Low-Intensity pulsed ultrasound promotes chondrogenic progenitor cell migration via focal adhesion kinase pathway

Ultrasound in Medicine and Biology

Volumn 40, Issue 6, 2014, Pages 1177-1186

  Jang, Kee W ^a,b   Ding, Lei ^a   Seol, Dongrim ^a   Lim, Tae Hong ^b   Buckwalter, Joseph A ^a,c   Martin, James A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b University of Iowa   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Articular cartilage; Cell migration; Focal adhesion kinase; Low intensity pulsed ultrasound; Post traumatic osteoarthritis

Indexed keywords

ADHESION; AMINO ACIDS; BIOCHEMISTRY; CARTILAGE; CELL CULTURE; PHOSPHORYLATION; REPAIR;

ARTICULAR CARTILAGES; CELL MIGRATION; FOCAL ADHESION KINASE; LOW-INTENSITY PULSED ULTRASOUND; POST-TRAUMATIC OSTEOARTHRITIS;

ENZYMES;

FOCAL ADHESION KINASE; FORMYLMETHIONYLLEUCYLPHENYLALANINE; HIGH MOBILITY GROUP B1 PROTEIN; PROTEIN TYROSINE KINASE INHIBITOR; TYROSINE; FOCAL ADHESION KINASE 1;

ARTICLE; ASSAY; CELL MIGRATION; CELL STIMULATION; CHONDROGENESIS; CHONDROGENIC PROGENITOR CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ECHOGRAPHY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXPLANT; LOW INTENSITY PULSED ULTRASOUND; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN DOMAIN; SCRATCH ASSAY; STEM CELL; WESTERN BLOTTING; ANIMAL; ARTICULAR CARTILAGE; BOVINAE; CARTILAGE CELL; CELL MOTION; CYTOLOGY; METABOLISM; OSTEOARTHRITIS; PHOSPHORYLATION; ULTRASOUND THERAPY; WOUND HEALING;

ANIMALS; BLOTTING, WESTERN; CARTILAGE, ARTICULAR; CATTLE; CELL MOVEMENT; CHONDROCYTES; FOCAL ADHESION KINASE 1; MICROSCOPY, CONFOCAL; OSTEOARTHRITIS; PHOSPHORYLATION; STEM CELLS; ULTRASONIC THERAPY; WOUND HEALING;

EID: 84899980821     PISSN: 03015629     EISSN: 1879291X     Source Type: Journal    
DOI: 10.1016/j.ultrasmedbio.2013.12.007     Document Type: Article

References (68)

