Regulation of actin dynamics and protein trafficking during spermatogenesis-Insights into a complex process

Critical Reviews in Biochemistry and Molecular Biology

Volumn 48, Issue 2, 2013, Pages 153-172

  Su, Wenhui ^a,b   Mruk, Dolores D ^a   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Actin cytoskeleton; Ectoplasmic specialization; Protein trafficking; Seminiferous epithelial cycle; Spermatogenesis; Testis

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; ACTIN RELATED PROTEIN 3; INTERLEUKIN 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN CDC42; PROTEIN TYROSINE KINASE; STEROID;

ACTIN FILAMENT; ENDOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEMINIFEROUS TUBULE EPITHELIUM; SPERMATOGENESIS; TESTIS;

ACTINS; ANIMALS; CELL ADHESION; CONTRACTILE PROTEINS; CYTOKINES; CYTOSKELETON; HUMANS; MALE; MICROFILAMENT PROTEINS; NEUROPEPTIDES; PROTEIN TRANSPORT; SEMINIFEROUS EPITHELIUM; SERTOLI CELLS; SPERMATOGENESIS; TESTIS;

MAMMALIA;

EID: 84875621531     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2012.758084     Document Type: Review

References (232)

1. Ahmed S, Goh WI, Bu W. (2010). I-BAR domains, IRSp53 and filopodium formation. Semin Cell Dev Biol 21:350-6
2. Aitken A. (2006). 14-3-3 proteins: a historic overview. Semin Cancer Biol 16:162-72
3. Al-Sadi R, Boivin M, Ma T. (2009). Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci 14:2765-78
4. Amlani S, Vogl A. (1988). Changes in the distribution of microtubules and intermediate filaments in mammalian Sertoli cells during spermatogenesis. Anat Rec 220:143-60
5. Anitei M, Hoflack B. (2011). Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nat Cell Biol 14:11-19
6. Aronova S, Wedaman K, Anderson S, et al. (2007). Probing the membrane environment of the TOR kinases reveals functional interactions between TORC1, actin, and membrane trafficking in Saccharomyces cerevisiae. Mol Biol Cell 18:2779-94
7. Assemat E, Bazellieres E, Pallesi-Pocachard E, et al. (2008). Polarity complex proteins. Biochim Biophys Acta 1778:614-30
8. Baek KH. (2004). Structural and functional conservation of the lgl recessive oncogenes (Review). Int J Oncol 24:1257-61
9. Balklava Z, Pant S, Fares H, Grant BD. (2007). Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 9:1066-73
10. Bartles J, Wierda A, Zheng L. (1996). Identification and characterization of espin, an actin-binding protein localized to the F-actin-rich junctional plaques of Sertoli cell ectoplasmic specializations. J Cell Sci 109:1229-39
11. Beardsley A, Robertson DM, O'Donnell L. (2006). A complex containing a6b1-integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J Endocrinol 190:759-70
12. Betschinger J, Eisenhaber F, Knoblich JA. (2005). Phosphorylationinduced autoinhibition regulates the cytoskeletal protein Lethal (2) giant larvae. Curr Biol 15:276-82
13. Betschinger J, Mechtler K, Knoblich JA. (2003). The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl. Nature 422:326-30
14. Bialucha CU, Ferber EC, Pichaud F, et al. (2007). p32 is a novel mammalian Lgl binding protein that enhances the activity of protein kinase Czeta and regulates cell polarity. J Cell Biol 178:575-81
15. Bilder D, Perrimon N. (2000). Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403:676-80
16. Biou V, Brinkhaus H, Malenka RC, Matus A. (2008). Interactions between drebrin and Ras regulate dendritic spine plasticity. Eur J Neurosci 27:2847-59
17. Boggiano JC, Fehon RG. (2012). Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev Cell 22:695-702
18. 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
19. Carreau S, Hess RA. (2010). Oestrogens and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365:1517-35
20. Cavey M, Rauzi M, Lenne PF, Lecuit T. (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453:751-6
21. Chaudhary J, Skinner MK. (2000). Characterization of a novel transcript of 14-3-3 theta in Sertoli cells. J Androl 21:730-8
22. Cheng CY, Lie PPY, Wong EWP, et al. (2011a). Adjudin disrupts spermatogenesis via the action of some unlikely partners: eps8, Arp2/3 complex, drebrin E, PAR6 and 14-3-3. Spermatogenesis 1:291-7
23. Cheng CY, Mruk DD. (2002). Cell junction dynamics in the testis: sertoli-germ cell interactions and male contraceptive development. Physiol Rev 82:825-74
24. Cheng CY, Mruk DD. (2009). Regulation of blood-testis barrier dynamics by focal adhesion kinase (FAK). An unexpected turn of events. Cell Cycle 8:3493-9
