Focal adhesion kinase and endothelial cell apoptosis

Microvascular Research

Volumn 83, Issue 1, 2012, Pages 56-63

  Lu, Qing ^a   Rounds, Sharon ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; FOCAL ADHESION KINASE; HOMOCYSTEINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ANOIKIS; APOPTOSIS; CARCINOGENESIS; CARDIOVASCULAR DISEASE; CELL ADHESION; CELL SURVIVAL; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE OVEREXPRESSION; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPOXIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REOXYGENATION; REVIEW; SIGNAL TRANSDUCTION;

ADENOSINE; ANIMALS; ANOIKIS; APOPTOSIS; CARDIOVASCULAR DISEASES; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; HOMOCYSTEINE; HUMANS; MONOMERIC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 82955233363     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2011.05.003     Document Type: Review

References (106)

1. Abedi H., Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J. Biol. Chem. 1997, 272:15442-15451.
2. Adams J., Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998, 281:1322-1326.
3. Albelda S.M., et al. Identification and characterization of cell-substratum adhesion receptors on cultured human endothelial cells. J. Clin. Invest. 1989, 83:1992-2002.
4. Al-Massarani G., et al. Impact of immunosuppressive treatment on endothelial biomarkers after kidney transplantation. Am. J. Transplant. 2008, 8:2360-2367.
5. Alvarez D.F., et al. Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: a novel mechanism of acute lung injury. Circ. Res. 2006, 99:988-995.
6. Aoudjit F., Vuori K. Matrix attachment regulates Fas-induced apoptosis in endothelial cells: a role for c-FLIP and implications for anoikis. J. Cell Biol. 2001, 152:633-643.
7. Bellas R.E., et al. FAK blunts adenosine-homocysteine-induced endothelial cell apoptosis: requirement for PI 3-kinase. Am. J Physiol. Lung Cell. Mol. Physiol. 2002, 282:L1135-L1142.
8. Boos C.J., et al. Relationship between circulating endothelial cells and the predicted risk of cardiovascular events in acute coronary syndromes. Eur. Heart J. 2007, 28:1092-1101.
9. Braren R., et al. Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol. 2006, 172:151-162.
10. Bull T.M., et al. Circulating endothelial cells in pulmonary hypertension. Thromb. Haemost. 2003, 90:698-703.
11. Cheng Y.F., Kramer R.H. Human microvascular endothelial cells express integrin-related complexes that mediate adhesion to the extracellular matrix. J. Cell. Physiol. 1989, 139:275-286.
12. Chong A.Y., et al. Endothelial dysfunction and damage in congestive heart failure: relation of flow-mediated dilation to circulating endothelial cells, plasma indexes of endothelial damage, and brain natriuretic peptide. Circulation 2004, 110:1794-1798.
13. Cohen L.A., Guan J.L. Mechanisms of focal adhesion kinase regulation. Curr. Cancer Drug Targets 2005, 5:629-643.
14. Crouch D.H., et al. Targeted proteolysis of the focal adhesion kinase pp 125 FAK during c-MYC-induced apoptosis is suppressed by integrin signalling. Oncogene 1996, 12:2689-2696.
15. Dawicki D.D., et al. Extracellular ATP and adenosine cause apoptosis of pulmonary artery endothelial cells. Am. J. Physiol. 1997, 273:L485-L494.
16. Dejana E., et al. Fibronectin and vitronectin regulate the organization of their respective Arg-Gly-Asp adhesion receptors in cultured human endothelial cells. J. Cell Biol. 1988, 107:1215-1223.
17. Del Papa N., et al. Circulating endothelial cells as a marker of ongoing vascular disease in systemic sclerosis. Arthritis Rheum. 2004, 50:1296-1304.
18. Del Re D.P., et al. RhoA/Rho kinase up-regulate Bax to activate a mitochondrial death pathway and induce cardiomyocyte apoptosis. J. Biol. Chem. 2007, 282:8069-8078.
19. Del Re D.P., et al. Focal adhesion kinase as a RhoA-activable signaling scaffold mediating Akt activation and cardiomyocyte protection. J. Biol. Chem. 2008, 283:35622-35629.
20. DiMichele L.A., et al. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ. Res. 2006, 99:636-645.
21. Dreyfuss D., et al. Spontaneous resolution of pulmonary edema caused by short periods of cyclic overinflation. J. Appl. Physiol. 1992, 72:2081-2089.
22. Du C., et al. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102:33-42.
23. El Solh A.A., et al. Hemostatic implications of endothelial cell apoptosis in obstructive sleep apnea. Sleep Breath. 2008, 12:331-337.
24. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 1994, 124:619-626.
25. Frisch S.M., et al. Control of adhesion-dependent cell survival by focal adhesion kinase. J. Cell Biol. 1996, 134:793-799.
26. Geiger B., et al. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2001, 2:793-805.
27. Gerber H.P., et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J. Biol. Chem. 1998, 273:30336-30343.
28. Gervais F.G., et al. Caspases cleave focal adhesion kinase during apoptosis to generate a FRNK-like polypeptide. J. Biol. Chem. 1998, 273:17102-17108.
