C-Src and c-Yes are two unlikely partners of spermatogenesis and their roles in blood-testis barrier dynamics

Advances in Experimental Medicine and Biology

Volumn 763, Issue , 2013, Pages 295-317

  Xiao, Xiang ^a   Mruk, Dolores D ^a   Cheng, Faith L ^a   Cheng, C Yan ^a  

^a POPULATION COUNCIL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATENIN; CAVEOLIN; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE P60; PROTEIN KINASE YES; PROTEIN ZO1; VERY LATE ACTIVATION ANTIGEN 6;

AMINO TERMINAL SEQUENCE; ARTICLE; BASEMENT MEMBRANE; BLOOD TESTIS BARRIER; CELL ADHESION; CELL CYCLE PROGRESSION; CELL FUNCTION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; HUMAN; IMMUNOREACTIVITY; MEIOSIS; MOLECULAR DYNAMICS; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; UBIQUITINATION;

EID: 84934436574     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-4711-5_15     Document Type: Article

References (172)

1. De Rooij DG. Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21 :776-798
2. Ren HP, Russell LD. Clonal development of interconnected germ cells in the rat and its relationship to the segmental and subsegmental organization of spermatogenesis. Am J Anat 1991; 192:121-128
3. Ehmcke J, W istuba J, Sehlatt S. Spermatogonial stem cells: Questions, models and perspectives. Hum Reprod Update 2006; 12:275-282
4. De Kretser D, Kerr J. The cytology of the testis. In: Knobil E, Neill J, Ewing L, Greenwald G, Markert C, PfaffD, eds. The Physiology of Reproduction, Vol. I. New York: Raven Press, 1988: 837-932
5. Shaha C, Tripathi R, Mishra DP. Male germ cell apoptosis: Regulation and biology. Philos Trans R Soc Lond B BioI Sci 2010; 365:1501-1515
6. Brehm R, Steger K. Regulation of Sertoli cell and germ cell differentation. Adv Anat Embryol Cell BioI 2005; 181:1-93
7. Vogl A W, Vaid KS, Guttman JA. The Sertoli cell cytoskeleton. Adv Exp Med Bioi 2008; 636: 186-211
8. Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endoer Rev 2004; 25:747-806
9. Cheng CY, MrukDD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82:825-874
10. O'Donnell L, Nicholls PK, 0' Bryan MK et al. Spermiation: The process of sperm release. Spermatogenesis 2011; 1:14-35
11. Cheng CY, MrukDD. A local autoerine axis in the testes that regulates spermatogenesis. N at Rev Endoerinol 2010; 6:380-395
12. Russell L. Movement of spermatoeytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977; 148:313-328
13. Dym M, Fawcett DW. The blood-Testis barrier in the rat and the physiological eompartmentation of the seminiferous epithelium. Bioi Reprod 1970; 3:308-326
14. Cheng CY, Mruk DD. An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: A biochemical and molecular perspective. Crit Rev Bioehem Mol BioI 2009; 44:245-263
15. Setehell BP. Blood-Testis barrier, junctional and transport proteins and spermatogenesis. Adv Exp Med Bioi 2008; 636:212-233
16. Setehell BP. The functional significance of the blood-Testis barrier. J Andro11980; 1:3-10
17. Mruk DD, Cheng CY. Tight junctions in the testis: New perspectives. Philos Trans R Soc Lond B BioI Sci 2010; 365:1621-1635
18. Lie PP, Cheng CY, Mruk DD. The biology of the desmosome-like junetion-A versatile anchoring junction and signal transducer in the seminiferous epithelium.lnt Rev Cell Mol BioI 2011; 286:223-269
19. Russell L. Observations on rat Sertoli ectoplasmic ('junctional') specializations in their association with germ cells of the rat testis. Tissue Cell 1977; 9:475-498
20. Wong EWP, Cheng CY. Polarity proteins and cell-cell interactions in the testis. Tnt Rev Cell Mol Bioi 2009; 278:309-353
