Focal Adhesion Kinase Plays a Role in Osteoblast Mechanotransduction In Vitro but Does Not Affect Load-Induced Bone Formation In Vivo

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Castillo, Alesha B ^a,b,c   Blundo, Jennifer T ^c,d   Chen, Julia C ^d   Lee, Kristen L ^d   Yereddi, Nikitha Reddy ^d   Jang, Eugene ^d   Kumar, Shefali ^d   Tang, W Joyce ^a   Zarrin, Sarah ^a   Kim, Jae Beom ^b   Jacobs, Christopher R ^a,c,d  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Stanford University   (United States)

^d Department of Earth and Environmental Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; FLUID FLOW; GENE EXPRESSION; GENE INACTIVATION; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; MALE; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; SHEAR FLOW; SITE DIRECTED MUTAGENESIS; WEIGHT BEARING; WILD TYPE;

ADAPTATION, BIOLOGICAL; ANIMALS; BODY WEIGHT; BONE AND BONES; CELL LINE; DINOPROSTONE; FEMALE; FOCAL ADHESION KINASE 2; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; GENE DELETION; GENE EXPRESSION; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOGENESIS; PHOSPHORYLATION; PROTEIN TRANSPORT; ULNA;

MUS;

EID: 84866684728     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043291     Document Type: Article

References (56)

