Osteogenic differentiation of rat bone marrow stromal cells by various intensities of low-intensity pulsed ultrasound

Ultrasonics

Volumn 51, Issue 3, 2011, Pages 281-288

  Angle, S R ^a,b   Sena, K ^a   Sumner, D R ^a,b   Virdi, A S ^a,b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b University of Illinois at Chicago   (United States)

Author keywords

Bone marrow derived stromal cells; Fracture healing; Low intensity pulsed ultrasound; Osteogenesis

Indexed keywords

ALKALINE PHOSPHATASE ACTIVITY; BONE CELLS; BONE GROWTH; BONE HEALING; BONE MARROW DERIVED STROMAL CELLS; BONE REGENERATION; CELL ACTIVATION; CLINICAL THERAPY; CLINICAL USE; FRACTURE HEALING; IN-CELL; IN-VIVO; INTRACELLULAR SIGNALING PATHWAYS; LOW-INTENSITY PULSED ULTRASOUND; MECHANICAL SIGNALS; OSTEOBLAST DIFFERENTIATION; OSTEOGENESIS; OSTEOGENIC CELLS; OSTEOGENIC DIFFERENTIATION; PHENOTYPIC RESPONSE; POSITIVE EFFECTS; RAT BONE MARROW; SOFT TISSUE; TARGET SITES;

BIOMINERALIZATION; BONE; CELLS; FRACTURE; MINERALOGY; PHOSPHATASES; REPAIR; ULTRASONICS;

CYTOLOGY;

ALKALINE PHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ANIMAL; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; ENZYMOLOGY; EQUIPMENT DESIGN; MALE; METABOLISM; METHODOLOGY; NONPARAMETRIC TEST; PHOSPHORYLATION; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; STROMA CELL; TRANSDUCER; ULTRASOUND THERAPY; WESTERN BLOTTING;

ALKALINE PHOSPHATASE; ANIMALS; BLOTTING, WESTERN; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; EQUIPMENT DESIGN; MALE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; OSTEOGENESIS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; STROMAL CELLS; TRANSDUCERS; ULTRASONIC THERAPY;

EID: 78650953490     PISSN: 0041624X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ultras.2010.09.004     Document Type: Article

References (71)