21. Siu MKY, Cheng CY. Dynamic cross-Talk between cells and the extracellular matrix in the testis. Bioessays 2004; 26:978-992
22. Van HHN, Mruk DD, Lee WM, et al. Ectoplasmic specialization: A friend or a foe of spermatogenesis? Bioessays 2007; 29:36-48
23. Wong EWP, Mruk DD, Cheng CY. Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Bioehem Biophys Acta 2008; 1778:692-708
24. Van HHN, Mruk DD, Wong EWP, et al. An autoerine axis in the testis that coordinates spermiation and blood-Testis barrier restructuring during spermatogenesis. Proe Natl Aead Sci USA 2008; 105 :8950-8955
25. Young JS, Guttman JA, Vaid KS et al. Tubulobulbar complexes are intercellular podosome-like structures that internalize intact intercellular junctions during epithelial remodeling events in the rat testis. BioI Reprod 2009; 80: 162-174
26. Young JS, Guttman JA, Vaid KS et al. Cortaetin (CTTN), N-WASP (WASL) and c1athrin (CLTC) arc present at podosome-like tubulobulbar complexes in the rat testis. BioI Reprod 2009; 80: 153-161
27. Kusumi N, Watanabe M, Yamada H et al. Implication of amphiphysin I and dynamin 2 in tubulobulbar complex formation and spermatid release. Cell Struet Funet 2007; 32: 101-113
28. Russell L, Clermont Y. Anchoring device between Sertoli cells and late spermatids in rat seminiferous tubules. Anat Ree 1976; 185:259-278
29. Russell LD. Observations on the inter-relationships of Sertoli cells at the level of the blood-Testis barrier: Evidence for formation and resorption ofSertoli-Sertoli tubulobulbar complexes during the spermatogenic cycle of the rat. Am J Anat 1979; 155:259-279
30. Summy JM, Sudol M, Eek MJ, et al. Specificity in signaling by e-Yes. Front Biosei 2003; 8:s 185-205
31. Thomas SM, Brugge JS. Cellular functions regulated by Sre family kinases. Annu Rev Cell Dev BioI 1997; 13:513-609
32. Engen JR, Wales TE, Hoehrein JM et al. Structure and dynamic regulation ofSre-family kinases. Cell Mol Life Sci 2008; 65:3058-3073
33. Kim LC, Song L, Haura EB. Sre kinasesas therapeutic targets for cancer. Nat Rev Clin Oneo12009; 6:587-595
34. Yeatman n. A renaissance for SRC. Nat Rev Cancer 2004; 4:470-480
35. Martin GS. The hunting of the Sre. Nat Rev Mol Cell BioI 2001; 2:467-475
36. Koegl M, Ziatkine P, LeySC et al' Palmitoylation of multiple Sre-familykinasesatahomologous N-Terminal motif. Bioehem J 1994; 303:749-753
37. Murray D, Ben-Tal N, Honig Bet al. Electrostatic interaction of myristoylated proteins with membranes: Simple physics, complicated biology. Structure 1997; 5:985-989
38. Sandilands E, Brunton VG, Frame MC. The membrane targeting and spatial activation of Src, Yes and Fyn is influenced by palmitoylation and distinct RhoB/RhoD endosome requirements. J Cell Sci 2007; 120:2555-2564
39. Sato I, Obata Y, Kasahara K, et al. Differential trafficking of Src, L yn, Yes and Fyn is specified by the state ofpalmitoylation in the SH4 domain. J Cell Sci 2009; 122:965-975
40. Oneyama C, lino T, Saito K, et al. Transforming potential of Src family kinases is limited by the cholesterol-enriched membrane microdomain. Mol Cell BioI 2009 29 6462-6472
41. Cai H, Smith DA, Memarzadeh S, et al. Differential transformation capacity of Src family kinases during the initiation of prostate cancer. Proc Natl Acad Sci USA 2011; 108:6579-6584
42. Nusrat A, Parkos CA, Verkade P, et al. Tight junctions are membrane microdomains. J Cell Sci 2000; 113:1771-1781
43. Summy JM, Qian Y, Jiang BH, et al. The SH4-Unique-SH3-SH2 domains dictate specificity in signaling that differentiate c-Yes from c-Src. J Cell Sci 2003; 116:2585-2598
44. Patwardhan P, Resh MD. Myristoylation and membrane binding regulate c-Src stability and kinase activity. Mol Cell BioI 2010; 30:4094-4107