1. Chen CS, Tan J, Tien J, (2004) Mechanotransduction at cell-matrix and cell-cell contacts. Annu Rev Biomed Eng 6: 275-302.
2. Litzenberger JB, Tang WJ, Castillo AB, Jacobs CR, (2009) Deletion of beta-1 Integrins from cortical osteocytes reduces load-induced bone formation. Cellular and Molecular Bioengineering.
3. Cary LA, Guan JL, (1999) Focal adhesion kinase in integrin-mediated signaling. Front Biosci 4: D102-113.
4. Miyauchi A, Gotoh M, Kamioka H, Notoya K, Sekiya H, et al. (2006) AlphaVbeta3 integrin ligands enhance volume-sensitive calcium influx in mechanically stretched osteocytes. J Bone Miner Metab 24: 498-504.
5. Ishida T, Peterson TE, Kovach NL, Berk BC, (1996) MAP kinase activation by flow in endothelial cells. Role of beta 1 integrins and tyrosine kinases. Circ Res 79: 310-316.
6. Hanks SK, Calalb MB, Harper MC, Patel SK, (1992) Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc Natl Acad Sci U S A 89: 8487-8491.
7. Kapur S, Baylink DJ, Lau KH, (2003) Fluid flow shear stress stimulates human osteoblast proliferation and differentiation through multiple interacting and competing signal transduction pathways. Bone 32: 241-251.
8. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB, et al. (1992) pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci U S A 89: 5192-5196.
9. Hungerford JE, Compton MT, Matter ML, Hoffstrom BG, Otey CA, (1996) Inhibition of pp125FAK in cultured fibroblasts results in apoptosis. J Cell Biol 135: 1383-1390.
10. Xu LH, Owens LV, Sturge GC, Yang X, Liu ET, et al. (1996) Attenuation of the expression of the focal adhesion kinase induces apoptosis in tumor cells. Cell Growth Differ 7: 413-418.
11. Wozniak MA, Modzelewska K, Kwong L, Keely PJ, (2004) Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692: 103-119.
12. Sieg DJ, Hauck CR, Schlaepfer DD, (1999) Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 112 (Pt 16):: 2677-2691.
13. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, et al. (2000) FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2: 249-256.
14. Ma A, Richardson A, Schaefer EM, Parsons JT, (2001) Serine phosphorylation of focal adhesion kinase in interphase and mitosis: a possible role in modulating binding to p130(Cas). Mol Biol Cell 12: 1-12.
15. Lee HS, Millward-Sadler SJ, Wright MO, Nuki G, Salter DM, (2000) Integrin and mechanosensitive ion channel-dependent tyrosine phosphorylation of focal adhesion proteins and beta-catenin in human articular chondrocytes after mechanical stimulation. J Bone Miner Res 15: 1501-1509.
16. Orr AW, Murphy-Ullrich JE, (2004) Regulation of endothelial cell function BY FAK and PYK2. Front Biosci 9: 1254-1266.
17. Wen H, Blume PA, Sumpio BE, (2009) Role of integrins and focal adhesion kinase in the orientation of dermal fibroblasts exposed to cyclic strain. Int Wound J 6: 149-158.
18. Young SR, Gerard-O'Riley R, Kim JB, Pavalko FM, (2009) Focal adhesion kinase is important for fluid shear stress-induced mechanotransduction in osteoblasts. J Bone Miner Res 24: 411-424.
19. Li S, Kim M, Hu YL, Jalali S, Schlaepfer DD, et al. (1997) Fluid shear stress activation of focal adhesion kinase. Linking to mitogen-activated protein kinases. J Biol Chem 272: 30455-30462.
20. Petzold T, Orr AW, Hahn C, Jhaveri K, Parsons JT, et al. (2009) Focal adhesion kinase modulates activation of NF-{kappa}B by flow in endothelial cells. Am J Physiol Cell Physiol.
21. Rezzonico R, Cayatte C, Bourget-Ponzio I, Romey G, Belhacene N, et al. (2003) Focal adhesion kinase pp125FAK interacts with the large conductance calcium-activated hSlo potassium channel in human osteoblasts: potential role in mechanotransduction. J Bone Miner Res 18: 1863-1871.
22. Chow JW, Chambers TJ, (1994) Indomethacin has distinct early and late actions on bone formation induced by mechanical stimulation. Am J Physiol 267: E287-292.
23. Lean JM, Mackay AG, Chow JW, Chambers TJ, (1996) Osteocytic expression of mRNA for c-fos and IGF-I: an immediate early gene response to an osteogenic stimulus. Am J Physiol 270: E937-945.
24. Kim J, Leucht P, Luppen CA, Park YJ, Beggs HE, et al. (2007) Reconciling the roles of FAK in osteoblast differentiation, osteoclast remodeling, and bone regeneration. Bone 41: 39-51.
25. Leucht P, Kim JB, Currey JA, Brunski J, Helms JA, (2007) FAK-Mediated mechanotransduction in skeletal regeneration. PLoS ONE 2: e390.
26. Mitra SK, Hanson DA, Schlaepfer DD, (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6: 56-68.
27. Delmas P, Nauli SM, Li X, Coste B, Osorio N, et al. (2004) Gating of the polycystin ion channel signaling complex in neurons and kidney cells. Faseb J 18: 740-742.