25. Cheng CY, Mruk DD. (2010). A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 6:380-95
26. Cheng CY, Mruk DD. (2011a). Actin binding proteins and spermiogenesis: some unexpected findings. Spermatogenesis 1:99-104
27. Cheng CY, Mruk DD. (2011b). Regulation of spermiogenesis, spermiation and blood-testis barrier dynamics: novel insights from studies on Eps8 and Arp3. Biochem J 435:553-62
28. Cheng CY, Mruk DD. (2012b). The blood-testis barrier and its implications for male contraception. Pharmacol Rev 64:16-64
29. Cheng J, Watkins SC, Walker WH. (2007). Testosterone activates mitogen-activated protein kinase via Src kinase and the epidermal growth factor receptor in Sertoli cells. Endocrinology 148:2066-74
30. Cheng YH, Wong EWP, Cheng CY. (2011). Cancer/testis (CT) antigens, carcinogenesis and spermatogenesis. Spermatogenesis 1:209-20
31. Chlenski A, Ketels KV, Korovaitseva GI, et al. (2000). Organization and expression of the human zo-2 gene (tjp-2) in normal and neoplastic tissues. Biochim Biophys Acta 1493:319-24
32. Chung NPY, 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 142:1878-88
33. Cohen D, Musch A, Rodriguez-Boulan E. (2001). Selective control of basolateral membrane protein polarity by cdc42. Traffic 2:556-64
34. Conn CS, Qian SB. (2011). mTOR signaling in protein homeostasis: less is more? Cell Cycle 10:1940-7
35. de Kretser DM, Kerr JB. (1988). The cytology of the testis. In: Knobil E, Neill JB, Ewing LL, et al., eds. The physiology of reproduction. Vol. 1. New York: Raven Press, 837-932
36. Dow LE, Elsum IA, King CL, et al. (2008). Loss of human Scribble cooperates with H-Ras to promote cell invasion through deregulation of MAPK signalling. Oncogene 27:5988-6001
37. Dow LE, Kauffman JS, Caddy J, et al. (2007). The tumour-suppressor Scribble dictates cell polarity during directed epithelial migration: regulation of Rho GTPase recruitment to the leading edge. Oncogene 26:2272-82
38. Dubrovskaya V, Lavigne AC, Davidson I, et al. (1996). Distinct domains of hTAFII100 are required for functional interaction with transcription factor TFIIF beta (RAP30) and incorporation into the TFIID complex. EMBO J 15:3702-12
39. Ellenbroek SI, Iden S, Collard JG. (2012). Cell polarity proteins and cancer. Semin Cancer Biol 22:208-15
40. Fagerholm S, Morrice N, Gahmberg CG, Cohen P. (2002). Phosphorylation of the cytoplasmic domain of the integrin CD18 chain by protein kinase C isoforms in leukocytes. J Biol Chem 277:1728-38
41. Franca LR, Auharek SA, Hess RA, et al. (2012). Blood-tissue barriers: morphofunctional and immunological aspects of the blood-testis and blood-epididymal barriers. Adv Exp Med Biol 763:237-59
42. Fujita E, Tanabe Y, Hirose T, et al. (2007). Loss of partitioningdefective- 3/isotype-specific interacting protein (par-3/ASIP) in the elongating spermatid of RA175 (IGSF4A/SynCAM)-deficient mice. Am J Pathol 171:1800-10
43. Gerard N, Syed V, Jegou B. (1992). Lipopolysaccharide, latex beads and residual bodies are potent activators of Sertoli cell interleukin-1 alpha production. Biochem Biophys Res Commun 185:154-61
44. Glaunsinger BA, Weiss RS, Lee SS, Javier R. (2001). Link of the unique oncogenic properties of adenovirus type 9 E4-ORF1 to a select interaction with the candidate tumor suppressor protein ZO-2. EMBO J 20:5578-86
45. Gliki G, Ebnet K, Aurrand-Lions M, et al. (2004). Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 431:320-4
46. Gohla A, Bokoch GM. (2002). 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr Biol 12:1704-10
47. Goldstein B, Macara IG. (2007). The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13:609-22
48. Gonnord P, Blouin CM, Lamaze C. (2012). Membrane trafficking and signaling: two sides of the same coin. Semin Cell Dev Biol 23:154-64
49. Green KJ, Getsios S, Troyanovsky S, Godsel LM. (2010). Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol 2:a000125
50. Green KJ, Simpson CL. (2007). Desmosomes: new perspectives on a classic. J Invest Dermatol 127:2499-515
51. Grintsevich EE, Galkin VE, Orlova A, et al. (2010). Mapping of drebrin binding site on F-actin. J Mol Biol 398:542-54
52. Guttman JA, Obinata T, Shima J, et al. (2004). Non-muscle cofilin is a component of tubulobulbar complexes in the testis. Biol Reprod 70:805-12
53. Hall JE, Fu W, Schaller MD. (2011). Focal adhesion kinase: exploring FAK structure to gain insight into function. Int Rev Cell Mol Biol 288:185-225
