Targeting focal adhesion kinase in fibrotic diseases

BioDrugs

Volumn 27, Issue 1, 2013, Pages 15-23

  Lagares, David ^a   Kapoor, Mohit ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ALPHA SMOOTH MUSCLE ACTIN; CORTICOSTEROID; ENDOTHELIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; ERYTHROCYTE BAND 4.1 PROTEIN; EZRIN; FIBROBLAST GROWTH FACTOR; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; HEPARIN; IMMUNOSUPPRESSIVE AGENT; INTEGRIN; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; MOESIN; PAXILLIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PF 562271; PF 573228; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROSTAGLANDIN E2; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; RADIXIN; SHORT HAIRPIN RNA; STRESS ACTIVATED PROTEIN KINASE; TALIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ALZHEIMER DISEASE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ATHEROSCLEROSIS; CATALYSIS; CELL ADHESION; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CORTICOSTEROID THERAPY; CYTOPLASM; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FIBROGENESIS; FIBROSING ALVEOLITIS; GENE EXPRESSION; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPERTENSION; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; IN VIVO STUDY; LUNG FIBROBLAST; LUNG FIBROSIS; MYOFIBROBLAST; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; STELLATE CELL; SYSTEMIC SCLEROSIS;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; MYOFIBROBLASTS; PROTEIN KINASE INHIBITORS; PULMONARY FIBROSIS; SCLERODERMA, SYSTEMIC;

EID: 84873363835     PISSN: 11738804     EISSN: 1179190X     Source Type: Journal    
DOI: 10.1007/s40259-012-0003-4     Document Type: Review

References (79)