28. Tadokoro S, Shattil SJ, Eto K, Tai V, Liddington RC, et al. (2003) Talin binding to integrin beta tails: a final common step in integrin activation. Science 302: 103-106.
29. Clark EA, Brugge JS, (1995) Integrins and signal transduction pathways: the road taken. Science 268: 233-239.
30. Sasaki H, Nagura K, Ishino M, Tobioka H, Kotani K, et al. (1995) Cloning and characterization of cell adhesion kinase beta, a novel protein-tyrosine kinase of the focal adhesion kinase subfamily. J Biol Chem 270: 21206-21219.
31. Xiong W, Parsons JT, (1997) Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J Cell Biol 139: 529-539.
32. Kim JB, Leucht P, Lam K, Luppen C, Ten Berge D, et al. (2007) Bone regeneration is regulated by wnt signaling. J Bone Miner Res 22: 1913-1923.
33. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH, (1995) Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts-correlation with prostaglandin upregulation. Biochem Biophys Res Commun 217: 640-648.
34. Robling AG, Turner CH, (2002) Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone 31: 562-569.
35. Wang HB, Dembo M, Hanks SK, Wang Y, (2001) Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci U S A 98: 11295-11300.
36. Pirone DM, Liu WF, Ruiz SA, Gao L, Raghavan S, et al. (2006) An inhibitory role for FAK in regulating proliferation: a link between limited adhesion and RhoA-ROCK signaling. J Cell Biol 174: 277-288.
37. Lim ST, Chen XL, Lim Y, Hanson DA, Vo TT, et al. (2008) Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol Cell 29: 9-22.
38. Ilic D, Furuta Y, Suda T, Atsumi T, Fujimoto J, et al. (1995) Focal adhesion kinase is not essential for in vitro and in vivo differentiation of ES cells. Biochem Biophys Res Commun 209: 300-309.
39. Monfoulet L, Rabier B, Chassande O, Fricain JC, (2009) Drilled Hole Defects in Mouse Femur as Models of Intramembranous Cortical and Cancellous Bone Regeneration. Calcif Tissue Int.
40. Colnot C, (2009) Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J Bone Miner Res 24: 274-282.
41. Lee DY, Li YS, Chang SF, Zhou J, Ho HM, et al. (2009) Oscillatory flow-induced proliferation of osteoblast-like cells is mediated by {alpha}v{beta}3 and {beta}1 integrins through synergistic interactions of FAK and Shc with PI3K and the Akt/mTOR/p70S6K pathway. J Biol Chem.
42. Santos A, Bakker AD, Zandieh-Doulabi B, de Blieck-Hogervorst JM, Klein-Nulend J, (2009) Early activation of the beta-catenin pathway in osteocytes is mediated by nitric oxide, phosphatidyl inositol-3 kinase/Akt, and focal adhesion kinase. Biochem Biophys Res Commun.
43. Schlaepfer DD, Hunter T, (1996) Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol Cell Biol 16: 5623-5633.
44. Weis SM, Lim ST, Lutu-Fuga KM, Barnes LA, Chen XL, et al. (2008) Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J Cell Biol 181: 43-50.
45. Sieg DJ, Ilic D, Jones KC, Damsky CH, Hunter T, et al. (1998) Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK- cell migration. EMBO J 17: 5933-5947.
46. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, et al. (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178: 1053-1064.
47. Buckbinder L, Crawford DT, Qi H, Ke HZ, Olson LM, et al. (2007) Proline-rich tyrosine kinase 2 regulates osteoprogenitor cells and bone formation, and offers an anabolic treatment approach for osteoporosis. Proc Natl Acad Sci U S A 104: 10619-10624.
48. Nguyen KT, Robling AG, Turner CH (2009) Knockout of Pyk2 improves the mechanical loading response of bone; Pittsburgh, PA.
49. Jacobs CR, Yellowley CE, Davis BR, Zhou Z, Cimbala JM, et al. (1998) Differential effect of steady versus oscillating flow on bone cells. J Biomech 31: 969-976.
50. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, et al. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377: 539-544.
51. Beggs HE, Schahin-Reed D, Zang K, Goebbels S, Nave KA, et al. (2003) FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40: 501-514.
52. Dacquin R, Starbuck M, Schinke T, Karsenty G, (2002) Mouse alpha1(I)-collagen promoter is the best known promoter to drive efficient Cre recombinase expression in osteoblast. Dev Dyn 224: 245-251.
53. Hildebrand T, Rüegsegger P, (1997) Quantification of Bone Microarchitecture with the Structure Model Index. Computer methods in biomechanics and biomedical engineering 1: 15-23.
54. Robling A, Li J, Shultz KL, Beamer W, Turner C, (2003) Evidence for a skeletal mechanosensitivity gene on mouse chromosome 4. The FASEB Journal 17: 324-326.
55. Castillo AB, Alam I, Tanaka SM, Levenda J, Li J, et al. (2006) Low-amplitude, broad-frequency vibration effects on cortical bone formation in mice. Bone 39: 1087-1096.
56. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610.