Focal adhesion signaling in heart failure

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 6, 2014, Pages 1101-1111

  Samarel, Allen M ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Costameres; Focal adhesion kinase; PYK2; Talin; Vinculin

Indexed keywords

BETA ADRENERGIC RECEPTOR BLOCKING AGENT; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; LAMININ; PAXILLIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; TALIN; VINCULIN;

COSTAMERE; EXTRACELLULAR MATRIX; FOCAL ADHESION; HEART FAILURE; HEART MUSCLE CELL; HEART PERFORMANCE; HEMODYNAMIC STRESS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SARCOMERE; SIGNAL TRANSDUCTION; ANIMAL; GENETICS; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY;

ANIMALS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HEART FAILURE; HUMANS; MECHANOTRANSDUCTION, CELLULAR; SARCOMERES;

EID: 84901932435     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1456-8     Document Type: Review

References (93)

1. Anthis NJ, Haling JR, Oxley CL, Memo M, Wegener KL, Lim CJ, Ginsberg MH, Campbell ID (2009) Beta integrin tyrosine phosphorylation is a conserved mechanism for regulating talin-induced integrin activation. J Biol Chem 284(52):36700-36710
2. Anthis NJ, Wegener KL, Ye F, Kim C, Goult BT, Lowe ED, Vakonakis I, Bate N, Critchley DR, Ginsberg MH, Campbell ID (2009) The structure of an integrin/talin complex reveals the basis of inside-out signal transduction. EMBO J 28(22):3623-3632
3. Bayer AL, Ferguson AG, Lucchesi PA, Samarel AM (2001) Pyk2 expression and phosphorylation in neonatal and adult cardiomyocytes. J Mol Cell Cardiol 33(5):1017-1030 (Pubitemid 32545335)
4. Bayer AL, Heidkamp MC, Howes AL, Heller Brown J, Byron KL, Samarel AM (2003) Protein kinase Cε-dependent activation of proline-rich tyrosine kinase 2 in neonatal rat ventricular myocytes. J Mol Cell Cardiol 35(9):1121-1133 (Pubitemid 37083256)
5. Bayer AL, Heidkamp MC, Patel N, Porter MJ, Engman SJ, Samarel AM (2002) PYK2 expression and phosphorylation increases in pressure overload-induced left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 283(2):H695-H706 (Pubitemid 34790865)
6. Blaukat A, Ivankovic-Dikic I, Gronroos E, Dolfi F, Tokiwa G, Vuori K, Dikic I (1999) Adaptor proteins Grb2 and Crk couple Pyk2 with activation of specific mitogen-activated protein kinase cascades. J Biol Chem 274(21):14893-14901
7. Burchfield JS, Xie M, Hill JA (2013) Pathological ventricular remodeling: mechanisms: part 1 of 2. Circulation 128(4):388-400
8. Campbell ID, Ginsberg MH (2004) The talin-tail interaction places integrin activation on FERM ground. Trends Biochem Sci 29(8):429-435 (Pubitemid 39061087)
9. Chen MH, Kerkela R, Force T (2008) Mechanisms of cardiac dysfunction associated with tyrosine kinase inhibitor cancer therapeutics. Circulation 118(1):84-95
10. Chu M, Iyengar R, Koshman YE, Kim T, Russell B, Martin JL, Heroux AL, Robia SL, Samarel AM (2011) Serine-910 phosphorylation of focal adhesion kinase is critical for sarcomere reorganization in cardiomyocyte hypertrophy. Cardiovasc Res 92(3):409-419
11. Conti FJ, Monkley SJ, Wood MR, Critchley DR, Muller U (2009) Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junctions. Development 136(21):3597-3606
12. Corsi JM, Rouer E, Girault JA, Enslen H (2006) Organization and post-transcriptional processing of focal adhesion kinase gene. BMC Genomics 7:198
13. Dabiri GA, Turnacioglu KK, Sanger JM, Sanger JW (1997) Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci U S A 94(17):9493-9498 (Pubitemid 27357857)
14. DiMichele LA, Doherty JT, Rojas M, Beggs HE, Reichardt LF, Mack CP, Taylor JM (2006) Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ Res 99(6):636-645 (Pubitemid 44401455)
