An occludin-focal adhesion kinase protein complex at the blood-testis barrier: A study using the cadmium model

Endocrinology

Volumn 150, Issue 7, 2009, Pages 3336-3344

  Siu, Erica R ^a   Wong, Elissa W P ^a   Mruk, Dolores D ^a   Sze, K L ^a   Porto, Catarina S ^b   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM CHLORIDE; FOCAL ADHESION KINASE; OCCLUDIN;

ANIMAL CELL; ARTICLE; BLOOD TESTIS BARRIER; CELL CULTURE; CELL INTERACTION; CONTROLLED STUDY; DESMOSOME; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATOCYTE; TIGHT JUNCTION; ULTRASTRUCTURE;

ANIMALS; BLOOD-TESTIS BARRIER; CADMIUM CHLORIDE; FOCAL ADHESION KINASE 1; MALE; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PERMEABILITY; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SERTOLI CELLS; TIGHT JUNCTIONS;

EID: 67649635971     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1741     Document Type: Article

References (48)

1. Russell LD 1977 Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148:313-328 (Pubitemid 8075867)
2. de Kretser D, Kerr J 1988 The cytology of the testis. In: Knobil E, Neill J, Ewing L, Greenwald G, Markert C, Pfaff D, eds. The physiology of reproduction. New York: Raven Press; 837-932
3. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED 1990 Histological and histopathological evaluation of the testis. Clearwater, FL: Cache River Press
4. Wong CH, Cheng CY 2005 The blood-testis barrier: its biology, regulation and physiological role in spermatogenesis. Curr Top Dev Biol 71:263-296
5. Siu MK, Mruk DD, Lee WM, Cheng CY 2003 Adhering junction dynamics in the testis are regulated by an interplay of β 1-integrin and focal adhesion complex-associated proteins. Endocrinology 144:2141-2163 (Pubitemid 36543354)
6. Beardsley A, Robertson DM, O'Donnell L 2006 A complex containing α6β1- integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J Endocrinol 190:759-770 (Pubitemid 44560251)
7. Usatyuk PV, Parinandi NL, Natarajan V 2006 Redox regulation of 4-hydroxy- 2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. J Biol Chem 281:35554-35566 (Pubitemid 46036589)
8. Galen B, Cheshenko N, Tuyama A, Ramratnam B, Herold BC 2006 Access to nectin favors herpes simplex virus infection at the apical surface of polarized human epithelial cells. J Virol 80:12209-12218 (Pubitemid 44904371)
9. Ozaki M, Ogita H, Takai Y 2007 Involvement of integrin-induced activation of protein kinase C in the formation of adherens junctions. Genes Cells 12:651-662 (Pubitemid 46824962)
10. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J 2007 Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87:545-564 (Pubitemid 47084680)
11. Parsons JT 2003 Focal adhesion kinase: the first ten years. J Cell Sci 116:1409-1416 (Pubitemid 36527488)
12. Vandenbroucke E, Mehta D, Minshall R, Malik AB 2008 Regulation of endothelial junctional permeability. Ann NY Acad Sci 1123:134-145
13. Janecki A, Jakubowiak A, Steinberger A 1992 Effect of cadmium chloride on transepithelial electrical resistance of Sertoli cell monolayers in two-compartment cultures-a new model for toxicological investigations of the "bloodtestis" barrier in vitro. Toxicol Appl Pharmacol 112:51-57
14. Chung NP, Cheng CY 2001 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 142:1878-1888
15. Cheng CY, Mather JP, Byer AL, Bardin CW 1986 Identification of hormonally responsive proteins in primary Sertoli cell culture medium by anion-exchange high performance liquid chromatography. Endocrinology 118:480-488 (Pubitemid 16162759)
16. Siu MK, Wong CH, Lee WM, Cheng CY 2005 Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J Biol Chem 280:25029-25047 (Pubitemid 40934595)
17. Galdieri M, Ziparo E, Palombi F, Russo MA, Stefanini M 1981 Pure Sertoli cell cultures: a new model for the study of somatic-germ cell interactions. J Androl 2:249-254
18. Lee NP, Mruk DD, Conway AM, Cheng CY 2004 Zyxin, axin, and Wiskott- Aldrich syndrome protein are adaptors that link the cadherin/catenin protein complex to the cytoskeleton at adherens junctions in the seminiferous epithelium of the rat testis. J Androl 25:200-215 (Pubitemid 38240662)
19. Lui WY, Lee WM, Cheng CY 2003 Transforming growth factor-β3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol Reprod 68:1597-1612 (Pubitemid 36519763)
20. Li JC, Lee TW, Mruk TD, Cheng CY 2001 Regulation of Sertoli cell myotubularin (rMTM) expression by germ cells in vitro. J Androl 22:266-277 (Pubitemid 32174188)
21. Lui WY, Lee WM, Cheng CY 2001 Transforming growth factor-β 3 perturbs the inter-Sertoli tight junction permeability barrier in vitro possibly mediated via its effects on occludin, zonula occludens-1, and claudin-11. Endocrinology 142:1865-1877
