The heat-induced reversible change in the blood-testis barrier (BTB) is regulated by the androgen receptor (AR) via the partitioning-defective protein (Par) polarity complex in the mouse

Biology of Reproduction

Volumn 89, Issue 1, 2013, Pages

  Li, Xi Xia ^a,b   Chen, Su Ren ^a,b   Shen, Bin ^c   Yang, Jun Ling ^a   Ji, Shao Yang ^a   Wen, Qing ^a   Zheng, Qiao Song ^a   Li, Lei ^a   Zhang, Jun ^a   Hu, Zhao Yuan ^a   Huang, Xing Xu ^c   Liu, Yi Xun ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NANJING UNIVERSITY   (China)

Author keywords

Androgen receptor; Blood testis barrier; Heat stress; Polarity complex; Sertoli cells; Testis

Indexed keywords

ALPHA CATENIN; ANDROGEN RECEPTOR; ATYPICAL PROTEIN KINASE C; BETA CATENIN; FLUTAMIDE; MULTIPROTEIN COMPLEX; NERVE CELL ADHESION MOLECULE; PARTITIONING DEFECTIVE PROTEIN POLARITY COMPLEX; PROTEIN; PROTEIN CDC42; PROTEIN KINASE C; PROTEIN PAR3; PROTEIN PAR6; PROTEIN ZO1; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; BLOOD TESTIS BARRIER; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HEAT STRESS; HEAT TREATMENT; IN VIVO STUDY; MALE; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; SERTOLI CELL;

EID: 84889048497     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.109405     Document Type: Article

References (56)

