Activation of NF-κB by fluid shear stress, but not TNF-α, requires focal adhesion kinase in osteoblasts

Bone

Volumn 47, Issue 1, 2010, Pages 74-82

  Young, Suzanne R L ^a   Gerard O'Riley, Rita ^a   Harrington, Maureen ^a   Pavalko, Fredrick M ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FAK; I B; Mechanotransduction; NF B; Osteoblasts

Indexed keywords

FOCAL ADHESION KINASE; I KAPPA B ALPHA; I KAPPA B BETA; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P105; TUMOR NECROSIS FACTOR ALPHA; I KAPPA B; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; NFKB1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; OSTEOBLAST; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SHEAR STRESS; ANIMAL; CELL NUCLEUS; DRUG EFFECT; ENZYMOLOGY; FLOW KINETICS; GENETICS; MECHANICAL STRESS; METABOLISM; PHOSPHORYLATION; PROMOTER REGION;

ANIMALS; CELL NUCLEUS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; I-KAPPA B PROTEINS; MICE; NF-KAPPA B P50 SUBUNIT; OSTEOBLASTS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RHEOLOGY; STRESS, MECHANICAL; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77954761017     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.03.014     Document Type: Article

References (49)

1. Piekarski K., Munro M. Transport mechanism operating between blood supply and osteocytes in long bones. Nature 1977, 269:80-82.
2. Turner C.H., Pavalko F.M. Mechanotransduction and functional response of the skeleton to physical stress: the mechanisms and mechanics of bone adaptation. J Orthop Sci 1998, 3:346-355.
3. Young S.R., Gerard-O'Riley R., Kim J.B., Pavalko F.M. Focal adhesion kinase is important for fluid shear stress-induced mechanotransduction in osteoblasts. J Bone Miner Res 2009, 24:411-424.
4. Chang J., Wang Z., Tang E., Fan Z., McCauley L., Franceschi R., Guan K., Krebsbach P.H., Wang C.Y. Inhibition of osteoblastic bone formation by nuclear factor-kappaB. Nat Med 2009, 15:682-689.
5. Chen N.X., Geist D.J., Genetos D.C., Pavalko F.M., Duncan R.L. Fluid shear-induced NFkappaB translocation in osteoblasts is mediated by intracellular calcium release. Bone 2003, 33:399-410.
6. Nanes M.S. Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology. Gene 2003, 321:1-15.
7. Makaida N., Mahe Y., Matsushima K. J Biol Chem 1990, 265:21128-21133.
8. Vig E., Green M., Liu Y., Yu K.Y., Kwon H.J., Tian J., Goebl M.G., Harrington M.A. SIMPL is a tumor necrosis factor-specific regulator of nuclear factor-kappaB activity. J Biol Chem 2001, 276:7859-7866.
9. Kim J.B., Leucht P., Luppen C.A., Park Y.J., Beggs H.E., Damsky C.H., Helms J.A. Reconciling the roles of FAK in osteoblast differentiation, osteoclast remodeling, and bone regeneration. Bone 2007, 41:39-51.
10. Jacobs C.R., Yellowley C.E., Davis B.R., Zhou Z., Cimbala J.M., Donahue H.J. Differential effect of steady versus oscillating flow on bone cells. J Biomech 1998, 31:969-976.
11. Sheffield J.B., Graff D., Li H.P. A solid-phase method for the quantitation of protein in the presence of sodium dodecyl sulfate and other interfering substances. Anal Biochem 1987, 166:49-54.
12. Chen L.F., Greene W.C. Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 2004, 5:392-401.
13. Petzold T., Orr A.W., Hahn C., Jhaveri K.A., Parsons J.T., Schwartz M.A. Focal adhesion kinase modulates activation of NF-kappaB by flow in endothelial cells. Am J Physiol Cell Physiol 2009, 297:C814-C822.
14. Ponik S.M., Triplett J.W., Pavalko F.M. Osteoblasts and osteocytes respond differently to oscillatory and unidirectional fluid flow profiles. J Cell Biochem 2007, 100:794-807.