45. Harris KF, Shoji I, Cooper EM, et al. Ubiquitin-mediated degradation of active Src tyrosine kinase. Proc Natl Acad Sci USA 1999; 96:13738-13743
46. AI-Khalili 0, Duke BJ, Zeltwanger S, et al. Cloning of the proto-oncogene c-src from rat testis. DNA Seq 2001; 12:425-429
47. Ariki M, Tanabe 0, Usui H, et al.Identification of auto phosphorylation sites in c-Y es purified from rat liver plasma membranes. J Biochem 1997; 121 :104-111
48. Ia KK, Mills RD, Hossain MI, et al. Structural elements and allosteric mechanisms governing regulation and catalysis of CSK-family kinases and their inhibition of Src-family kinases. Growth Factors 2010; 28:329-350
49. Shvartsman DE, Donaldson JC, Diaz B, et al. Src kinase activity and SH2 domain regulate the dynamics of Src association with lipid and protein targets. J Cell BioI 2007; 178:675-686
50. Guarino M. Src signaling in cancer invasion. J Cell Physiol2010; 223:14-26
51. Aleshin A, Finn RS. SRC: A century of science brought to the clinic. Neoplasia 2010; 12:599-607
52. Park J, Meisler AI, Cartwright CA. c-Yes tyrosine kinase activity in human colon carcinoma. Oncogene 1993; 8:2627-2635
53. Talamonti MS, Roh MS, Curley SA, et al. Increase in activity and level ofpp60c-src in progressive stages of human colorectal cancer. J Clin Invest 1993; 91:53-60
54. Rahman MA, Senga T, Ito S, et al. S-nitrosylation at cysteine 498 of c-Src tyrosine kinase regulates nitric oxide-mediated cell invasion. J BioI Chern 2010; 285:3806-3814
55. Woodcock SA, Rooney C, Liontos M, et al. SRC-induced disassembly of ad her ens junctions requires localized phosphorylation and degradation of the rac activator tiaml. Mol Cell 2009; 33:639-653
56. Mathew S, George SP, Wang Y, et al. Potential molecular mechanism for c-Src kinase-mediated regulation of intestinal cell migration. J BioI Chern 2008; 283:22709-22722
57. Avizienyte E, Keppler M, Sandilands E, et al. An active Src kinase-fl-Actin association is linked to actin dynamics at the periphery of colon cancer cells. Exp Cell Res 2007; 313:3175-3188
58. Tsygankova OM, Ma C, Tang W, et al. Downregulation of Rap I GAP in human tumor cells alters celli matrix and cell/cell adhesion. Mol Cell BioI 20 10; 30:3262-3274
59. Wadhawan A, Smith C, Nicholson RI, et al. Src- mediatedregulationofhomotypic cell adhesion: Implications for cancer progression and opportunities for therapeutic intervention. Cancer Treat Rev 20 II ; 37 :234-241
60. Weis S, Cui J, Barnes L, et al. Endothelial barrier disruption by VEGF-mediated Src activity potentiates tumor cell extravasation and metastasis. J Cell BioI 2004; 167:223-229
61. Kharas MG, Daley GQ. From hen house to bedside: Tracing Hanafusa's legacy from avian leukemia viruses to Src to ABL and beyond. Genes Cancer 20 II; I: 1164-1169
62. Montero JC, Seoane Ruzo S, Ocana A, et al. Inhibition of Src family kinases and receptor tyrosine kinases by dasatinib: Possible combinations in solid tumors. Clin Cancer Res 2011; 17:5546-5552
63. Sancier F, Dumont A, Sirvent A, et al. Specific oncogenic activity of the Src-family tyrosine kinase c-Y es in colon carcinoma cells. PLoS ONE 2011; 6:c17237
64. Hamamura K, Tsuji M, Hotta H, et al. Functional activation of SRC family kinase Yes is essential for the enhanced malignant properties of human melanoma cells expressing ganglioside GD3. J BioI Chern 2011; 286:18526-18537
65. Sandilands E, Frame MC. Endosomal trafficking ofSrc tyrosine kinase. Trends Cell BioI 2008; 18:322-329
66. Kasahara K, Nakayama Y, Yamaguchi N. v-Src and c-Src, nonpalmitoylated Src-family kinases, induce perinuclear accumulation oflysosomes through Rab7 in a kinase activity-independent manner. Cancer Lett 2008; 262:19-27
