Chapter 7 Polarity Proteins and Cell-Cell Interactions in the Testis

International Review of Cell and Molecular Biology

Volumn 278, Issue C, 2009, Pages 309-353

  Wong, Elissa W P ^a   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

Author keywords

Adherens junction; Blood testis barrier; Ectoplasmic specialization; Germ cells; Seminiferous epithelial cycle; Sertoli cells; Spermatogenesis; Testis; Tight junction

Indexed keywords

ACTIN; CELL MEMBRANE PROTEIN; CYTOKINE; EPIDERMAL GROWTH FACTOR RECEPTOR; LAMININ; PDZ PROTEIN; PROTEIN 14 3 3; PROTEIN CDC42; PROTEIN CRUMB; PROTEIN KINASE C; PROTEIN PAR; PROTEIN SCRIBBLE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TESTOSTERONE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; PROTEIN;

AUTOCRINE EFFECT; BASEMENT MEMBRANE; BLOOD TESTIS BARRIER; CELL ADHESION; CELL INTERACTION; CELL MEMBRANE; CELL POLARITY; FILOPODIUM; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SEMINIFEROUS TUBULE EPITHELIUM; SPERMATOGENESIS; TESTIS CELL; UBIQUITINATION; CELL COMMUNICATION; MALE; METABOLISM; PHYSIOLOGY; TESTIS;

MAMMALIA; RATTUS;

CELL COMMUNICATION; CELL POLARITY; HUMANS; MALE; PROTEINS; TESTIS;

EID: 73349126135     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1937-6448(09)78007-4     Document Type: Review

References (220)

1. Adams A.E., Johnson D.I., Longnecker R.M., Sloat B.F., and Pringle J.R. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111 (1990) 131-142
2. Aitken A. 14-3-3 proteins: a historic overview. Semin. Cancer Biol. 16 (2006) 162-172
3. Al-Sadi R., Boivin M., and Ma T. Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci. 14 (2009) 2765-2778
4. Andras I.E., Pu H., Deli M.A., Nath A., Hennig B., and Toborek M. HIV-1 Tat protein alters tight junction protein expression and distribution in cultured brain endothelial cells. J. Neurosci. Res. 74 (2003) 255-265
5. Ang A.L., Taguchi T., Francis S., Folsch H., Murrells L.J., Pypaert M., et al. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Biol. 167 (2004) 531-543
6. Asanuma K., Yanagida-Asanuma E., Faul C., Tomino Y., Kim K., and Mundel P. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat. Cell Biol. 8 (2006) 485-491
7. Assemat E., Bazellieres E., Pallesi-Pocachard E., Le Bivic A., and Massey-Harroche D. Polarity complex proteins. Biochim. Biophys. Acta 1778 (2008) 614-630
8. Balklava Z., Pant S., Fares H., and Grant B.D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9 (2007) 1066-1073
9. Bazellieres E., Assemat E., Arsanto J.P., Le Bivic A., and Massey-Harroche D. Crumbs proteins in epithelial morphogenesis. Front Biosci. 14 (2009) 2149-2169
10. Berthouze M., Venkataramanan V., Li Y., and Shenoy S.K. The deubiquitinases USP33 and USP20 coordinate beta2 adrenergic receptor recycling and resensitization. EMBO J. 28 (2009) 1684-1696
11. Bialkowska K., Zaffran Y., Meyer S.C., and Fox J.E. 14-3-3 zeta mediates integrin-induced activation of Cdc42 and Rac. Platelet glycoprotein Ib-IX regulates integrin-induced signaling by sequestering 14-3-3 zeta. J. Biol. Chem. 278 (2003) 33342-33350
12. Bollag G., and McCormick F. Regulators and effectors of Ras proteins. Annu. Rev. Cell Biol. 7 (1991) 601-632
13. Bose R., and Wrana J.L. Regulation of Par6 by extracellular signals. Curr. Opin. Cell Biol. 18 (2006) 206-212
14. Boureux A., Vignal E., Faure S., and Fort P. Evolution of the Rho family of Ras-like GTPases in eukaryotes. Mol. Biol. Evol. 24 (2007) 203-216
15. Boutros T., Chevet E., and Metrakos P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol. Rev. 60 (2008) 261-310
16. Bridges D., and Moorhead G.B. 14-3-3 proteins: a number of functions for a numbered protein. Sci. STKE 2005 (2005) re10
17. Carreau S., de Vienne C., and Galeraud-Denis I. Aromatase and estrogens in man reproduction: a review and latest advances. Adv. Med. Sci. 53 (2008) 139-144
18. Cereijido M., Contreras R.G., and Shoshani L. Cell adhesion, polarity, and epithelia in the dawn of metazoans. Physiol. Rev. 84 (2004) 1229-1262
19. Cereijido M., Contreras R.G., Shoshani L., Flores-Benitez D., and Larre I. Tight junction and polarity interaction in the transporting epithelial phenotype. Biochim. Biophys. Acta 1778 (2008) 770-793
20. Cerione R.A. Cdc42: new roads to travel. Trends Cell. Biol. 14 (2004) 127-132
21. Chahdi A., and Sorokin A. Protein kinase A-dependent phosphorylation modulates beta1Pix guanine nucleotide exchange factor activity through 14-3-3beta binding. Mol. Cell. Biol. 28 (2008) 1679-1687
22. Chardin P. Function and regulation of Rnd proteins. Nat. Rev. Mol. Cell Biol. 7 (2006) 54-62
