ErbB/integrin signaling interactions in regulation of myocardial cell-cell and cell-matrix interactions

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 4, 2013, Pages 909-916

  Pentassuglia, Laura ^a   Sawyer, Douglas B ^b  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cardiomyocyte; FAK; Heart; Integrin; Neuregulin; Nrg1

Indexed keywords

ALPHA6BETA4 INTEGRIN; ATRIAL NATRIURETIC FACTOR; BETA INTEGRIN; BRAIN NATRIURETIC PEPTIDE; COLLAGEN TYPE 1; COLLAGEN TYPE 6; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 4; FOCAL ADHESION KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN HEAVY CHAIN BETA; MYOSIN II; PAXILLIN; REACTIVE OXYGEN METABOLITE; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 5; VINCULIN;

ACTIN FILAMENT; APOPTOSIS; BINDING AFFINITY; CATALYSIS; CELL ADHESION; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CELL INTERACTION; CELL METABOLISM; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME INHIBITION; EXTRACELLULAR MATRIX; GENE OVEREXPRESSION; HEART DEVELOPMENT; HEART MUSCLE CELL; HEART PROTECTION; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

CARDIOMEGALY; CELL COMMUNICATION; EXTRACELLULAR MATRIX; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION REGULATION; HUMANS; INTEGRINS; ISOENZYMES; MYOCARDIAL ISCHEMIA; MYOCARDIUM; MYOCYTES, CARDIAC; NEUREGULIN-1; ONCOGENE PROTEINS V-ERBB; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84875070234     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.12.007     Document Type: Review

References (140)

1. Gassmann M., Casagranda F., Orioli D., Simon H., Lai C., Klein R., Lemke G. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 1995, 378:390-394.
2. Lee K.F., Simon H., Chen H., Bates B., Hung M.C., Hauser C. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 1995, 378:394-398.
3. Meyer D., Birchmeier C. Multiple essential functions of neuregulin in development. Nature 1995, 378:386-390.
4. Crone S.A., Zhao Y.Y., Fan L., Gu Y., Minamisawa S., Liu Y., Peterson K.L., Chen J., Kahn R., Condorelli G., Ross J., Chien K.R., Lee K.F. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat. Med. 2002, 8:459-465.
5. Garcia-Rivello H., Taranda J., Said M., Cabeza-Meckert P., Vila-Petroff M., Scaglione J., Ghio S., Chen J., Lai C., Laguens R.P., Lloyd K.C., Hertig C.M. Dilated cardiomyopathy in Erb-b4-deficient ventricular muscle. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:H1153-H1160.
6. Pentassuglia L., Sawyer D.B. The role of neuregulin-1beta/ErbB signaling in the heart. Exp. Cell Res. 2009, 315:627-637.
7. Fassler R., Rohwedel J., Maltsev V., Bloch W., Lentini S., Guan K., Gullberg D., Hescheler J., Addicks K., Wobus A.M. Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J. Cell Sci. 1996, 109(Pt 13):2989-2999.
8. Shai S.Y., Harpf A.E., Babbitt C.J., Jordan M.C., Fishbein M.C., Chen J., Omura M., Leil T.A., Becker K.D., Jiang M., Smith D.J., Cherry S.R., Loftus J.C., Ross R.S. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res. 2002, 90:458-464.
9. Nakaoka Y., Nishida K., Narimatsu M., Kamiya A., Minami T., Sawa H., Okawa K., Fujio Y., Koyama T., Maeda M., Sone M., Yamasaki S., Arai Y., Koh G.Y., Kodama T., Hirota H., Otsu K., Hirano T., Mochizuki N. Gab family proteins are essential for postnatal maintenance of cardiac function via neuregulin-1/ErbB signaling. J. Clin. Invest. 2007, 117:1771-1781.
10. Dunty J.M., Gabarra-Niecko V., King M.L., Ceccarelli D.F., Eck M.J., Schaller M.D. FERM domain interaction promotes FAK signaling. Mol. Cell. Biol. 2004, 24:5353-5368.
11. Kuramochi Y., Cote G.M., Guo X., Lebrasseur N.K., Cui L., Liao R., Sawyer D.B. Cardiac endothelial cells regulate reactive oxygen species-induced cardiomyocyte apoptosis through neuregulin-1beta/erbB4 signaling. J. Biol. Chem. 2004, 279:51141-51147.
12. Fang S.J., Wu X.S., Han Z.H., Zhang X.X., Wang C.M., Li X.Y., Lu L.Q., Zhang J.L. Neuregulin-1 preconditioning protects the heart against ischemia/reperfusion injury through a PI3K/Akt-dependent mechanism. Chin. Med. J. (Engl) 2010, 123:3597-3604.
