Focal adhesion kinase modulates activation of NF-κB by flow in endothelial cells

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 4, 2009, Pages

  Petzold, Tobias ^a,b   Orr, A Wayne ^a,b   Hahn, Cornelia ^a,b   Jhaveri, Krishna A ^a,b   Parsons, J Thomas ^b   Schwartz, Martin Alexander ^a,b,c  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c University of Virginia   (United States)

Author keywords

Atherosclerosis; Fluid shear stress; Integrin signaling; Mechanotransduction

Indexed keywords

FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; HYDROGEN PEROXIDE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; SERINE; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR RELA; TUBULIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; ATHEROGENESIS; CELL NUCLEUS; CONTROLLED STUDY; ENDOTHELIUM CELL; FLOW; GENE INDUCTION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SHEAR STRESS;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HYDROGEN PEROXIDE; I-KAPPA B KINASE; INTEGRINS; INTERCELLULAR ADHESION MOLECULE-1; MICE; NF-KAPPA B; PHOSPHORYLATION; PROTEIN TRANSPORT; RAC GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 70349909871     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00226.2009     Document Type: Article

References (58)

1. Adli M, Baldwin AS. IKK-i/IKKepsilon controls constitutive, cancer cell-associated NF-kappaB activity via regulation of Ser-536 p65/RelA phosphorylation. J Biol Chem 281: 26976-26984, 2006. (Pubitemid 44401726)
2. Beggs HE, Schahin-Reed D, Zang K, Goebbels S, Nave KA, Gorski J, Jones KR, Sretavan D, Reichardt LF. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40: 501-514, 2003. (Pubitemid 37494700)
3. Bhullar IS, Li YS, Miao H, Zandi E, Kim M, Shyy JY, Chien S. Fluid shear stress activation of IkappaB kinase is integrin-dependent. J Biol Chem 273: 30544-30549, 1998. (Pubitemid 28545531)
4. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98: 147-157, 1999. (Pubitemid 29344903)
5. Chan BMC, Hemler ME. Multiple functional forms of the integrin VLA-2 can be derived from a single α2 cDNA clone: interconversion of forms induced by an anti-β1 antibody. J Cell Biol 120: 537-543, 1993. (Pubitemid 23040091)
6. Chen LF, Greene WC. Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 5: 392-401, 2004.
7. Chien S. Effects of disturbed flow on endothelial cells. Ann Biomed Eng 36: 554-562, 2008.
8. Collins T, Cybulsky MI. NF-kappaB: pivotal mediator or innocent bystander in atherogenesis? J Clin Invest 107: 255-264, 2001. (Pubitemid 32157955)
9. Cunningham KS, Gotlieb AI. The role of shear stress in the pathogenesis of atherosclerosis. Lab Invest 85: 9-23, 2005. (Pubitemid 40128037)
10. Del Pozo MA, Price LS, Alderson NB, Ren XD, Schwartz MA. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J 19: 2008-2014, 2000.
11. Denk A, Goebeler M, Schmid S, Berberich I, Ritz O, Lindemann D, Ludwig S, Wirth T. Activation of NF-kappa B via the Ikappa B kinase complex is both essential and sufficient for proinflammatory gene expression in primary endothelial cells. J Biol Chem 276: 28451-28458, 2001. (Pubitemid 37391556)
12. Dusserre N, L'Heureux N, Bell KS, Stevens HY, Yeh J, Otte LA, Loufrani L, Frangos JA. PECAM-1 interacts with nitric oxide synthase in human endothelial cells: implication for flow-induced nitric oxide synthase activation. Arterioscler Thromb Vasc Biol 24: 1796 - 1802, 2004.
13. 1: regulation of the functional response by soluble fibronectin. J Cell Biol 121: 155-162, 1993.
14. Feaver RE, Hastings NE, Pryor A, Blackman BR. GRP78 upregulation by atheroprone shear stress via p38-, alpha2beta1-dependent mechanism in endothelial cells. Arterioscler Thromb Vasc Biol 28: 1534-1541, 2008.
15. Frangos JA, Eskin SG, McIntire LV, Ives CL. Flow effects on prostacyclin production by cultured human endothelial cells. Science 227: 1477-1479, 1985. (Pubitemid 15146990)