23. Chaudhary J., and Skinner M.K. Characterization of a novel transcript of 14-3-3 theta in Sertoli cells. J. Androl. 21 (2000) 730-738
24. Chen Z.J., and Sun L.J. Nonproteolytic functions of ubiquitin in cell signaling. Mol. Cell 33 (2009) 275-286
25. Cheng C.Y., and Mruk D.D. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol. Rev. 82 (2002) 825-874
26. Chhabra E.S., and Higgs H.N. The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9 (2007) 1110-1121
27. Chuang C.K., Lee K.H., Fan C.T., and Su Y.S. FSH-sensitive murine Sertoli cell lines immortalized by human telomerase gene hTERT express the androgen receptor in response to TNF-alpha stimulation. Biosci. Rep. 27 (2007) 403-411
28. Cline E.G., and Nelson W.J. Characterization of mammalian Par 6 as a dual-location protein. Mol. Cell. Biol. 27 (2007) 4431-4443
29. Cohen D., Musch A., and Rodriguez-Boulan E. Selective control of basolateral membrane protein polarity by cdc42. Traffic 2 (2001) 556-564
30. Coureuil M., Mikaty G., Miller F., Lecuyer H., Bernard C., Bourdoulous S., et al. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 325 (2009) 83-87
31. d'Azzo A., Bongiovanni A., and Nastasi T. E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 6 (2005) 429-441
32. de Kretser D., and Kerr J. The cytology of the testis. In: Knobil E., Neill J., Ewing L., Greenwald G., Markert C., and Pfaff D. (Eds). The Physiology of Reproduction (1988), Raven Press, New York 837-932
33. Delfino F.J., Boustead J.N., Fix C., and Walker W.H. NF-kappaB and TNF-alpha stimulate androgen receptor expression in Sertoli cells. Mol. Cell. Endocrinol. 201 (2003) 1-12
34. DerMardirossian C., and Bokoch G.M. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15 (2005) 356-363
35. Di Agostino S., Rossi P., Geremia R., and Sette C. The MAPK pathway triggers activation of Nek2 during chromosome condensation in mouse spermatocytes. Development 129 (2002) 1715-1727
36. Doherty G.J., and McMahon H.T. Mechanisms of endocytosis. Annu. Rev. Biochem. 78 (2009) 857-902
37. Du X., Harris S.J., Tetaz T.J., Ginsberg M.H., and Berndt M.C. Association of a phospholipase A2 (14-3-3 protein) with the platelet glycoprotein Ib-IX complex. J. Biol. Chem. 269 (1994) 18287-18290
38. Du X., Fox J.E., and Pei S. Identification of a binding sequence for the 14-3-3 protein within the cytoplasmic domain of the adhesion receptor, platelet glycoprotein Ib alpha. J. Biol. Chem. 271 (1996) 7362-7367
39. Duffield A., Caplan M.J., and Muth T.R. Protein trafficking in polarized cells. Int. Rev. Cell Mol. Biol. 270 (2008) 145-179
40. Etienne-Manneville S. Cdc42-the centre of polarity. J. Cell Sci. 117 (2004) 1291-1300
41. Etienne-Manneville S., Manneville J.B., Nicholls S., Ferenczi M.A., and Hall A. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J. Cell Biol. 170 (2005) 895-901
42. Fagerholm S., Morrice N., Gahmberg C.G., and Cohen P. Phosphorylation of the cytoplasmic domain of the integrin CD18 chain by protein kinase C isoforms in leukocytes. J. Biol. Chem. 277 (2002) 1728-1738
43. Fujita Y., Krause G., Scheffner M., Zechner D., Leddy H.E., Behrens J., et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4 (2002) 222-231
44. Fujita E., Tanabe Y., Hirose T., Aurrand-Lions M., Kasahara T., Imhof B.A., et al. Loss of partitioning-defective-3/isotype-specific interacting protein (par-3/ASIP) in the elongating spermatid of RA175 (IGSF4A/SynCAM)-deficient mice. Am. J. Pathol. 171 (2007) 1800-1810
45. Fukuhara A., Shimizu K., Kawakatsu T., Fukuhara T., and Takai Y. Involvement of nectin-activated Cdc42 small G protein in organization of adherens and tight junctions in Madin-Darby canine kidney cells. J. Biol. Chem. 278 (2003) 51885-51893
46. Gao L., Macara I.G., and Joberty G. Multiple splice variants of Par3 and of a novel related gene, Par3L, produce proteins with different binding properties. Gene 294 (2002) 99-107
47. Garcia-Guzman M., Dolfi F., Russello M., and Vuori K. Cell adhesion regulates the interaction between the docking protein p130(Cas) and the 14-3-3 proteins. J. Biol. Chem. 274 (1999) 5762-5768
48. Garcia-Mata R., and Burridge K. Catching a GEF by its tail. Trends Cell Biol. 17 (2007) 36-43
49. Garrard S.M., Capaldo C.T., Gao L., Rosen M.K., Macara I.G., and Tomchick D.R. Structure of Cdc42 in a complex with the GTPase-binding domain of the cell polarity protein, Par6. EMBO J. 22 (2003) 1125-1133
50. Georgiou M., Marinari E., Burden J., and Baum B. Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr. Biol. 18 (2008) 1631-1638