15. Chiu J.J., Lee P.L., Chang S.F., Chen L.J., Lee C.I., Lin K.M., Usami S., Chien S. Shear stress regulates gene expression in vascular endothelial cells in response to tumor necrosis factor-alpha: a study of the transcription profile with complementary DNA microarray. J Biomed Sci 2005, 12:481-502.
16. Chiu J.J., Lee P.L., Chen C.N., Lee C.I., Chang S.F., Chen L.J., Lien S.C., Ko Y.C., Usami S., Chien S. Shear stress increases ICAM-1 and decreases VCAM-1 and E-selectin expressions induced by tumor necrosis factor-[alpha] in endothelial cells. Arterioscler Thromb Vasc Biol 2004, 24:73-79.
17. Davis M.E., Grumbach I.M., Fukai T., Cutchins A., Harrison D.G. Shear stress regulates endothelial nitric-oxide synthase promoter activity through nuclear factor kappaB binding. J Biol Chem 2004, 279:163-168.
18. Du W., Mills I., Sumpio B.E. Cyclic strain causes heterogeneous induction of transcription factors, AP-1, CRE binding protein and NF-kB, in endothelial cells: species and vascular bed diversity. J Biomech 1995, 28:1485-1491.
19. Ganguli A., Persson L., Palmer I.R., Evans I., Yang L., Smallwood R., Black R., Qwarnstrom E.E. Distinct NF-kappaB regulation by shear stress through Ras-dependent IkappaBalpha oscillations: real-time analysis of flow-mediated activation in live cells. Circ Res 2005, 96:626-634.
20. Gosgnach W., Messika-Zeitoun D., Gonzalez W., Philipe M., Michel J.B. Shear stress induces iNOS expression in cultured smooth muscle cells: role of oxidative stress. Am J Physiol Cell Physiol 2000, 279:C1880-C1888.
21. 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 2000, 60:182-188.
22. Khachigian L.M., Resnick N., Gimbrone M.A., Collins T. Nuclear factor-kappa B interacts functionally with the platelet-derived growth factor B-chain shear-stress response element in vascular endothelial cells exposed to fluid shear stress. J Clin Invest 1995, 96:1169-1175.
23. Lan Q., Mercurius K.O., Davies P.F. Stimulation of transcription factors NF kappa B and AP1 in endothelial cells subjected to shear stress. Biochem Biophys Res Commun 1994, 201:950-956.
24. Mohan S., Hamuro M., Koyoma K., Sorescu G.P., Jo H., Natarajan M. High glucose induced NF-kappaB DNA-binding activity in HAEC is maintained under low shear stress but inhibited under high shear stress: role of nitric oxide. Atherosclerosis 2003, 171:225-234.
25. Mohan S., Koyoma K., Thangasamy A., Nakano H., Glickman R.D., Mohan N. Low shear stress preferentially enhances IKK activity through selective sources of ROS for persistent activation of NF-kappaB in endothelial cells. Am J Physiol Cell Physiol 2007, 292:C362-C371.
26. Mohan S., Mohan N., Valente A.J., Sprague E.A. Regulation of low shear flow-induced HAEC VCAM-1 expression and monocyte adhesion. Am J Physiol 1999, 276:C1100-C1107.
27. Nagel T., Resnick N., Dewey C.F., Gimbrone M.A. Vascular endothelial cells respond to spatial gradients in fluid shear stress by enhanced activation of transcription factors. Arterioscler Thromb Vasc Biol 1999, 19:1825-1834.
28. Resnick N., Yahav H., Khachigian L.M., Collins T., Anderson K.R., Dewey F.C., Gimbrone M.A. Endothelial gene regulation by laminar shear stress. Adv Exp Med Biol 1997, 430:155-164.
29. Silacci P., Formentin K., Bouzourene K., Daniel F., Brunner H.R., Hayoz D. Unidirectional and oscillatory shear stress differentially modulate NOS III gene expression. Nitric Oxide 2000, 4:47-56.
30. Sun H.W., Li C.J., Chen H.Q., Lin H.L., Lv H.X., Zhang Y., Zhang M. Involvement of integrins, MAPK, and NF-kappaB in regulation of the shear stress-induced MMP-9 expression in endothelial cells. Biochem Biophys Res Commun 2007, 353:152-158.
31. Yang Q.W., Mou L., Lv F.L., Wang J.Z., Wang L., Zhou H.J., Gao D. Role of Toll-like receptor 4/NF-kappaB pathway in monocyte-endothelial adhesion induced by low shear stress and ox-LDL. Biorheology 2005, 42:225-236.