15. Domingos PP, Fonseca PM, Nadruz W Jr, Franchini KG (2002) Load-induced focal adhesion kinase activation in the myocardium: role of stretch and contractile activity. Am J Physiol Heart Circ Physiol 282(2):H556-H564 (Pubitemid 34654979)
16. Eble DM, Strait JB, Govindarajan G, Lou J, Byron KL, Samarel AM (2000) Endothelin-induced cardiac myocyte hypertrophy: role for focal adhesion kinase. Am J Physiol Heart Circ Physiol 278(5):H1695-H1707 (Pubitemid 30395584)
17. Ervasti JM (2003) Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278(16):13591-13594
18. Fassler R, Rohwedel J, Maltsev V, Bloch W, Lentini S, Guan K, Gullberg D, Hescheler J, Addicks K, Wobus AM (1996) Differentiation and integrity of cardiac muscle cells are impaired in the absence of β1 integrin. J Cell Sci 109(Pt 13):2989-2999 (Pubitemid 27029269)
19. Frame MC, Patel H, Serrels B, Lietha D, Eck MJ (2010) The FERM domain: organizing the structure and function of FAK. Nat Rev Mol Cell Biol 11(11):802-814
20. Franchini KG, Torsoni AS, Soares PH, Saad MJ (2000) Early activation of the multicomponent signaling complex associated with focal adhesion kinase induced by pressure overload in the rat heart. Circ Res 87(7):558-565
21. Gopalan SM, Flaim C, Bhatia SN, Hoshijima M, Knoell R, Chien KR, Omens JH, McCulloch AD (2003) Anisotropic stretch-induced hypertrophy in neonatal ventricular myocytes micropatterned on deformable elastomers. Biotechnol Bioeng 81(5):578-587 (Pubitemid 36222316)
22. Guo J, Sabri A, Elouardighi H, Rybin V, Steinberg SF (2006) Alpha1-adrenergic receptors activate AKT via a Pyk2/PDK-1 pathway that is tonically inhibited by novel protein kinase C isoforms in cardiomyocytes. Circ Res 99(12):1367-1375 (Pubitemid 44949672)
23. Hagel M, George EL, Kim A, Tamimi R, Opitz SL, Turner CE, Imamoto A, Thomas SM (2002) The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol Cell Biol 22(3):901-915 (Pubitemid 34053067)
24. Hakim ZS, DiMichele LA, Doherty JT, Homeister JW, Beggs HE, Reichardt LF, Schwartz RJ, Brackhan J, Smithies O, Mack CP, Taylor JM (2007) Conditional deletion of focal adhesion kinase leads to defects in ventricular septation and outflow tract alignment. Mol Cell Biol 27(15):5352-5364 (Pubitemid 47124390)
25. Hakim ZS, DiMichele LA, Rojas M, Meredith D, Mack CP, Taylor JM (2009) FAK regulates cardiomyocyte survival following ischemia/reperfusion. J Mol Cell Cardiol 46(2):241-248
26. Hart DL, Heidkamp MC, Iyengar R, Vijayan K, Szotek EL, Barakat JA, Leya M, Henze M, Scrogin K, Henderson KK, Samarel AM (2008) CRNK gene transfer improves function and reverses the myosin heavy chain isoenzyme switch during post-myocardial infarction left ventricular remodeling. J Mol Cell Cardiol 45(1):93-105
27. Heidkamp MC, Bayer AL, Kalina JA, Eble DM, Samarel AM (2002) GFP-FRNK disrupts focal adhesions and induces anoikis in neonatal rat ventricular myocytes. Circ Res 90(12):1282-1289 (Pubitemid 34787410)
28. Heidkamp MC, Scully BT, Vijayan K, Engman SJ, Szotek EL, Samarel AM (2005) PYK2 regulates SERCA2 gene expression in neonatal rat ventricular myocytes. Am J Physiol Cell Physiol 289(2):C471-C482 (Pubitemid 41008894)
29. Hirotani S, Higuchi Y, Nishida K, Nakayama H, Yamaguchi O, Hikoso S, Takeda T, Kashiwase K, Watanabe T, Asahi M, Taniike M, Tsujimoto I, Matsumura Y, Sasaki T, Hori M, Otsu K (2004) Ca2+-sensitive tyrosine kinase Pyk2/CAKβ-dependent signaling is essential for G-protein-coupled receptor agonist-induced hypertrophy. J Mol Cell Cardiol 36(6):799-807 (Pubitemid 38639765)
30. Honda H, Oda H, Nakamoto T, Honda Z, Sakai R, Suzuki T, Saito T, Nakamura K, Nakao K, Ishikawa T, Katsuki M, Yazaki Y, Hirai H (1998) Cardiovascular anomaly, impaired actin bundling and resistance to Src-induced transformation in mice lacking p130Cas. Nat Genet 19(4):361-365 (Pubitemid 28357908)
31. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377(6549):539-544