51. Gliki G., Ebnet K., Aurrand-Lions M., Imhof B.A., and Adams R.H. Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 431 (2004) 320-324
52. Gohla A., and Bokoch G.M. 14-3-3 regulates actin dynamics by stabilizing phosphorylated cofilin. Curr. Biol. 12 (2002) 1704-1710
53. Goldstein B., and Macara I.G. The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13 (2007) 609-622
54. Gonzalez-Mariscal L., Tapia R., and Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 1778 (2008) 729-756
55. Gupton S.L., and Gertler F.B. Filopodia: the fingers that do the walking. Sci. STKE 2007 (2007) re5
56. Hall C., Sin W.C., Teo M., Michael G.J., Smith P., Dong J.M., et al. α2-chimerin, an SH2-containing GTPase-activating protein for the Ras-related protein p21rac derived by alternate splicing of the human n-chimerin gene, is selectively expressed in brain regions and testes. Mol. Cell. Biol. 13 (1993) 4986-4998
57. Han D.C., Rodriguez L.G., and Guan J.L. Identification of a novel interaction between integrin beta1 and 14-3-3beta. Oncogene 20 (2001) 346-357
58. Harris K.P., and Tepass U. Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J. Cell Biol. 183 (2008) 1129-1143
59. Haugsten E.M., Malecki J., Bjorklund S.M., Olsnes S., and Wesche J. Ubiquitination of fibroblast growth factor receptor 1 is required for its intracellular sorting but not for its endocytosis. Mol. Biol. Cell 19 (2008) 3390-3403
60. Heasman S.J., and Ridley A.J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9 (2008) 690-701
61. Hekman M., Wiese S., Metz R., Albert S., Troppmair J., Nickel J., et al. Dynamic changes in C-Raf phosphorylation and 14-3-3 protein binding in response to growth factor stimulation: differential roles of 14-3-3 protein binding sites. J. Biol. Chem. 279 (2004) 14074-14086
62. Hess R.A. Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 1 (2003) 52
63. Hess R.A., and de Franca L.R. Spermatogenesis and cycle of the seminiferous epithelium. In: Cheng C.Y. (Ed). Molecular Mechanisms in Spermatogenesis (2008), Landes Bioscience/Springer Science+Business Media, LLC, Austin, TX 1-15
64. Heusser K., Yuan H., Neagoe I., Tarasov A.I., Ashcroft F.M., and Schwappach B. Scavenging of 14-3-3 proteins reveals their involvement in the cell-surface transport of ATP-sensitive K+ channels. J. Cell Sci. 119 (2006) 4353-4363
65. Hicke L., and Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19 (2003) 141-172
66. Honda T., Shimizu K., Kawakatsu T., Fukuhara A., Irie K., Nakamura T., et al. Cdc42 and Rac small G proteins activated by trans-interactions of nectins are involved in activation of c-Jun N-terminal kinase, but not in association of nectins and cadherin to form adherens junctions, in fibroblasts. Genes Cells 8 (2003) 481-491
67. Huang S.H., Zhao L., Sun Z.P., Li X.Z., Geng Z., Zhang K.D., et al. Essential role of Hrs in endocytic recycling of full-length TrkB receptor but not its isoform TrkB.T1. J. Biol. Chem. 284 (2009) 15126-15136
68. Hurd T.W., Fan S., Liu C.J., Kweon H.K., Hakansson K., and Margolis B. Phosphorylation-dependent binding of 14-3-3 to the polarity protein Par3 regulates cell polarity in mammalian epithelia. Curr. Biol. 13 (2003) 2082-2090
69. Hurd T.W., Gao L., Roh M.H., Macara I.G., and Margolis B. Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell Biol. 5 (2003) 137-142
70. Huveneers S., and Danen E.H. Adhesion signaling-crosstalk between integrins, Src and Rho. J. Cell Sci. 122 (2009) 1059-1069
71. Iden S., and Collard J.G. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat. Rev. Mol. Cell Biol. 9 (2008) 846-859
72. Inselman A., and Handel M.A. Mitogen-activated protein kinase dynamics during the meiotic G2/MI transition of mouse spermatocytes. Biol. Reprod. 71 (2004) 570-578
73. Izaki T., Kamakura S., Kohjima M., and Sumimoto H. Phosphorylation-dependent binding of 14-3-3 to Par3beta, a human Par3-related cell polarity protein. Biochem. Biophys. Res. Commun. 329 (2005) 211-218
74. Izumi G., Sakisaka T., Baba T., Tanaka S., Morimoto K., and Takai Y. Endocytosis of E-cadherin regulated by Rac and Cdc42 small G proteins through IQGAP1 and actin filaments. J. Cell Biol. 166 (2004) 237-248
75. Jaffe A.B., and Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21 (2005) 247-269
76. Jin J., Smith F.D., Stark C., Wells C.D., Fawcett J.P., Kulkarni S., et al. Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14 (2004) 1436-1450
77. Joberty G., Petersen C., Gao L., and Macara I.G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2 (2000) 531-539