22. Lee NP, Cheng CY 2003 Regulation of Sertoli cell tight junction dynamics in the rat testis via the nitric oxide synthase/soluble guanylate cyclase/3′,5′-cyclic guanosine monophosphate/protein kinase G signaling pathway: an in vitro study. Endocrinology 144:3114-3129 (Pubitemid 36819914)
23. Yan HH, Mruk DD, Lee WM, Cheng CY 2008 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 22:1945-1959 (Pubitemid 351811471)
24. Yan HH, Cheng CY 2005 Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc Natl Acad Sci USA 102:11722-11727 (Pubitemid 41170793)
25. Li MW, Xia W, Mruk DD, Wang CQ, Yan HH, Siu MK, Lui WY, Lee WM, Cheng CY 2006 TNF α reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol 190:313-329 (Pubitemid 44288369)
26. Meng J, Holdcraft RW, Shima JE, Griswold MD, Braun RE 2005 Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci USA 102:16696-16700 (Pubitemid 41688839)
27. Furuse M, Itoh M, Hirase T, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S 1994 Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J Cell Biol 127:1617-1626 (Pubitemid 24380900)
28. Furuse M, Sasaki H, Tsukita S 1999 Manner of interaction of heterogeneous claudin species withinandbetween tight junction strands. J Cell Biol147:891-903
29. Cheng CY, Mruk DD 2002 Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 82:825-874
30. Gumbiner B 2000 Regulation of cadherin adhesive activity. J Cell Biol 148:399-404 (Pubitemid 30682554)
31. Xia W, Wong EWP, Mruk DD, Cheng CY 2009 TGF-β3 and TNFα perturb blood-testis barrier (BTB) dynamics by accelerating the clathrin-mediated endocytosis of integral membrane proteins: a new concept of BTB regulation during spermatogenesis. Dev Biol 327:48-61
32. Setchell BP 2008 Blood-testis barrier, junctional and transport proteins and spermatogenesis. In: Cheng CY, ed. Molecular mechanisms in spermatogenesis. Austin, TX: Landes Bioscience/Springer Science; 212-233
33. Pelletier RM, Byers SW 1992 The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc Res Tech 20:3-33
34. Sakakibara A, Furuse M, Saitou M, Ando-Akatsuka Y, Tsukita S 1997 Possible involvement of phosphorylation of occludin in tight junction formation. J Cell Biol 137:1393-1401 (Pubitemid 27265950)
35. Tsukamoto T, Nigam S 1999 Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. Am J Physiol 276(5 Pt 2):F737-F750 (Pubitemid 29249693)
36. Cordenonsi M, Mazzon E, Derigo L, Baraldo S, Meggio F, Citi S 1997 Occludin dephosphorylation in early development of Xenopus laevis. J Cell Sci 110:3131-3139
37. Reyes CD, Petrie TA, García AJ 2008 Mixed extracellular matrix ligands synergistically modulate integrin adhesin and signaling. J Cell Physiol 217:450-458
38. Eisinger DA, Ammer H 2008 δ-Opioid receptors activate ERK/MAP kinase via integrin-stimulated receptor tyrosine kinases. Cell Signal 20:2324-2331
39. Bouchard V, Harnois C, Demers MJ, Thibodeau S, Laquerre V, Gauthier R, Vézina A, Noël D, Fujita N, Tsuruo T, Arguin M, Vachon PH 2008 β1-integrin/FAK/Src signaling in intestinal epithelial crypt cell survival: integration of complex regulatory mechanisms. Apoptosis 13:531-542
40. Boutros T, Chevet E, Metrakos P 2008 Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol Rev 60:261-310
41. Wong EW, Mruk DD, Cheng CY 2008 Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim Biophys Acta 1778:692-708
42. 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 epithelium contain α6β1 integrins, and their formation is controlled by follicle-stimulating hormone. Biol Reprod 58:371-378 (Pubitemid 28099101)
43. Palombi F, Salanova M, Tarone G, Farini D, Stefanini M 1992 Distribution of β1 integrin subunit in rat seminiferous epithelium. Biol Reprod 47:1173-1182
44. Yan HH, Cheng CY 2006 Laminin α3 forms a complex with β3 and γ3 chains that serves as the ligand for α6β1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 281:17286-17303 (Pubitemid 43909538)
45. Siu MK, Cheng CY 2004 Interactions of proteases, protease inhibitors, and the β1 integrin/laminin γ3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 70:945-964 (Pubitemid 38387703)
46. Yan HH, Mruk DD, Wong EW, Lee WM, Cheng CY 2008 An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 105:8950-8955
47. Sasaki T, Giltay R, Talts U, Timpl R, Talts JF 2002 Expression and distribution of laminin α1 and α2 chains in embryonic and adult mouse tissues: an immunochemical approach. Exp Cell Res 275:185-199 (Pubitemid 34948361)
48. Mulholland DJ, Dedhar S, Vogl AW 2001 Rat seminiferous epithelium contains a unique junction (ectoplasmic specialization) with signaling properties both of cell/cell and cell/matrix junctions. Biol Reprod 64:396-407 (Pubitemid 32044651)