67. Lowell CA, Soriano P. Knockouts of Src-family kinases: Stiff bones, wimpy T-cells and bad memories. Genes Dev 1996; 10:1845-1857
68. Sudol M, Greulich H, Newman L, et al. A novel Yes-related kinase, Yrk, is expressed at elevated levels in neural and hematopoietic tissues. Oncogene 1993; 8:823-831
69. Goupil S, La Salle S, Trasler JM, et al. Developmental expression of SRC-related tyrosine kinases in the mouse testis. J Andro12011; 32:95-110
70. Bordeleau LJ, Leclerc P. Expression of hek-Tr, a truncated form of the sre-related tyrosine kinase hek, in bovine spermatozoa and testis. Mol Reprod Dev 2008; 75:828-837
71. Kierszenbaum AL, Rivkin E, Talmor-Cohen A, et al. Expression of full-length and truncated Fyn tyrosine kinase transcripts and encoded proteins during spermatogenesis and localization during acrosome biogenesis and fertilization. Mol Reprod Dev 2009; 76:832-843
72. Lee NP, Cheng CY. Protein kinases and adherens junction dynamics in the seminiferous epithelium of the rat testis. J Cell Physiol 2005; 202:344-360
73. Wang W, Wine RN, Chapin RE. Rat testicular Sre: Normal distribution and involvement in ethylene glycol monomethyl ether-induced apoptosis. Toxieol Appl Pharmaeol 2000; 163: 125-134
74. Wong CH, Cheng CY. The blood-Testis barrier: Its biology, regulation and physiological role in spermatogenesis. Curr Top Dev BioI 2005; 71 :263-296
75. Van HH, Cheng CY. Laminin a3 forms a complex with 133 and y3 chains that serves as the ligand for a6j3l-integrinatthe apical ectoplasmic specialization in adultrattestes. JBiol Chern 2006; 281: 17286-17303
76. Zhang J, Wong CH, Xia W, et al. Regulation of Sertoli-germ cell adherens junction dynamics via changes in protein-protein interactions of the N-eadherin-j3-eatenin protein complex which are possibly mediated by e-Sre and myotubularin-related protein 2: An in vivo study using an androgen suppression model. Endocrinology 2005; 146: 1268-1284
77. Siu MK, Wong CH, Lee WM, et al. Sertoli-germ cell anchoring j unction dynamics in the testis arc regulated by an interplay of lipid and protein kinases. J BioI Chern 2005; 280:25029-25047
78. Siu MK, Mruk DD, Lee WM, et al. Adhering junction dynamics in the testis arc regulated by an interplay of j3l-integrin and focal adhesion complex-Associated proteins. Endocrinology 2003; 144:2141-2163
79. Lie PP, Cheng CY, Mruk DD. Crosstalk between desmoglein-2/desmoeollin-2/ Sre kinase and coxsackie and adenovirus reeeptor/ZO-I protein complexes, regulates blood-Testis barrier dynamics. Int J Bioehem Cell BioI 2010; 42:975-986
80. Wang CQ, Mruk DD, Lee WM, et al. Coxsackie and adenovirus receptor (CAR) is a product ofSertoli and germ cells in rat testes which is localized at the Sertoli-Sertoli and Sertoli-germ cell interface. Exp Cell Res 2007; 313: 1373-1392
81. Yi Z, Li L, Matsushima GK, et al. A novel role for e-Sre and STAT3 in apoptotie cell-mediated MerTK-dependent immunoregulation of dendritic cells. Blood 2009; 114:3191-3198
82. Li MW, Mruk DD, Lee WM, et al. Connexin 43 and plakophilin-2 as a protein complex that regulates blood-Testis barrier dynamics. Proe Natl Aead Sci USA 2009; 106: I 0213-1 0218
83. Xiao X, Mruk DD, Lee WM, et al. e-Y es regulates cell adhesion at the blood-Testis barrier and the apical ectoplasmic specialization in the seminiferous epithelium of rat testes. Int J Bioehem Cell BioI 20 II; 43:651-665
84. Caires K, Broady J, McLean D. Maintaining the male germline: Regulation of spermatogonia II stem cells. J Endoerinol201O; 205:133-145