13. Fukazawa R., Miller T.A., Kuramochi Y., Frantz S., Kim Y.D., Marchionni M.A., Kelly R.A., Sawyer D.B. Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J. Mol. Cell. Cardiol. 2003, 35:1473-1479.
14. Timolati F., Ott D., Pentassuglia L., Giraud M.N., Perriard J.C., Suter T.M., Zuppinger C. Neuregulin-1 beta attenuates doxorubicin-induced alterations of excitation-contraction coupling and reduces oxidative stress in adult rat cardiomyocytes. J. Mol. Cell. Cardiol. 2006, 41:845-854.
15. Bian Y., Sun M., Silver M., Ho K.K., Marchionni M.A., Caggiano A.O., Stone J.R., Amende I., Hampton T.G., Morgan J.P., Yan X. Neuregulin-1 attenuated doxorubicin-induced decrease in cardiac troponins. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H1974-H1983.
16. Suk Kim H., Hidaka K., Morisaki T. Expression of ErbB receptors in ES cell-derived cardiomyocytes. Biochem. Biophys. Res. Commun. 2003, 309:241-246.
17. Kim H.S., Cho J.W., Hidaka K., Morisaki T. Activation of MEK-ERK by heregulin-beta1 promotes the development of cardiomyocytes derived from ES cells. Biochem. Biophys. Res. Commun. 2007, 361:732-738.
18. Pentassuglia L., Graf M., Lane H., Kuramochi Y., Cote G., Timolati F., Sawyer D.B., Zuppinger C., Suter T.M. Inhibition of ErbB2 by receptor tyrosine kinase inhibitors causes myofibrillar structural damage without cell death in adult rat cardiomyocytes. Exp. Cell Res. 2009, 315:1302-1312.
19. Baliga R.R., Pimental D.R., Zhao Y.Y., Simmons W.W., Marchionni M.A., Sawyer D.B., Kelly R.A. NRG-1-induced cardiomyocyte hypertrophy. Role of PI-3-kinase, p70(S6K), and MEK-MAPK-RSK. Am. J. Physiol. 1999, 277:H2026-H2037.
20. Giraud M.N., Fluck M., Zuppinger C., Suter T.M. Expressional reprogramming of survival pathways in rat cardiocytes by neuregulin-1beta. J. Appl. Physiol. 2005, 99:313-322.
21. Zhao Y.Y., Sawyer D.R., Baliga R.R., Opel D.J., Han X., Marchionni M.A., Kelly R.A. Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. J. Biol. Chem. 1998, 273:10261-10269.
22. Jacamo R.O., Rozengurt E. A truncated FAK lacking the FERM domain displays high catalytic activity but retains responsiveness to adhesion-mediated signals. Biochem. Biophys. Res. Commun. 2005, 334:1299-1304.
23. Parsons J.T. Focal adhesion kinase: the first ten years. J. Cell Sci. 2003, 116:1409-1416.
24. Schlaepfer D.D., Hauck C.R., Sieg D.J. Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol. 1999, 71:435-478.
25. Hildebrand J.D., Schaller M.D., Parsons J.T. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions. J. Cell Biol. 1993, 123:993-1005.
26. Dixon R.D., Chen Y., Ding F., Khare S.D., Prutzman K.C., Schaller M.D., Campbell S.L., Dokholyan N.V. New insights into FAK signaling and localization based on detection of a FAT domain folding intermediate. Structure 2004, 12:2161-2171.
27. Schlaepfer D.D., Mitra S.K. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 2004, 14:92-101.
28. Cox B.D., Natarajan M., Stettner M.R., Gladson C.L. New concepts regarding focal adhesion kinase promotion of cell migration and proliferation. J. Cell. Biochem. 2006, 99:35-52.
29. Liu G., Guibao C.D., Zheng J. Structural insight into the mechanisms of targeting and signaling of focal adhesion kinase. Mol. Cell. Biol. 2002, 22:2751-2760.
30. Han D.C., Guan J.L. Association of focal adhesion kinase with Grb7 and its role in cell migration. J. Biol. Chem. 1999, 274:24425-24430.
31. Endo M., Yamashita T. Inactivation of Ras by p120GAP via focal adhesion kinase dephosphorylation mediates RGMa-induced growth cone collapse. J. Neurosci. 2009, 29:6649-6662.
32. Zhang X., Chattopadhyay A., Ji Q.S., Owen J.D., Ruest P.J., Carpenter G., Hanks S.K. Focal adhesion kinase promotes phospholipase C-gamma1 activity. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9021-9026.