54. Han DC, Rodriguez LG, Guan JL. (2001). Identification of a novel interaction between integrin beta1 and 14-3-3beta. Oncogene 20:346-57
55. Hara Y, Yamagata K, Oguchi K, Baba T. (2008). Nuclear localization of profilin III-ArpM1 complex in mouse spermiogenesis. FEBS Lett 582:2998-3004
56. Hartwig JH, Stossel TP. (1975). Isolation and properties of actin, myosin, and a new actinbinding protein in rabbit alveolar macrophages. J Biol Chem 250:5696-705
57. Hayashi K, Ishikawa R, Kawai-Hirai R, et al. (1999). Domain analysis of the actin-binding and actin-remodeling activities of drebrin. Exp Cell Res 253:673-80
58. Heasman SJ, Ridley AJ. (2008). Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9:690-701
59. Hertzog M, Milanesi F, Hazelwood L, et al. (2010). Molecular basis for the dual function of Eps8 on actin dynamics: bundling and capping. PLoS Biol 8:e1000387
60. Hough CD, Woods DF, Park S, Bryant PJ. (1997). Organizing a functional junctional complex requires specific domains of the Drosophila MAGUK Discs large. Genes Dev 11:3242-53
61. Iden S, Collard JG. (2008). Crosstalk between small GTPases and polarity proteins in cell polarization. Nature Rev Mol Cell Biol 9:846-59
62. Iden S, Rehder D, August B, et al. (2006). A distinct PAR complex associates physically with VE-cadherin in vertebrate endothelial cells. EMBO Rep 7:1239-46
63. Inoki K, Mori H, Wang J, et al. (2011). mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. J Clin Invest 121:2181-96
64. Insall RH, Machesky LM. (2009). Actin dynamics at the leading edge: from simple machinery to complex networks. Dev Cell 17:310-22
65. Ishikawa R, Hayashi K, Shirao T, et al. (1994). Drebrin, a developmentassociated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J Biol Chem 269:29928-33
66. Ivanov AI, Young C, Den Beste K, et al. (2010). Tumor suppressor scribble regulates assembly of tight junctions in the intestinal epithelium. Am J Pathol 176:134-45
67. Jaffe AB, Hall A. (2005). Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-69
68. 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 ''blood-testis'' barrier in vitro. Toxicol Appl Pharmacol 112:51-7
69. Jin J, Smith FD, Stark C, et al. (2004). Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr Biol 14:1436-50
70. Joberty G, Petersen C, Gao L, Macara IG. (2000). The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol 2:531-9
71. Kamberov E, Makarova O, Roh M, et al. (2000). Molecular cloning and characterization of Pals, proteins associated with mLin-7. J Biol Chem 275:11425-31
72. Klezovitch O, Fernandez TE, Tapscott SJ, Vasioukhin V. (2004). Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev 18:559-71
73. Koch M, Olson P, Albus A, et al. (1999). Characterization and expression of the laminin g3 chain: a novel, non-basement membrane-associated, laminin chain. J Cell Biol 145:605-18
74. Kroschewski R, Hall A, Mellman I. (1999). Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells. Nat Cell Biol 1:8-13
75. Laprise P, Chailler P, Houde M, et al. (2002). Phosphatidylinositol 3-kinase controls human intestinal epithelial cell differentiation by promoting adherens junction assembly and p38 MAPK activation. J Biol Chem 277:8226-34
76. Laprise P, Viel A, Rivard N. (2004). Human homolog of disc-large is required for adherens junction assembly and differentiation of human intestinal epithelial cells. J Biol Chem 279:10157-66
77. Lee NPY, 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 25:200-15
78. Lee NPY, Mruk DD, Lee WM, Cheng CY. (2003). Is the cadherin/ catenin complex a functional unit of cell-cell-actin-based adherens junctions (AJ) in the rat testis? Biol Reprod 68:489-508
79. Legouis R, Jaulin-Bastard F, Schott S, et al. (2003). Basolateral targeting by leucine-rich repeat domains in epithelial cells. EMBO Rep 4:1096-102
80. Lemmers C, Medina E, Delgrossi MH, et al. (2002). hINADl/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J Biol Chem 277:25408-15
81. Li D, Roberts R. (2001). WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell Mol Life Sci 58:2085-97
82. Li MW, Mruk DD, Cheng CY. (2009a). Mitogen-activated protein kinases in male reproductive function. Trends Mol Med 15:159-68
83. Li MW, Mruk DD, Lee WM, Cheng CY. (2009b). Cytokines and junction restructuring events during spermatogenesis in the testis: an emerging concept of regulation. Cytokine Growth Factor Rev 20:329-38
84. Li MW, Xia W, Mruk DD, et al. (2006). Tumor necrosis factor {alpha} reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol 190:313-29