32. Ilic D, Kovacic B, McDonagh S, Jin F, Baumbusch C, Gardner DG, Damsky CH (2003) Focal adhesion kinase is required for blood vessel morphogenesis. Circ Res 92(3):300-307 (Pubitemid 36258552)
33. Infante JR, Camidge DR, Mileshkin LR, Chen EX, Hicks RJ, Rischin D, Fingert H, Pierce KJ, Xu H, Roberts WG, Shreeve SM, Burris HA, Siu LL (2012) Safety, pharmacokinetic, and pharmacodynamic phase I dose-escalation trial of PF-00562271, an inhibitor of focal adhesion kinase, in advanced solid tumors. J Clin Oncol 30(13):1527-1533
34. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, Hess HF, Waterman CM (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468(7323):580-584
35. Kodama H, Fukuda K, Takahashi T, Sano M, Kato T, Tahara S, Hakuno D, Sato T, Manabe T, Konishi F, Ogawa S (2002) Role of EGF receptor and Pyk2 in endothelin-1-induced ERK activation in rat cardiomyocytes. J Mol Cell Cardiol 34(2):139-150 (Pubitemid 35222824)
36. 2+/calmodulin to FERM F2 α2 helix and thus forming its dimer. Biochem J 410(3):513-523
37. Koshman YE, Patel N, Chu M, Iyengar R, Kim T, Lewis W, Goldspink PH, Samarel AM (2012) Mechanical load up-regulates CTGF gene expression in isolated cardiomyocytes and in animal models of heart failure. J Mol Cell Cardiol 53:S18, abstract
38. Cas mediate both sarcomeric organization and activation of genes associated with cardiac myocyte hypertrophy. Mol Biol Cell 12(8):2290-2307
39. Kuppuswamy D, Kerr C, Narishige T, Kasi VS, Menick DR, Gt C (1997) Association of tyrosine-phosphorylated c-Src with the cytoskeleton of hypertrophying myocardium. J Biol Chem 272(7):4500-4508 (Pubitemid 27078529)
40. Lang D, Glukhov AV, Efimova T, Efimov IR (2011) Role of Pyk2 in cardiac arrhythmogenesis. Am J Physiol Heart Circ Physiol 301(3):H975-H983
41. Laser M, Willey CD, Jiang W, Gt C, Menick DR, Zile MR, Kuppuswamy D (2000) Integrin activation and focal complex formation in cardiac hypertrophy. J Biol Chem 275(45):35624-35630
42. Lele TP, Thodeti CK, Pendse J, Ingber DE (2008) Investigating complexity of protein-protein interactions in focal adhesions. Biochem Biophys Res Commun 369(3):929-934
43. 1 integrin gene excision in the adult murine cardiac myocyte causes defective mechanical and signaling responses. Am J Pathol 180(3):952-962
44. Lietha D, Cai X, Ceccarelli DF, Li Y, Schaller MD, Eck MJ (2007) Structural basis for the autoinhibition of focal adhesion kinase. Cell 129(6):1177-1187 (Pubitemid 46891044)
45. Lim Y, Han I, Jeon J, Park H, Bahk YY, Oh ES (2004) Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J Biol Chem 279(28):29060-29065 (Pubitemid 38915776)
46. Manso AM, Li R, Monkley SJ, Cruz NM, Ong S, Lao DH, Koshman YE, Gu Y, Peterson KL, Chen J, Abel ED, Samarel AM, Critchley DR, Ross RS (2013) Talin1 has unique expression versus talin 2 in the heart and modifies the hypertrophic response to pressure overload. J Biol Chem 288(6):4252-4264
47. Mansour H, de Tombe PP, Samarel AM, Russell B (2004) Restoration of resting sarcomere length after uniaxial static strain is regulated by protein kinase Cε and focal adhesion kinase. Circ Res 94(5):642-649 (Pubitemid 38387747)
48. Marin TM, Clemente CF, Santos AM, Picardi PK, Pascoal VD, Lopes-Cendes I, Saad MJ, Franchini KG (2008) Shp2 negatively regulates growth in cardiomyocytes by controlling focal adhesion kinase/Src and mTOR pathways. Circ Res 103(8):813-824
49. Melendez J, Turner C, Avraham H, Steinberg SF, Schaefer E, Sussman MA (2004) Cardiomyocyte apoptosis triggered by RAFTK/Pyk2 via Src kinase is antagonized by paxillin. J Biol Chem 279(51):53516-53523 (Pubitemid 40051858)
50. Melendez J, Welch S, Schaefer E, Moravec CS, Avraham S, Avraham H, Sussman MA (2002) Activation of Pyk2/Related focal adhesion tyrosine kinase and focal adhesion kinase in cardiac remodeling. J Biol Chem 277(47):45203-45210 (Pubitemid 36159124)
51. Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6(1):56-68 (Pubitemid 40064899)
52. Mitra SK, Schlaepfer DD (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18(5):516-523 (Pubitemid 44332916)
53. Nadruz W Jr, Corat MA, Marin TM, Guimaraes Pereira GA, Franchini KG (2005) Focal adhesion kinase mediates MEF2 and c-Jun activation by stretch: role in the activation of the cardiac hypertrophic genetic program. Cardiovasc Res 68:87-97 (Pubitemid 41253559)
54. Okigaki M, Davis C, Falasca M, Harroch S, Felsenfeld DP, Sheetz MP, Schlessinger J (2003) Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc Natl Acad Sci U S A 100(19):10740-10745 (Pubitemid 37140098)
55. Oudit GY, Kassiri Z, Zhou J, Liu QC, Liu PP, Backx PH, Dawood F, Crackower MA, Scholey JW, Penninger JM (2008) Loss of PTEN attenuates the development of pathological hypertrophy and heart failure in response to biomechanical stress. Cardiovasc Res 78(3):505-514 (Pubitemid 351769769)
56. Pandey P, Avraham S, Kumar S, Nakazawa A, Place A, Ghanem L, Rana A, Kumar V, Majumder PK, Avraham H, Davis RJ, Kharbanda S (1999) Activation of p38 mitogen-activated protein kinase by PYK2/related adhesion focal tyrosine kinase-dependent mechanism. J Biol Chem 274(15):10140-10144
57. Pardo JV, Siliciano JD, Craig SW (1983) A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci U S A 80(4):1008-1012 (Pubitemid 13118076)
58. Pardo JV, Siliciano JD, Craig SW (1983) Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers. J Cell Biol 97(4):1081-1088 (Pubitemid 13019368)
59. Park SY, Avraham HK, Avraham S (2004) RAFTK/Pyk2 activation ismediated by trans-acting autophosphorylation in a Src-independent manner. J Biol Chem 279(32):33315-33322 (Pubitemid 39062979)
60. Peng X, Kraus MS, Wei H, Shen TL, Pariaut R, Alcaraz A, Ji G, Cheng L, Yang Q, Kotlikoff MI, Chen J, Chien K, Gu H, Guan JL (2006) Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J Clin Invest 116(1):217-227 (Pubitemid 43121807)
61. Peng X, Wu X, Druso JE, Wei H, Park AY, Kraus MS, Alcaraz A, Chen J, Chien S, Cerione RA, Guan JL (2008) Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc Natl Acad Sci U S A 105(18):6638-6643 (Pubitemid 351754559)
62. Perricone AJ, Bivona BJ, Jackson FR, Vander Heide RS (2013) Conditional knockout of myocyte ocal adhesion kinase abrogates ischemic preconditioning in adult murine hearts. J Am Heart Assoc 2(5):e000457
63. 1D-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am J Physiol Heart Circ Physiol 279(6):H2916-H2926
64. Porter MJ, Bayer AL, Samarel AM (2004) Regulation of PYK2 gene expression during cardiomyocyte hypertrophy. J Mol Cell Cardiol 34(7):A11, abstract
65. Riggs D, Yang Z, Kloss J, Loftus JC (2011) The Pyk2 FERM regulates Pyk2 complex formation and phosphorylation. Cell Signal 23:288-296
66. Sabri A, Rafiq K, Seqqat R, Kolpakov MA, Dillon R, Dell'italia LJ (2008) Sympathetic activation causes focal adhesion signaling alteration in early compensated volume overload attributable to isolated mitral regurgitation in the dog. Circ Res 102(9):1127-1136 (Pubitemid 351667867)
67. Samarel AM (2005) Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol 289(6):H2291-H2301
68. Sanger JW, Wang J, Fan Y, White J, Sanger JM (2010) Assembly and dynamics of myofibrils. J Biomed Biotechnol 2010:858606
69. src. Mol Cell Biol 14(3):1680-1688
70. Schlaepfer DD, Mitra SK, Ilic D (2004) Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta 1692(2-3):77-102 (Pubitemid 38898737)
71. Schwartz MA (2009) Cell biology. The force is with us. Science 323(5914):588-589
72. Schwartzbauer G, Robbins J (2001) The tumor suppressor gene PTEN can regulate cardiac hypertrophy and survival. J Biol Chem 276(38):35786-35793
73. Senetar MA, Moncman CL, McCann RO (2007) Talin2 is induced during striated muscle differentiation and is targeted to stable adhesion complexes in mature muscle. Cell Motil Cytoskeleton 64(3):157-173