85. Nakagawa T, Nabeshima Y, Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 2007; 12: 195-206
86. Phillips BT, Gassei K, Orwig KE. Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B BioI Sci 2010; 365: 1663-1678
87. De Rooij DG. The spermatogonial stem cell niche. Mierose Res Tech 2009; 72:580-585
88. Oatley JM, Avarboek MR, Brinster RL. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Sre family kinase signaling. J BioI Chern 2007; 282:25842-25851
89. Buageaw A, Sukhwani M, Ben-Yehudah A, et al. GDNF family receptor al phenotype of spermatogonial stem cells in immature mouse testes. BioI Reprod 2005; 73: 1011-1016
90. Dettin L, Ravindranath N, Hofmann MC, et al. Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. BioI Reprod 2003; 69: 1565-1571
91. Hofmann MC, Braydieh-Stolle L, Dym M. Isolation of male germ-line stem cells: Influence of GDNF. Dev BioI 2005; 279:114-124
92. Von Sehonfeldt V, Wistuba J, Sehlatt S. Notch-I, e-kit and GFRa-1 are developmentally regulated markers for premeiotie germ cells. Cytogenet Genome Res 2004; 105:235-239
93. Braydieh-Stolle L, Kostereva N, Dym M, et al. Role ofSre family kinases and N-Mye in spermatogonial stem cell proliferation. Dev BioI 2007; 304:34-45
94. Lee MY, Lee SH, Park JH, et al. Interaction of galeetin-I with eaveolae induces mouse embryonic stem cell proliferation through the Sre, ERas, Akt and mTOR signaling pathways. Cell Mol Life Sci 2009; 66:1467-1478
95. Nishio H, Tokuda M, Itano T, et al. pp60c-src expression in rat spermatogenesis. Biochem Biophys Res Commun 1995; 206:502-510
96. Wine RN, Chapin RE. Adhesion and signaling proteins spatiotemporally associated with spermiation in thc rat. J Andro11999; 20: 198-213
97. Mruk DD, Wong CH, Silvestrini B, et al. A male contraceptive targeting germ cell adhesion. Nat Med 2006; 12: 1323-1328
98. Mok KW, Mruk DD, Lie PP, et al. Adjudin, a potential male contraceptive, exerts its effects locally in the scminifcrous epithelium of mammalian testes. Reproduction 20 II; 141 :571-580
99. Cheng CY, Mruk DD, Silvestrini B, et al. AF-2364 [1-(2,4-dichlorobenzyl)- 1 H-indazole-3-carbohydrazide 1 is a potential male contraceptive: A review of recent data. Contraception 2005; 72:251-261
100. Cheng CY, Mruk DD. New frontiers in nonhormonal male contraception. Contraception201 0; 82:476-482
101. Mruk DD, Silvestrini B, Cheng CY. Anchoringjunctions as drug targets: Role in contraceptive development. Pharmacol Rev 2008; 60: 146-180
102. Palacios F, Tushir JS, Fujita Y, et al. Lysosomal targeting of E-cadherin: A unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Bioi 2005; 25 :389-402
103. Shen Y, Hirsch DS, Sasiela CA, et al. Cdc42 regulates E-cadherin ubiquitination and degradation through an epidermal growth factor receptor to Src-mediated pathway. J BioI Chern 2008; 283:5127-5137
104. Kale G, Naren AP, Sheth P, et al. Tyrosine phosphorylation of occludin attenuates its interactions with ZO-I, ZO-2 and ZO-3. Biochem Biophys Res Commun 2003; 302:324-329
105. Elias BC, Suzuki T, Seth A, et al. Phosphorylation ofTyr-398 and Tyr-402 inoccludin prevents its interaction with ZO-I and destabilizes its assembly at the tight junctions. J BioI Chern 2009; 284:1559-1569
106. Sabath E, Negoro H, Beaudry S, et al. Gal2 regulates protein interactions within the MDCK cell tight junction and inhibits tight-junction assembly. J Cell Sci 2008; 121:814-824
107. Chen JX, Xu LL, Wang XC, et al. Involvement of c-Src/ST A T3 signal in EGF-induced proliferation of rat spermatogonial stem cells. Mol Cell Endocrinol 20 II; Epub ahead of press
