Optimal intensity shock wave promotes the adhesion and migration of rat osteoblasts via integrin β1-mediated expression of phosphorylated focal adhesion kinase

Journal of Biological Chemistry

Volumn 287, Issue 31, 2012, Pages 26200-26212

  Xu, Jian Kun ^a   Chen, Hong Jiang ^a   Li, Xue Dong ^a   Huang, Zhong Lian ^a   Xu, Huan ^a   Yang, Hai Long ^a   Hu, Jun ^a  

^a SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION RATE; BONE FRACTURE; CELLULAR MECHANISMS; FOCAL ADHESION KINASE; INTEGRINS; OSTEOBLAST ADHESION; SIGNALING PATHWAYS; SINGLE PERIOD; SURFACE EXPRESSION; VEHICLE CONTROL; WESTERN BLOTTING; WOUND HEALING;

AMINO ACIDS; CONTROL SYSTEM SYNTHESIS; ENZYMES; FLOW CYTOMETRY; MOLECULES; OSTEOBLASTS; PHOSPHORYLATION; PIGMENTS; SHOCK WAVES;

ADHESION;

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ALPHA5 INTEGRIN; BETA CATENIN; BETA1 INTEGRIN; FOCAL ADHESION KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL COUNT; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CELL SPREADING; CELL SURVIVAL; CELL SUSPENSION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; EX VIVO STUDY; EXTRACORPOREAL LITHOTRIPSY; FEMALE; GENE EXPRESSION REGULATION; MALE; MOLECULAR INTERACTION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIGENS, CD29; BETA CATENIN; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION; HIGH-ENERGY SHOCK WAVES; INTEGRIN ALPHA5; MALE; MAP KINASE SIGNALING SYSTEM; OSTEOBLASTS; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; SKULL; WNT SIGNALING PATHWAY;

RATTUS;

EID: 84864382244     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349811     Document Type: Article

References (67)