74. Senyo SE, Koshman YE, Russell B (2007) Stimulus interval, rate and direction differentially regulate phosphorylation for mechanotransduction in neonatal cardiac myocytes. FEBS Lett 581(22):4241-4247 (Pubitemid 47307336)
75. Seqqat R, Guo X, Rafiq K, Kolpakov MA, Guo J, Koch WJ, Houser SR, Dell'italia LJ, Sabri A (2012) Beta1-adrenergic receptors promote focal adhesion signaling downregulation and myocyte apoptosis in acute volume overload. J Mol Cell Cardiol 53(2):240-249
76. 1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res 90(4):458-464
77. Sharp WW, Simpson DG, Borg TK, Samarel AM, Terracio L (1997) Mechanical forces regulate focal adhesion and costamere assembly in cardiac myocytes. Am J Physiol 273(2 Pt 2):H546-H556
78. Sieg DJ, Ilic D, Jones KC, Damsky CH, Hunter T, Schlaepfer DD (1998) Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK-cell migration. EMBO J 17(20):5933-5947 (Pubitemid 28474788)
79. Simpson DG, Majeski M, Borg TK, Terracio L (1999) Regulation of cardiac myocyte protein turnover and myofibrillar structure in vitro by specific directions of stretch. Circ Res 85(10):e59-e69
80. Stout AL, Wang J, Sanger JM, Sanger JW (2008) Tracking changes in Z-band organization during myofibrillogenesis with FRET imaging. Cell Motil Cytoskeleton 65(5):353-367 (Pubitemid 351657151)
81. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, de Pereda JM, Ginsberg MH, Calderwood DA (2003) Talin binding to integrin beta tails: a final common step in integrin activation. Science 302(5642):103-106 (Pubitemid 37210697)
82. Taniyama Y, Weber DS, Rocic P, Hilenski L, Akers ML, Park J, Hemmings BA, Alexander RW, Griendling KK (2003) Pyk2- and Src-dependent tyrosine phosphorylation of PDK1 regulates focal adhesions. Mol Cell Biol 23(22):8019-8029 (Pubitemid 37377495)
83. Taylor JM, Rovin JD, Parsons JT (2000) A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes. J Biol Chem 275(25):19250-19257 (Pubitemid 30422897)
84. Tokiwa G, Dikic I, Lev S, Schlessinger J (1996) Activation of Pyk2 by stress signals and coupling with JNK signaling pathway. Science 273(5276):792-794 (Pubitemid 26271523)
85. Torsoni AS, Constancio SS, Nadruz W Jr, Hanks SK, Franchini KG (2003) Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ Res 93(2):140-147 (Pubitemid 36919701)
86. ROCK by pressure overload in rat heart. Am J Physiol Cell Physiol 284(6):C1411-C1419
87. Wang J, Shaner N, Mittal B, Zhou Q, Chen J, Sanger JM, Sanger JW (2005) Dynamics of Z-band based proteins in developing skeletal muscle cells. Cell Motil Cytoskeleton 61(1):34-48 (Pubitemid 40604949)
88. Wei H, Vander Heide RS (2010) Ischemic preconditioning and heat shock activate Akt via a focal adhesion kinase-mediated pathway in Langendorff-perfused adult rat hearts. Am J Physiol Heart Circ Physiol 298(1):H152-H157
89. Weis SM, Lim ST, Lutu-Fuga KM, Barnes LA, Chen XL, Gothert JR, Shen TL, Guan JL, Schlaepfer DD, Cheresh DA (2008) Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J Cell Biol 181(1):43-50 (Pubitemid 351519763)
90. Xu W, Baribault H, Adamson ED (1998) Vinculin knockout results in heart and brain defects during embryonic development. Development 125(2):327-337 (Pubitemid 28064445)
91. Ye F, Hu G, Taylor D, Ratnikov B, Bobkov AA, McLean MA, Sligar SG, Taylor KA, Ginsberg MH (2010) Recreation of the terminal events in physiological integrin activation. J Cell Biol 188(1):157-175
92. Yi XP, Zhou J, Huber L, Qu J, Wang X, Gerdes AM, Li F (2006) Nuclear compartmentalization of FAK and FRNK in cardiac myocytes. Am J Physiol Heart Circ Physiol 290(6):H2509-H2515 (Pubitemid 43846081)
93. Zemljic-Harpf A, Manso AM, Ross RS (2009) Vinculin and talin: focus on the myocardium. J Investig Med 57(8):849-855