1. M.E. Bolander Regulation of fracture repair by growth factors Proc. Soc. Exp. Biol. Med. 200 1992 165 170
2. M. Hadjiargyrou, K. McLeod, J.P. Ryaby, and C. Rubin Enhancement of fracture healing by low intensity ultrasound Clin. Orthop. 355 Suppl 1998 216 229
3. S.D. Cook, J.P. Ryaby, J. McCabe, J.J. Frey, J.D. Heckman, and T.K. Kristiansen Acceleration of tibia and distal radius fracture healing in patients who smoke Clin. Orthop. 337 1997 198 207
4. L.R. Duarte The stimulation of bone growth by ultrasound Arch. Orthop. Trauma Surg. 101 1983 153 159
5. J.D. Heckman, J.P. Ryaby, J. McCabe, J.J. Frey, and R.F. Kilcoyne Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound J. Bone Joint Surg. 76A 1994 26 34
6. W. Klug, W.G. Franke, and H.G. Knoch Scintigraphic control of bone-fracture healing under ultrasonic stimulation: an animal experimental study Eur. J. Nucl. Med. 11 1986 494 497
7. T.K. Kristiansen, J.P. Ryaby, J. McCabe, J.J. Frey, and L.R. Roe Accelerated healing of distal radial fractures with the use of specific, low-intensity ultrasound. A multicenter, prospective, randomized, double-blind, placebo-controlled study J. Bone Joint Surg. 79A 1997 961 973
8. S. Takikawa, N. Matsui, T. Kokubu, M. Tsunoda, H. Fujioka, K. Mizuno, and Y. Azuma Low-intensity pulsed ultrasound initiates bone healing in rat nonunion fracture model J. Ultrasound Med. 20 2001 197 205
9. M. Tanzer, E. Harvey, A. Kay, P. Morton, and J.D. Bobyn Effect of noninvasive low intensity ultrasound on bone growth into porous-coated implants J. Orthop. Res. 14 1996 901 906
10. A. Maddi, H. Hai, S.T. Ong, L. Sharp, M. Harris, and S. Meghji Long wave ultrasound may enhance bone regeneration by altering OPG/RANKL ratio in human osteoblast-like cells Bone 39 2006 283 288
11. K. Naruse, Y. Mikuni-Takagaki, Y. Azuma, M. Ito, T. Oota, K. Kameyama, and M. Itoman Anabolic response of mouse bone-marrow-derived stromal cell clone ST2 cells to low-intensity pulsed ultrasound Biochem. Biophys. Res. Commun. 268 2000 216 220
12. K. Sena, R.M. Leven, K. Mazhar, D.R. Sumner, and A.S. Virdi Early gene response to low-intensity pulsed ultrasound in rat osteoblastic cells Ultrasound Med. Biol. 31 2005 703 708
13. S.J. Warden, J.M. Favaloro, K.L. Bennell, J.M. McMeeken, K.W. Ng, J.D. Zajac, and J.D. Wark Low-intensity pulsed ultrasound stimulates a bone-forming response in UMR-106 cells Biochem. Biophys. Res. Commun. 286 2001 443 450
14. T. Takayama, N. Suzuki, K. Ikeda, T. Shimada, A. Suzuki, M. Maeno, K. Otsuka, and K. Ito Low-intensity pulsed ultrasound stimulates osteogenic differentiation in ROS 17/2.8 cells Life Sci. 80 2007 965 971
15. Y. Azuma, M. Ito, Y. Harada, H. Takagi, T. Ohta, and S. Jingushi Low-intensity pulsed ultrasound accelerates rat femoral fracture healing by acting on the various cellular reactions in the fracture callus J. Bone Miner. Res. 16 2001 671 680
16. R.L. Juliano, and S. Haskill Signal transduction from the extracellular matrix J. Cell Biol. 120 1993 577 585
17. A.J. Maniotis, C.S. Chen, and D.E. Ingber Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure Proc. Natl. Acad. Sci. USA 94 1997 849 854
18. J.H. Wang, and B.P. Thampatty An introductory review of cell mechanobiology Biomech. Model. Mechanobiol. 5 2006 1 16
19. M. Hadjiargyrou, K. McLeod, J.P. Ryaby, and C. Rubin Enhancement of fracture healing by low intensity ultrasound Clin. Orthop. 355 Suppl 1998 S216 S229
20. K.-H. Yang, J. Parvizi, S.-J. Wang, D.G. Lewallen, R.R. Kinnick, J.F. Greenleaf, and M.E. Bolander Exposure to low-intensity ultrasound increases aggrecan gene expression in a rat femur fracture model J. Orthop. Res. 14 1996 802 809
21. J.S. Sun, R.C. Hong, W.H. Chang, L.T. Chen, F.H. Lin, and H.C. Liu In vitro effects of low-intensity ultrasound stimulation on the bone cells J. Biomed. Mater. Res. 57 2001 449 456
22. P.A. Nolte, A. van der Krans, P. Patka, I.M. Janssen, J.P. Ryaby, and G.H. Albers Low-intensity pulsed ultrasound in the treatment of nonunions J. Trauma-Injury Infect. Crit. Care 51 2001 693 702
23. D. Gebauer, E. Mayr, E. Orthner, and J.P. Ryaby Low-intensity pulsed ultrasound: effects on nonunions Ultrasound Med. Biol. 31 2005 1391 1402
24. W. Sato, T. Matsushita, and K. Nakamura Acceleration of increase in bone mineral content by low-intensity ultrasound energy in leg lengthening J. Ultrasound Med. 18 1999 699 702
25. A. Shimazaki, K. Inui, Y. Azuma, N. Nishimura, and Y. Yamano Low-intensity pulsed ultrasound accelerates bone maturation in distraction osteogenesis in rabbits J. Bone Joint Surg. 82 2000 1077 1082
26. M.G. Uglow, R.A. Peat, M.S. Hile, L.E. Bilston, E.J. Smith, and D.G. Little Low-intensity ultrasound stimulation in distraction osteogenesis in rabbits Clin. Orthop. 2003 303 312
27. Z.J. Zhang, J. Huckle, C.A. Francomano, and R.G. Spencer The effects of pulsed low, intensity ultrasound on chondrocyte viability, proliferation, gene expression and matrix production Ultrasound Med. Biol. 29 2003 1645 1651