32. Zhu C.H., Ying D.J., Mi J.H., Zhu X.H., Sun J.S., Cui X.P. Low shear stress regulates monocyte adhesion to oxidized lipid-induced endothelial cells via an IkappaBalpha dependent pathway. Biorheology 2004, 41:127-137.
33. Avvisato C.L., Yang X., Shah S., Hoxter B., Li W., Gaynor R., Pestell R., Tozeren A., Byers S.W. Mechanical force modulates global gene expression and beta-catenin signaling in colon cancer cells. J Cell Sci 2007, 120:2672-2682.
34. Bhullar I.S., Li Y.S., Miao H., Zandi E., Kim M., Shyy J.Y., Chien S. Fluid shear stress activation of IkappaB kinase is integrin-dependent. J Biol Chem 1998, 273:30544-30549.
35. Hay D.C., Beers C., Cameron V., Thomson L., Flitney F.W., Hay R.T. Activation of NF-kappaB nuclear transcription factor by flow in human endothelial cells. Biochim Biophys Acta 2003, 1642:33-44.
36. Partridge J., Carlsen H., Enesa K., Chaudhury H., Zakkar M., Luong L., Kinderlerer A., Johns M., Blomhoff R., Mason J.C., Haskard D.O., Evans P.C. Laminar shear stress acts as a switch to regulate divergent functions of NF-kappaB in endothelial cells. FASEB J 2007, 21:3553-3561.
37. Shaik S.S., Soltau T.D., Chaturvedi G., Totapally B., Hagood J.S., Andrews W.W., Athar M., Voitenok N.N., Killingsworth C.R., Patel R.P., Fallon M.B., Maheshwari A. Low intensity shear stress increases endothelial ELR+CXC chemokine production via a focal adhesion kinase-p38{beta} MAPK-NF-{kappa}B pathway. J Biol Chem 2009, 284:5945-5955.
38. Kumar A., Murphy R., Robinson P., Wei L., Boriek A.M. Cyclic mechanical strain inhibits skeletal myogenesis through activation of focal adhesion kinase, Rac-1 GTPase, and NF-kappaB transcription factor. FASEB J 2004, 18:1524-1535.
39. Wang Y., Chang J., Li Y.C., Li Y.S., Shyy J.Y., Chien S. Shear stress and VEGF activate IKK via the Flk-1/Cbl/Akt signaling pathway. Am J Physiol Heart Circ Physiol 2004, 286:H685-H692.
40. 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 2003, 278:29359-29365.
41. Rezzonico R., Cayatte C., Bourget-Ponzio I., Romey G., Belhacene N., Loubat A., Rocchi S., Van Obberghen E., Girault J.A., Rossi B., Schmid-Antomarchi H. Focal adhesion kinase pp 125FAK interacts with the large conductance calcium-activated hSlo potassium channel in human osteoblasts: potential role in mechanotransduction. J Bone Miner Res 2003, 18:1863-1871.
42. Donahue T.L., Haut T.R., Yellowley C.E., Donahue H.J., Jacobs C.R. Mechanosensitivity of bone cells to oscillating fluid flow induced shear stress may be modulated by chemotransport. J Biomech 2003, 36:1363-1371.
43. Riddle R.C., Hippe K.R., Donahue H.J. Chemotransport contributes to the effect of oscillatory fluid flow on human bone marrow stromal cell proliferation. J Orthop Res 2008, 26:918-924.
44. Franzoso G., Carlson L., Xing L., Poljak L., Shores E.W., Brown K.D., Leonardi A., Tran T., Boyce B.F., Siebenlist U. Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev 1997, 11:3482-3496.
45. Iotsova V., Caamano J., Loy J., Yang Y., Lewin A., Bravo R. Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat Med 1997, 3:1285-1289.
46. Abu-Amer Y., Darwech I., Otero J. Role of the NF-kappaB axis in immune modulation of osteoclasts and bone loss. Autoimmunity 2008, 41:204-211.
47. Jimi E., Ghosh S. Role of nuclear factor-kappaB in the immune system and bone. Immunol Rev 2005, 208:80-87.
48. Xu J., Wu H.F., Ang E.S., Yip K., Woloszyn M., Zheng M.H., Tan R.X. NF-kappaB modulators in osteolytic bone diseases. Cytokine Growth Factor Rev 2009, 20:7-17.
49. Kurokouchi K., Jacobs C.R., Donahue H.J. Oscillating fluid flow inhibits TNF-alpha -induced NF-kappa B activation via an Ikappa B kinase pathway in osteoblast-like UMR106 cells. J Biol Chem 2001, 276:13499-13504.