1. Katzenstein AL, Myers JL. Idiopathic pulmonary fibrosis: clinical relevance of pathologic classification. Am J Respir Crit Care Med. 1998;157(4 Pt 1):1301-15.
2. Varga J, Abraham D. Systemic sclerosis: a prototypic multisystem fibrotic disorder. J Clin Invest. 2007;117(3):557-67.
3. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest. 2007;117(3):524-9.
4. Gabbiani G. The myofibroblast: a key cell for wound healing and fibrocontractive diseases. Prog Clin Biol Res. 1981;54:183-94.
5. Chen SJ, et al. Stimulation of type I collagen transcription in human skin fibroblasts by TGF-beta: involvement of Smad 3. J Invest Dermatol. 1999;112(1):49-57.
6. Pannu J, et al. Increased levels of transforming growth factor beta receptor type I and up-regulation of matrix gene program: a model of scleroderma. Arthritis Rheum. 2006;54(9):3011-21.
7. Ishida W, et al. Intracellular TGF-beta receptor blockade abrogates Smad-dependent fibroblast activation in vitro and in vivo. J Invest Dermatol. 2006;126(8):1733-44.
8. Sime PJ, et al. Adenovector-mediated gene transfer of active transforming growth factor-beta1 induces prolonged severe fibrosis in rat lung. J Clin Invest. 1997;100(4):768-76.
9. Lagares D, et al. Endothelin 1 contributes to the effect of transforming growth factor beta1 on wound repair and skin fibrosis. Arthritis Rheum. 2010;62(3):878-89.
10. Serini G, et al. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J Cell Biol. 1998;142(3):873-81.
11. Shi-Wen X, et al. Endogenous endothelin-1 signaling contributes to type I collagen and CCN2 overexpression in fibrotic fibroblasts. Matrix Biol. 2007;26(8):625-32.
12. Shi-Wen X, et al. Constitutive ALK5-independent c-Jun N-terminal kinase activation contributes to endothelin-1 overexpression in pulmonary fibrosis: evidence of an autocrine endothelin loop operating through the endothelin A and B receptors. Mol Cell Biol. 2006;26(14):5518-27.
13. Liu F, et al. Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol. 2010;190(4):693-706.
14. Mimura Y, et al. Constitutive phosphorylation of focal adhesion kinase is involved in the myofibroblast differentiation of scleroderma fibroblasts. J Invest Dermatol. 2005;124(5):886-92.
15. Kanner SB, et al. Monoclonal antibodies to individual tyrosine-phosphorylated protein substrates of oncogene-encoded tyrosine kinases. Proc Natl Acad Sci USA. 1990;87(9):3328-32.
16. Hanks SK, et al. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc Natl Acad Sci USA. 1992;89(18):8487-91.
17. Kornberg L, et al. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J Biol Chem. 1992;267(33):23439-42.
18. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005;6(1):56-68.
19. Parsons JT. Focal adhesion kinase: the first ten years. J Cell Sci. 2003;116(Pt 8):1409-16.
20. Girault JA, et al. The N-termini of FAK and JAKs contain divergent band 4.1 domains. Trends Biochem Sci. 1999;24(2):54-7.
21. Sieg DJ, et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol. 2000;2(5):249-56.
22. Streblow DN, et al. Human cytomegalovirus chemokine receptor US28-induced smooth muscle cell migration is mediated by focal adhesion kinase and Src. J Biol Chem. 2003;278(50):50456-65.
23. Schaller MD, et al. Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J Cell Biol. 1995;130(5):1181-7.
24. Hildebrand JD, Schaller MD, Parsons JT. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp 125FAK, to cellular focal adhesions. J Cell Biol. 1993;123(4):993-1005.
25. Schaller MD, Borgman CA, Parsons JT. Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp 125FAK. Mol Cell Biol. 1993;13(2):785-91.
26. Toutant M, et al. Alternative splicing controls the mechanisms of FAK autophosphorylation. Mol Cell Biol. 2002;22(22):7731-43.
27. Calalb MB, Polte TR, Hanks SK. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol. 1995;15(2):954-63.
28. Schaller MD, et al. Autophosphorylation of the focal adhesion kinase, pp 125FAK, directs SH2-dependent binding of pp60src. Mol Cell Biol. 1994;14(3):1680-8.
29. Owen JD, et al. Induced focal adhesion kinase (FAK) expression in FAK-null cells enhances cell spreading and migration requiring both auto- and activation loop phosphorylation sites and inhibits adhesion-dependent tyrosine phosphorylation of Pyk2. Mol Cell Biol. 1999;19(7):4806-18.
30. Owens LV, et al. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res. 1995;55(13):2752-5.
31. Zhang C, et al. Focal adhesion kinase expressed by nerve cell lines shows increased tyrosine phosphorylation in response to Alzheimer's A beta peptide. J Biol Chem. 1994;269(41):25247-50.
32. Shahrara S, et al. Differential expression of the FAK family kinases in rheumatoid arthritis and osteoarthritis synovial tissues. Arthritis Res Ther. 2007;9(5):R112.
33. Franchini KG, Clemente CF, Marin TM. Focal adhesion kinase signaling in cardiac hypertrophy and failure. Braz J Med Biol Res. 2009;42(1):44-52.
34. Rice DC, et al. Src autophosphorylation is an early event in pressure-mediated signaling pathways in isolated resistance arteries. Hypertension. 2002; 39(2 Pt 2): 502-7.
35. Morla AO, Mogford JE. Control of smooth muscle cell proliferation and phenotype by integrin signaling through focal adhesion kinase. Biochem Biophys Res Commun. 2000;272(1):298-302.
36. Thannickal VJ, et al. Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem. 2003;278(14):12384-9.
37. Vittal R, et al. Modulation of prosurvival signaling in fibroblasts by a protein kinase inhibitor protects against fibrotic tissue injury. Am J Pathol. 2005;166(2):367-75.
38. Shi-wen X, et al. Requirement of transforming growth factor beta-activated kinase 1 for transforming growth factor beta-induced alpha-smooth muscle actin expression and extracellular matrix contraction in fibroblasts. Arthritis Rheum. 2009;60(1):234-41.
39. Liu S, et al. FAK is required for TGFbeta-induced JNK phosphorylation in fibroblasts: implications for acquisition of a matrix-remodeling phenotype. Mol Biol Cell. 2007;18(6):2169-78.
40. Hayashida T, et al. MAP-kinase activity necessary for TGFbeta1-stimulated mesangial cell type I collagen expression requires adhesion-dependent phosphorylation of FAK tyrosine 397. J Cell Sci. 2007;120(Pt 23):4230-40.