1. Danno S, Itoh K, Matsuda T, Fujita J. Decreased expression of mouse Rbm3, a cold-shock protein, in Sertoli cells of cryptorchid testis. Am J Pathol 2000; 156:1685-1692.
2. Lue YH. Single exposure to heat induces stage-specific germ cell apoptosis in rats: role of intratesticular testosterone on stage specificity. Endocrinology 1999; 140:1709-1717.
3. Zhang XS, Lue YH, Guo SH, Yuan JX, Hu ZY, Han CS, Hikim A, Swerdloff RS, Wang C, Liu YX. Expression of HSP105 and HSP60 during germ cell apoptosis in the heat-treated testes of adult cynomolgus monkeys (Macaca fascicularis). Front Biosci 2005; 10:3110-3121.
4. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25:747-806.
5. Cheng CY, Mruk DD. An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective. Crit Rev Biochem Mol Biol 2009; 44:245-263.
6. Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 2010; 6:380-395.
7. 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.
8. Lui WY, Mruk DD, Lee WM, Cheng CY. Adherens junction dynamics in the testis and spermatogenesis. J Androl 2003; 24:1-14.
9. Lui WY, Lee WM, Cheng CY. Transforming growth factor-beta3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology 2001; 142:1865-1877.
10. Fink C, Weigel R, Hembes T, Lauke-Wettwer H, Kliesch S, Bergmann M, Brehm RH. Altered expression of ZO-1 and ZO-2 in Sertoli cells and loss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 2006; 8:1019-1027.
11. Li MW, Xia W, Mruk DD, Wang CQ, Yan HH, Siu MK, Lui WY, Lee WM, Cheng CY. Tumor necrosis factor falphag reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol 2006; 190: 313-329.
12. 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.
13. Guo J, Tao SX, Chen M, Shi YQ, Zhang ZQ, Li YC, Zhang XS, Hu ZY, Liu YX. Heat treatment induces liver receptor homolog-1 expression in monkey and rat Sertoli cells. Endocrinology 2007; 148:1255-1265.
14. Zhang XS, Zhang ZH, Jin X, Wei P, Hu XQ, Chen M, Lu CL, Lue YH, Hu ZY, Hikim APS. Dedifferentiation of adult monkey Sertoli cells through activation of extracellularly regulated kinase 1/2 induced by heat treatment. Endocrinology 2006; 147:1237-1245.
15. Cai H, Ren Y, Li XX, Yang JL, Zhang CP, Chen M, Fan CH, Hu XQ, Hu ZY, Gao F, Liu YX. Scrotal heat stress causes a transient alteration in tight junctions and induction of TGF-beta expression. Int J Androl 2011; 34: 352-362.
16. Chen M, Cai H, Yang JL, Lu CL, Liu T, Yang W, Guo J, Hu XQ, Fan CH, Hu ZY, Gao F, Liu YX. Effect of heat stress on expression of junctionassociated molecules and upstream factors androgen receptor and Wilms' tumor 1 in monkey Sertoli cells. Endocrinology 2008; 149:4871-4882.
17. Wang RS, Yeh S, Chen LM, Lin HY, Zhang C, Ni J, Wu CC, di Sant'Agnese PA, Tzeng CR, Chang C. Androgen receptor in Sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes. Endocrinology 2006; 147:5624-5633.
18. Wu RC, Jiang M, Beaudet AL, Wu MY. ARID4A and ARID4B regulate male fertility, a functional link to the AR and RB pathways. Proc Natl Acad Sci U S A 2013; 110:4616-4621.
19. Ruhayel Y, Lundin K, Giwercman Y, Halldén C, Willén M, Giwercman A. Androgen receptor gene GGN and CAG polymorphisms among severely oligozoospermic and azoospermic Swedish men. Hum Reprod 2004; 19:2076-2083.
20. Regadera J, Martínez-García F, González-Peramato P, Serrano A, Nistal M, Suárez-Quian C. Androgen receptor expression in Sertoli cells as a function of seminiferous tubule maturation in the human cryptorchid testis. J Clin Endocrinol Metab 2001; 86:413-421.
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. Willems A, Batlouni SR, Esnal A, Swinnen JV, Saunders PT, Sharpe RM, Franca LR, De Gendt K, Verhoeven G. Selective ablation of the androgen receptor in mouse Sertoli cells affects Sertoli cell maturation, barrier formation and cytoskeletal development. PLoS ONE 2010; 5:e14168.
23. Wong EW, Mruk DD, Lee WM, Cheng CY. Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci U S A 2008; 105:9657-9662.
24. Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2000; 2:540-547.
25. Joberty G, Petersen C, Gao L, Macara IG. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2000; 2: 531-539.
26. Ohno S. Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol 2001; 13:641-648.
27. Suzuki A, Ohno S. The PAR-aPKC system: lessons in polarity. J Cell Sci 2006; 119:979-987.
28. Chen XY, Macara IG. Par-3 controls tight junction assembly through the Rac exchange factor Tiam1. Nat Cell Biol 2005; 7:U262-U272.