1. Cacchio, A., Giordano, L., Colafarina, O., Rompe, J. D., Tavernese, E., Ioppolo, F., Flamini, S., Spacca, G., and Santilli, V. (2009) Extracorporeal shock-wave therapy compared with surgery for hypertrophic long-bone nonunions. J. Bone Joint Surg. Am. 91, 2589-2597
2. Moretti, B., Notarnicola, A., Garofalo, R., Moretti, L., Patella, S., Marlinghaus, E., and Patella, V. (2009) Shock waves in the treatment of stress fractures. Ultrasound Med. Biol. 35, 1042-1049
3. Beutler, S., Regel, G., Pape, H. C., Machtens, S., Weinberg, A. M., Kremeike, I., Jonas, U., and Tscherne, H. (1999) [Extracorporeal shock wave therapy for delayed union of long bone fractures. preliminary results of a prospective cohort study]. Unfallchirurg 102, 839-847
4. Ikeda, K., Tomita, K., and Takayama, K. (1999) Application of extracorporeal shock wave on bone. Preliminary report. J. Trauma 47, 946-950
5. Wang, C. J., Chen, H. S., Chen, C. E., and Yang, K. D. (2001) Treatment of nonunions of long bone fractures with shock waves. Clin. Orthop. Relat. Res. 387, 95-101
6. Wang, C. J., Huang, H. Y., Chen, H. H., Pai, C. H., and Yang, K. D. (2001) Effect of shock wave therapy on acute fractures of the tibia. A study in a dog model. Clin. Orthop. Relat. Res. 387, 112-118
7. Birnbaum, K., Wirtz, D. C., Siebert, C. H., and Heller, K. D. (2002) Use of extracorporeal shock wave therapy (ESWT) in the treatment of nonunions. A review of the literature. Arch. Orthop. Trauma Surg. 122, 324-330 (Pubitemid 36097231)
8. McClure, S., and Dorfmüller, C. (2003) Extracorporeal shock wave therapy. Theory and equipment. Clin. Techniques Equine Pract. 2, 348-357 (Pubitemid 41115755)
9. Rompe, J. D., Rosendahl, T., Schöllner, C., and Theis, C. (2001) High-energy extracorporeal shock wave treatment of nonunions. Clin. Orthop. Relat. Res. 387, 102-111 (Pubitemid 32510329)
10. Rivilis, I., Milkiewicz, M., Boyd, P., Goldstein, J., Brown, M. D., Egginton, S., Hansen, F. M., Hudlicka, O., and Haas, T. L. (2002) Differential involvement of MMP-2and VEGF during muscle stretch- versus shear stress-induced angiogenesis. Am. J. Physiol. Heart. Circ. Physiol. 283, H1430-H1438
11. Wang, F. S., Yang, K. D., Kuo, Y. R., Wang, C. J., Sheen-Chen, S. M., Huang, H. C., and Chen, Y. J. (2003) Temporal and spatial expression of bone morphogenetic proteins in extracorporeal shock wave-promoted healing of segmental defect. Bone 32, 387-396 (Pubitemid 36407539)
12. Chen, Y. J., Wurtz, T., Wang, C. J., Kuo, Y. R., Yang, K. D., Huang, H. C., and Wang, F. S. (2004) Recruitment of mesenchymal stem cells and expression of TGF-β1 and VEGF in the early stage of shock wave-promoted bone regeneration of segmental defect in rats. J. Orthop. Res. 22, 526-534 (Pubitemid 38489729)
13. Wang, F. S., Wang, C. J., Chen, Y. J., Chang, P. R., Huang, Y. T., Sun, Y. C., Huang, H. C., Yang, Y. J., and Yang, K. D. (2004) Ras induction of superoxide activates ERK-dependent angiogenic transcription factor HIF-1αand VEGF-A expression in shock wave-stimulated osteoblasts. J. Biol. Chem. 279, 10331-10337
14. Jun, H., Da, X., Aibin, Z., and Jiangnan, Z. (2006) Extracorporeal shock wave promotes postnatal human bone marrow stromal cells osteogenesis in vivo. Prog. Biochem. Biophys. 33, 452-457
15. Steinbach, P., Hofstädter, F., Nicolai, H., Rössler, W., and Wieland, W. (1992) In vitro investigations on cellular damage induced by high energy shock waves. Ultrasound Med. Biol. 18, 691-699
16. Tuckwell, D. S., and Humphries, M. J. (1993) Molecular and cellular biology of integrins. Crit. Rev. Oncol. Hematol. 15, 149-171 (Pubitemid 24013567)