1. Amano M., Chihara K., Kimura K., Fukata Y., Nakamura N., Matsuura Y., Kaibuchi K. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 1997, 275:1308-1311.
2. Buckwalter J.A., Brown T.D. Joint injury, repair, and remodeling: roles in post-traumatic osteoarthritis. Clin Orthop Relat Res 2004, 423:7-16.
3. Buckwalter J.A., Mankin H.J. Articular cartilage: Degeneration and osteoarthritis, repair, regeneration, and transplantation. Instr Course Lect 1998, 47:487-504.
4. Buckwalter J.A., Mankin H.J., Grodzinsky A.J. Articular cartilage and osteoarthritis. Instr Course Lect 2005, 54:465-480.
5. Buckwalter J.A., Martin J.A. Sports and osteoarthritis. Curr Opin Rheumatol 2004, 16:634-639.
6. Cabrita M.A., Jones L.M., Quizi J.L., Sabourin L.A., McKay B.C., Addison C.L. Focal adhesion kinase inhibitors are potent anti-angiogenic agents. Mol Oncol 2011, 5:517-526.
7. Calalb M.B., Zhang X.E., Polte T.R., Hanks S.K. Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem Biophys Res Commun 1996, 228:662-668.
8. Carrigan S.O., Pink D.B., Stadnyk A.W. Neutrophil transepithelial migration in response to the chemoattractant fMLP but not C5a is phospholipase D-dependent and related to the use of CD11b/CD18. JLeukoc Biol 2007, 82:1575-1584.
9. Cary L.A., Chang J.F., Guan J.L. Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. JCell Sci 1996, 109(Pt 7):1787-1794.
10. Chaturvedi L.S., Gayer C.P., Marsh H.M., Basson M.D. Repetitive deformation activates Src-independent FAK-dependent ERK motogenic signals in human Caco-2 intestinal epithelial cells. Am J Physiol Cell Physiol 2008, 294:C1350-C1361.
11. Choi C.K., Vicente-Manzanares M., Zareno J., Whitmore L.A., Mogilner A., Horwitz A.R. Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat Cell Biol 2008, 10:1039-1050.
12. Ciccimaro E., Hanks S.K., Blair I.A. Quantification of focal adhesion kinase activation loop phosphorylation as a biomarker of Src activity. Mol Pharmacol 2009, 75:658-666.
13. Clark E.A., Brugge J.S. Integrins and signal transduction pathways: The road taken. Science 1995, 268:233-239.
14. Cook S.D., Salkeld S.L., Popich-Patron L.S., Ryaby J.P., Jones D.G., Barrack R.L. Improved cartilage repair after treatment with low-intensity pulsed ultrasound. Clin Orthop Relat Res 2001, S231-S243.
15. Critchley D.R., Gingras A.R. Talin at a glance. JCell Sci 2008, 121:1345-1347.
16. Cui J.H., Park S.R., Park K., Choi B.H., Min B.H. Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation invivo. Tissue Eng 2007, 13:351-360.
17. Dalecki D. Mechanical bioeffects of ultrasound. Annu Rev Biomed Eng 2004, 6:229-248.
18. Degryse B., Bonaldi T., Scaffidi P., Muller S., Resnati M., Sanvito F., Arrigoni G., Bianchi M.E. The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. JCell Biol 2001, 152:1197-1206.
19. Ebisawa K., Hata K., Okada K., Kimata K., Ueda M., Torii S., Watanabe H. Ultrasound enhances transforming growth factor beta-mediated chondrocyte differentiation of human mesenchymal stem cells. Tissue Eng 2004, 10:921-929.
20. Filaferro M., Novi C., Ruggieri V., Genedani S., Alboni S., Malagoli D., Calo G., Guerrini R., Vitale G. Neuropeptide S stimulates human monocyte chemotaxis via NPS receptor activation. Peptides 2013, 39:16-20.
21. Fowlkes J.B., Abramowicz J.S., Church C.C., Holland C.K., Miller D.L., O'Brien W.D., Sanghvi N.T., Stratmeyer M.E., Zachary J.E., Inst B.C.A. American Institute of Ultrasound in Medicine consensus report on potential bioeffects of diagnostic ultrasound. JUltrasound Med 2008, 27:503-515.
22. Giancotti F.G., Ruoslahti E. Integrin signaling. Science 1999, 285:1028-1032.
23. Goodwin W., McCabe D., Sauter E., Reese E., Walter M., Buckwalter J.A., Martin J.A. Rotenone prevents impact-induced chondrocyte death. JOrthop Res 2010, 28:1057-1063.
