Epidermal growth factor receptor pathway substrate 8 (Eps8) is a novel regulator of cell adhesion and the blood-testis barrier integrity in the seminiferous epithelium

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2555-2567

  Lie, Pearl P Y ^a   Mruk, Dolores D ^a   Lee, Will M ^b   Yan Cheng, C ^a  

^a POPULATION COUNCIL   (United States)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Actin; Actin dynamics; Germ cells; Sertoli cells; Spermatogenesis

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 8; F ACTIN; OCCLUDIN; PROTEIN ZO1; RNA; UNCLASSIFIED DRUG; 1 (2,4 DICHLOROBENZYL)INDAZOLE 3 CARBOHYDRAZIDE; 1-(2,4-DICHLOROBENZYL)INDAZOLE-3-CARBOHYDRAZIDE; ACTIN; EPS8 PROTEIN, RAT; HYDRAZINE DERIVATIVE; INDAZOLE DERIVATIVE; PRIMER DNA; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD TESTIS BARRIER; CELL ADHESION; CELL CULTURE; CELL ISOLATION; CELL JUNCTION; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; GERM CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KNOCKOUT GENE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; TESTIS; ANIMAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; SPERMATID; SPERMATOGENESIS; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ACTINS; ADHERENS JUNCTIONS; ANIMALS; BASE SEQUENCE; BLOOD-TESTIS BARRIER; CELL ADHESION; CELLS, CULTURED; DNA PRIMERS; HYDRAZINES; INDAZOLES; MALE; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SPERMATIDS; SPERMATOGENESIS;

EID: 68849115313     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.06-070573     Document Type: Article

References (59)