16. Funakoshi-Tago M, Sonoda Y, Tanaka S, Hashimoto K, Tago K, Tominaga S, Kasahara T. Tumor necrosis factor-induced nuclear factor kappaB activation is impaired in focal adhesion kinase-deficient fibroblasts. J Biol Chem 278: 29359-29365, 2003. (Pubitemid 36935853)
17. Gilbert SF, Migeon BR. D-valine as a selective agent for normal human and rodent epithelial cells in culture. Cell 5: 11-17, 1975.
18. Gimbrone MA Jr, Topper JN, Nagel T, Anderson KR, Garcia-Cardena G. Endothelial dysfunction, hemodynamic forces, and atherogenesis. Ann NY Acad Sci 902: 230-239; discussion 239-240, 2000. (Pubitemid 30389128)
19. Hahn C, Schwartz MA. The role of cellular adaptation to mechanical forces in atherosclerosis. Arterioscler Thromb Vasc Biol 28: 2101-2107, 2008.
20. Hajra L, Evans AI, Chen M, Hyduk SJ, Collins T, Cybulsky MI. The NF-kappa B signal transduction pathway in aortic endothelial cells is primed for activation in regions predisposed to atherosclerotic lesion formation. Proc Natl Acad Sci USA 97: 9052-9057, 2000. (Pubitemid 30626672)
21. Hu J, Nakano H, Sakurai H, Colburn NH. Insufficient p65 phosphorylation at S536 specifically contributes to the lack of NF-kappaB activation and transformation in resistant JB6 cells. Carcinogenesis 25: 1991-2003, 2004.
22. Imberti B, Morigi M, Zoja C, Angioletti S, Abbate M, Remuzzi A, Remuzzi G. Shear stress-induced cytoskeleton rearrangement mediates NF-kappaB-dependent endothelial expression of ICAM-1. Microvasc Res 60: 182-188, 2000. (Pubitemid 30667060)
23. Jiang X, Takahashi N, Matsui N, Tetsuka T, Okamoto T. The NFkappa B activation in lymphotoxin beta receptor signaling depends on the phosphorylation of p65 at serine 536. J Biol Chem 278: 919-926, 2003. (Pubitemid 36790766)
24. Koshida R, Rocic P, Saito S, Kiyooka T, Zhang C, Chilian WM. Role of focal adhesion kinase in flow-induced dilation of coronary arterioles. Arterioscler Thromb Vasc Biol 25: 2548-2553, 2005. (Pubitemid 43732277)
25. 2-mediated activation of NFkappaB-inducing kinase. J Biol Chem 281: 1495-1505, 2006.
26. Li S, Kim M, Hu YL, Jalali S, Schlaepfer DD, Hunter T, Chien S, Shyy JY. Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J Biol Chem 272: 30455-30462, 1997. (Pubitemid 27512256)
27. Li S, Butler P, Wang Y, Hu Y, Han DC, Usami S, Guan JL, Chien S. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proc Natl Acad Sci USA 99: 3546-3551, 2002. (Pubitemid 34252144)
28. Libby P. Inflammation in atherosclerosis. Nature 420: 868-874, 2002.
29. Lin T, Zeng L, Liu Y, DeFea K, Schwartz MA, Chien S, Shyy JY. Rho-ROCK-LIMK-cofilin pathway regulates shear stress activation of sterol regulatory element binding proteins. Circ Res 92: 1296-1304, 2003. (Pubitemid 36773471)
30. Liu Y, Chen BP, Lu M, Zhu Y, Stemerman MB, Chien S, Shyy JY. Shear stress activation of SREBP1 in endothelial cells is mediated by integrins. Arterioscler Thromb Vasc Biol 22: 76-81, 2002. (Pubitemid 34076235)
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275, 1951.
32. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 282: 2035-2042, 1999.
33. Mohan S, Mohan N, Sprague EA. Differential activation of NF-κB in human aortic endothelial cells conditioned to specific flow environments. Am J Physiol Cell Physiol 273: C572-C578, 1997. (Pubitemid 27396150)
34. Nagai T, Yamakawa N, Aota S, Yamada SS, Akiyama SK, Olden K, Yamada KM. Monoclonal antibody characterization of two distant sites required for function of the central cell-binding domain of fibronectin in cell adhesion, cell migration, and matrix assembly. J Cell Biol 114: 1295-1305, 1991. (Pubitemid 21909887)
35. Nakashima Y, Raines EW, Plump AS, Breslow JL, Ross R. Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Arterioscler Thromb Vasc Biol 18: 842-851, 1998. (Pubitemid 28267666)
36. Okazaki T, Sakon S, Sasazuki T, Sakurai H, Doi T, Yagita H, Okumura K, Nakano H. Phosphorylation of serine 276 is essential for p65 NF-kappaB subunit-dependent cellular responses. Biochem Biophys Res Commun 300: 807-812, 2003. (Pubitemid 36259833)