24. Green T.P., Fennell M., Whittaker R., Curwen J., Jacobs V., Allen J., Logie A., Hargreaves J., Hickinson D.M., Wilkinson R.W., Elvin P., Boyer B., Carragher N., Ple P.A., Bermingham A., Holdgate G.A., Ward W.H., Hennequin L.F., Davies B.R., Costello G.F. Preclinical anticancer activity of the potent, oral Src inhibitor AZD0530. Mol Oncol 2009, 3:248-261.
25. Gurkan I., Ranganathan A., Yang X., Horton W.E., Todman M., Huckle J., Pleshko N., Spencer R.G. Modification of osteoarthritis in the guinea pig with pulsed low-intensity ultrasound treatment. Osteoarthritis Cartilage 2010, 18:724-733.
26. Hanks S.K., Calalb M.B., Harper M.C., Patel S.K. Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc Natl Acad Sci USA 1992, 89:8487-8491.
27. Hauck C.R., Sieg D.J., Hsia D.A., Loftus J.C., Gaarde W.A., Monia B.P., Schlaepfer D.D. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res 2001, 61:7079-7090.
28. Horwitz A.R., Parsons J.T. Cell migration-Movin' on. Science 1999, 286:1102-1103.
29. Howe A., Aplin A.E., Alahari S.K., Juliano R.L. Integrin signaling and cell growth control. Curr Opin Cell Biol 1998, 10:220-231.
30. Humphries J.D., Wang P., Streuli C., Geiger B., Humphries M.J., Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. JCell Biol 2007, 179:1043-1057.
31. Huveneers S., Danen E.H.J. Adhesion signaling: Crosstalk between integrins, Src and Rho. JCell Sci 2009, 122:1059-1069.
32. Ilic D., Furuta Y., Kanazawa S., Takeda N., Sobue K., Nakatsuji N., Nomura S., Fujimoto J., Okada M., Yamamoto T. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995, 377:539-544.
33. Khanna A., Nelmes R.T., Gougoulias N., Maffulli N., Gray J. The effects of LIPUS on soft-tissue healing: A review of literature. Br Med Bull 2009, 89:169-182.
34. Kinoshita M., Hynynen K. Mechanism of porphyrin-induced sonodynamic effect: Possible role of hyperthermia. Radiat Res 2006, 165:299-306.
35. Korstjens C.M., van der Rijt R.H., Albers G.H., Semeins C.M., Klein-Nulend J. Low-intensity pulsed ultrasound affects human articular chondrocytes invitro. Med Biol Eng Comput 2008, 46:1263-1270.
36. Lai C.H., Chen S.C., Chiu L.H., Yang C.B., Tsai Y.H., Zuo C.S., Chang W.H., Lai W.F. Effects of low-intensity pulsed ultrasound, dexamethasone/TGF-beta1 and/or BMP-2 on the transcriptional expression of genes in human mesenchymal stem cells: Chondrogenic vs. osteogenic differentiation. Ultrasound Med Biol 2010, 36:1022-1033.
37. Lauffenburger D.A., Horwitz A.F. Cell migration: A physically integrated molecular process. Cell 1996, 84:359-369.
38. Lee H.J., Choi B.H., Min B.H., Son Y.S., Park S.R. Low-intensity ultrasound stimulation enhances chondrogenic differentiation in alginate culture of mesenchymal stem cells. Artifi Organs 2006, 30:707-715.
39. Lim S.T., Longley R.L., Couchman J.R., Woods A. Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha. JBiol Chem 2003, 278:13795-13802.
40. Martin J.A., Buckwalter J.A. Aging, articular cartilage chondrocyte senescence and osteoarthritis. Biogerontology 2002, 3:257-264.
41. Martin J.A., Buckwalter J.A. The role of chondrocyte senescence in the pathogenesis of osteoarthritis and in limiting cartilage repair. JBone Joint Surg Am 2003, 85(Suppl 2):106-110.
42. Martin J.A., McCabe D., Walter M., Buckwalter J.A., McKinley T.O. N-Acetylcysteine inhibits post-impact chondrocyte death in osteochondral explants. JBone Joint Surg Am 2009, 91:1890-1897.
43. Merlot S., Firtel R.A. Leading the way: directional sensing through phosphatidylinositol 3-kinase and other signaling pathways. JCell Sci 2003, 116:3471-3478.
44. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: In command and control of cell motility. Nat Rev Mol Cell Biol 2005, 6:56-68.
45. Mofrad M.R., Golji J., Abdul Rahim N.A., Kamm R.D. Force-induced unfolding of the focal adhesion targeting domain and the influence of paxillin binding. Mech Chem Biosyst 2004, 1:253-265.
46. Naito K., Watari T., Muta T., Furuhata A., Iwase H., Igarashi M., Kurosawa H., Nagaoka I., Kaneko K. Low-intensity pulsed ultrasound (LIPUS) increases the articular cartilage type II collagen in a rat osteoarthritis model. JOrthop Res 2010, 28:361-369.