85. Li MW, Xiao X, Mruk DD, et al. (2011). Actin-binding protein drebrin E is involved in junction dynamics during spermatogenesis. Spermatogenesis 1:123-36
86. Li MWM, Mruk DD, Cheng CY. (2012). Gap junctions and blood-tissue barriers. Adv Exp Med Biol 763:260-80
87. Lie PP, Chan AY, Mruk DD, Lee WM, Cheng CY. (2010b). Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 107:11411-16
88. Lie PPY, Cheng CY, Mruk DD. (2009b). Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem Sci 34:366-73
89. Lie PP, Cheng CY, Mruk DD. (2011). Interleukin-1alpha is a regulator of the blood-testis barrier. FASEB J 25:1244-53
90. Lie PP, Mruk DD, Lee WM, Cheng CY. (2009a). 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 J 23:2555-67
91. Lie PP, Mruk DD, Lee WM, Cheng CY. (2010a). Cytoskeletal dynamics and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365:1581-92
92. Lie PP, Mruk DD, Mok KW, et al. (2012). Focal adhesion kinase-Tyr407 and -Tyr397 exhibit antagonistic effects on blood-testis barrier dynamics in the rat. Proc Natl Acad Sci USA 109:12562-7
93. Lin D, Edwards AS, Fawcett JP, et al. (2000). A mammalian PAR-3- PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2:540-7
94. Liu L, Chen L, Chung J, Huang S. (2008). Rapamycin inhibits F-actin reorganization and phosphorylation of focal adhesion proteins. Oncogene 27:4998-5010
95. Lui WY, Lee WM, Cheng CY. (2001). 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 142:1865-77
96. Lui WY, Lee WM, Cheng CY. (2003a). Rho GTPases and spermatogenesis. Biochim Biophys Acta 1593:121-9
97. Lui WY, Lee WM, Cheng CY. (2003b). Sertoli-germ cell adherens junction dynamics in the testis are regulated by RhoB GTPase via the ROCK/LIMK signaling pathway. Biol Reprod 68:2189-206
98. Lui WY, Mruk DD, Cheng CY. (2005). Interactions among IQGAP1, Cdc42, and the cadherin/catenin protein complex regulate Sertoligerm cell adherens junction dynamics in the testis. J Cell Physiol 202:49-66
99. Lui WY, Wong CH, Mruk DD, Cheng CY. (2003c). TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 144:1139-42
100. Lutzelschwab R, Klambt C, Rossa R, Schmidt O. (1987). A protein product of the Drosophila recessive tumor gene, l (2) giant gl, potentially has cell adhesion properties. EMBO J 6:1791-7
101. Macara IG, Spang A. (2006). Closing the GAP between polarity and vesicle transport. Cell 125:419-21
102. Magnuson B, Ekim B, Fingar DC. (2012). Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 441:1-21
103. Majoul I, Shirao T, Sekino Y, Duden R. (2007). Many faces of drebrin: from building dendritic spines and stabilizing gap junctions to shaping neurite-like cell processes. Histochem Cell Biol 127: 355-61
104. Makarova O, Roh MH, Liu CJ, et al. (2003). Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene 302:21-9
105. Manabe N, Hirai S, Imai F, et al. (2002). Association of ASIP/mPAR-3 with adherens junctions of mouse neuroepithelial cells. Dev Dyn 225:61-9
106. Mege RM, Gavard J, Lambert M. (2006). Regulation of cell-cell junctions by the cytoskeleton. Curr Opin Cell Biol 18:541-8
107. Meng J, Holdcraft RW, Shima JE, et al. (2005). Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci USA 102:16696-70
108. Metais JY, Navarro C, Santoni MJ, et al. (2005). hScrib interacts with ZO-2 at the cell-cell junctions of epithelial cells. FEBS Lett 579:3725-30
109. Michel D, Arsanto JP, Massey-Harroche D, et al. (2005). PATJ connects and stabilizes apical and lateral components of tight junctions in human intestinal cells. J Cell Sci 118:4049-57
110. Mironova E, Millette CF. (2008). Expression of the diaphanous-related formin proteins mDia1 and mDia2 in the rat testis. Dev Dyn 237:2170-6
111. Mitra SK, Schlaepfer DD. (2006). Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18:516-23
112. Mogilner A, Allard J, Wollman R. (2012). Cell polarity: quantitative modeling as a tool in cell biology. Science 336:175-9
113. Mok KW, Mruk DD, Cheng CY. (2013a). Regulation of blood-testis barrier (BTB) dynamics during spermatogenesis via the ''yin'' and ''yang'' effects of the mammalian target of rapamycin complex 1 (mTORC1) and mTORC2. Int Rev Cell Mol Biol 301:291-358. Available from: http://dxdoiorg/101016/B978-0-12-407704- 1. 00006-3
114. Mok KW, Mruk DD, Lee WM, Cheng CY. (2012a). Spermatogonial stem cells alone are not sufficient to re-initiate spermatogenesis in the rat testis following adjudin-induced infertility. Int J Androl 35:86-101