78. Kanmogne G.D., Primeaux C., and Grammas P. HIV-1 gp120 proteins alter tight junction protein expression and brain endothelial cell permeability: implications for the pathogenesis of HIV-associated dementia. J. Neuropathol. Exp. Neurol. 64 (2005) 498-505
79. Kawakatsu T., Shimizu K., Honda T., Fukuhara T., Hoshino T., and Takai Y. Trans-interactions of nectins induce formation of filopodia and lamellipodia through the respective activation of Cdc42 and Rac small G proteins. J. Biol. Chem. 277 (2002) 50749-50755
80. Kemphues K.J., Priess J.R., Morton D.G., and Cheng N.S. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52 (1988) 311-320
81. Kodama A., Takaishi K., Nakano K., Nishioka H., and Takai Y. Involvement of Cdc42 small G protein in cell-cell adhesion, migration, and morphology of MDCK cells. Oncogene 18 (1999) 3996-4006
82. Kohjima M., Noda Y., Takeya R., Saito N., Takeuchi K., and Sumimoto H. PAR3beta, a novel homologue of the cell polarity protein PAR3, localizes to tight junctions. Biochem. Biophys. Res. Commun. 299 (2002) 641-646
83. Kroschewski R., Hall A., and Mellman I. Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells. Nat. Cell Biol. 1 (1999) 8-13
84. Lau A.S., and Mruk D.D. Rab8B GTPase and junction dynamics in the testis. Endocrinology 144 (2003) 1549-1563
85. Le T.L., Yap A.S., and Stow J.L. Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146 (1999) 219-232
86. Leblond C.P., and Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann. N. Y. Acad. Sci. 55 (1952) 548-573
87. Lee N.P., and Cheng C.Y. 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 (2003) 3114-3129
88. Leibfried A., Fricke R., Morgan M.J., Bogdan S., and Bellaiche Y. Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr. Biol. 18 (2008) 1639-1648
89. Lemmers C., Medina E., Delgrossi M.H., Michel D., Arsanto J.P., and Le Bivic A. hINADl/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J. Biol. Chem. 277 (2002) 25408-25415
90. Leung T., How B.E., Manser E., and Lim L. Germ cell beta-chimaerin, a new GTPase-activating protein for p21rac, is specifically expressed during the acrosomal assembly stage in rat testis. J. Biol. Chem. 268 (1993) 3813-3816
91. Leyt J., Melamed-Book N., Vaerman J.P., Cohen S., Weiss A.M., and Aroeti B. Cholesterol-sensitive modulation of transcytosis. Mol. Biol. Cell 18 (2007) 2057-2071
92. Li M.W., Xia W., Mruk D.D., Wang C.Q., Yan H.H., Siu M.K., et al. Tumor necrosis factor α reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J. Endocrinol. 190 (2006) 313-329
93. Li M.W., Mruk D.D., and Cheng C.Y. Mitogen-activated protein kinases in male reproductive function. Trends Mol. Med. 15 (2009) 159-168
94. Lie P.P., Cheng C.Y., and Mruk D.D. Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem. Sci. 34 (2009) 366-373
95. Light Y., Paterson H., and Marais R. 14-3-3 antagonizes Ras-mediated Raf-1 recruitment to the plasma membrane to maintain signaling fidelity. Mol. Cell. Biol. 22 (2002) 4984-4996
96. Lin D., Edwards A.S., Fawcett J.P., Mbamalu G., Scott J.D., and Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol. 2 (2000) 540-547
97. Loirand G., Guilluy C., and Pacaud P. Regulation of Rho proteins by phosphorylation in the cardiovascular system. Trends Cardiovasc. Med. 16 (2006) 199-204
98. Lui W.Y., and Cheng C.Y. Regulation of cell junction dynamics by cytokines in the testis: a molecular and biochemical perspective. Cytokine Growth Factor Rev. 18 (2007) 299-311
99. Lui W.Y., Lee W.M., and Cheng C.Y. Transforming growth factor-β3 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 (2001) 1865-1877
100. Lui W.Y., Lee W.M., and Cheng C.Y. Rho GTPases and spermatogenesis. Biochim. Biophys. Acta 1593 (2003) 121-129
101. Lui W.Y., Lee W.M., and Cheng C.Y. Sertoli-germ cell adherens junction dynamics in the testis are regulated by RhoB GTPase via the ROCK/LIMK signaling pathway. Biol. Reprod. 68 (2003) 2189-2206
102. Lui W.Y., Lee W.M., and Cheng C.Y. Transforming growth factor β-3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol. Reprod. 68 (2003) 1597-1612
103. Lui W.Y., Wong C.H., Mruk D.D., and Cheng C.Y. TGF-β3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 144 (2003) 1139-1142
104. Lui W.Y., Mruk D.D., and Cheng C.Y. Interactions among IQGAP1, Cdc42, and the cadherin/catenin protein complex regulate Sertoli-germ cell adherens junction dynamics in the testis. J. Cell Physiol. 202 (2005) 49-66
105. Makarova O., Roh M.H., Liu C.J., Laurinec S., and Margolis B. Mammalian crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene 302 (2003) 21-29