1. Pelletier, R. M., and Byers, S. W. (1992) The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc. Res. Tech. 20, 3-33
2. 2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinology 146, 1893-1908
3. Clermont, Y. (1972) Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198-235
4. Parvinen, M. (1982) Regulation of the seminiferous epithelium. Endocr. Rev. 3, 404-417
5. Carlier, M. F., and Pantaloni, D. (2007) Control of actin assembly dynamics in cell motility. J. Biol. Chem. 282, 23005-23009 (Pubitemid 47311896)
6. DeMali, K. A., and Burridge, K. (2003) Coupling membrane protrusion and cell adhesion. J. Cell Sci. 116, 2389-2397 (Pubitemid 36790121)
7. Lanzetti, L. (2007) Actin in membrane trafficking. Curr. Opin. Cell Biol. 19, 453-458
8. Li, R., and Gundersen, G. G. (2008) Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat. Rev. Mol. Cell Biol. 9, 860-873
9. Pollard, T. D. (1999) Introduction to actin and actin-binding proteins. In Guidebook to the Cytoskeletal and Motor Proteins (Kreis, T., and Vale, R., eds) pp. 3-11, Oxford University Press, New York
10. Disanza, A., Carlier, M. F., Stradal, T. E. B., Didry, D., Frittoli, E., Confalonieri, S., Croce, A., Wehland, J., Di Fiore, P. P., and Scita, G. (2004) Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat. Cell Biol. 6, 1180-1188 (Pubitemid 39625116)
11. Higgs, H. N. (2004) There goes the neighbourhood: Eps8 joins the barbed-end crowd. Nat. Cell Biol. 6, 1147-1149
12. Disanza, A., Mantoani, S., Hertzog, M., Gerboth, S., Frittoli, E., Steffen, A., Berhoerster, K., Kreienkamp, H., Milanesi, F., Di Fiore, P. P., Ciliberto, A., Stradal, T. E. B., and Scita, G. (2006) Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nat. Cell Biol. 8, 1337-1347 (Pubitemid 44835108)
13. Scita, G., Tenca, P., Areces, L. B., Tocchetti, A., Frittoli, E., Giardina, G., Ponzanelli, I., Sini, P., Innocenti, M., and Di Fiore, P. P. (2001) An effector region in Eps8 is responsible for the activation of the Rac-specific GEF activity of Sos-1 and for the proper localization of the Rac-based actin-polymerizing machine. J. Cell Biol. 154, 1031-1044 (Pubitemid 34286182)
14. Offenhauser, N., Borgonovo, A., Disanza, A., Romano, P., Ponzanelli, I., Iannolo, G., Di Fiore, P. P., and Scita, G. (2004) The eps8 family of proteins links growth factor stimulation to actin reorganization generating functional redundancy in the Ras/Rac pathway. Mol. Biol. Cell 15, 91-98 (Pubitemid 38044946)
15. Vogl, A. W., Vaid, K. S., and Guttman, J. A. (2008) The Sertoli cell cytoskeleton. In Molecular Mechanisms in Spermatogenesis (Cheng, C. Y., ed) pp. 186-211, Landes Bioscience/Springer Science, Austin, TX, USA
16. Wong, E. W. P., Mruk, D. D., and Cheng, C. Y. (2008) Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim. Biophys. Acta 1778, 692-708
17. Toyama, Y., Maekawa, M., and Yuasa, S. (2003) Ectoplasmic specializations in the Sertoli cells: new vistas based on genetic defects and testicular toxicology. Anat. Sci. Int. 78, 1-16 (Pubitemid 37062667)
18. Vogl, A. W., Pfeiffer, D. C., Mulholland, D., Kimel, G., and Guttman, J. A. (2000) Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch. Histol. Cytol. 63, 1-15 (Pubitemid 30202188)
19. Yan, H. H. Y., Mruk, D. D., Lee, W. M., and Cheng, C. Y. (2007) Ectoplasmic specialization: a friend or a foe of spermatogenesis? Bioessays 29, 36-48
20. Mruk, D. D., and Cheng, C. Y. (2004) Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr. Rev. 25, 747-806
21. Mruk, D. D., Siu, M. K. Y., Conway, A. M., Lee, N. P. Y., Lau, A. S. N., and Cheng, C. Y. (2003) Role of tissue inhibitor of metalloproteases-1 in junction dynamics in the testis. J. Androl. 24, 510-523
22. Orth, J. M. (1982) Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat. Rec. 203, 485-492
23. Galdieri, M., Ziparo, E., Palombi, F., Russo, M., and Stefanini, M. (1981) Pure Sertoli cell cultures: a new model for the study of somatic-germ cell interactions. J. Androl. 5, 249-259
24. Lee, N. P. Y., Mruk, D. D., Conway, A. M., and Cheng, C. Y. (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
25. Aravindan, G. R., Pineau, C., Bardin, C. W., and Cheng, C. Y. (1996) Ability of trypsin in mimicking germ cell factors that affecf Sertoli cell secretory function. J. Cell. Physiol. 168, 123-133 (Pubitemid 26233440)
26. Pineau, C., Syed, V., Bardin, C. W., Jegou, B., and Cheng, C. Y. (1993) Germ cell-conditioned medium contains multiple factors that modulate the secretion of testins, clusterin, and transferrin by Sertoli cells. J. Androl. 14, 87-98 (Pubitemid 23264403)
27. Cheng, C. Y., Silvestrini, B., Grima, J., Mo, M. Y., Zhu, L. J., Johansson, E., Saso, L., Leone, M. G., Palmery, M., and Mruk, D. D. (2001) Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol. Reprod. 65, 449-461 (Pubitemid 32702309)
28. Mruk, D. D., Silvestrini, B., and Cheng, C. Y. (2008) Anchoring junctions as drug targets: role in contraceptive development. Pharmacol. Rev. 60, 146-180 (Pubitemid 351962007)
29. Cheng, C. Y., Mather, J. P., Byer, A. L., and Bardin, C. W. (1986) Identification of hormonally responsive proteins in primary Sertoli cell culture medium by anion-exchange high performance liquid chromatography. Endocrinology 118, 480-488
30. Siu, M. K. Y., Wong, C. H., Lee, W. M., and Cheng, C. Y. (2005) Sertoli-germ cell anchoring junction dynamics in the tesis are regulated by an interplay of lipid and protein kinases. J. Biol. Chem. 280, 25029-25047
31. Chung, N. P., Mruk, D. D., Mo, M. Y., Lee, W. M., and Cheng, C. Y. (2001) A 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. 65, 1340-1351