37. Orr AW, Sanders JM, Bevard M, Coleman E, Sarembock IJ, Schwartz MA. The subendothelial extracellular matrix modulates NF-kappaB activation by flow: a potential role in atherosclerosis. J Cell Biol 169: 191-202, 2005. (Pubitemid 40562925)
38. Orr AW, Ginsberg MH, Shattil SJ, Deckmyn H, Schwartz MA. Matrix-specific suppression of integrin activation in shear stress signaling. Mol Biol Cell 17: 4686-4697, 2006. (Pubitemid 44665739)
39. Orr AW, Stockton R, Simmers MB, Sanders JM, Sarembock IJ, Blackman BR, Schwartz MA. Matrix-specific p21-activated kinase activation regulates vascular permeability in atherogenesis. J Cell Biol 176: 719-727, 2007. (Pubitemid 46333985)
40. Orr AW, Hahn C, Blackman BR, Schwartz MA. p21-activated kinase signaling regulates oxidant-dependent NF-kappa B activation by flow. Circ Res 103: 671-679, 2008.
41. Osawa M, Masuda M, Kusano K, Fujiwara K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J Cell Biol 158: 773-785, 2002. (Pubitemid 34920115)
42. Parsons JT, Martin KH, Slack JK, Taylor JM, Weed SA. Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene 19: 5606-5613, 2000.
43. Perkins ND. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene 25: 6717-6730, 2006. (Pubitemid 44657848)
44. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 274: 30353-30356, 1999. (Pubitemid 129576764)
45. Schlaepfer DD, Hauck CR, Sieg DJ. Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478, 1999.
46. Schreck R, Rieber P, Baeuerle PA. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10: 2247-2258, 1991. (Pubitemid 21905698)
47. Shen TL, Park AY, Alcaraz A, Peng X, Jang I, Koni P, Flavell RA, Gu H, Guan JL. Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J Cell Biol 169: 941-952, 2005. (Pubitemid 41002870)
48. Srinivasan S, Hatley ME, Reilly KB, Danziger EC, Hedrick CC. Modulation of PPARalpha expression and inflammatory interleukin-6 production by chronic glucose increases monocyte/endothelial adhesion. Arterioscler Thromb Vasc Biol 24: 851-857, 2004. (Pubitemid 38620862)
49. Sulciner DJ, Irani K, Yu ZX, Ferrans VJ, Goldschmidt-Clermont P, Finkel T. rac1 regulates a cytokine-stimulated, redox-dependent pathway necessary for NF-kappaB activation. Mol Cell Biol 16: 7115-7121, 1996. (Pubitemid 26389771)
50. Tai LK, Zheng Q, Pan S, Jin ZG, Berk BC. Flow activates ERK1/2 and endothelial nitric oxide synthase via a pathway involving PECAM1, SHP2, and Tie2. J Biol Chem 280: 29620-29624, 2005. (Pubitemid 41177037)
51. Tilghman RW, Slack-Davis JK, Sergina N, Martin KH, Iwanicki M, Hershey ED, Beggs HE, Reichardt LF, Parsons JT. Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J Cell Sci 118: 2613-2623, 2005. (Pubitemid 40932887)
52. Tzima E, del Pozo MA, Shattil SJ, Chien S, Schwartz MA. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J 20: 4639-4647, 2001. (Pubitemid 32848617)
53. Tzima E, Del Pozo MA, Kiosses WB, Mohamed SA, Li S, Chien S, Schwartz MA. Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J 21: 6791-6800, 2002. (Pubitemid 36014551)
54. Tzima E, Kiosses WB, del Pozo MA, Schwartz MA. Localized cdc42 activation, detected using a novel assay, mediates microtubule organizing center positioning in endothelial cells in response to fluid shear stress. J Biol Chem 278: 31020-31023, 2003. (Pubitemid 36994615)
55. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437: 426-431, 2005. (Pubitemid 41613506)
56. Wang H, Joseph JA. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27: 612-616, 1999. (Pubitemid 29408648)
57. Weis SM, Lim ST, Lutu-Fuga KM, Barnes LA, Chen XL, Gothert JR, Shen TL, Guan JL, Schlaepfer DD, Cheresh DA. Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J Cell Biol 181: 43-50, 2008.
58. Yang F, Tang E, Guan K, Wang CY. IKK beta plays an essential role in the phosphorylation of RelA/p65 on serine 536 induced by lipopolysaccharide. J Immunol 170: 5630-5635, 2003. (Pubitemid 36617854)