106. Matsuda M., Kubo A., Furuse M., and Tsukita S. A peculiar internalization of claudins, tight junction-specific adhesion molecules, during the intercellular movement of epithelial cells. J. Cell Sci. 117 (2004) 1247-1257
107. Matsumine A., Ogai A., Senda T., Okumura N., Satoh K., Baeg G.H., et al. Binding of APC to the human homolog of the Drosophila discs large tumor suppressor protein. Science 272 (1996) 1020-1023
108. Matthiesson K.L., McLachlan R.I., O'Donnell L., Frydenberg M., Robertson D.M., Stanton P.G., et al. The relative roles of follicle-stimulating hormone and luteinizing hormone in maintaining spermatogonial maturation and spermiation in normal men. J. Clin. Endocrinol. Metab. 91 (2006) 3962-3969
109. Mattila P.K., and Lappalainen P. Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9 (2008) 446-454
110. Mellman I., and Nelson W.J. Coordinated protein sorting, targeting, and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9 (2008) 833-845
111. Meng J., Holdcraft R.W., Shima J.E., Griswold M.D., and Braun R.E. Androgens regulate the permeability of the blood-testis barrier. Proc. Natl. Acad. Sci. USA 102 (2005) 16696-16700
112. Merrifield C.J., Feldman M.E., Wan L., and Almers W. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat. Cell Biol. 4 (2002) 691-698
113. Moon S.Y., and Zheng Y. Rho GTPase-activating proteins in cell regulation. Trends Cell. Biol. 13 (2003) 13-22
114. Morrison D.K. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol. 19 (2009) 16-23
115. Morton D.G., Shakes D.C., Nugent S., Dichoso D., Wang W., Golden A., et al. The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Dev. Biol. 241 (2002) 47-58
116. Mrowiec T., and Schwappach B. 14-3-3 proteins in membrane protein transport. Biol. Chem. 387 (2006) 1227-1236
117. Mruk D.D., and Cheng C.Y. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr. Rev. 25 (2004) 747-806
118. Mruk D.D., and Cheng C.Y. Delivering non-hormonal contraceptives to men: advances and obstacles. Trends Biotechnol. 26 (2008) 90-99
119. Mruk D., Zhu L.J., Silvestrini B., Lee W.M., and Cheng C.Y. Interactions of proteases and protease inhibitors in Sertoli-germ cell cocultures preceding the formation of specialized Sertoli-germ cell junctions in vitro. J. Androl. 18 (1997) 612-622
120. Mruk D.D., Siu M.K., Conway A.M., Lee N.P., Lau A.S., and Cheng C.Y. Role of tissue inhibitor of metalloproteases-1 in junction dynamics in the testis. J. Androl. 24 (2003) 510-523
121. Mruk D.D., Lau A.S., Sarkar O., and Xia W. Rab4A GTPase catenin interactions are involved in cell junction dynamics in the testis. J. Androl. 28 (2007) 742-754
122. Mruk D.D., Silvestrini B., and Cheng C.Y. Anchoring junctions as drug targets: role in contraceptive development. Pharmacol. Rev. 60 (2008) 146-180
123. Mulholland D.J., Dedhar S., and Vogl A.W. Rat seminiferous epithelium contains a unique junction (ectoplasmic specialization) with signaling properties both of cell/cell and cell/matrix junctions. Biol. Reprod. 64 (2001) 396-407
124. Musch A., Cohen D., Kreitzer G., and Rodriguez-Boulan E. cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. EMBO J. 20 (2001) 2171-2179
125. Muslin A.J., and Lau J.M. Differential functions of 14-3-3 isoforms in vertebrate development. Curr. Top. Dev. Biol. 65 (2005) 211-228
126. Nakagawa S., and Huibregtse J.M. 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 (2000) 8244-8253
127. Nakamuta S., Endo H., Higashi Y., Kousaka A., Yamada H., Yano M., et al. Human immunodeficiency virus type 1 gp120-mediated disruption of tight junction proteins by induction of proteasome-mediated degradation of zonula occludens-1 and -2 in human brain microvascular endothelial cells. J. Neurovirol. 14 (2008) 186-195
128. Nelson W.J. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 36 (2008) 149-155
129. O'Kelly I., Butler M.H., Zilberberg N., and Goldstein S.A. Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111 (2002) 577-588
130. Otani T., Ichii T., Aono S., and Takeichi M. Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J. Cell Biol. 175 (2006) 135-146
131. Ozdamar B., Bose R., Barrios-Rodiles M., Wang H.R., Zhang Y., and Wrana J.L. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307 (2005) 1603-1609
132. Page S.T., Amory J.K., and Bremner W.J. Advances in male contraception. Endocr. Rev. 29 (2008) 465-493
133. Palombi F., Salanova M., Tarone G., Farini D., and Stefanini M. Distribution of beta 1 integrin subunit in rat seminiferous epithelium. Biol. Reprod. 47 (1992) 1173-1182
