880
Views
35
CrossRef citations to date
0
Altmetric
Review

Focal adhesion kinase is a regulator of F-actin dynamics

New insights from studies in the testis

, &
Article: e25385 | Received 28 Mar 2013, Accepted 08 Jun 2013, Published online: 21 Jun 2013

References

  • de Kretser DM, Kerr JB. The cytology of the testis. in The Physiology of Reproduction. Vol. 1 (eds. Knobil, E., et al.) 837-932 (Raven Press, New York, 1988).
  • Sharpe RM. Regulation of spermatogenesis. In: The Physiology of Reproduction. Eds. Knobil, E., Neill, J.D. New York, Raven Press. pp. 1363-1434 (1994).
  • Ehmcke J, Schlatt S. A revised model for spermatogonial expansion in man: lessons from non-human primates. Reproduction 2006; 132:673 - 80; http://dx.doi.org/10.1530/rep.1.01081; PMID: 17071768
  • Cheng CY, Mruk DD. The blood-testis barrier and its implications for male contraception. Pharmacol Rev 2012; 64:16 - 64; http://dx.doi.org/10.1124/pr.110.002790; PMID: 22039149
  • Pelletier RM. The blood-testis barrier: the junctional permeability, the proteins and the lipids. Prog Histochem Cytochem 2011; 46:49 - 127; http://dx.doi.org/10.1016/j.proghi.2011.05.001; PMID: 21705043
  • França LR, Auharek SA, Hess RA, Dufour JM, Hinton BT. Blood-tissue barriers: morphofunctional and immunological aspects of the blood-testis and blood-epididymal barriers. Adv Exp Med Biol 2012; 763:237 - 59; PMID: 23397628
  • Setchell BP. Blood-testis barrier, junctional and transport proteins and spermatogenesis. Adv Exp Med Biol 2008; 636:212 - 33; http://dx.doi.org/10.1007/978-0-387-09597-4_12; PMID: 19856170
  • Cheng CYE. Biology and Regulation of Blood-Tissue Barriers. Austin, TX, Landes Bioscience/Springer Science+Business Media, LLC. pp. 1-361 (2012).
  • Vogl AW, Vaid KS, Guttman JA. The Sertoli cell cytoskeleton. Adv Exp Med Biol 2008; 636:186 - 211; http://dx.doi.org/10.1007/978-0-387-09597-4_11; PMID: 19856169
  • Fawcett DW, Leak LV, Heidger PM Jr.. Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil Suppl 1970; 10:105 - 22; PMID: 4951168
  • Fawcett D. Ultrastructure and function of the Sertoli cell. in Handbook of Physiology., Vol. 5 (eds. Hamilton, D. & Greep, R.) 21-25 (American Physiological Society, Washington, DC, 1975).
  • Russell LD. Observations on rat Sertoli ectoplasmic (‘junctional’) specializations in their association with germ cells of the rat testis. Tissue Cell 1977; 9:475 - 98; http://dx.doi.org/10.1016/0040-8166(77)90007-6; PMID: 929577
  • Russell LD. The blood-testis barrier and its formation relative to spermatocyte maturation in the adult rat: a lanthanum tracer study. Anat Rec 1978; 190:99 - 111; http://dx.doi.org/10.1002/ar.1091900109; PMID: 626419
  • Russell LD. Observations on the inter-relationships of Sertoli cells at the level of the blood- testis barrier: evidence for formation and resorption of Sertoli-Sertoli tubulobulbar complexes during the spermatogenic cycle of the rat. Am J Anat 1979; 155:259 - 79; http://dx.doi.org/10.1002/aja.1001550208; PMID: 474448
  • Russell LD, Clermont Y. Anchoring device between Sertoli cells and late spermatids in rat seminiferous tubules. Anat Rec 1976; 185:259 - 78; http://dx.doi.org/10.1002/ar.1091850302; PMID: 937734
  • Wolski KM, Perrault C, Tran-Son-Tay R, Cameron DF. Strength measurement of the Sertoli-spermatid junctional complex. J Androl 2005; 26:354 - 9; http://dx.doi.org/10.2164/jandrol.04142; PMID: 15867003