17. Schneider, G. B., Whitson, S. W., and Cooper, L. F. (1999) Restricted and coordinated expression of β3-integrin and bone sialoprotein during cultured osteoblast differentiation. Bone 24, 321-327 (Pubitemid 29134970)
18. Clover, J., Dodds, R. A., and Gowen, M. (1992) J. Cell Sci. 103, 267-271
19. Gronowicz, G. A., and McCarthy, M. B. (1995) Glucocorticoids inhibit the attachment of osteoblasts to bone extracellular matrix proteins and decrease β1-integrin levels. Endocrinology 136, 598-608
20. Hynes, R. (2002) Integrins. Bidirectional, allosteric signaling machines. Cell 110, 673-687
21. Siebers, M. C., Walboomers, X. F., van den Dolder, J., Leeuwenburgh, S. C., Wolke, J. G., and Jansen, J. A. (2008) The behavior of osteoblast-like cells on various substrates with functional blocking of integrin-β1 and integrin-β3. J. Mater. Sci. Mater. Med. 19, 861-868 (Pubitemid 351236752)
22. Wang, L., Zhao, G., Olivares-Navarrete, R., Bell, B. F., Wieland, M., Cochran, D. L., Schwartz, Z., and Boyan, B. D. (2006) Integrin β1 silencing in osteoblasts alters substrate-dependent responses to 1,25-dihydroxyvitamin D3. Biomaterials 27, 3716-3725
23. Yang, R. S., Lin, W. L., Chen, Y. Z., Tang, C. H., Huang, T. H., Lu, B. Y., and Fu, W. M. (2005) Regulation by ultrasound treatment on the integrin expression and differentiation of osteoblasts. Bone 36, 276-283
24. Guan, J. L. (1997) Focal adhesion kinase in integrin signaling. Matrix Biol. 16, 195-200
25. Tang, C. H., Yang, R. S., Liou, H. C., and Fu, W. M. (2003) Enhancement of fibronectin synthesis and fibrillogenesis by BMP-4 in cultured rat osteoblast. J. Bone. Miner. Res. 18, 502-511
26. Cheng, S. L., Lai, C. F., Fausto, A., Chellaiah, M., Feng, X., McHugh, K. P., Teitelbaum, S. L., Civitelli, R., Hruska, K. A., Ross, F. P., and Avioli, L. V. (2000) Regulation of αVβ3 and αVβ5 integrins by dexamethasone in normal human osteoblastic cells. J. Cell. Biochem. 77, 265-276 (Pubitemid 30176655)
27. Wang, F. S., Wang, C. J., Huang, H. J., Chung, H., Chen, R. F., and Yang, K. D. (2001) Physical shock wave mediates membrane hyperpolarization and Ras activation for osteogenesis in human bone marrow stromal cells. Biochem. Biophys. Res. Commun. 287, 648-655 (Pubitemid 32912763)
28. Uslu, M. M., Bozdogan, O., Güney, S., Bilgili, H., Kaya, U., Olcay, B., and Korkusuz, F. (1999) The effect of extracorporeal shock wave treatment (ESWT) on bone defects. An experimental study. Bull. Hosp. Joint Dis. 58, 114-118 (Pubitemid 29444946)
29. Schaden, W., Fischer, A., and Sailler, A. (2001) Extracorporeal shock wave therapy of nonunion or delayed osseous union. Clin. Orthop. Relat. Res. 387, 90-94 (Pubitemid 32510327)
30. Wang, C. J., Weng, L. H., Chou, W. Y., Hsu, S. L., Ko, J. Y., Ko, S. F., and Huang, C. C. (2012) Extracorporeal shock wave therapy enhances early tendon-bone healing and reduces bone tunnel enlargement in hamstring autograft anterior cruciate ligament reconstruction. Am. J. Sports. Med., in press
31. Hofmann, A., Ritz, U., Hessmann, M. H., Alini, M., Rommens, P. M., and Rompe, J. D. (2008) Extracorporeal shock wave-mediated changes in proliferation, differentiation, and gene expression of human osteoblasts. J. Trauma 65, 1402-1410
32. Seidl, M., Steinbach, P., Wörle, K., and Hofstädter, F. (1994) Induction of stress fibers and intercellular gaps in human vascular endothelium by shock waves. Ultrasonics 32, 397-400 (Pubitemid 124019332)
33. Brakebusch, C., Bouvard, D., Stanchi, F., Sakai, T., and Fässler, R. (2002) Integrins in invasive growth. J. Clin. Invest. 109, 999-1006 (Pubitemid 34408573)
34. Damsky, C. H., and Ilić, D. (2002) Integrin signaling. It's where the action is. Curr. Opin. Cell Biol. 14, 594-602 (Pubitemid 35247743)
35. Moursi, A. M., Globus, R. K., and Damsky, C. H. (1997) J. Cell Sci. 110, 2187-2196