108. Chen JX, Wang XC, Wang JL, et al. Proto-oncogene c-Src regulates the viability of rat spermatogonial stem cells in vitro through phosphorylated signal transducer and activator oftranscription-3. Sheng Li Xue Bao 2008; 60:391-396
109. Walker WH Non-elassical actions oftestosterone and spermatogenesis. Philos Trans R Soc LondB BioI Sci 2010; 365:1557-1569
110. Walker WHo Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis 20 II; I: 116-120
111. Shupe J Cheng J Puri P et al. Regulation of Sertoli-germ cell adhesion and sperm release by FSH and nonclassical testosterone signaling. Mol Endocrinol 2011 25 238-252
112. Chen YH, Lu Q, Goodenough DA, et al. Nonreceptor tyrosine kinase c-Yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Mol BioI Cell 2002; 13:1227-1237
113. Nusrat A, Chen JA, Foley CS, et al. The coiled-coil domain of occludin can act to organize structural and functional elements of the epithelial tight junction. J BioI Chern 2000; 275:29816-29822
114. Su L, Cheng CY, Mruk DD. Adjudin-mediated Sertoli-germ cell junction disassembly affects Sertoli cell barrier function in vitro and in vivo. lnt J Biochem Cell BioI 2010; 42: 1864-1875
115. Xia W, Mruk DD, Lee WM, et al. Cytokines and junction restructuring during spermatogenesis-A lesson to learn from the testis. Cytokine Growth Factor Rev 2005; 16:469-493
116. Li MWM, Mruk DD, Lee WM, et al. Cytokines and junction restructuring events during spermatogenesis in the testis: An emerging concept of regulation. Cytokine Growth Factor Rev 2009; 20:329-338
117. Hansen CG, Nichols BJ. Exploring the caves: Cavins, caveolins and caveolae. Trends Cell Bioi 2010; 20: 177-186
118. Su L, Mruk DD, Lee WM, et al. Differential effects oftestosterone and TGF-133 on endocytic vesicle-mediated protein trafficking events at the blood-Testis barrier. Exp Cell Res 2010; 316:2945-2960
119. Luton F, Verges M, Vaerman JP, et al. The SRC family protein tyrosine kinase p62yes controls polymeric IgA transcytosis in vivo. Mol Cell 1999; 4:627-632
120. Su T, Bryant DM, Luton F, et al. A kinase cascade leading to Rab II-FIP5 controls transcytosis of the polymeric immunoglobulin receptor. Nat Cell BioI 2010; 12: 1143-1153
121. Wong EW, Mruk DD, Lee WM, et al. Par3IPar6 polarity complex coordinates apical ectoplasmic specialization and blood-Testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008; 105:9657-9662
122. lden S, Collard JG. Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell BioI 2008; 9:846-859
123. Wong EWP, Sun S, Li MWM, et al. 14-3-3 protein regulates cell adhesion in the seminiferous epithelium ofrat testes. Endocrinology 2009; 150:4713-4723
124. Wong EWP, Mruk DD, Lee WM, et al. Regulation of blood-Testis barrier dynamics by TGF-fl3 is a Cdc42-dependent protein trafficking event. Proc Natl Acad Sci USA 2010; 107:11399-11404
125. Xia W, Wong CH, Lee NPY, et al. Disruption ofSertoli-genn cell adhesion function in the seminiferous epithelium of the rat testis can be limited to adherens junctions without affecting the blood-Testis barrier integrity: An in vivo study using an androgen suppression model. J Cell Physiol2005; 205:141-157
126. Siu ER, Wong EWP, Mruk DD, et al. Anoecludin-foeal adhesion kinase protein complex atthe blood-Testis barrier: A study using the cadmium model. Endocrinology 2009; 150:3336-3344
127. Siu ER, Wong EWP, Mruk DD, et al. Focal adhesion kinase is a blood-Testis barrier regulator. Proe Natl Aead Sci USA 2009; 106:9298-9303
128. Boutros T, Chevet E, Metrakos P. Mitogen-Activated protein (MAP) kinase/MAP kinase phosphatase regulation: Roles in cell growth, death and cancer. Phannaeol Rev 2008; 60:261-310