134. Parvinen M. Regulation of the seminiferous epithelium. Endocr. Rev. 3 (1982) 404-417
135. Perego L., and Berruti G. 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 (1997) 370-379
136. Peterson F.C., Penkert R.R., Volkman B.F., and Prehoda K.E. Cdc42 regulates the Par-6 PDZ domain through an allosteric CRIB-PDZ transition. Mol. Cell 13 (2004) 665-676
137. Pickart C.M., and Fushman D. Polyubiquitin chains: polymeric protein signals. Curr. Opin. Chem. Biol. 8 (2004) 610-616
138. Polishchuk R., Di Pentima A., and Lippincott-Schwartz J. Delivery of raft-associated, GPI-anchored proteins to the apical surface of polarized MDCK cells by a transcytotic pathway. Nat. Cell Biol. 6 (2004) 297-307
139. Pozuelo Rubio M., Geraghty K.M., Wong B.H., Wood N.T., Campbell D.G., Morrice N., et al. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation, and trafficking. Biochem. J. 379 (2004) 395-408
140. Qin Y., Capaldo C., Gumbiner B.M., and Macara I.G. The mammalian scribble polarity protein regulates epithelial cell adhesion and migration through E-cadherin. J. Cell Biol. 171 (2005) 1061-1071
141. Rajalingam K., and Rudel T. Ras-Raf signaling needs prohibitin. Cell Cycle 4 (2005) 1503-1505
142. Rajalingam K., Wunder C., Brinkmann V., Churin Y., Hekman M., Sievers C., et al. Prohibitin is required for Ras-induced Raf-MEK-ERK activation and epithelial cell migration. Nat. Cell Biol. 7 (2005) 837-843
143. Reyes-Turcu F.E., Ventii K.H., and Wilkinson K.D. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78 (2009) 363-397
144. Ridley A.J. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16 (2006) 522-529
145. Rodriguez-Boulan E., Kreitzer G., and Musch A. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 6 (2005) 233-247
146. Roh M.H., Liu C.J., Laurinec S., and Margolis B. The carboxyl terminus of zona occludens-3 binds and recruits a mammalian homologue of discs lost to tight junctions. J. Biol. Chem. 277 (2002) 27501-27509
147. Roh M.H., Makarova O., Liu C.J., Shin K., Lee S., Laurinec S., et al. The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell Biol. 157 (2002) 161-172
148. Rojas R., Ruiz W.G., Leung S.M., Jou T.S., and Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 12 (2001) 2257-2274
149. Rossman K.L., Der C.J., and Sondek J. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6 (2005) 167-180
150. Russell L. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am. J. Anat. 148 (1977) 313-328
151. Russell L.D. Morphological and functional evidence for Sertoli-germ cell relationships. In: Russell L.D., and Griswold M.D. (Eds). The Sertoli Cell (1993), Cache River Press, Clearwater 365-390
152. Sakurai-Yageta M., Recchi C., Le Dez G., Sibarita J.B., Daviet L., Camonis J., et al. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181 (2008) 985-998
153. Salanova M., Stefanini M., De Curtis I., and Palombi F. Integrin receptor alpha 6 beta 1 is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol. Reprod. 52 (1995) 79-87
154. Sallee J.L., Wittchen E.S., and Burridge K. Regulation of cell adhesion by protein-tyrosine phosphatases: II. Cell-cell adhesion. J. Biol. Chem. 281 (2006) 16189-16192
155. Samarin S., and Nusrat A. Regulation of epithelial apical junctional complex by Rho family GTPases. Front Biosci. 14 (2009) 1129-1142
156. Santoni M.J., Pontarotti P., Birnbaum D., and Borg J.P. The LAP family: a phylogenetic point of view. Trends Genet. 18 (2002) 494-497
157. Schlessinger K., McManus E.J., and Hall A. Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J. Cell Biol. 178 (2007) 355-361
158. Seifert J.R., and Mlodzik M. Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat. Rev. Genet. 8 (2007) 126-138
159. Shaha C. Estrogens and spermatogenesis. In: Cheng C.Y. (Ed). Molecular Mechanisms in Spermatogenesis (2008), Landes Bioscience/Springer Science+Business Media, LLC, Austin, TX 42-64
160. Sharpe R.M. Regulation of spermatogenesis. In: Knobil E., and Neil J.D. (Eds). The Physiology of Reproduction (1994), Raven Press, New York 1363-1434
161. Shen L., Weber C.R., and Turner J.R. The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J. Cell Biol. 181 (2008) 683-695
162. Shen Y., Hirsch D.S., Sasiela C.A., and Wu W.J. Cdc42 regulates E-cadherin ubiquitination and degradation through an epidermal growth factor receptor to Src-mediated pathway. J. Biol. Chem. 283 (2008) 5127-5137
163. Shikano S., Coblitz B., Wu M., and Li M. 14-3-3 proteins: regulation of endoplasmic reticulum localization and surface expression of membrane proteins. Trends Cell Biol. 16 (2006) 370-375