  • Russell LD, Goh JC, Rashed RMA, Vogl AW. The consequences of actin disruption at Sertoli ectoplasmic specialization sites facing spermatids after in vivo exposure of rat testis to cytochalasin D. Biol Reprod 1988; 39:105 - 18; http://dx.doi.org/10.1095/biolreprod39.1.105; PMID: 3207792
  • Hess RA, Renato de Franca L. Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol 2008; 636:1 - 15; http://dx.doi.org/10.1007/978-0-387-09597-4_1; PMID: 19856159
  • Mruk DD, Silvestrini B, Cheng CY. Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 2008; 60:146 - 80; http://dx.doi.org/10.1124/pr.107.07105; PMID: 18483144
  • O’Donnell L, Nicholls PK, O’Bryan MK, McLachlan RI, Stanton PG. Spermiation: The process of sperm release. Spermatogenesis 2011; 1:14 - 35; http://dx.doi.org/10.4161/spmg.1.1.14525; PMID: 21866274
  • Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nat Rev Endocrinol 2010; 6:380 - 95; http://dx.doi.org/10.1038/nrendo.2010.71; PMID: 20571538
  • Hanks SK. Messenger ribonucleic acid encoding an apparent isoform of phosphorylase kinase catalytic subunit is abundant in the adult testis. Mol Endocrinol 1989; 3:110 - 6; http://dx.doi.org/10.1210/mend-3-1-110; PMID: 2915644
  • Siu MKY, Mruk DD, Lee WM, Cheng CY. Adhering junction dynamics in the testis are regulated by an interplay of β 1-integrin and focal adhesion complex-associated proteins. Endocrinology 2003; 144:2141 - 63; http://dx.doi.org/10.1210/en.2002-221035; PMID: 12697723
  • André E, Becker-André M. Expression of an N-terminally truncated form of human focal adhesion kinase in brain. Biochem Biophys Res Commun 1993; 190:140 - 7; http://dx.doi.org/10.1006/bbrc.1993.1022; PMID: 8422239
  • Whitney GS, Chan PY, Blake J, Cosand WL, Neubauer MG, Aruffo A, et al. Human T and B lymphocytes express a structurally conserved focal adhesion kinase, pp125FAK. DNA Cell Biol 1993; 12:823 - 30; http://dx.doi.org/10.1089/dna.1993.12.823; PMID: 7692878
  • Wine RN, Chapin RE. Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 1999; 20:198 - 213; PMID: 10232655
  • Mulholland DJ, Dedhar S, Vogl AW. Rat seminiferous epithelium contains a unique junction (Ectoplasmic specialization) with signaling properties both of cell/cell and cell/matrix junctions. Biol Reprod 2001; 64:396 - 407; http://dx.doi.org/10.1095/biolreprod64.1.396; PMID: 11133699
  • Hall JE, Fu W, Schaller MD. Focal adhesion kinase: exploring Fak structure to gain insight into function. Int Rev Cell Mol Biol 2011; 288:185 - 225; http://dx.doi.org/10.1016/B978-0-12-386041-5.00005-4; PMID: 21482413
  • Lim ST, Mikolon D, Stupack DG, Schlaepfer DD. FERM control of FAK function: implications for cancer therapy. Cell Cycle 2008; 7:2306 - 14; PMID: 18677107
  • Dym M. Basement membrane regulation of Sertoli cells. Endocr Rev 1994; 15:102 - 15; PMID: 8156935
  • Siu MKY, Cheng CY. Dynamic cross-talk between cells and the extracellular matrix in the testis. Bioessays 2004; 26:978 - 92; http://dx.doi.org/10.1002/bies.20099; PMID: 15351968
  • Beardsley A, Robertson DM, O’Donnell L. A complex containing α6β1-integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J Endocrinol 2006; 190:759 - 70; http://dx.doi.org/10.1677/joe.1.06867; PMID: 17003277
  • Lie PPY, Mruk DD, Mok KW, Su L, Lee WM, Cheng CY. Focal adhesion kinase-Tyr407 and -Tyr397 exhibit antagonistic effects on blood-testis barrier dynamics in the rat. Proc Natl Acad Sci USA 2012; 109:12562 - 7; http://dx.doi.org/10.1073/pnas.1202316109; PMID: 22797892
  • Schlaepfer DD, Hanks SK, Hunter T, van der Geer P. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 1994; 372:786 - 91; PMID: 7997267