129. Serrels A, Canel M, Brunton VG, et al. Sre/FAK-mediated regulation of E-eadherin as a mechanism for controlling collective cell movement: Insights from in vivo imaging. Cell Adh Migr 20 II; 5 :360-365
130. Mitra SK, Sehlaepfer DD. Integrin-regulated FAK-Sre signaling in nonnal and cancer cells. Curr Opin Cell Bioi 2006; 18:516-523
131. Lee NPY, Cheng CY. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: Is this a potential target for male contraceptive development. Hum Reprod Update 2004; 10:349-369
132. Marcotte R, Smith HW, Sanguin-Gendreau V, et al. Mammary epithelial-specific disruption of e-Sre impairs cell cycle progression and tumorigenesis. Proe Natl Aead Sci USA 20 II; Epub ahead of press
133. Kruewel T, Sehenone S, Radi M, et al. Molecular characterization ofe-Abl/e-Sre kinase inhibitors targeted against murine tumour progenitor cells that express stem cell markers. PLoS One 2010; 5:e41413
134. Migliaccio A, Castoria G, Aurieehio F. Analysis of androgen receptor rapid actions in cellular signaling pathways: Reeeptor/sre association. Methods Mol Bioi 201 I; 776:361-370
135. Saad F. Sre as a therapeutic target in men with prostate cancer and bone metastases. BJU Int 2009; 103:4 34-440
136. Tan AR, Swain SM. Therapeutic strategies for triple-negative breast cancer. Cancer J 2008; 14:343-351
137. Capitani M, Sallese M. The KDELreeeptor:newfunetions for an old protein. FESB Lett2009; 583:3863-3871
138. Hu J, Mukhopadhyay A, Truesdell P, et al. Cde42-interaeting protein 4 is a Sre substrate that regulates invadopodia and invasiveness of breast tumors by promoting MTI-MMP endocytosis. J Cell Sci 20 II; 124: 1739-1751
139. Medts T, De Diesbaeh P, Cominelli A, et al. Acute ligand-independent Sre activation mimics low EGF-induced EGFR surface signalling and redistribution into recycling endosomes. Exp Cell Res 20 1 0; 316:3239-3253
140. Park MA, Reinehr R, Haussinger D, et al. Sorafenib activates CD95 and promotes autophagy and cell death via Sre family kinases in gastrointestinal tumor cells. Mol Cancer Ther 2010; 9:2220-2231
141. Chung BM, Raja SM, Clubb RJ, et al. Aberrant trafficking ofNSCLC-Assoeiated EGFR mutants through the endoeytie recycling pathway promotes interaction with Sre. BMC Cell BioI 2009; 10:84
142. Dym M. Basement membrane regulation ofSertoli cells. Endoer Rev 1994; 15:102-115
143. Klinghoffer RA, Saehsenmaier C, Cooper JA, et al. Sre family kinases arc required for integrin but not PDGFR signal transduction. EMBO J 1999; 18:2459-2471
144. Paul R, Obennaier B, Van Ziffle J, et al. Myeloid Sre kinases regulate phagocytosis and oxidative burst in pneumococcal meningitis by activating NADPH oxidase. J Leukoe Bioi 2008; 84: 1141-1150
145. Nelson MP, Christmann BS, Werner JL et a1.IL-33 andM2a alveolar maerophages promote lung defense against the atypical fungal pathogen pneumoeystis murina. J Immunol 2011; 186:2372-2381
146. Stein PL, Vogel H, Soriano P. Combined deficiencies of Sre, Fyn and Yes tyrosine kinases in mutant mice. Genes Dev 1994; 8:1999-2007
147. Calautti E, Cabodi S, Stein PL, et al. Tyrosine phosphorylation and sre family kinases control keratinoeyte cell-cell adhesion. J Cell Bioi 1998; 141: 1449-1465
148. Lowell CA, Niwa M, Soriano P, et al. Deficiency of the Hek and Sre tyrosine kinases results in extreme levels of extramedullary hematopoiesis. Blood 1996; 87: 1780-1792
149. Yu CC, Yen TS, Lowell CA, et al. Lupus-like kidney disease in mice deficient in the Sre family tyrosine kinases Lyn and Fyn. Curr Bioi 2001; II :34-38
150. Lowell CA, Fumagalli L, Berton G. Deficiency of Sre family kinases p59/61hek and p58e-fgr results in defective adhesion-dependent neutrophil functions. J Cell Bioi 1996; 133 :895-91 O.