36. Schlaepfer, D. D., Hauck, C. R., and Sieg, D. J. (1999) Signaling through focal adhesion kinase. Prog. Biophys. Mol. Biol. 71, 435-478 (Pubitemid 29156312)
37. Parsons, J. T., Martin, K. H., Slack, J. K., Taylor, J. M., and Weed, S. A. (2000) Focal adhesion kinase. A regulator of focal adhesion dynamics and cell movement. Oncogene 19, 5606-5613
38. Schaller, M. D. (2001) Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim. Biophys. Acta 1540, 1-21
39. Nakayamada, S., Okada, Y., Saito, K., Tamura, M., and Tanaka, Y. (2003) β1 integrin/focal adhesion kinase-mediated signaling induces intercellular adhesion molecule 1 and receptor activator of nuclear factor κB ligand on osteoblasts and osteoclast maturation. J. Biol. Chem. 278, 45368-45374 (Pubitemid 37432673)
40. Ilić, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544
41. Owen, J. D., Ruest, P. J., Fry, D. W., and Hanks, S. K. (1999) 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. 19, 4806-4818 (Pubitemid 29289519)
42. Sieg, D. J., Hauck, C. R., and Schlaepfer, D. D. (1999) J. Cell Sci. 112, 2677-2691
43. Chaturvedi, L. S., Marsh, H. M., and Basson, M. D. (2007) Src and focal adhesion kinase mediate mechanical strain-induced proliferation and ERK1/2 phosphorylation in human H441 pulmonary epithelial cells. Am. J. Physiol. Cell. Physiol. 292, C1701-C1713 (Pubitemid 47080558)
44. Hatton, J. P., Pooran, M., Li, C. F., Luzzio, C., and Hughes-Fulford, M. (2003) A short pulse of mechanical force induces gene expression and growth in MC3T3-E1 osteoblasts via an ERK1/2 pathway. J. Bone Miner. Res. 18, 58-66 (Pubitemid 36008340)
45. Lai, C. F., Chaudhary, L., Fausto, A., Halstead, L. R., Ory, D. S., Avioli, L. V., and Cheng, S. L. (2001) ERK is essential for growth, differentiation, integrin expression, and cell function in human osteoblastic cells. J. Biol. Chem. 276, 14443-14450
46. Huang, D., Khoe, M., Befekadu, M., Chung, S., Takata, Y., Ilic, D., and Bryer-Ash, M. (2007) Focal adhesion kinase mediates cell survival via NF-κB and ERK signaling pathways. Am. J. Physiol. Cell. Physiol. 292, C1339-C1352 (Pubitemid 46631732)
47. Lee, H. S., Millward-Sadler, S. J., Wright, M. O., Nuki, G., and Salter, D. M. (2000) Integrin and mechanosensitive ion channel-dependent tyrosine phosphorylation of focal adhesion proteins and β-catenin in human articular chondrocytes after mechanical stimulation. J. Bone Miner. Res. 15, 1501-1509 (Pubitemid 30484519)
48. Yee, K. L., Weaver, V. M., and Hammer, D. A. (2008) Integrin-mediated signaling through the MAP kinase pathway. IET Syst. Biol. 2, 8-15 (Pubitemid 351217538)
49. Lee, D. Y., Yeh, C. R., Chang, S. F., Lee, P. L., Chien, S., Cheng, C. K., and Chiu, J. J. (2008) Integrin-mediated expression of bone formation-related genes in osteoblast-like cells in response to fluid shear stress. Roles of extracellular matrix, Shc, and mitogen-activated protein kinase. J. Bone Miner. Res. 23, 1140-1149 (Pubitemid 351915736)
50. Lau, K. H., Kapur, S., Kesavan, C., and Baylink, D. J. (2006) Up-regulation of the Wnt, estrogen receptor, insulin-like growth factor-I, and bone morphogenetic protein pathways in C57BL/6J osteoblasts as opposed to C3H/HeJ osteoblasts in part contributes to the differential anabolic response to fluid shear. J. Biol. Chem. 281, 9576-9588 (Pubitemid 43864676)
51. Robinson, J. A., Chatterjee-Kishore, M., Yaworsky, P. J., Cullen, D. M., Zhao, W., Li, C., Kharode, Y., Sauter, L., Babij, P., Brown, E. L., Hill, A. A., Akhter, M. P., Johnson, M. L., Recker, R. R., Komm, B. S., and Bex, F. J. (2006) Wnt/β-catenin signaling is a normal physiological response to mechanical loading in bone. J. Biol. Chem. 281, 31720-31728 (Pubitemid 46043263)
52. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J., and Weis, W. I. (2005) α-Catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin filament assembly. Cell 123, 903-915 (Pubitemid 41721035)
53. Yamada, S., Pokutta, S., Drees, F., Weis, W. I., and Nelson, W. J. (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123, 889-901 (Pubitemid 41721034)
54. Faux, M. C., Coates, J. L., Kershaw, N. J., Layton, M. J., and Burgess, A. W. (2010) Independent interactions of phosphorylated β-catenin with E-cadherin at cell-cell contacts and APC at cell protrusions. PLoS One 5, e14127
55. Batra, N., Burra, S., Siller-Jackson, A. J., Gu, S., Xia, X., Weber, G. F., DeSimone, D., Bonewald, L. F., Lafer, E. M., Sprague, E., Schwartz, M. A., and Jiang J. X. (2012) Mechanical stress-activated integrin α5β1 induces opening of connexin 43 hemichannels. Proc. Natl. Acad. Sci. U.S.A. 109, 3359-3364
56. Katsumi, A., Naoe, T., Matsushita, T., Kaibuchi, K., Schwartz, M. A. (2005) Integrin activation and matrix binding mediate cellular responses to mechanical stretch. J. Biol. Chem. 280, 16546-16549 (Pubitemid 41389109)
57. Tzima, E., del Pozo, M. A., Shattil, S. J., Chien, S., Schwartz, M.A. (2001) Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 20, 4639-4647 (Pubitemid 32848617)
58. Warden, S. J., Favaloro, J. M., Bennell, K. L., McMeeken, J. M., Ng, K. W., Zajac, J. D., and Wark, J. D. (2001) Low-intensity pulsed ultrasound stimulates a bone-forming response in UMR-106 cells. Biochem. Biophys. Res. Commun. 286, 443-450 (Pubitemid 32912966)
59. Rubin, C. T., Gross, T. S., McLeod, K. J., and Bain, S. D. (1995) Morphologic stages in lamellar bone formation stimulated by a potent mechanical stimulus. J. Bone Miner. Res. 10, 488-495
60. iprotein and ERK-dependent pathways mediate ultrasound promotion of osteogenic transcription in human osteoblasts. FEBS Lett. 554, 154-158
61. Plotkin, L. I., Mathov, I., Aguirre, J. I., Parfitt, A. M., Manolagas, S. C., and Bellido, T. (2005) Mechanical stimulation prevents osteocyte apoptosis. Requirement of integrins, Src kinases, and ERKs. Am. J. Physiol. Cell. Physiol. 289, C633-C643 (Pubitemid 41192673)
62. Humphries, M. J., Travis, M. A., Clark, K., and Mould, A. P. (2004) Mechanisms of integration of cells and extracellular matrices by integrins. Biochem. Soc. Trans. 32, 822-825 (Pubitemid 39524388)
63. Tarone, G., Hirsch, E., Brancaccio, M., De Acetis, M., Barberis, L., Balzac, F., Retta, S. F., Botta, C., Altruda, F., and Silengo, L. (2000) Integrin function and regulation in development. Int. J. Dev. Biol. 44, 725-731
64. Klingbeil, C. K., Hauck, C. R., Hsia, D. A., Jones, K. C., Reider, S. R., and Schlaepfer, D. D. (2001) Targeting Pyk2 to β1-integrin-containing focal contacts rescues fibronectin-stimulated signaling and haptotactic motility defects of focal adhesion kinase-null cells. J. Cell Biol. 152, 97-110 (Pubitemid 32102440)
65. Hsia, D. A., Lim, S. T., Bernard-Trifilo, J. A., Mitra, S. K., Tanaka, S., den Hertog, J., Streblow, D. N., Ilic, D., Ginsberg, M. H., and Schlaepfer, D. D. (2005) Integrin α4β1 promotes focal adhesion kinase-independent cell motility via α4 cytoplasmic domain-specific activation of c-Src. Mol. Cell. Biol. 25, 9700-9712 (Pubitemid 41507866)
66. Schlaepfer, D. D., Jones, K. C., and Hunter, T. (1998) Multiple Grb2- mediated integrin-stimulated signaling pathways to ERK2/mitogenactivated protein kinase. Summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol. Cell. Biol. 18, 2571-2585 (Pubitemid 28183427)
67. National Institutes of Health (1996) Guide for the Care of Use of Laboratory Animals, NIH Publication 85-23, National Institutes of Health, Bethesda, MD