  • Schlaepfer DD, Hunter T. Integrin signalling and tyrosine phosphorylation: just the FAKs?. Trends Cell Biol 1998; 8:151 - 7; http://dx.doi.org/10.1016/S0962-8924(97)01172-0; PMID: 9695829
  • Boutros T, Chevet E, Metrakos P. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol Rev 2008; 60:261 - 310; http://dx.doi.org/10.1124/pr.107.00106; PMID: 18922965
  • Tomar A, Schlaepfer DD. Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 2009; 21:676 - 83; http://dx.doi.org/10.1016/j.ceb.2009.05.006; PMID: 19525103
  • Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, et al. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 1995; 55:2752 - 5; PMID: 7796399
  • Sanchez AM, Flamini MI, Baldacci C, Goglia L, Genazzani AR, Simoncini T. Estrogen receptor-α promotes breast cancer cell motility and invasion via focal adhesion kinase and N-WASP. Mol Endocrinol 2010; 24:2114 - 25; http://dx.doi.org/10.1210/me.2010-0252; PMID: 20880986
  • Slack JK, Adams RB, Rovin JD, Bissonette EA, Stoker CE, Parsons JT. Alterations in the focal adhesion kinase/Src signal transduction pathway correlate with increased migratory capacity of prostate carcinoma cells. Oncogene 2001; 20:1152 - 63; http://dx.doi.org/10.1038/sj.onc.1204208; PMID: 11313859
  • Wang S, Basson MD. Protein kinase B/AKT and focal adhesion kinase: two close signaling partners in cancer. Anticancer Agents Med Chem 2011; 11:993 - 1002; http://dx.doi.org/10.2174/187152011797927661; PMID: 22023045
  • Ma WW. Development of focal adhesion kinase inhibitors in cancer therapy. Anticancer Agents Med Chem 2011; 11:638 - 42; http://dx.doi.org/10.2174/187152011796817628; PMID: 21787276
  • Wehrle-Haller B. Assembly and disassembly of cell matrix adhesions. Curr Opin Cell Biol 2012; 24:569 - 81; http://dx.doi.org/10.1016/j.ceb.2012.06.010; PMID: 22819514
  • Cobb BS, Schaller MD, Leu TH, Parsons JT. Stable association of pp60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, pp125FAK. Mol Cell Biol 1994; 14:147 - 55; PMID: 7505391
  • Xing Z, Chen HC, Nowlen JK, Taylor SJ, Shalloway D, Guan JL. Direct interaction of v-Src with the focal adhesion kinase mediated by the Src SH2 domain. Mol Biol Cell 1994; 5:413 - 21; PMID: 8054685
  • Bolós V, Gasent JM, López-Tarruella S, Grande E. The dual kinase complex FAK-Src as a promising therapeutic target in cancer. Onco Targets Ther 2010; 3:83 - 97; http://dx.doi.org/10.2147/OTT.S6909; PMID: 20616959
  • Bianchi M, De Lucchini S, Marin O, Turner DL, Hanks SK, Villa-Moruzzi E. Regulation of FAK Ser-722 phosphorylation and kinase activity by GSK3 and PP1 during cell spreading and migration. Biochem J 2005; 391:359 - 70; http://dx.doi.org/10.1042/BJ20050282; PMID: 15975092
  • Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003; 114:469 - 82; http://dx.doi.org/10.1016/S0092-8674(03)00605-6; PMID: 12941275
  • Siu MKY, Wong CH, Xia W, Mruk DD, Lee WM, Cheng CY. The β1-integrin-p-FAK-p130Cas-DOCK180-RhoA-vinculin is a novel regulatory protein complex at the apical ectoplasmic specialization in adult rat testes. Spermatogenesis 2011; 1:73 - 86; http://dx.doi.org/10.4161/spmg.1.1.15452; PMID: 21866278
  • Siu MKY, Wong CH, Lee WM, Cheng CY. Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J Biol Chem 2005; 280:25029 - 47; http://dx.doi.org/10.1074/jbc.M501049200; PMID: 15870075
  • Cheng CY, Mruk DD. Regulation of spermiogenesis, spermiation and blood-testis barrier dynamics: novel insights from studies on Eps8 and Arp3. Biochem J 2011; 435:553 - 62; http://dx.doi.org/10.1042/BJ20102121; PMID: 21486226