33. Reiske H.R., Kao S.C., Cary L.A., Guan J.L., Lai J.F., Chen H.C. Requirement of phosphatidylinositol 3-kinase in focal adhesion kinase-promoted cell migration. J. Biol. Chem. 1999, 274:12361-12366.
34. Schaller M.D., Hildebrand J.D., Shannon J.D., Fox J.W., Vines R.R., Parsons J.T. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 1994, 14:1680-1688.
35. Ohba T., Ishino M., Aoto H., Sasaki T. Interaction of two proline-rich sequences of cell adhesion kinase beta with SH3 domains of p130Cas-related proteins and a GTPase-activating protein, Graf. Biochem. J. 1998, 330(Pt 3):1249-1254.
36. Polte T.R., Hanks S.K. Interaction between focal adhesion kinase and Crk-associated tyrosine kinase substrate p130Cas. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:10678-10682.
37. Calalb M.B., Zhang X., Polte T.R., Hanks S.K. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 1996, 228:662-668.
38. Schlaepfer D.D., Broome M.A., Hunter T. Fibronectin-stimulated signaling from a focal adhesion kinase-c-Src complex: involvement of the Grb2, p130cas, and Nck adaptor proteins. Mol. Cell. Biol. 1997, 17:1702-1713.
39. Ishii I., Tomizawa A., Kawachi H., Suzuki T., Kotani A., Koshushi I., Itoh H., Morisaki N., Bujo H., Saito Y., Ohmori S., Kitada M. Histological and functional analysis of vascular smooth muscle cells in a novel culture system with honeycomb-like structure. Atherosclerosis 2001, 158:377-384.
40. Morla A.O., Mogford J.E. Control of smooth muscle cell proliferation and phenotype by integrin signaling through focal adhesion kinase. Biochem. Biophys. Res. Commun. 2000, 272:298-302.
41. Fluck M., Carson J.A., Gordon S.E., Ziemiecki A., Booth F.W. Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am. J. Physiol. 1999, 277:C152-C162.
42. Cappello R.E., Estrada-Gutierrez G., Irles C., Giono-Cerezo S., Bloch R.J., Nataro J.P. Effects of the plasmid-encoded toxin of enteroaggregative Escherichia coli on focal adhesion complexes. FEMS Immunol. Med. Microbiol. 2011, 61:301-314.
43. Kovacic-Milivojevic B., Roediger F., Almeida E.A., Damsky C.H., Gardner D.G., Ilic D. Focal adhesion kinase and p130Cas mediate both sarcomeric organization and activation of genes associated with cardiac myocyte hypertrophy. Mol. Biol. Cell 2001, 12:2290-2307.
44. Kuramochi Y., Guo X., Sawyer D.B. Neuregulin activates erbB2-dependent src/FAK signaling and cytoskeletal remodeling in isolated adult rat cardiac myocytes. J. Mol. Cell. Cardiol. 2006, 41:228-235.
45. Vartanian T., Goodearl A., Lefebvre S., Park S.K., Fischbach G. Neuregulin induces the rapid association of focal adhesion kinase with the erbB2-erbB3 receptor complex in schwann cells. Biochem. Biophys. Res. Commun. 2000, 271:414-417.
46. Cance W.G., Liu E.T. Protein kinases in human breast cancer. Breast Cancer Res. Treat. 1995, 35:105-114.
47. Ignatoski K.M., Maehama T., Markwart S.M., Dixon J.E., Livant D.L., Ethier S.P. ERBB-2 overexpression confers PI 3' kinase-dependent invasion capacity on human mammary epithelial cells. Br. J. Cancer 2000, 82:666-674.
48. Vadlamudi R.K., Sahin A.A., Adam L., Wang R.A., Kumar R. Heregulin and HER2 signaling selectively activates c-Src phosphorylation at tyrosine 215. FEBS Lett. 2003, 543:76-80.
49. Villa-Moruzzi E. Tyrosine phosphatases in the HER2-directed motility of ovarian cancer cells: Involvement of PTPN12, ERK5 and FAK. Anal. Cell. Pathol. (Amst.) 2011, 34:101-112.
50. Roovers K., Wagner S., Storbeck C.J., O'Reilly P., Lo V., Northey J.J., Chmielecki J., Muller W.J., Siegel P.M., Sabourin L.A. The Ste20-like kinase SLK is required for ErbB2-driven breast cancer cell motility. Oncogene 2009, 28:2839-2848.
51. Ponnusamy M.P., Singh A.P., Jain M., Chakraborty S., Moniaux N., Batra S.K. MUC4 activates HER2 signalling and enhances the motility of human ovarian cancer cells. Br. J. Cancer 2008, 99:520-526.