41. Dun ZN, et al. Specific shRNA targeting of FAK influenced collagen metabolism in rat hepatic stellate cells. World J Gastroenterol. 2010;16(32):4100-6.
42. Deng B, et al. Focal adhesion kinase mediates TGF-beta1-induced renal tubular epithelial-to-mesenchymal transition in vitro. Mol Cell Biochem. 2010;340(1-2):21-9.
43. Greenberg RS, et al. FAK-dependent regulation of myofibroblast differentiation. FASEB J. 2006;20(7):1006-8.
44. Swigris JJ, Brown KK. The role of endothelin-1 in the pathogenesis of idiopathic pulmonary fibrosis. BioDrugs. 2010;24(1):49-54.
45. Lagares D, et al. Inhibition of focal adhesion kinase prevents experimental lung fibrosis and myofibroblast formation. Arthritis Rheum. 2012;64(5):1653-64.
46. Ding Q, et al. Focal adhesion kinase (FAK)-related non-kinase inhibits myofibroblast differentiation through differential MAPK activation in a FAK-dependent manner. J Biol Chem. 2008;283(40):26839-49.
47. Thomas PE, et al. PGE(2) inhibition of TGF-beta1-induced myofibroblast differentiation is Smad-independent but involves cell shape and adhesion-dependent signaling. Am J Physiol Lung Cell Mol Physiol. 2007;293(2):L417-28.
48. Liu S, et al. Loss of beta1 integrin in mouse fibroblasts results in resistance to skin scleroderma in a mouse model. Arthritis Rheum. 2009;60(9):2817-21.
49. Kulkarni AA, et al. PPAR-gamma ligands repress TGFbeta-induced myofibroblast differentiation by targeting the PI3 K/Akt pathway: implications for therapy of fibrosis. PLoS One. 2011;6(1):e15909.
50. Jelaska A, Korn JH. Role of apoptosis and transforming growth factor beta1 in fibroblast selection and activation in systemic sclerosis. Arthritis Rheum. 2000;43(10):2230-9.
51. Xia H, et al. Focal adhesion kinase is upstream of phosphatidylinositol 3-kinase/Akt in regulating fibroblast survival in response to contraction of type I collagen matrices via a beta 1 integrin viability signaling pathway. J Biol Chem. 2004;279(31):33024-34.
52. Wen LP, et al. Cleavage of focal adhesion kinase by caspases during apoptosis. J Biol Chem. 1997;272(41):26056-61.
53. Horowitz JC, et al. Combinatorial activation of FAK and AKT by transforming growth factor-beta1 confers an anoikis-resistant phenotype to myofibroblasts. Cell Signal. 2007;19(4):761-71.
54. Reif S, et al. The role of focal adhesion kinase-phosphatidylinositol 3-kinase-akt signaling in hepatic stellate cell proliferation and type I collagen expression. J Biol Chem. 2003;278(10):8083-90.
55. Xia H, et al. Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis. J Exp Med. 2008;205(7):1659-72.
56. Horowitz JC, et al. Survivin expression induced by endothelin-1 promotes myofibroblast resistance to apoptosis. Int J Biochem Cell Biol. 2012;44(1):158-69.
57. Pardo A, Selman M. Molecular mechanisms of pulmonary fibrosis. Front Biosci. 2002;7:d1743-61.
58. Ilic D, et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 1995;377(6549):539-44.
59. Kumagai N, et al. Lysophosphatidic acid induces tyrosine phosphorylation and activation of MAP-kinase and focal adhesion kinase in cultured Swiss 3T3 cells. FEBS Lett. 1993;329(3):273-6.
60. Chen HC, Guan JL. Stimulation of phosphatidylinositol 3'-kinase association with foca adhesion kinase by platelet-derived growth factor. J Biol Chem. 1994;269(49):31229-33.
61. Tangkijvanich P, et al. Platelet-derived growth factor-BB and lysophosphatidic acid distinctly regulate hepatic myofibroblast migration through focal adhesion kinase. Exp Cell Res. 2002;281(1):140-7.
62. Cai GQ, et al. Downregulation of FAK-related non-kinase mediates the migratory phenotype of human fibrotic lung fibroblasts. Exp Cell Res. 2010;316(9):1600-9.
63. Wong VW, et al. Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling. Nat Med. 2012;18(1):148-52.
64. Essayem S, et al. Hair cycle and wound healing in mice with a keratinocyte-restricted deletion of FAK. Oncogene. 2006;25(7):1081-9.
65. Schultze A, Fiedler W. Therapeutic potential and limitations of new FAK inhibitors in the treatment of cancer. Expert Opin Investig Drugs. 2010;19(6):777-88.
66. Schultze A, Fiedler W. Clinical importance and potential use of small molecule inhibitors of focal adhesion kinase. Anticancer Agents Med Chem. 2011;11(7):593-9.
67. Roberts WG, et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 2008;68(6):1935-44.
68. Wendt MK, Schiemann WP. Therapeutic targeting of the focal adhesion complex prevents oncogenic TGF-beta signaling and metastasis. Breast Cancer Res. 2009;11(5):R68.
69. Garamszegi N, et al. Extracellular matrix-induced transforming growth factor-beta receptor signaling dynamics. Oncogene. 2010;29(16):2368-80.
70. Kim KK, et al. Epithelial cell alpha3beta1 integrin links beta-catenin and Smad signaling to promote myofibroblast formation and pulmonary fibrosis. J Clin Invest. 2009;119(1):213-24.
71. Liu S, et al. Expression of integrin beta1 by fibroblasts is required for tissue repair in vivo. J Cell Sci. 2010;123(Pt 21):3674-82.
72. Planas-Silva MD, et al. Role of c-Src and focal adhesion kinase in progression and metastasis of estrogen receptor-positive breast cancer. Biochem Biophys Res Commun. 2006;341(1):73-81.
73. Bolos V, et al. The dual kinase complex FAK-Src as a promising therapeutic target in cancer. Onco Targets Ther. 2010;3:83-97.
74. Hong S, et al. The role of focal adhesion kinase in the TGF-beta-induced myofibroblast transdifferentiation of human Tenon's fibroblasts. Korean J Ophthalmol. 2012;26(1):45-8.
75. Dalla Costa AP, et al. FAK mediates the activation of cardiac fibroblasts induced by mechanical stress through regulation of the mTOR complex. Cardiovasc Res. 2010; 86(3): 421-31.
76. Chan MW, et al. FAK, PIP5KIgamma and gelsolin cooperatively mediate force-induced expression of alpha-smooth muscle actin. J Cell Sci. 2009;122(Pt 15):2769-81.
77. DiMichele LA, et al. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ Res. 2006;99(6):636-45.
78. Peng X, et al. Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J Clin Invest. 2006;116(1):217-27.
79. Clemente CF, et al. Targeting focal adhesion kinase with small interfering RNA prevents and reverses load-induced cardiac hypertrophy in mice. Circ Res. 2007;101(12):1339-48.