115. Mok KW, Mruk DD, Lee WM, Cheng CY. (2013b). Rictor/mTORC2 regulates blood-testis barrier dynamics via its effects on gap junction communications and actin filament network. FASEB J (in press) DOI:101096/fj12-212977
116. Mok KW, Mruk DD, Silvestrini B, Cheng CY. (2012b). rpS6 regulates blood-testis barrier dynamics by affecting F-actin organization and protein recruitment. Endocrinology 153:5036-48
117. Mooren OL, Galletta BJ, Cooper JA. (2012). Roles of actin assembly in endocytosis. Annu Rev Biochem 81:661-86
118. Morrison DK. (2009). The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19:16-23
119. Morton DG, Shakes DC, Nugent S, et al. (2002). The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Dev Biol 241:47-58
120. Mruk DD, Cheng CY. (2004a). Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol Metab 15:439-47
121. Mruk DD, Cheng CY. (2004b). 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
122. Mruk DD, Cheng CY. (2008). Delivering non-hormonal contraceptives to men: advances and obstacles. Trends Biotechnol 26:90-9
123. Mruk DD, Cheng CY. (2011). The myotubularin family of lipid phosphatases in disease and in spermatogenesis. Biochem J 433:253-62
124. Mruk DD, Silvestrini B, Cheng CY. (2008). Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 60:146-80
125. 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
126. Musch A, Cohen D, Kreitzer G, Rodriguez-Boulan E. (2001). cdc42 regulates the exit of apical and basolateral proteins from the trans- Golgi network. EMBO J 20:2171-9
127. Musch A, Cohen D, Yeaman C, et al. (2002). Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells. Mol Biol Cell 13:158-68
128. Nagasaka K, Pim D, Massimi P, et al. (2010). The cell polarity regulator hScrib controls ERK activation through a KIM site-dependent interaction. Oncogene 29:5311-21
129. Nakagawa S, Huibregtse JM. (2000). Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol Cell Biol 20:8244-53
130. Nakamura F, Stossel TP, Hartwig JH. (2011). The filamins: organizers of cell structure and function. Cell Adh Migr 5:160-9
131. Noatynska A, Gotta M. (2012). Cell polarity and asymmetric cell division: the C. elegans early embryo. Essays Biochem 53:1-14
132. O'Donnell L, Meachem SJ, Stanton PG, McLachlan RI. (2006). Endocrine regulation of spermatogenesis. In: Neill JD, ed. Physiology of reproduction. 3rd ed. Amsterdam: Elsevier, 1017-69
133. O'Donnell L, Nicholls PK, O'Bryan MK, et al. (2011). Spermiation: the process of sperm release. Spermatogenesis 1:14-35
134. O'Donnell L, Robertson KM, Jones ME, Simpson ER. (2001). Estrogen and spermatogenesis. Endocr Rev 22:289-318
135. Ohtoshi A, Maeda T, Higashi H, et al. (2000). Human p55(CDC)/Cdc20 associates with cyclin A and is phosphorylated by the cyclin A-Cdk2 complex. Biochem Biophys Res Commun 268:530-4
136. Otani T, Ichii T, Aono S, Takeichi M. (2006). Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J Cell Biol 175:135-46
137. Ozaki-Kuroda K, Nakanishi H, Ohta H, et al. (2002). Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 12:1145-50
138. Parvinen M. (1982). Regulation of the seminiferous epithelium. Endocr Rev 3:404-17
139. Peitsch WK, Grund C, Kuhn C, et al. (1999). Drebrin is a widespread actin-associating protein enriched at junctional plaques, defining a specific microfilament anchorage system in polar epithelial cells. Eur J Cell Biol 78:767-78
140. Peitsch WK, Hofmann I, Pratzel S, et al. (2001). Drebrin particles: components in the ensemble of proteins regulating actin dynamics of lamellipodia and filopodia. Eur J Cell Biol 80:567-79
141. Pellegrin S, Mellor H. (2007). Actin stress fibres. J Cell Sci 120: 3491-9
142. Pelletier RM. (2011). The blood-testis barrier: the junctional permeability, the proteins and the lipids. Prog Histochem Cytochem 46:49-127
143. Perego L, Berruti G. (1997). Molecular cloning and tissue-specific expression of the mouse homologue of the rat brain 14-3-3 theta protein: characterization of its cellular and developmental pattern of expression in the male germ line. Mol Reprod Dev 47:370-9
144. Pozuelo Rubio M, Geraghty KM, Wong BH, et al. (2004). 14-3-3- affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem J 379:395-408
145. Qin Y, Capaldo C, Gumbiner BM, Macara IG. (2005). The mammalian Scribble polarity protein regulates epithelial cell adhesion and migration through E-cadherin. J Cell Biol 171:1061-71