52. Lahlou H., Sanguin-Gendreau V., Frame M.C., Muller W.J. Focal adhesion kinase contributes to proliferative potential of ErbB2 mammary tumour cells but is dispensable for ErbB2 mammary tumour induction in vivo. Breast Cancer Res. 2012, 14:R36.
53. Xu M., Bower K.A., Chen G., Shi X., Dong Z., Ke Z., Luo J. Ethanol enhances the interaction of breast cancer cells over-expressing ErbB2 with fibronectin. Alcohol. Clin. Exp. Res. 2010, 34:751-760.
54. Xu Y., Benlimame N., Su J., He Q., Alaoui-Jamali M.A. Regulation of focal adhesion turnover by ErbB signalling in invasive breast cancer cells. Br. J. Cancer 2009, 100:633-643.
55. Yang X.H., Flores L.M., Li Q., Zhou P., Xu F., Krop I.E., Hemler M.E. Disruption of laminin-integrin-CD151-focal adhesion kinase axis sensitizes breast cancer cells to ErbB2 antagonists. Cancer Res. 2010, 70:2256-2263.
56. Furuta Y., Ilic D., Kanazawa S., Takeda N., Yamamoto T., Aizawa S. Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene 1995, 11:1989-1995.
57. Vallejo-Illarramendi A., Zang K., Reichardt L.F. Focal adhesion kinase is required for neural crest cell morphogenesis during mouse cardiovascular development. J. Clin. Invest. 2009, 119:2218-2230.
58. Hakim Z.S., DiMichele L.A., Doherty J.T., Homeister J.W., Beggs H.E., Reichardt L.F., Schwartz R.J., Brackhan J., Smithies O., Mack C.P., Taylor J.M. Conditional deletion of focal adhesion kinase leads to defects in ventricular septation and outflow tract alignment. Mol. Cell. Biol. 2007, 27:5352-5364.
59. Zajac B., Hakim Z.S., Cameron M.V., Smithies O., Taylor J.M. Quantification of myocyte chemotaxis: a role for FAK in regulating directional motility. Methods Mol. Biol. 2012, 843:111-123.
60. Hakuno D., Takahashi T., Lammerding J., Lee R.T. Focal adhesion kinase signaling regulates cardiogenesis of embryonic stem cells. J. Biol. Chem. 2005, 280:39534-39544.
61. Peng X., Wu X., Druso J.E., Wei H., Park A.Y., Kraus M.S., Alcaraz A., Chen J., Chien S., Cerione R.A., Guan J.L. Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6638-6643.
62. Taylor J.M., Rovin J.D., Parsons J.T. A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes. J. Biol. Chem. 2000, 275:19250-19257.
63. Eble D.M., Strait J.B., Govindarajan G., Lou J., Byron K.L., Samarel A.M. Endothelin-induced cardiac myocyte hypertrophy: role for focal adhesion kinase. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H1695-H1707.
64. Laser M., Willey C.D., Jiang W., Cooper G.T., Menick D.R., Zile M.R., Kuppuswamy D. Integrin activation and focal complex formation in cardiac hypertrophy. J. Biol. Chem. 2000, 275:35624-35630.
65. Pham C.G., Harpf A.E., Keller R.S., Vu H.T., Shai S.Y., Loftus J.C., Ross R.S. Striated muscle-specific beta(1D)-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H2916-H2926.
66. Peng X., Kraus M.S., Wei H., Shen T.L., Pariaut R., Alcaraz A., Ji G., Cheng L., Yang Q., Kotlikoff M.I., Chen J., Chien K., Gu H., Guan J.L. Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J. Clin. Invest. 2006, 116:217-227.
67. DiMichele L.A., Doherty J.T., Rojas M., Beggs H.E., Reichardt L.F., Mack C.P., Taylor J.M. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ. Res. 2006, 99:636-645.
68. Rafiq K., Kolpakov M.A., Abdelfettah M., Streblow D.N., Hassid A., Dell'Italia L.J., Sabri A. Role of protein-tyrosine phosphatase SHP2 in focal adhesion kinase down-regulation during neutrophil cathepsin G-induced cardiomyocytes anoikis. J. Biol. Chem. 2006, 281:19781-19792.
69. Heidkamp M.C., Bayer A.L., Kalina J.A., Eble D.M., Samarel A.M. GFP-FRNK disrupts focal adhesions and induces anoikis in neonatal rat ventricular myocytes. Circ. Res. 2002, 90:1282-1289.
70. Qin J., Liu Z.X. FAK-related nonkinase attenuates hypertrophy induced by angiotensin-II in cultured neonatal rat cardiac myocytes. Acta Pharmacol. Sin. 2006, 27:1159-1164.
