. Haywood M, Spaliviero J, Jimemez M, King NJ, Handelsman DJ, Allan CM. Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone. Endocrinology 2003; 144:509-517.
35. Handelsman DJ, Spaliviero JA, Simpson JM, Allan CM, Singh J. Spermatogenesis without gonadotropins: maintenance has a lower testosterone threshold than initiation. Endocrinology 1999; 140: 3938-3946.
36. Pileri SA, Roncador G, Ceccarelli C, Piccioli M, Briskomatis A, Sabattini E, Ascani S, Santini D, Piccaluga PP, Leone O, Damiani S, Ercolessi C, et al. Antigen retrieval techniques in immunohistochemistry: comparison of different methods. J Pathol 1997; 183:116-123.
37. Allan CM, Couse JF, Simanainen U, Spaliviero J, Jimenez M, Rodriguez K, Korach KS, Handelsman DJ. Estradiol induction of spermatogenesis is mediated via an estrogen receptor-falphag mechanism involving neuroendocrine activation of follicle-stimulating hormone secretion. Endocrinology 2010; 151:2800-2810.
38. Pelletier RM. A novel perspective: the occluding zonule encircles the apex of the Sertoli cell as observed in birds. Am J Anat 1990; 188:87-108.
39. Setchell BP (ed.). Blood-testis barrier, junctional and transport proteins and spermatogenesis. In: Cheng CY, Austin TX (eds.), Molecular Mechanisms in Spermatogenesis. Landes Bioscience/Springer Science+-Business Media, LLC: New York; 2008:212-33.
40. Carette D, Weider K, Gilleron J, Giese S, Dompierre J, Bergmann M, Brehm R, Denizot JP, Segretain D, Pointis G. Major involvement of connexin 43 in seminiferous epithelial junction dynamics and male fertility. Dev Biol 2010; 346:54-67.
41. Lindsey JS, Wilkinson MF. Pem: a testosterone- and LH-regulated homeobox gene expressed in mouse Sertoli cells and epididymis. Dev Biol 1996; 179:471-484.
42. O'Shaughnessy PJ, Verhoeven G, De Gendt K, Monteiro A, Abel MH. Direct action through the sertoli cells is essential for androgen stimulation of spermatogenesis. Endocrinology 2010; 151:2343-2348.
43. Lim P, Robson M, Spaliviero J, McTavish KJ, Jimenez M, Zajac JD, Handelsman DJ, Allan CM. Sertoli cell androgen receptor DNA binding domain is essential for the completion of spermatogenesis. Endocrinology 2009; 150:4755-4765.
44. Abel MH, Baban D, Lee S, Charlton HM, O'Shaughnessy PJ. Effects of FSH on testicular mRNA transcript levels in the hypogonadal mouse. J Mol Endocrinol 2009; 42:291-303.
45. Nicholls PK, Harrison CA, Gilchrist RB, Farnworth PG, Stanton PG. Growth differentiation factor 9 is a germ cell regulator of Sertoli cell function. Endocrinology 2009; 150:2481-2490.
46. Li MW, Mruk DD, Lee WM, Cheng CY. Cytokines and junction restructuring events during spermatogenesis in the testis: an emerging concept of regulation. Cytokine Growth Factor Rev 2009; 20:329-338.
47. Yan HH, Mruk DD, Lee WM, Cheng CY. Blood-testis barrier dynamics are regulated by testosterone and cytokines via their differential effects on the kinetics of protein endocytosis and recycling in Sertoli cells. FASEB J 2008; 22:1945-1959.
48. Cameron DF, Muffly KE, Nazian SJ. Development of Sertoli cell binding competency in the peripubertal rat. J Androl 1998; 19:573-579.
49. Muffly KE, Nazian SJ, Cameron DF. Effects of follicle-stimulating hormone on the junction-related Sertoli cell cytoskeleton and daily sperm production in testosterone-treated hypophysectomized rats. Biol Reprod 1994; 51:158-166.
50. Sluka P, O'Donnell L, Bartles JR, Stanton PG. FSH regulates the formation of adherens junctions and ectoplasmic specialisations between rat Sertoli cells in vitro and in vivo. J Endocrinol 2006; 189:381-395.
51. Zhang FP, Pakarainen T, Poutanen M, Toppari J, Huhtaniemi I. The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. Proc Natl Acad Sci U S A 2003; 100:13692-13697.
52. Li MW, Mruk DD, Lee WM, Cheng CY. Connexin 43 and plakophilin-2 as a protein complex that regulates blood-testis barrier dynamics. Proc Natl Acad Sci U S A 2009; 106:10213-10218.
53. Domanskyi A, Zhang FP, Nurmio M, Palvimo JJ, Toppari J, Janne OA. Expression and localization of androgen receptor-interacting protein-4 in the testis. Am J Physiol Endocrinol Metab 2007; 292:E513-E522.