164. Shin K., Fogg V.C., and Margolis B. Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22 (2006) 207-235
165. Siu M.K., and Cheng C.Y. 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 (2004) 945-964
166. Siu M.K., Lee W.M., and Cheng C.Y. 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 (2003) 371-387
167. Siu M.K., Wong C.H., Lee W.M., and Cheng C.Y. Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J. Biol. Chem. 280 (2005) 25029-25047
168. Siu E.R., Mruk D.D., Porto C.S., and Cheng C.Y. Cadmium-induced testicular injury. Toxicol. Appl. Pharmacol. 238 (2009) 240-249
169. Somanath P.R., and Byzova T.V. 14-3-3β-Rac1-p21 activated kinase signaling regulates Akt1-mediated cytoskeletal organization, lamellipodia formation, and fibronectin matrix assembly. J. Cell Physiol. 218 (2009) 394-404
170. Stoffler H.E., Honnert U., Bauer C.A., Hofer D., Schwarz H., Muller R.T., Drenckhahn D., and Bahler M. Targeting of the myosin-I myr 3 to intercellular adherens type junctions induced by dominant active Cdc42 in HeLa cells. J. Cell Sci. 111 (1998) 2779-2788
171. Sun I., Wong E., Li M., Lee W., and Cheng C.Y. 14-3-3 and its binding partners are regulators of protein-protein interactions during spermatogenesis. J. Endocrinol. 202 (2009) 327-336
172. Takai Y., Sasaki T., and Matozaki T. Small GTP-binding proteins. Physiol. Rev. 81 (2001) 153-208
173. Takenawa T., and Miki H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114 (2001) 1801-1809
174. Tcherkezian J., and Lamarche-Vane N. Current knowledge of the large RhoGAP family of proteins. Biol. Cell 99 (2007) 67-86
175. Toure A., Dorseuil O., Morin L., Timmons P., Jegou B., Reibel L., et al. MgcRacGAP, a new human GTPase-activating protein for Rac and Cdc42 similar to Drosophila rotundRacGAP gene product, is expressed in male germ cells. J. Biol. Chem. 273 (1998) 6019-6023
176. Toure A., Morin L., Pineau C., Becq F., Dorseuil O., and Gacon G. Tat1, a novel sulfate transporter specifically expressed in human male germ cells and potentially linked to rhogtpase signaling. J. Biol. Chem. 276 (2001) 20309-20315
177. Traweger A., Wiggin G., Taylor L., Tate S.A., Metalnikov P., and Pawson T. Protein phosphatase 1 regulates the phosphorylation state of the polarity scaffold Par-3. Proc. Natl. Acad. Sci. USA 105 (2008) 10402-10407
178. Tu S., Wu W.J., Wang J., and Cerione R.A. Epidermal growth factor-dependent regulation of Cdc42 is mediated by the Src tyrosine kinase. J. Biol. Chem. 278 (2003) 49293-49300
179. Tuma P.L., and Hubbard A.L. Transcytosis: crossing cellular barriers. Physiol. Rev. 83 (2003) 871-932
180. Valencia A., Chardin P., Wittinghofer A., and Sander C. The Ras protein family: evolutionary tree and role of conserved amino acids. Biochemistry 30 (1991) 4637-4648
181. Vasioukhin V., Bauer C., Yin M., and Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100 (2000) 209-219
182. Vetter I.R., and Wittinghofer A. The guanine nucleotide-binding switch in three dimensions. Science 294 (2001) 1299-1304
183. Vogl A.W., Pfeiffer D.C., Redenbach D.M., and Grove B. Sertoli cell cytoskeleton. In: Russell L.D., and Griswold M.D. (Eds). The Sertoli Cell (1993), Cache River Press, Clearwater 39-86
184. Vogl A.W., Vaid K.S., and Guttman J.A. The Sertoli cell cytoskeleton. In: Cheng C.Y. (Ed). Molecular Mechanisms in Spermatogenesis (2008), Landes Bioscience/Springer Science, Austin, TX 186-211
185. Walker W.H. Molecular mechanisms of testosterone action in spermatogenesis. Steroids 74 (2009) 602-607
186. Walker W.H., and Cheng J. FSH and testosterone signaling in Sertoli cells. Reproduction 130 (2005) 15-28
187. Walsh S.V., Hopkins A.M., and Nusrat A. Modulation of tight junction structure and function by cytokines. Adv. Drug Deliv. Rev. 41 (2000) 303-313
188. Wang Q., Hurd T.W., and Margolis B. Tight junction protein Par6 interacts with an evolutionarily conserved region in the amino terminus of PALS1/stardust. J. Biol. Chem. 279 (2004) 30715-30721
189. Wang R.S., Yeh S., Chen L.M., Lin H.Y., Zhang C., Ni J., et al. Androgen receptor in Sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes. Endocrinology 147 (2006) 5624-5633
190. Wang Q., Chen X.W., and Margolis B. PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol. Biol. Cell 18 (2007) 874-885
191. Wang X., Nie J., Zhou Q., Liu W., Zhu F., Chen W., et al. Downregulation of Par-3 expression and disruption of Par complex integrity by TGF-beta during the process of epithelial to mesenchymal transition in rat proximal epithelial cells. Biochim. Biophys. Acta 1782 (2008) 51-59