29. Golubovskaya V.M., et al. Direct interaction of the N-terminal domain of focal adhesion kinase with the N-terminal transactivation domain of p53. J. Biol. Chem. 2005, 280:25008-25021.
30. Golubovskaya V.M., et al. Focal adhesion kinase and cancer. Histol. Histopathol. 2009, 24:503-510.
31. Groenendyk J., Michalak M. Endoplasmic reticulum quality control and apoptosis. Acta. Biochim. Pol. 2005, 52:381-395.
32. Guan J.L., Shalloway D. Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 1992, 358:690-692.
33. Guan J.L., et al. Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul. 1991, 2:951-964.
34. Hakim Z.S., et al. FAK regulates cardiomyocyte survival following ischemia/reperfusion. J. Mol. Cell. Cardiol. 2009, 46:241-248.
35. Halder J., et al. Therapeutic efficacy of a novel focal adhesion kinase inhibitor TAE226 in ovarian carcinoma. Cancer Res. 2007, 67:10976-10983.
36. Harrington E.O., et al. Adenosine induces endothelial apoptosis by activating protein tyrosine phosphatase: a possible role of p38alpha. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279:L733-L742.
37. Harrington E.O., et al. Protein tyrosine phosphatase-dependent proteolysis of focal adhesion complexes in endothelial cell apoptosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 2001, 280:L342-L353.
38. Harrington E.O., et al. Endothelial cell apoptosis. Endothelial Biomedicine 2007, 1081-1097. Cambridge University Press, New York, NY. W.C. Aird (Ed.).
39. Hauser R., Probst R. The influence of systematic primary-tone level variation L2-L1 on the acoustic distortion product emission 2f1-f2 in normal human ears. J. Acoust. Soc. Am. 1991, 89:280-286.
40. Hippenstiel S., et al. Rho protein inactivation induced apoptosis of cultured human endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L830-L838.
41. Huang D., et al. Focal adhesion kinase mediates cell survival via NF-kappaB and ERK signaling pathways. Am. J. Physiol. Cell Physiol. 2007, 292:C1339-C1352.
42. Hung R., Chow A. Dissecting the "end game": clinical relevance, molecular mechanisms and laboratory assessment of apoptosis. Clin. Invest. Med. 2004, 27:324-344.
43. Hungerford J.E., et al. Inhibition of pp 125FAK in cultured fibroblasts results in apoptosis. J. Cell Biol. 1996, 135:1383-1390.
44. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
45. Ilic D., et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995, 377:539-544.
46. Ilic D., et al. Extracellular matrix survival signals transduced by focal adhesion kinase suppress p53-mediated apoptosis. J. Cell Biol. 1998, 143:547-560.
47. Ilic D., et al. Focal adhesion kinase is required for blood vessel morphogenesis. Circ. Res. 2003, 92:300-307.
48. 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.
49. Kennedy S.G., et al. The PI 3-kinase/Akt signaling pathway delivers an anti-apoptotic signal. Genes Dev. 1997, 11:701-713.
50. Kerr J., et al. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 1972, 26:239-257.
51. Khwaja A., et al. Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 1997, 16:2783-2793.
52. Klionsky D.J., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
53. Kramer K., et al. Isoprenylcysteine carboxyl methyltransferase activity modulates endothelial cell apoptosis. Mol. Biol. Cell 2003, 14:848-857.
54. Kurenova E., et al. Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein. Mol. Cell. Biol. 2004, 24:4361-4371.
55. Lampka M., et al. Circulating endothelial cells in coronary artery disease. Kardiol. Pol. 2010, 68:1100-1105.
56. Li H., et al. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas-pathway of apoptosis. Cell 1998, 94:491-501.
57. Li L., et al. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001, 412:95-99.
58. Li X., et al. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J. Biol. Chem. 2002, 277:15309-15316.
59. Lietha D., et al. Structural basis for the autoinhibition of focal adhesion kinase. Cell 2007, 129:1177-1187.
60. Lim S.T., et al. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell. 2008, 29:9-22.
61. Lim S.T., et al. FERM control of FAK function: implications for cancer therapy. Cell Cycle 2008, 7:2306-2314.
62. Lim Y., et al. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J. Cell Biol. 2008, 180:187-203.
63. Lim S.T., et al. Pyk2 inhibition of p53 as an adaptive and intrinsic mechanism facilitating cell proliferation and survival. J. Biol. Chem. 2010, 285:1743-1753.
64. Lin J.H., et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007, 318:944-949.
65. Liu G., et al. Structural insight into the mechanisms of targeting and signaling of focal adhesion kinase. Mol. Cell. Biol. 2002, 22:2751-2760.
66. Lu Q., Rounds S. Pulmonary endothelial cell death: implications for lung disease pathogenesis. The Pulmonary Endothelium: Function in Health and Disease 2009, 243-260. John Wiley & Sons, Ltd, Chichester, UK. N.F. Voelkel, S. Rounds (Eds.).
67. Lu Q., et al. Isoprenylcysteine carboxyl methyltransferase modulates endothelial monolayer permeability: involvement of RhoA carboxyl methylation. Circ. Res. 2004, 94:306-315.