71. Lee K.S., Park J.H., Lee S., Lim H.J., Park H.Y. PPARdelta activation inhibits angiotensin II induced cardiomyocyte hypertrophy by suppressing intracellular Ca2+ signaling pathway. J. Cell. Biochem. 2009, 106:823-834.
72. Chu M., Iyengar R., Koshman Y.E., Kim T., Russell B., Martin J.L., Heroux A.L., Robia S.L., Samarel A.M. Serine-910 phosphorylation of focal adhesion kinase is critical for sarcomere reorganization in cardiomyocyte hypertrophy. Cardiovasc. Res. 2011, 92:409-419.
73. Clemente C.F., Xavier-Neto J., Dalla Costa A.P., Consonni S.R., Antunes J.E., Rocco S.A., Pereira M.B., Judice C.C., Strauss B., Joazeiro P.P., Matos-Souza J.R., Franchini K.G. Focal adhesion kinase governs cardiac concentric hypertrophic growth by activating the AKT and mTOR pathways. J. Mol. Cell. Cardiol. 2012, 52:493-501.
74. Franchini K.G., Torsoni A.S., Soares P.H., Saad M.J. Early activation of the multicomponent signaling complex associated with focal adhesion kinase induced by pressure overload in the rat heart. Circ. Res. 2000, 87:558-565.
75. Domingos P.P., Fonseca P.M., Nadruz W., Franchini K.G. Load-induced focal adhesion kinase activation in the myocardium: role of stretch and contractile activity. Am. J. Physiol. Heart Circ. Physiol. 2002, 282:H556-H564.
76. Borges L., Bigarella C.L., Baratti M.O., Crosara-Alberto D.P., Joazeiro P.P., Franchini K.G., Costa F.F., Saad S.T. ARHGAP21 associates with FAK and PKCzeta and is redistributed after cardiac pressure overload. Biochem. Biophys. Res. Commun. 2008, 374:641-646.
77. Fonseca P.M., Inoue R.Y., Kobarg C.B., Crosara-Alberto D.P., Kobarg J., Franchini K.G. Targeting to C-terminal myosin heavy chain may explain mechanotransduction involving focal adhesion kinase in cardiac myocytes. Circ. Res. 2005, 96:73-81.
78. Torsoni A.S., Constancio S.S., Nadruz W., Hanks S.K., Franchini K.G. Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ. Res. 2003, 93:140-147.
79. Senyo S.E., Koshman Y.E., Russell B. Stimulus interval, rate and direction differentially regulate phosphorylation for mechanotransduction in neonatal cardiac myocytes. FEBS Lett. 2007, 581:4241-4247.
80. Sbroggio M., Bertero A., Velasco S., Fusella F., De Blasio E., Bahou W.F., Silengo L., Turco E., Brancaccio M., Tarone G. ERK1/2 activation in heart is controlled by melusin, focal adhesion kinase and the scaffold protein IQGAP1. J. Cell Sci. 2011, 124:3515-3524.
81. Yi X.P., Zhou J., Huber L., Qu J., Wang X., Gerdes A.M., Li F. Nuclear compartmentalization of FAK and FRNK in cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H2509-H2515.
82. Yi X.P., Wang X., Gerdes A.M., Li F. Subcellular redistribution of focal adhesion kinase and its related nonkinase in hypertrophic myocardium. Hypertension 2003, 41:1317-1323.
83. Umar S., Hessel M., Steendijk P., Bax W., Schutte C., Schalij M., van der Wall E., Atsma D., van der Laarse A. Activation of signaling molecules and matrix metalloproteinases in right ventricular myocardium of rats with pulmonary hypertension. Pathol. Res. Pract. 2007, 203:863-872.
84. Marin T.M., Clemente C.F., Santos A.M., Picardi P.K., Pascoal V.D., Lopes-Cendes I., Saad M.J., Franchini K.G. Shp2 negatively regulates growth in cardiomyocytes by controlling focal adhesion kinase/Src and mTOR pathways. Circ. Res. 2008, 103:813-824.
85. Wei H., Vander Heide R.S. Heat stress activates AKT via focal adhesion kinase-mediated pathway in neonatal rat ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H561-H568.
86. Cheng Z., DiMichele L.A., Hakim Z.S., Rojas M., Mack C.P., Taylor J.M. Targeted focal adhesion kinase activation in cardiomyocytes protects the heart from ischemia/reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 2012, 32:924-933.
87. Hakim Z.S., DiMichele L.A., Rojas M., Meredith D., Mack C.P., Taylor J.M. FAK regulates cardiomyocyte survival following ischemia/reperfusion. J. Mol. Cell. Cardiol. 2009, 46:241-248.