151. Lowell CA, Soriano P, Varmus HE. Functional overlap in the sre gene family: Inactivation ofhek and fgr impairs natural immunity. Genes Dev 1994; 8:387-398
152. Suen PW, Hie D, Caveggion E, et al. Impaired integrin-mediated signal transduction, altered eytoskel, et al structure and reduced motility in HeklFgr deficient maerophages. J Cell Sci 1999; 112:4067-4078
153. Kim H, Laing M, Muller W. e-Sre-null mice exhibit defects in nonnal mammary gland development and ERa signaling. Oncogene 2005; 24:5629-5636
154. Soriano P, Montgomery C, Geske R, et al. Targeted disruption of the e-sre proto-oncogene leads to osteopetrosis in mice. Cell 1991; 64:693-702
155. Boyce BF, Yoneda T, Lowe C, et al. Requirement ofpp60e-sre expression for osteoelasts to form ruffled borders and resorb bone in mice. J Clin Invest 1992; 90: 1622-1627
156. Eliceiri BP, Paul R, Schwartzberg PL, et al. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999; 4:915-924
157. Eliceiri BP, Puente XS, Hood m, et al. Src-mediated coupling of focal adhesion kinase to integrin in vascular endothelial growth factor signaling. J Cell BioI 2002; 157: 149-160
158. Roby KF, Son DS, Taylor CC, et al. Alterations in reproductive function in SRC tyrosine kinase knockout mice. Endocrine 2005; 26:169-176
159. Criscuoli ML, Nguyen M, Eliceiri BP. Tumor metastasis butnottumor growth is dependent on Src-mediated vascular permeability. Blood 2005; 105: 1508-1514
160. Appleby MW, Gross JA, Cooke MP, et al. Defective T-cell receptor signaling in mice lacking the thymic isoform ofp59fyn. Cell 1992; 70:751-763
161. Stein PL, Lee HM, Rich S, Soriano P. pp59fyn mutant mice display differential signaling in thymocytes and peripheral T-cells. Cell 1992; 70:741-750
162. Maekawa M, Toyama Y, Yasuda M, et al. Fyn tyrosine kinase in Sertoli cells is involved in mouse spermatogenesis. BioI Reprod 2002; 66:211-221
163. Luo J, McGinnis LK, Kinsey WH. Role ofFyn kinase in oocyte developmental potential. Reprod Fertil Dev 2010; 22:966-976
164. Umemori H, Sato S, Yagi T, et al. Initial events of myelination involve Fyn tyrosine kinase signalling. Nature 1994; 367:572-576
165. Molina TJ, Kishihara K, Siderovski DP, et al. Profound block in thymocyte development in mice lacking p561ck. Nature 1992; 357:161-164
166. Omri B, Blancher C, Neron B, et al. Retinal dysplasia in mice lackingp56lck. Oncogene 1998; 16:2351-2356
167. Dal Porto JM, Burke K, Cambier JC. Regulation of BCR signal transduction in B-1 cells requires the expression of the Src family kinase Lck. Immunity 2004; 21 :443-453
168. Vicentini L, Mazzi P, Caveggion E, et al. Fgr deficiency results in defective eosinophil recruitment to the lung during allergic airway inflammation. J Immunol 2002; 168:6446-6454
169. Scapini P, Pereira S, Zhang H, et al. Multiple roles ofLyn kinase in myeloid cell signaling and function. Immunol Rev 2009; 228:23-40
170. Goldenberg-Furmanov M, Stein I, Pikarsky E, et al. Lyn is a target gene for prostate cancer: Sequence-based inhibition induces regression of human tumor xenografts. Cancer Res 2004; 64: I 058-1 066
171. Nishizumi H, Taniuchi I, Yamanashi Y, et al. Impaired proliferation of peripheral B cells and indication of autoimmune disease in Iyn-deficient mice. Immunity 1995; 3:549-560
172. Laird RM, Laky K, Hayes SM. Unexpected role for the B cell-specific Src family kinase B lymphoid kinase in the development ofIL-17-producing yo T-cells. J Immunol 2010; 185:6518-6527