  • Cheng CY, Mruk DD. Actin binding proteins and spermiogenesis: Some unexpected findings. Spermatogenesis 2011; 1:99 - 104; http://dx.doi.org/10.4161/spmg.1.2.16913; PMID: 22319657
  • Cheng CY, Lie PPY, Wong EWP, Mruk DD, Silvestrini B. Adjudin disrupts spermatogenesis via the action of some unlikely partners: Eps8, Arp2/3 complex, drebrin E, PAR6 and 14-3-3. Spermatogenesis 2011; 1:291 - 7; http://dx.doi.org/10.4161/spmg.1.4.18393; PMID: 22332112
  • Vogl AW, Young JS, Du M. New insights into roles of tubulobulbar complexes in sperm release and turnover of blood-testis barrier. Int Rev Cell Mol Biol 2013; 303:319 - 55; http://dx.doi.org/10.1016/B978-0-12-407697-6.00008-8; PMID: 23445814
  • Lie PPY, Mruk DD, Lee WM, Cheng CY. 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 2009; 23:2555 - 67; http://dx.doi.org/10.1096/fj.06-070573; PMID: 19293393
  • Qian X, Mruk DD, Wong EWP, Lie PPY, Cheng CY. Palladin is a regulator of actin filament bundles at the ectoplasmic specialization in adult rat testes. Endocrinology 2013; 154:1907 - 20; http://dx.doi.org/10.1210/en.2012-2269; PMID: 23546604
  • Lie PPY, Chan AYN, Mruk DD, Lee WM, Cheng CY. Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 2010; 107:11411 - 6; http://dx.doi.org/10.1073/pnas.1001823107; PMID: 20534520
  • Xiao X, Mruk DD, Cheng CY. c-Yes regulates cell adhesion at the apical ectoplasmic specialization-blood-testis barrier axis via its effects on protein recruitment and distribution. Am J Physiol Endocrinol Metab 2013; 304:E145 - 59; http://dx.doi.org/10.1152/ajpendo.00422.2012; PMID: 23169788
  • Campbell M, Humphries P. The blood-retina barrier: tight junctions and barrier modulation. Adv Exp Med Biol 2012; 763:70 - 84; PMID: 23397619
  • Easton AS. Regulation of permeability across the blood-brain barrier. Adv Exp Med Biol 2012; 763:1 - 19; PMID: 23397617
  • Ashraf T, Kis O, Banerjee N, Bendayan R. Drug transporters at brain barriers: expression and regulation by neurological disorders. Adv Exp Med Biol 2012; 763:20 - 69; PMID: 23397618
  • Russell LD, Peterson RN. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 1985; 94:177 - 211; http://dx.doi.org/10.1016/S0074-7696(08)60397-6; PMID: 3894273
  • Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25:747 - 806; http://dx.doi.org/10.1210/er.2003-0022; PMID: 15466940
  • Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 1970; 3:308 - 26; PMID: 4108372
  • Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82:825 - 74; PMID: 12270945
  • Siu ER, Wong EW, Mruk DD, Sze KL, Porto CS, Cheng CY. An occludin-focal adhesion kinase protein complex at the blood-testis barrier: a study using the cadmium model. Endocrinology 2009; 150:3336 - 44; http://dx.doi.org/10.1210/en.2008-1741; PMID: 19213829
  • Siu ER, Wong EWP, Mruk DD, Porto CS, Cheng CY. Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 2009; 106:9298 - 303; http://dx.doi.org/10.1073/pnas.0813113106; PMID: 19470647
  • Puri P, Walker WH. The tyrosine phosphatase SHP2 regulates Sertoli cell junction complexes. Biol Reprod 2013; 88:59; http://dx.doi.org/10.1095/biolreprod.112.104414; PMID: 23325809
  • Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat 1952; 90:167 - 215; http://dx.doi.org/10.1002/aja.1000900202; PMID: 14923625
  • Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972; 52:198 - 236; PMID: 4621362
  • Clermont Y. The cycle of the seminiferous epithelium in man. Am J Anat 1963; 112:35 - 51; http://dx.doi.org/10.1002/aja.1001120103; PMID: 14021715