32. Russell, L. D., Saxena, N. K., and Weber, J. E. (1987) Intratesticular injection as a method to assess the potential toxicity of various agents to study mechanisms of normal spermatogenesis. Gamete Res. 17, 43-56
33. Di Fiore, P. P., and Scita, G. (2002) Eps8 in the midst of GTPases. Int. J. Biochem. Cell Biol. 34, 1178-1183
34. Russell, L. D., Goh, J. C., Rashed, R. M., and Vogl, A. W. (1988) The consequences of actin disruption at Sertoli ectoplasmic specialization sites facing spermatids after in vivo exposure of rat testis to cytochalasin D. Biol. Reprod. 39, 105-118
35. Lui, W., Lee, W. M., and Cheng, C. Y. (2003) Rho GTPases and spermatogenesis. Biochim. Biophys. Acta 1593, 121-129
36. Yan, H. H. Y., and Cheng, C. Y. (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
37. Russell, L. D., Saxena, N. K., and Turner, T. T. (1989) Cytoskeletal involvment in spermiation and sperm transport. Tissue Cell 21, 361-379
38. Vogl, A. W., Pfeiffer, D. C., Redenbach, D. M., and Grove, B. D. (1993) Sertoli cell cytoskeleton. In The Sertoli Cell (Russell, L. D., and Griswold, M. D., eds) pp. 39-86, Cache River Press, Clearwater, FL, USA
39. Guttman, J. A., Kimel, G. H., and Vogl, A. W. (2000) Dynein and plus-end microtubule-dependent motors are associated with specialized Sertoli cell junction plaques (ectoplasmic specializations). J. Cell Sci. 113, 2167-2176
40. Miller, M. G., Mulholland, D. J., and Vogl, A. W. (1999) Rat testis motor proteins associated with spermatid translocation (dynein) and spermatid flagella (kinesin-II). Biol. Reprod. 60, 1047-1056
41. Vaid, K. S., Guttman, J. A., Singaraja, R. R., and Vogl, A. W. (2007) A kinesin is present at unique Sertoli/spermatid adherens junctions in rat and mouse testes. Biol. Reprod. 77, 1037-1048
42. Velichkova, M., Guttman, J. A., Warren, C., Eng, L., Kline, K., Vogl, A. W., and Hasson, T. (2002) A human homologue of Drosophila kelch associates with myosin-VIIa in specialized adhesion junctions. Cell Motil. Cytoskelet. 51, 147-164 (Pubitemid 34246089)
43. D'Souza, R., Pathak, S., Upadhyay, R., Gaonkar, R., D'Souza, S., Sonawane, S., Gill-Sharma, M., and Balasinor, N. H. (2009) Disruption of tubulobulbar complex by high intratesticular estrogens leading to failed spermiation. [E-pub ahead of print] Endocrinology doi: 10.1210/en.2008-1232
44. Burridge, K., and Wennerberg, K. (2004) Rho and Rac take center stage. Cell 116, 167-179 (Pubitemid 38167310)
45. Wiebe, J. P., Kowalik, A., Gallardi, R. L., Egeler, O., and Clubb, B. H. (2000) Glycerol disrupts tight junction-associated actin microfilaments, occludin, and microtubules in Sertoli cells. J. Androl. 21, 625-635 (Pubitemid 30688260)
46. Wiebe, J. P., Barr, K. J., and Buckingham, K. D. (1989) Sustained azoospermia in squirrel monkey, Saimiri sciureus, resulting from a single intratesticular glycerol injection. Contraception 39, 447-457
47. Wiebe, J. P., and Barr, K. J. (1984) Suppression of spermatogenesis without inhibition of steroidogenesis by 1,2,3-trihydroxypropane solution. Life Sci. 34, 1747-1754
48. De Kretser, D. M., and Kerr, J. B. (1988) The cytology of the testis. In The Physiology of Reproduction (Knobil, E., Neill, J. B., Ewing, L. L., Greenwald, G. S., Markert, C. L., and Pfaff, D. W., eds) pp. 837-932, Raven Press, New York
49. Jou, T., Schneeberger, E. E., and Nelson, W. J. (1998) Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases. J. Cell Biol. 142, 101-115 (Pubitemid 28341143)
50. MacCalman, C. D., Getsios, S., Farookhi, R., and Blaschuk, O. W. (1997) Estrogens potentiate the stimulatory effects of follicle-stimulating hormone on N-cadherin messenger ribonucleic acid levels in cultured mouse Sertoli cells. Endocrinology 138, 41-48 (Pubitemid 27009403)
51. Meng, J., Holdcraft, R. W., Shima, J. E., Griswold, M. D., and Braun, R. E. (2005) Androgens regulate the permeability of the blood-testis barrier. Proc. Natl. Acad. Sci. U. S. A. 102, 16696-16700 (Pubitemid 41688839)
52. Wang, R., Yeh, S., Chen, L., Lin, H., Zhang, C., Ni, J., Wu, C., di Sant'Agnese, P. A., DeMesy-Bentley, K. L., Tzeng, C., and Chang, C. (2006) Androgen receptor in Sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes. Endocrinology 147, 5624-5633 (Pubitemid 44833479)
53. Yan, H. H. Y., Mruk, D. D., Lee, W. M., and Cheng, C. Y. (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
54. Xia, W., Wong, E. W. P., Mruk, D. D., and Cheng, C. Y. (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
55. Siu, M. K. Y., Lee, W. M., and Cheng, C. Y. (2003) The interplay of collagen IV, tumor necrosis factor-α, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell-tight junction dynamics in the rat testis. Endocrinology 144, 371-387
56. Lui, W. Y., Wong, C. H., Mruk, D. D., and Cheng, C. Y. (2003) TGF-β3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 144, 1139-1142
57. Calderwood, D. A., Fujioka, Y., de Pereda, J. M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C., and Ginsberg, M. H. (2003) Integrin β cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. U. S. A. 100, 2272-2277 (Pubitemid 36297489)
58. Maa, M., Lee, J., Chen, Y., Chen, Y., Lee, Y., Wang, S., Huang, C., Chow, N., and Leu, T. (2007) Eps8 facilitates cellular growth and motility of colon cancer cells by increasing the expression and activity of focal adhesion kinase. J. Biol. Chem. 282, 19399-19409 (Pubitemid 47100113)
59. Yan, H. H. Y., Mruk, D. D., Wong, E. W. P., Lee, W. M., and Cheng, C. Y. (2008) An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc. Natl. Acad. Sci. U. S. A. 105, 8950-8955