146. Redenbach DM, Vogl AW. (1991). Microtubule polarity in Sertoli cells: a model for microtubule-based spermatid transport. Eur J Cell Biol 54:277-90
147. Ridley AJ. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522-9
148. Roh MH, Fan S, Liu CJ, Margolis B. (2003). The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J Cell Sci 116:2895-906
149. Roh MH, Liu CJ, Laurinec S, Margolis B. (2002a). The carboxyl terminus of zona occludens-3 binds and recruits a mammalian homologue of discs lost to tight junctions. J Biol Chem 277:27501-9
150. Roh MH, Makarova O, Liu CJ, et al. (2002b). The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J Cell Biol 157:161-72
151. Roh MH, Margolis B. (2003). Composition and function of PDZ protein complexes during cell polarization. Am J Physiol Renal Physiol 285:F377-87
152. Rotkopf S, Hamberg Y, Aigaki T, et al. (2011). The WASp-based actin polymerization machinery is required in somatic support cells for spermatid maturation and release. Development 138: 2729-39
153. Russell LD. (1977). Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 148:313-28
154. Russell LD. (1979). Further observations on tubulobulbar complexes formed by late spermatids and Sertoli cells in the rat testis. Anat Rec 194:213-32
155. Russell LD, Peterson RN. (1985). Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 94:177-211
156. Russell LD, Ren HP, Sinha Hikim I, et al. (1990). A comparative study in twelve mammalian species of volume densities, volumes, and numerical densities of selected testis components, emphasizing those related to the Sertoli cell. Am J Anat 188:21-30
157. Sarkar O, Mathur PP, Cheng CY, Mruk DD. (2008). Interleukin 1 alpha (IL1A) is a novel regulator of the blood-testis barrier in the rat. Biol Reprod 78:445-54
158. Sharpe RM. (1994). Regulation of spermatogenesis. In: Knobil E, Neill JD, eds. The physiology of reproduction. New York: Raven Press, 1363-434
159. Shin K, Straight S, Margolis B. (2005). PATJ regulates tight junction formation and polarity in mammalian epithelial cells. J Cell Biol 168:705-11
160. Shin K, Fogg VC, Margolis B. (2006). Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22:207-35
161. Shirao T. (1995). The roles of microfilament-associated proteins, drebrins, in brain morphogenesis: a review. J Biochem 117:231-6
162. Shirao T, Hayashi K, Ishikawa R, et al. (1994). Formation of thick, curving bundles of actin by drebrin A expressed in fibroblasts. Exp Cell Res 215:145-53
163. Shivas JM, Skop AR. (2012). Arp2/3 mediates early endosome dynamics necessary for the maintenance of PAR asymmetry in Caenorhabditis elegans. Mol Biol Cell 23:1917-27
164. Shorning BY, Griffiths D, Clarke AR. (2011). Lkb1 and Pten synergise to suppress mTOR-mediated tumorigenesis and epithelialmesenchymal transition in the mouse bladder. PLoS One 6:e16209
165. Simpson CL, Patel DM, Green KJ. (2011). Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis. Nat Rev Mol Cell Biol 12:565-80
166. Singh R, Wang B, Shirvaikar A, et al. (1999). The IL-1 receptor and Rho directly associate to drive cell activation in inflammation. J Clin Invest 103:1561-70
167. Siu MK, Cheng CY. (2004). Interactions of proteases, protease inhibitors, and the beta1 integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 70:945-64
168. Siu MK, Lee WM, Cheng CY. (2003a). The interplay of collagen IV, tumor necrosis factor-alpha, 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 144:371-87
169. Siu MK, Mruk DD, Lee WM, Cheng CY. (2003b). Adhering junction dynamics in the testis are regulated by an interplay of beta 1-integrin and focal adhesion complex-associated proteins. Endocrinology 144:2141-63
170. 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 280:25029-47
171. Siu ER, Wong EW, Mruk DD, et al. (2009a). Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 106:9298-303
172. Siu ER, Wong EW, Mruk DD, et al. (2009b). An occludin-focal adhesion kinase protein complex at the blood-testis barrier: a study using the cadmium model. Endocrinology 150:3336-44
173. Smith BE, Braun RE. (2012). Germ cell migration across Sertoli cell tight junctions. Science 338:798-802
174. Steinberger E. (1971). Hormonal control of mammalian spermatogenesis. Physiol Rev 51:1-22
175. Straight SW, Chen L, Karnak D, Margolis B. (2001). Interaction with mLin-7 alters the targeting of endocytosed transmembrane proteins in mammalian epithelial cells. Mol Biol Cell 12:1329-40