68. McLean G.W., et al. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat. Rev. Cancer 2005, 5:505-515.
69. Mechtersheimer G., et al. In situ expression of beta 1, beta 3 and beta 4 integrin subunits in non-neoplastic endothelium and vascular tumours. Virchows Arch. 1994, 425:375-384.
70. Meredith J.E., et al. The extracellular matrix as a cell survival factor. Mol. Biol. Cell 1993, 4:953-961.
71. Mitra S.K., Schlaepfer D.D. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 2006, 18:516-523.
72. Murata T., et al. Localization of FAK is related with colorectal carcinogenesis. Int. J. Oncol. 2008, 32:791-796.
73. O'Brien R.F., et al. Studies on the mechanism of decreased angiotensin I conversion in rat lungs injured with alpha-naphthylthiourea. Exp. Lung. Res. 1985, 8:243-259.
74. Ossovskaya V., et al. FAK nuclear export signal sequences. FEBS Lett. 2008, 582:2402-2406.
75. Parsons J.T. Focal adhesion kinase: the first ten years. J. Cell Sci. 2003, 116:1409-1416.
76. Peng X., et al. Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J. Clin. Invest. 2006, 116:217-227.
77. Peng X., et al. 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.
78. Pierschbacher M.D., Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 1984, 309:30-33.
79. Playford M.P., Schaller M.D. The interplay between Src and integrins in normal and tumor biology. Oncogene 2004, 23:7928-7946.
80. Polte T.R., Hanks S.K. Complexes of focal adhesion kinase (FAK) and Crk-associated substrate (p130(Cas)) are elevated in cytoskeleton-associated fractions following adhesion and Src transformation. Requirements for Src kinase activity and FAK proline-rich motifs. J. Biol. Chem. 1997, 272:5501-5509.
81. Qi J.H., Claesson-Welsh L. VEGF-induced activation of phosphoinositide 3-kinase is dependent on focal adhesion kinase. Exp. Cell Res. 2001, 263:173-182.
82. Quilici J., et al. Circulating endothelial cell count as a diagnostic marker for non-ST-elevation acute coronary syndromes. Circulation 2004, 110:1586-1591.
83. Renshaw M.W., et al. Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J. Cell Biol. 1999, 147:611-618.
84. Roberts W.G., et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 2008, 68:1935-1944.
85. Rounds S., et al. Mechanism of extracellular ATP- and adenosine-induced apoptosis of cultured pulmonary artery endothelial cells. Am. J. Physiol. 1998, 275:L379-L388.
86. Ruoslahti E., Reed J.C. Anchorage dependence, integrins, and apoptosis. Cell 1994, 77:477-478.
87. Rutkowski D.T., et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 2006, 4:e374.
88. Schaller M.D. Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J. Cell Sci. 2010, 123:1007-1013.
89. Schaller M.D., et al. Autophosphorylation of the focal adhesion kinase, pp 125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 1994, 14:1680-1688.
90. Schwartz M.A., Shattil S.J. Signaling networks linking integrins and rho family GTPases. Trends Biochem. Sci. 2000, 25:388-391.
91. Shen T.L., et al. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 2005, 169:941-952.
92. Slee E., et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspase-2, -3, -6, -7, and -10 in a caspase-9-dependent manner. J. Cell Biol. 1999, 144:281-292.
93. Sluimer J.C., et al. Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J. Am. Coll. Cardiol. 2009, 53:1517-1527.
94. Sood A.K., et al. Adrenergic modulation of focal adhesion kinase protects human ovarian cancer cells from anoikis. J. Clin. Invest. 2010, 120:1515-1523.
95. Sowemimo-Coker S.O., et al. Increased circulating endothelial cells in sickle cell crisis. Am. J. Hematol. 1989, 31:263-265.
96. Susin S., et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
97. Suzuki T., et al. Eicosapentaenoic acid protects endothelial cells against anoikis through restoration of cFLIP. Hypertension 2003, 42:342-348.
98. Szegezdi E., et al. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann. N. Y. Acad. Sci. 2003, 1010:186-194.
99. Tamatani M., et al. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J. Biol. Chem. 1999, 274:8531-8538.
100. Tamura M., et al. PTEN interactions with focal adhesion kinase and suppression of the extracellular matrix-dependent phosphatidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 1999, 274:20693-20703.
101. Thome M., et al. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 1997, 386:517-521.
102. Wang C., et al. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 1998, 281:1680-1683.
103. Yang Q., et al. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis protein (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev. 2003, 17:1487-1496.
104. Zamir E., Geiger B. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell Sci. 2001, 114:3583-3590.
105. Zou H., et al. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 1999, 274:11549-11556.
106. Zouq N.K., et al. FAK engages multiple pathways to maintain survival of fibroblasts and epithelia: differential roles for paxillin and p130Cas. J. Cell Sci. 2009, 122:357-367.