29. Anahara R, Toyama Y, Mori C. Flutamide induces ultrastructural changes in spermatids and the ectoplasmic specialization between the Sertoli cell and spermatids in mouse testes. Reprod Toxicol 2004; 18:589-596.
30. Katsuno M, Adachi H, Doyu M, Minamiyama M, Sang C, Kobayashi Y, Inukai A, Sobue G. Leuprorelin rescues polyglutamine-dependent phenotypes in a transgenic mouse model of spinal and bulbar muscular atrophy. Nat Med 2003; 9:768-773.
31. Anahara R, Toyama Y, Maekawa M, Kai M, Ishino F, Toshimori K, Mori C. Flutamide depresses expression of cortactin in the ectoplasmic specialization between the Sertoli cells and spermatids in the mouse testis. Food Chem Toxicol 2006; 44:1050-1056.
32. Ramirez CL, Foley JE, Wright DA, Muller-Lerch F, Rahman SH, Cornu TI, Winfrey RJ, Sander JD, Fu F, Townsend JA, Cathomen T, Voytas DF, et al. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat Methods 2008; 5:374-375.
33. Sander JD, Maeder ML, Reyon D, Voytas DF, Joung JK, Dobbs D. ZiFiT (Zinc Finger Targeter): an updated zinc finger engineering tool. Nucleic Acids Res 2010; 38:W462-W468.
34. Sander JD, Zaback P, Joung JK, Voytas DF, Dobbs D. Zinc Finger Targeter (ZiFiT): an engineered zinc finger/target site design tool. Nucleic Acids Res 2007; 35:W599-W605.
35. Amrani N, Sachs MS, Jacobson A. Early nonsense: mRNA decay solves a translational problem. Nat Rev Mol Cell Biol 2006; 7:415-425.
36. Barrionuevo F, Georg I, Scherthan H, Lecureuil C, Guillou F, Wegner M, Scherer G. Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 2009; 327:301-312.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001; 25:402-408.
38. Zhao BX, Chen HZ, Lei NZ, Li GD, Zhao WX, Zhan YY, Liu B, Lin SC, Wu Q. p53 mediates the negative regulation of MDM2 by orphan receptor TR3. EMBO J 2006; 25:5703-5715.
39. Persson H, Ayer-Le Lievre C, Soder O, Villar MJ, Metsis M, Olson L, Ritzen M, Hokfelt T. Expression of beta-nerve growth factor receptor mRNA in Sertoli cells downregulated by testosterone. Science 1990; 247: 704-707.
40. Hu Z, Dandekar D, O'Shaughnessy PJ, De Gendt K, Verhoeven G, Wilkinson MF. Androgen-induced Rhox homeobox genes modulate the expression of AR-regulated genes. Mol Endocrinol 2010; 24:60-75.
41. Bhardwaj A, Shanker S, Song HW, Suzuki K, Orgebin-Crist MC, Wilkinson M. Spatial and temporal expression of Rhox5 homeobox gene in the epididymis is controlled by DNA methylation, androgen receptor, and GATA transcription factors. In: Abstracts of the 41st Annual Meeting of the Society for the Study of Reproduction, May 27-30, 2008, Kailua- Kona, Hawaii. Biol Reprod 2008; 78(suppl):Abstract 209.
42. Gye MC, Ohsako S. Effects of flutamide in the rat testis on the expression of occludin, an integral member of the tight junctions. Toxicol Lett 2003; 143:217-222.
43. Zhu ML, Kyprianou N. Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J 2010; 24:769-777.
44. Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 2009; 80:913-919.
45. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier a lesson from claudin-1-deficient mice. J Cell Biol 2002; 156:1099-1111.
46. 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.
47. Etienne-Manneville S, Hall A. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr Opin Cell Biol 2003; 15:67-72.
48. Nelson WJ. Adaptation of core mechanisms to generate cell polarity. Nature 2003; 422:766-774.
49. Rolls MM, Doe CQ. Cell polarity: from embryo to axon. Nature 2003; 421:905-906.
50. Wong EW, Mruk DD, Lee WM, Cheng CY. Regulation of blood-testis barrier dynamics by TGF-beta3 is a Cdc42-dependent protein trafficking event. Proc Natl Acad Sci U S A 2010; 107:11399-11404.
51. Nakayama M, Goto TM, Sugimoto M, Nishimura T, Shinagawa T, Ohno S, Amano M, Kaibuchi K. Rho-kinase phosphorylates PAR-3 and disrupts PAR complex formation. Dev Cell 2008; 14:205-215.
52. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 2000; 275:36803-36810.
53. Bakin AV, Rinehart C, Tomlinson AK, Arteaga CL. p38 mitogenactivated protein kinase is required for TGF beta-mediated fibroblastic transdifferentiation and cell migration. J Cell Sci 2002; 115:3193-3206.
54. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 2005; 307:1603-1609.
55. Viloria-Petit AM, Wrana JL. The TGFb-Par6 polarity pathway: linking the Par complex to EMT and breast cancer progression. Cell Cycle 2010; 9: 623-624.
56. Takekuni K, Ikeda W, Fujito T, Morimoto K, Takeuchi M, Monden M, Takai Y. Direct binding of cell polarity protein PAR-3 to cell-cell adhesion molecule nectin at neuroepithelial cells of developing mouse. J Biol Chem 2003; 278:5497-5500.