176. Su L, Cheng CY, Mruk DD. (2010). Adjudin-mediated Sertoli-germ cell junction disassembly affects Sertoli cell barrier function in vitro and in vivo. Int J Biochem Cell Biol 42:1864-75
177. Su W, Mruk DD, Cheng CY. (2012a). Filamin A: a regulator of blood-testis barrier assembly during post-natal development. Spermatogenesis 2:73-8
178. Su W, Mruk DD, Lie PPY, et al. (2012b). Filamin A is a regulator of blood-testis barrier assembly during postnatal development in the rat testis. Endocrinology 153:5023-35
179. Su WH, Mruk DD, Wong EWP, et al. (2012d). Polarity protein complex Scribble/Lgl/Dlg and epithelial cell barriers. Adv Exp Med Biol 763:149-70
180. Su WH, Wong EWP, Mruk DD, Cheng CY. (2012c). The Scribble/Lgl/ Dlg polarity protein complex is a regulator of blood-testis barrier dynamics and spermatid polarity during spermatogenesis. Endocrinology 153:6041-53
181. Sun S, Wong EW, Li MW, et al. (2009). 14-3-3 and its binding partners are regulators of protein-protein interactions during spermatogenesis. J Endocrinol 202:327-36
182. Suzuki A, Yamanaka T, Hirose T, et al. (2001). Atypical protein kinase C is involved in the evolutionarily conserved par protein complex and plays a critical role in establishing epithelia-specific junctional structures. J Cell Biol 152:1183-96
183. Syed V, Stephan JP, Gerard N, et al. (1995). Residual bodies activate Sertoli cell interleukin-1 alpha (IL-1 alpha) release, which triggers IL- 6 production by an autocrine mechanism, through the lipoxygenase pathway. Endocrinology 136:3070-8
184. Takekuni K, Ikeda W, Fujito T, et al. (2003). Direct binding of cell polarity protein PAR-3 to cell-cell adhesion molecule nectin at neuroepithelial cells of developing mouse. J Biol Chem 278:5497-500
185. Tang EI, Xiao X, Mruk DD, et al. (2012). Microtubule affinity-regulated kinase 4 (MARK4) is a component of the ectoplasmic specialization in the rat testis. Spermatogenesis 2:117-26
186. Tepass U. (2012). The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morplhogenesis, cell growth, and survival. Annu Rev Cell Dev Biol 28:655-85
187. Tubb B, Mulholland DJ, Volg AW, et al. (2002). Testis fascin (FSCN3): a novel paralog of the actin-bundling protein fascin expressed specifically in the elongate spermatid head. Exp Cell Res 275:92-109
188. Vaggi F, Disanza A, Milanesi F, et al. (2011). The Eps8/IRSp53/VASP network differentially controls actin capping and bundling in filopodia formation. PLoS Comput Biol 7:e1002088
189. Vaid KS, Guttman JA, Babyak N, et al. (2007). The role of dynamin 3 in the testis. J Cell Physiol 210:644-54
190. Vogl AW, Pfeiffer DC, Mulholland D, et al. (2000). Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch Histol Cytol 63:1-15
191. Vogl AW, Soucy LJ. (1985). Arrangement and possible function of actin filament bundles in ectoplasmic specializations of ground squirrel Sertoli cells. J Cell Biol 100:814-25
192. Vogl AW, Vaid KS, Guttman JA. (2008). The Sertoli cell cytoskeleton. Adv Exp Med Biol 636:186-211
193. Wahab-Wahlgren A, Holst M, Ayele D, et al. (2000). Constitutive production of interleukin-1alpha mRNA and protein in the developing rat testis. Int J Androl 23:360-5
194. Walker WH. (2010). Non-classical actions of testosterone and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365:1557-69
195. Walker WH. (2011). Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis 1:116-20
196. Walsh SV, Hopkins AM, Nusrat A. (2000). Modulation of tight junction structure and function by cytokines. Adv Drug Deliv Rev 41:303-13
197. Wang Q, Chen XW, Margolis B. (2007). PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol Biol Cell 18:874-85
198. Wang RS, Yeh S, Chen LM, et al. (2006). Androgen receptor in Sertoli cell is essential for germ cell nursery and junction complex formation in mouse testes. Endocrinology 147:5624-33
199. Wang F, Zhang Q, Cao J, et al. (2008). The microtubule plus end-binding protein EB1 is involved in Sertoli cell plasticity in testicular seminiferous tubules. Exp Cell Res 314:213-26
200. Weaver AM, Heuser JE, Karginov AV, et al. (2002). Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol 12:1270-8
201. Weaver AM, Young ME, Lee WL, Cooper JA. (2003). Integration of signals to the Arp2/3 complex. Curr Opin Cell Biol 15:23-30
202. Wells CD, Fawcett JP, Traweger A, et al. (2006). A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 125:535-48