192. Waterman M.J., Stavridi E.S., Waterman J.L., and Halazonetis T.D. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat. Genet. 19 (1998) 175-178
193. Weber J.E., Russell L.D., Wong V., and Peterson R.N. Three-dimensional reconstruction of a rat stage V Sertoli cell: II. Morphometry of Sertoli-Sertoli and Sertoli-germ-cell relationships. Am. J. Anat. 167 (1983) 163-179
194. Wells C.D., Fawcett J.P., Traweger A., Yamanaka Y., Goudreault M., Elder K., et al. A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 125 (2006) 535-548
195. Wennerberg K., and Der C.J. Rho-family GTPases: it's not only Rac and Rho (and I like it). J. Cell Sci. 117 (2004) 1301-1312
196. Witte H., and Bradke F. The role of the cytoskeleton during neuronal polarization. Curr. Opin. Neurobiol. 18 (2008) 479-487
197. Wong C.H., Mruk D.D., Lui W.Y., and Cheng C.Y. Regulation of blood-testis barrier dynamics: an in vivo study. J. Cell Sci. 117 (2004) 783-798
198. 2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinology 146 (2005) 1893-1908
199. Wong E.W., Mruk D.D., and Cheng C.Y. Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim. Biophys. Acta 1778 (2008) 692-708
200. Wong E.W., Mruk D.D., Lee W.M., and Cheng C.Y. Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc. Natl. Acad. Sci. USA 105 (2008) 9657-9662
201. Wong E.W., Sun S., Li M.W., Lee W.M., and Cheng C.Y. 14-3-3 protein regulates cell adhesion in the seminiferous epithelium of rat testes. Endocrinology (2009) 10.1210/en.2009-0427
202. Wong E.W.P., Mruk D.D., Lee W.M., and Cheng C.Y. Cdc42 regulates Sertoli cell blood-testis barrier dynamics via its effects on the events of cytokine-induced protein endocytosis (submitted) (2009)
203. Woodcock J.M., Murphy J., Stomski F.C., Berndt M.C., and Lopez A.F. The dimeric versus monomeric status of 14-3-3zeta is controlled by phosphorylation of Ser58 at the dimer interface. J. Biol. Chem. 278 (2003) 36323-36327
204. Wu H., Rossi G., and Brennwald P. The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol. 18 (2008) 397-404
205. Xia W., and Cheng C.Y. TGF-β3 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 (2005) 321-343
206. Xia W., Mruk D.D., Lee W.M., and Cheng C.Y. Differential interactions between transforming growth factor-β3/TβR1, TAB1, and CD2AP disrupt blood-testis barrier and Sertoli-germ cell adhesion. J. Biol. Chem. 281 (2006) 16799-16813
207. Xia W., Wong E.W., Mruk D.D., and Cheng C.Y. 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 (2009) 48-61
208. Yamada S., and Nelson W.J. Synapses: sites of cell recognition, adhesion, and functional specification. Annu. Rev. Biochem. 76 (2007) 267-294
209. Yamanaka T., and Ohno S. Role of Lgl/Dlg/Scribble in the regulation of epithelial junction, polarity, and growth. Front Biosci. 13 (2008) 6693-6707
210. Yamanaka T., Horikoshi Y., Suzuki A., Sugiyama Y., Kitamura K., Maniwa R., et al. PAR-6 regulates aPKC activity in a novel way and mediates cell-cell contact-induced formation of the epithelial junctional complex. Genes Cells 6 (2001) 721-731
211. Yamanaka T., Horikoshi Y., Sugiyama Y., Ishiyama C., Suzuki A., Hirose T., et al. Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr. Biol. 13 (2003) 734-743
212. Yan H.H., and Cheng C.Y. 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 (2006) 17286-17303
213. Yan H.H., Mruk D.D., Lee W.M., and Cheng C.Y. 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 (2008) 1945-1959
214. Yan H.H., Mruk D.D., Wong E.W., Lee W.M., and Cheng C.Y. An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc. Natl. Acad. Sci. USA 105 (2008) 8950-8955
215. Yeaman C., Grindstaff K.K., and Nelson W.J. New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol. Rev. 79 (1999) 73-98
216. Yuan H., Michelsen K., and Schwappach B. 14-3-3 dimers probe the assembly status of multimeric membrane proteins. Curr. Biol. 13 (2003) 638-646
217. Zahraoui A., Louvard D., and Galli T. Tight junction, a platform for trafficking and signaling protein complexes. J. Cell Biol. 151 (2000) F31-F36
218. Zhang X., Bi E., Novick P., Du L., Kozminski K.G., Lipschutz J.H., et al. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 276 (2001) 46745-46750
219. Zhang X., Zhu J., Yang G.Y., Wang Q.J., Qian L., Chen Y.M., et al. Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat. Cell Biol. 9 (2007) 743-754
220. Zhang X., Orlando K., He B., Xi F., Zhang J., Zajac A., et al. Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180 (2008) 145-158