88. Lal H., Verma S.K., Smith M., Guleria R.S., Lu G., Foster D.M., Dostal D.E. Stretch-induced MAP kinase activation in cardiac myocytes: differential regulation through beta1-integrin and focal adhesion kinase. J. Mol. Cell. Cardiol. 2007, 43:137-147.
89. Pasapera A.M., Schneider I.C., Rericha E., Schlaepfer D.D., Waterman C.M. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 2010, 188:877-890.
90. Arnaout M.A., Mahalingam B., Xiong J.P. Integrin structure, allostery, and bidirectional signaling. Annu. Rev. Cell Dev. Biol. 2005, 21:381-410.
91. Takada Y., Ye X., Simon S. The integrins. Genome Biol. 2007, 8:215.
92. Cavani A., Zambruno G., Marconi A., Manca V., Marchetti M., Giannetti A. Distinctive integrin expression in the newly forming epidermis during wound healing in humans. J. Invest. Dermatol. 1993, 101:600-604.
93. Rahilly M.A., Fleming S. Differential expression of integrin alpha chains by renal epithelial cells. J. Pathol. 1992, 167:327-334.
94. Virtanen I., Laitinen A., Tani T., Paakko P., Laitinen L.A., Burgeson R.E., Lehto V.P. Differential expression of laminins and their integrin receptors in developing and adult human lung. Am. J. Respir. Cell Mol. Biol. 1996, 15:184-196.
95. Wu J.E., Santoro S.A. Differential expression of integrin alpha subunits supports distinct roles during lung branching morphogenesis. Dev. Dyn. 1996, 206:169-181.
96. Arcangeli A., Becchetti A. Complex functional interaction between integrin receptors and ion channels. Trends Cell Biol. 2006, 16:631-639.
97. Kawasaki J., Davis G.E., Davis M.J. Regulation of Ca2+-dependent K+ current by alphavbeta3 integrin engagement in vascular endothelium. J. Biol. Chem. 2004, 279:12959-12966.
98. Basak S., Dhar R., Das C. Steroids modulate the expression of alpha4 integrin in mouse blastocysts and uterus during implantation. Biol. Reprod. 2002, 66:1784-1789.
99. Cody V., Davis P.J., Davis F.B. Molecular modeling of the thyroid hormone interactions with alpha v beta 3 integrin. Steroids 2007, 72:165-170.
100. Vellon L., Menendez J.A., Lupu R. AlphaVbeta3 integrin regulates heregulin (HRG)-induced cell proliferation and survival in breast cancer. Oncogene 2005, 24:3759-3773.
101. Yao K., Tan J., Ye P., Wang K., Xu W., ShenTu X., Tang X. Integrin beta1-mediated signaling is involved in transforming growth factor-beta2-promoted migration in human lens epithelial cells. Mol. Vis. 2007, 13:1769-1776.
102. Haenssen K.K., Caldwell S.A., Shahriari K.S., Jackson S.R., Whelan K.A., Klein-Szanto A.J., Reginato M.J. ErbB2 requires integrin alpha5 for anoikis resistance via Src regulation of receptor activity in human mammary epithelial cells. J. Cell Sci. 2010, 123:1373-1382.
103. Agouni A., Sourbier C., Danilin S., Rothhut S., Lindner V., Jacqmin D., Helwig J.J., Lang H., Massfelder T. Parathyroid hormone-related protein induces cell survival in human renal cell carcinoma through the PI3K Akt pathway: evidence for a critical role for integrin-linked kinase and nuclear factor kappa B. Carcinogenesis 2007, 28:1893-1901.
104. Kawano S., Mizutani K., Miyata M., Ikeda W., Takai Y. Interaction of integrin alpha(6)beta(4) with ErbB3 and implication in heregulin-induced ErbB3/ErbB2-mediated DNA synthesis. Genes Cells 2010, 15:995-1001.
105. Scarlett A., Parsons M.P., Hanson P.L., Sidhu K.K., Milligan T.P., Burrin J.M. Thyroid hormone stimulation of extracellular signal-regulated kinase and cell proliferation in human osteoblast-like cells is initiated at integrin alphaVbeta3. J. Endocrinol. 2008, 196:509-517.
106. Huang C., Park C.C., Hilsenbeck S.G., Ward R., Rimawi M.F., Wang Y.C., Shou J., Bissell M.J., Osborne C.K., Schiff R. beta1 integrin mediates an alternative survival pathway in breast cancer cells resistant to lapatinib. Breast Cancer Res. 2011, 13:R84.