203. Whitmarsh AJ. (2009). Filamin B: a scaffold for interferon signalling. EMBO Rep 10:349-51
204. Winters SJ, Moore JP. (2004). Intra-pituitary regulation of gonadotrophs in male rodents and primates. Reproduction 128:13-23
205. Winters SJ, Moore JP. (2007). Paracrine control of gonadotrophs. Semin Reprod Med 25:379-87
206. Witte H, Bradke F. (2008). The role of the cytoskeleton during neuronal polarization. Curr Opin Neurobiol 18:479-87
207. Wolski KM, Perrault C, Tran-Son-Tay R, Cameron DF. (2005). Strength measurement of the Sertoli-spermatid junctional complex. J Androl 26:354-9
208. Wong EW, Cheng CY. (2009). Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol Biol 278:309-53
209. Wong EWP, Cheng CY. (2011). Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol Sci 32:290-9
210. Wong EW, Mruk DD, Cheng CY. (2008a). Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim Biophys Acta 1778:692-708
211. Wong EW, Mruk DD, Lee WM, Cheng CY. (2008b). Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and bloodtestis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 105:9657-62
212. Wong EW, Mruk DD, Lee WM, Cheng CY. (2010). Regulation of bloodtestis barrier dynamics by TGF-b3 is a Cdc42-dependent protein trafficking event. Proc Natl Acad Sci USA 107:11399-404
213. Wong CH, Mruk DD, Lui WY, Cheng CY. (2004). Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 117:783-98
214. Wong EW, Sun S, Li MW, et al. (2009). 14-3-3 Protein regulates cell adhesion in the seminiferous epithelium of rat testes. Endocrinology 150:4713-23
215. Woods DF, Bryant PJ. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66:451-64
216. Xia W, Cheng CY. (2005). TGF-beta3 regulates anchoring junction dynamics in the seminiferous epithelium of the rat testis via the Ras/ ERK signaling pathway: an in vivo study. Dev Biol 280:321-43
217. Xia W, Mruk DD, Lee WM, Cheng CY. (2006). Differential interactions between transforming growth factor-beta3/TbetaR1, TAB1, and CD2AP disrupt blood-testis barrier and Sertoli-germ cell adhesion. J Biol Chem 281:16799-813
218. Xiao X, Mruk DD, Cheng FL, Cheng CY. (2012). c-Src and c-Yes are two unlikely partners of spermatogenesis and their roles in bloodtestis barrier dynamics. Adv Exp Med Biol 763:295-317
219. Xiao X, Mruk DD, Lee WM, Cheng CY. (2011). c-Yes regulates cell adhesion at the blood-testis barrier and the apical ectoplasmic specialization in the seminiferous epithelium of rat testes. Int J Biochem Cell Biol 43:651-65
220. Yamada S, Nelson WJ. (2007). Synapses: sites of cell recognition, adhesion, and functional specification. Annu Rev Biochem 76:267-94
221. Yamanaka T, Horikoshi Y, Izumi N, et al. (2006). Lgl mediates apical domain disassembly by suppressing the PAR-3-aPKC-PAR-6 complex to orient apical membrane polarity. J Cell Sci 119:2107-18
222. Yamanaka T, Horikoshi Y, Sugiyama Y, et al. (2003). Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr Biol 13:734-43
223. 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 102:11722-7
224. Yan HH, Cheng CY. (2006). Laminin alpha 3 forms a complex with beta3 and gamma3 chains that serves as the ligand for alpha 6beta1- integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 281:17286-303
225. 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 22:1945-59
226. Yazama F, Sawada H, Hirosawa K, et al. (1991). Deep-etch visualization of the Sertoli cell (blood-testis) barrier in the boar. Tissue Cell 23:235-46
227. Young JS, Guttman JA, Vaid KS, et al. (2009b). Cortactin (CTTN), N-WASP (WASL), and clathrin (CLTC) are present at podosome-like tubulobulbar complexes in the rat testis. Biol Reprod 80:153-61
228. Young JS, Guttman JA, Vaid KS, Vogl AW. (2009a). Tubulobulbar complexes are intercellular podosome-like structures that internalize intact intercellular junctions during epithelial remodeling events in the rat testis. Biol Reprod 80:162-74
229. Zeitler J, Hsu CP, Dionne H, Bilder D. (2004). Domains controlling cell polarity and proliferation in the Drosophila tumor suppressor Scribble. J Cell Biol 167:1137-46
230. Zhan L, Rosenberg A, Bergami KC, et al. (2008). Deregulation of scribble promotes mammary tumorigenesis and reveals a role for cell polarity in carcinoma. Cell 135:865-78
231. Zhou AX, Hartwig JH, Akyurek LM. (2010). Filamins in cell signaling, transcription and organ development. Trends Cell Biol 20:113-23
232. Zhou H, Huang S. (2010). The complexes of mammalian target of rapamycin. Curr Protein Pept Sci 11:409-24