47. Ogurtan Z., Celik I., Izci C., Boydak M., Alkan F., Yilmaz K. Effect of experimental therapeutic ultrasound on the distal antebrachial growth plates in one-month-old rabbits. Vet J 2002, 164:280-287.
48. Palumbo R., De Marchis F., Pusterla T., Conti A., Alessio M., Bianchi M.E. Src family kinases are necessary for cell migration induced by extracellular HMGB1. JLeukoc Biol 2009, 86:617-623.
49. Park S.R., Choi B.H., Min B.H. Low-intensity ultrasound (LIUS) as an innovative tool for chondrogenesis of mesenchymal stem cells (MSCs). Organogenesis 2007, 3:74-78.
50. Parsons J.T. Focal adhesion kinase: The first ten years. JCell Sci 2003, 116:1409-1416.
51. Parsons J.T., Martin K.H., Slack J.K., Taylor J.M., Weed S.A. Focal adhesion kinase: A regulator of focal adhesion dynamics and cell movement. Oncogene 2000, 19:5606-5613.
52. Parvizi J., Wu C.C., Lewallen D.G., Greenleaf J.F., Bolander M.E. Low-intensity ultrasound stimulates proteoglycan synthesis in rat chondrocytes by increasing aggrecan gene expression. JOrthop Res 1999, 17:488-494.
53. Petit V., Thiery J.P. Focal adhesions: Structure and dynamics. Biol Cell 2000, 92:477-494.
54. Preston R.C. Measurement and characterisation of the acoustic output of medical ultrasonic equipment. Part 2. Med Biol Eng Comput 1986, 24:225-234.
55. Sanchez-Bailon M.P., Calcabrini A., Gomez-Dominguez D., Morte B., Martin-Forero E., Gomez-Lopez G., Molinari A., Wagner K.U., Martin-Perez J. Src kinases catalytic activity regulates proliferation, migration and invasiveness of MDA-MB-231 breast cancer cells. Cell Signal 2012, 24:1276-1286.
56. Santos H.M., Lodeiro C., Capelo-Martínez J.L. The power of ultrasound. Ultrasound in Chemistry: Analytical Applications 2009, Wiley, New York. Capelo-Martínez (Ed.).
57. Sauter E., Buckwalter J.A., McKinley T.O., Martin J.A. Cytoskeletal dissolution blocks oxidant release and cell death in injured cartilage. JOrthop Res 2012, 30:593-598.
58. Schaller M.D. Cellular functions of FAK kinases: Insight into molecular mechanisms and novel functions. JCell Sci 2010, 123:1007-1013.
59. Schumann D., Kujat R., Zellner J., Angele M.K., Nerlich M., Mayr E., Angele P. Treatment of human mesenchymal stem cells with pulsed low intensity ultrasound enhances the chondrogenic phenotype invitro. Biorheology 2006, 43:431-443.
60. Seol D., McCabe D.J., Choe H., Zheng H., Yu Y., Jang K., Walter M.W., Lehman A.D., Ding L., Buckwalter J.A., Martin J.A. Chondrogenic progenitor cells respond to cartilage injury. Arthritis Rheum 2012, 64:3626-3637.
61. Sieg D.J., Hauck C.R., Ilic D., Klingbeil C.K., Schaefer E., Damsky C.H., Schlaepfer D.D. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2000, 2:249-256.
62. Sieg D.J., Hauck C.R., Schlaepfer D.D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. JCell Sci 1999, 112(Pt 16):2677-2691.
63. Ter Haar G. Ultrasound bioeffects and safety. Proc Inst Mech Eng H 2010, 224:363-373.
64. Zeqiri B., Bickley C.J. Anew anechoic material for medical ultrasonic applications. Ultrasound Med Biol 2000, 26:481-485.
65. Zhang Z.J., Huckle J., Francomano C.A., Spencer R.G. The influence of pulsed low-intensity ultrasound on matrix production of chondrocytes at different stages of differentiation: an explant study. Ultrasound Med Biol 2002, 28:1547-1553.
66. Zhang Z.J., Huckle J., Francomano C.A., Spencer R.G. The effects of pulsed low-intensity ultrasound on chondrocyte viability, proliferation, gene expression and matrix production. Ultrasound Med Biol 2003, 29:1645-1651.
67. Zhao X., Guan J.L. Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv Drug Deliv Rev 2011, 63:610-615.
68. Zhou S.X., Schmelz A., Seufferlein T., Li Y.P., Zhao J.S., Bachem M.G. Molecular mechanisms of low intensity pulsed ultrasound in human skin fibroblasts. JBiol Chem 2004, 279:54463-54469.