107. Berk B.C., Fujiwara K., Lehoux S. ECM remodeling in hypertensive heart disease. J. Clin. Invest. 2007, 117:568-575.
108. Bonapace S., Rossi A., Cicoira M., Golia G., Zanolla L., Franceschini L., Conte L., Marino P., Zardini P., Vassanelli C. Aortic stiffness correlates with an increased extracellular matrix turnover in patients with dilated cardiomyopathy. Am. Heart J. 2006, 152:e91-e96. (93).
109. Brancaccio M., Fratta L., Notte A., Hirsch E., Poulet R., Guazzone S., De Acetis M., Vecchione C., Marino G., Altruda F., Silengo L., Tarone G., Lembo G. Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat. Med. 2003, 9:68-75.
110. Jalali S., del Pozo M.A., Chen K., Miao H., Li Y., Schwartz M.A., Shyy J.Y., Chien S. Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1042-1046.
111. van der Wees C.G., Bax W.H., van der Valk E.J., van der Laarse A. Integrin stimulation induces calcium signalling in rat cardiomyocytes by a NO-dependent mechanism. Pflugers Arch. 2006, 451:588-595.
112. Suryakumar G., Kasiganesan H., Balasubramanian S., Kuppuswamy D. Lack of beta3 integrin signaling contributes to calpain-mediated myocardial cell loss in pressure-overloaded myocardium. J. Cardiovasc. Pharmacol. 2010, 55:567-573.
113. Keller R.S., Shai S.Y., Babbitt C.J., Pham C.G., Solaro R.J., Valencik M.L., Loftus J.C., Ross R.S. Disruption of integrin function in the murine myocardium leads to perinatal lethality, fibrosis, and abnormal cardiac performance. Am. J. Pathol. 2001, 158:1079-1090.
114. Critchley D.R. Cytoskeletal proteins talin and vinculin in integrin-mediated adhesion. Biochem. Soc. Trans. 2004, 32:831-836.
115. Humphries J.D., Wang P., Streuli C., Geiger B., Humphries M.J., Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 2007, 179:1043-1057.
116. Sieg D.J., Hauck C.R., Schlaepfer D.D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 1999, 112(Pt 16):2677-2691.
117. Bertagnolli M.E., Hudson L.A., Stetsenko G.Y. Selective association of the tyrosine kinases Src, Fyn, and Lyn with integrin-rich actin cytoskeletons of activated, nonaggregated platelets. Biochem. Biophys. Res. Commun. 1999, 260:790-798.
118. Chao W.T., Daquinag A.C., Ashcroft F., Kunz J. Type I PIPK-alpha regulates directed cell migration by modulating Rac1 plasma membrane targeting and activation. J. Cell Biol. 2010, 190:247-262.
119. Nojima Y., Morino N., Mimura T., Hamasaki K., Furuya H., Sakai R., Sato T., Tachibana K., Morimoto C., Yazaki Y., et al. Integrin-mediated cell adhesion promotes tyrosine phosphorylation of p130Cas, a Src homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 1995, 270:15398-15402.
120. Ohmori T., Yatomi Y., Inoue K., Satoh K., Ozaki Y. Tyrosine dephosphorylation, but not phosphorylation, of p130Cas is dependent on integrin alpha IIb beta 3-mediated aggregation in platelets: implication of p130Cas involvement in pathways unrelated to cytoskeletal reorganization. Biochemistry 2000, 39:5797-5807.
121. Sansing H.A., Sarkeshik A., Yates J.R., Patel V., Gutkind J.S., Yamada K.M., Berrier A.L. Integrin alphabeta1, alphavbeta, alpha6beta effectors p130Cas, Src and talin regulate carcinoma invasion and chemoresistance. Biochem. Biophys. Res. Commun. 2011, 406:171-176.
122. Vuori K., Ruoslahti E. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 1995, 270:22259-22262.
123. Critchley D.R. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu. Rev. Biophys. 2009, 38:235-254.
124. Gambaletta D., Marchetti A., Benedetti L., Mercurio A.M., Sacchi A., Falcioni R. Cooperative signaling between alpha(6)beta(4) integrin and ErbB-2 receptor is required to promote phosphatidylinositol 3-kinase-dependent invasion. J. Biol. Chem. 2000, 275:10604-10610.
125. Sieg D.J., Hauck C.R., Ilic D., Klingbeil C.K., Schaefer E., Damsky C.H., Schlaepfer D.D. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2000, 2:249-256.
126. Han J., Jenq W., Kefalides N.A. Integrin alpha2beta1 recognizes laminin-2 and induces C-erb B2 tyrosine phosphorylation in metastatic human melanoma cells. Connect. Tissue Res. 1999, 40:283-293.