  • Clermont Y, Leblond CP, Messier B. Duree du cycle de l'epithelium seminal du rat. Arch Anat Microsc Morphol Exp 1959; 48:37 - 56; PMID: 13810668
  • Parvinen M. Regulation of the seminiferous epithelium. Endocr Rev 1982; 3:404 - 17; http://dx.doi.org/10.1210/edrv-3-4-404; PMID: 6295753
  • Wong EWP, Cheng CY. Polarity proteins and cell-cell interactions in the testis. Int Rev Cell Mol Biol 2009; 278:309 - 53; http://dx.doi.org/10.1016/S1937-6448(09)78007-4; PMID: 19815182
  • Yan HHN, Mruk DD, Wong EWP, Lee WM, Cheng CY. An autocrine axis in the testis that coordinates spermiation and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008; 105:8950 - 5; http://dx.doi.org/10.1073/pnas.0711264105; PMID: 18579774
  • Yan HHN, Cheng CY. Laminin α 3 forms a complex with β3 and γ3 chains that serves as the ligand for α 6β1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 2006; 281:17286 - 303; http://dx.doi.org/10.1074/jbc.M513218200; PMID: 16608848
  • Siu MKY, Cheng CY. 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 2004; 70:945 - 64; http://dx.doi.org/10.1095/biolreprod.103.023606; PMID: 14645107
  • Koch M, Olson PF, Albus A, Jin W, Hunter DD, Brunken WJ, et al. Characterization and expression of the laminin γ3 chain: a novel, non-basement membrane-associated, laminin chain. J Cell Biol 1999; 145:605 - 18; http://dx.doi.org/10.1083/jcb.145.3.605; PMID: 10225960
  • Wong EWP, Cheng CY. NC1 domain of collagen α3(IV) derived from the basement membrane regulates Sertoli cell blood-testis barrier dynamics. Spermatogenesis 2013; 3:e25465; http://dx.doi.org/10.4161/spmg.25465
  • Su L, Mruk DD, Lie PPY, Silvestrini B, Cheng CY. A peptide derived from laminin-γ3 reversibly impairs spermatogenesis in rats. Nat Communs 2012; 3:1185; http://dx.doi.org/10.1038/ncomms2171
  • Yao PL, Lin YC, Richburg JH. TNF α-mediated disruption of spermatogenesis in response to Sertoli cell injury in rodents is partially regulated by MMP2. Biol Reprod 2009; 80:581 - 9; http://dx.doi.org/10.1095/biolreprod.108.073122; PMID: 19038859
  • Yao PL, Lin YC, Richburg JH. Mono-(2-ethylhexyl) phthalate-induced disruption of junctional complexes in the seminiferous epithelium of the rodent testis is mediated by MMP2. Biol Reprod 2010; 82:516 - 27; http://dx.doi.org/10.1095/biolreprod.109.080374; PMID: 19828778
  • Mazaud-Guittot S. Dissecting the phthalate-induced Sertoli cell injury: the fragile balance of proteases and their inhibitors. Biol Reprod 2011; 85:1091 - 3; http://dx.doi.org/10.1095/biolreprod.111.095976; PMID: 21900678
  • Wan HT, Mruk DD, Wong CKC, Cheng CY. The apical ES-BTB-BM functional axis is an emerging target for toxicant-induced infertility. Trends Mol Med 2013; In press http://dx.doi.org/10.1016/j.molmed.2013.03.006; PMID: 23643465
  • Lui WY, Wong CH, Mruk DD, Cheng CY. TGF-β3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 2003; 144:1139 - 42; http://dx.doi.org/10.1210/en.2002-0211; PMID: 12639893
  • Wong CH, Mruk DD, Lui WY, Cheng CY. Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 2004; 117:783 - 98; http://dx.doi.org/10.1242/jcs.00900; PMID: 14734653
  • Wong EWP, Lee WM, Cheng CY. Secreted Frizzled-related protein 1 (sFRP1) regulates spermatid adhesion in the testis via dephosphorylation of focal adhesion kinase and the nectin-3 adhesion protein complex. FASEB J 2013; 27:464 - 77; http://dx.doi.org/10.1096/fj.12-212514; PMID: 23073828
  • Xiao X, Mruk DD, Lee WM, Cheng CY. 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 2011; 43:651 - 65; http://dx.doi.org/10.1016/j.biocel.2011.01.008; PMID: 21256972