127. Moro L., Dolce L., Cabodi S., Bergatto E., Boeri Erba E., Smeriglio M., Turco E., Retta S.F., Giuffrida M.G., Venturino M., Godovac-Zimmermann J., Conti A., Schaefer E., Beguinot L., Tacchetti C., Gaggini P., Silengo L., Tarone G., Defilippi P. Integrin-induced epidermal growth factor (EGF) receptor activation requires c-Src and p130Cas and leads to phosphorylation of specific EGF receptor tyrosines. J. Biol. Chem. 2002, 277:9405-9414.
128. Falcioni R., Antonini A., Nistico P., Di Stefano S., Crescenzi M., Natali P.G., Sacchi A. Alpha 6 beta 4 and alpha 6 beta 1 integrins associate with ErbB-2 in human carcinoma cell lines. Exp. Cell Res. 1997, 236:76-85.
129. Tagliabue E., Ardini E., Pellegrini R., Campiglio M., Bufalino R., Jeschke M., Groner B., Colnaghi M.I., Menard S. Laminin activates the p185HER2 oncoprotein and mediates growth inhibition of breast carcinoma cells. Br. J. Cancer 1996, 74:1427-1433.
130. Campiglio M., Tagliabue E., Srinivas U., Pellegrini R., Martignone S., Menard S., Colnaghi M.I., Lombardi L., Marchisio P.C. Colocalization of the p185HER2 oncoprotein and integrin alpha 6 beta 4 in Calu-3 lung carcinoma cells. J. Cell. Biochem. 1994, 55:409-418.
131. Mocanu M.M., Fazekas Z., Petras M., Nagy P., Sebestyen Z., Isola J., Timar J., Park J.W., Vereb G., Szollosi J. Associations of ErbB2, beta1-integrin and lipid rafts on Herceptin (Trastuzumab) resistant and sensitive tumor cell lines. Cancer Lett. 2005, 227:201-212.
132. Lauritzen G., Stock C.M., Lemaire J., Lund S.F., Jensen M.F., Damsgaard B., Petersen K.S., Wiwel M., Ronnov-Jessen L., Schwab A., Pedersen S.F. The Na+/H+ exchanger NHE1, but not the Na+, HCO3(-) cotransporter NBCn1, regulates motility of MCF7 breast cancer cells expressing constitutively active ErbB2. Cancer Lett. 2012, 317:172-183.
133. Yoon S.O., Shin S., Lipscomb E.A. A novel mechanism for integrin-mediated ras activation in breast carcinoma cells: the alpha6beta4 integrin regulates ErbB2 translation and transactivates epidermal growth factor receptor/ErbB2 signaling. Cancer Res. 2006, 66:2732-2739.
134. Fan J., Cai B., Zeng M., Hao Y., Giancotti F.G., Fu B.M. Integrin beta4 signaling promotes mammary tumor cell adhesion to brain microvascular endothelium by inducing ErbB2-mediated secretion of VEGF. Ann. Biomed. Eng. 2011, 39:2223-2241.
135. Guo W., Pylayeva Y., Pepe A., Yoshioka T., Muller W.J., Inghirami G., Giancotti F.G. Beta 4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 2006, 126:489-502.
136. Adelsman M.A., McCarthy J.B., Shimizu Y. Stimulation of beta1-integrin function by epidermal growth factor and heregulin-beta has distinct requirements for erbB2 but a similar dependence on phosphoinositide 3-OH kinase. Mol. Biol. Cell 1999, 10:2861-2878.
137. Spangenberg C., Lausch E.U., Trost T.M., Prawitt D., May A., Keppler R., Fees S.A., Reutzel D., Bell C., Schmitt S., Schiffer I.B., Weber A., Brenner W., Hermes M., Sahin U., Tureci O., Koelbl H., Hengstler J.G., Zabel B.U. ERBB2-mediated transcriptional up-regulation of the alpha5beta1 integrin fibronectin receptor promotes tumor cell survival under adverse conditions. Cancer Res. 2006, 66:3715-3725.
138. Lindberg L.E., Hedjazifar S., Baeckstrom D. c-erbB2-induced disruption of matrix adhesion and morphogenesis reveals a novel role for protein kinase B as a negative regulator of alpha(2)beta(1) integrin function. Mol. Biol. Cell 2002, 13:2894-2908.
139. Hedjazifar S., Jenndahl L.E., Shimokawa H., Baeckstrom D. PKB mediates c-erbB2-induced epithelial beta1 integrin conformational inactivation through Rho-independent F-actin rearrangements. Exp. Cell Res. 2005, 307:259-275.
140. Baeckstrom D., Lu P.J., Taylor-Papadimitriou J. Activation of the alpha2beta1 integrin prevents c-erbB2-induced scattering and apoptosis of human mammary epithelial cells in collagen. Oncogene 2000, 19:4592-4603.