28. S.B. Barnett, H.D. Rott, G.R. ter Haar, M.C. Ziskin, and K. Maeda The sensitivity of biological tissue to ultrasound Ultrasound Med. Biol. 23 1997 805 812
29. K. Naruse, K. Urabe, T. Mukaida, T. Ueno, F. Migishima, A. Oikawa, Y. Mikuni-Takagaki, and M. Itoman Spontaneous differentiation of mesenchymal stem cells obtained from fetal rat circulation Bone 35 2004 850 858
30. E. Sant'Anna, R.M. Leven, A.S. Virdi, and D.R. Sumner Effect of combined ultrasound and BMP-2 stimulation on rat bone marrow stromal cell gene expression J. Orthop. Res. 23 2005 646 652
31. S.M. McCormick, V. Saini, Y. Yazicioglu, Z.N. Demou, and T.J. Royston Interdependence of pulsed ultrasound and shear stress effects on cell morphology and gene expression Ann. Biomed. Eng. 34 2006 436 445
32. M. Saito, K. Fujii, T. Tanaka, and S. Soshi Effect of low- and high-intensity pulsed ultrasound on collagen post-translational modifications in MC3T3-E1 osteoblasts Calcif. Tissue Int. 75 2004 384 395
33. Z.J. Zhang, J. Huckle, C.A. Francomano, and R.G. Spencer The effects of pulsed low-intensity ultrasound on chondrocyte viability, proliferation, gene expression and matrix production Ultrasound Med. Biol. 29 2003 1645 1651
34. T. Iwashina, J. Mochida, T. Miyazaki, T. Watanabe, S. Iwabuchi, K. Ando, T. Hotta, and D. Sakai Low-intensity pulsed ultrasound stimulates cell proliferation and proteoglycan production in rabbit intervertebral disc cells cultured in alginate Biomaterials 27 2006 354 361
35. N. Heybeli, A. Yesildag, O. Oyar, U.K. Gulsoy, M.A. Tekinsoy, and E.F. Mumcu Diagnostic ultrasound treatment increases the bone fracture-healing rate in an internally fixed rat femoral osteotomy model J. Ultrasound Med. 21 2002 1357 1363
36. J. Harle, V. Salih, F. Mayia, J.C. Knowles, and I. Olsen Effects of ultrasound on the growth and function of bone and periodontal ligament cells in vitro Ultrasound Med. Biol. 27 2001 579 586
37. O. Traub, and B.C. Berk Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force Arterioscler. Thromb. Vasc. Biol. 18 1998 677 685
38. P. Dent, A. Yacoub, P.B. Fisher, M.P. Hagan, and S. Grant MAPK pathways in radiation responses Oncogene 22 2003 5885 5896
39. S. Wadhwa, S. Choudhary, M. Voznesensky, M. Epstein, L. Raisz, and C. Pilbeam Fluid flow induces COX-2 expression in MC3T3-E1 osteoblasts via a PKA signaling pathway Biochem. Biophys. Res. Commun. 297 2002 46 51
40. J. Gebken, B. Luders, H. Notbohm, H.H. Klein, J. Brinckmann, P.K. Muller, and B. Batge Hypergravity stimulates collagen synthesis in human osteoblast-like cells: evidence for the involvement of p44/42 MAP-kinases (ERK 1/2) J. Biochem. 126 1999 676 682
41. S. Zhou, A. Schmelz, T. Seufferlein, Y. Li, J. Zhao, and M.G. Bachem Molecular mechanisms of low intensity pulsed ultrasound in human skin fibroblasts J. Biol. Chem. 279 2004 54463 54469
42. G.S. Stein, and J.B. Lian Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype Endocr. Rev. 14 1993 424 442
43. N. Fratzl-Zelman, P. Fratzl, H. Horandner, B. Grabner, F. Varga, A. Ellinger, and K. Klaushofer Matrix mineralization in MC3T3-E1 cell cultures initiated by beta-glycerophosphate pulse Bone 23 1998 511 520
44. K. Ikeda, T. Takayama, N. Suzuki, K. Shimada, K. Otsuka, and K. Ito Effects of low-intensity pulsed ultrasound on the differentiation of C2C12 cells Life Sci. 79 2006 1936 1943
45. D.J. Rickard, T.A. Sullivan, B.J. Shenker, P.S. Leboy, and I. Kazhdan Induction of rapid osteoblast differentiation in rat bone marrow stromal cell cultures by dexamethasone and BMP-2 Dev. Biol. 161 1994 218 228
46. J.E. Aubin, F. Liu, L. Malaval, and A.K. Gupta Osteoblast and chrondroblast differentiation Bone 17 1995 77S 83S
47. F. Liu, L. Malaval, and J.E. Aubin Global amplification polymerase chain reaction reveals novel transitional stages during osteoprogenitor differentiation J. Cell Sci. 116 2003 1787 1796
48. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
49. C.G. Bellows, J.E. Aubin, and J.N. Heersche Initiation and progression of mineralization of bone nodules formed in vitro: the role of alkaline phosphatase and organic phosphate Bone Miner. 14 1991 27 40
50. B. Ecarot-Charrier, F.H. Glorieux, R.M. van der, and G. Pereira Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture J. Cell Biol. 96 1983 639 643
51. H.C. Tenenbaum, Role of organic phosphate in mineralization of bone in vitro, J. Dent. Res. 60 Spec No. C (1981) 1586-1589.
52. K. Ibaraki, J.D. Termine, S.W. Whitson, and M.F. Young Bone matrix mRNA expression in differentiating fetal bovine osteoblasts J. Bone Miner. Res. 7 1992 743 754
53. A. Nanci, S. Zalzal, Y. Gotoh, and M.D. McKee Ultrastructural characterization and immunolocalization of osteopontin in rat calvarial osteoblast primary cultures Microsc. Res. Tech. 33 1996 214 231
54. N.H. Heng, P.D. N'Guessan, B.M. Kleber, J.P. Bernimoulin, and N. Pischon Enamel matrix derivative induces connective tissue growth factor expression in human osteoblastic cells J. Periodontol. 78 2007 2369 2379
55. X. Guo, J.E. Gough, P. Xiao, J. Liu, and Z. Shen Fabrication of nanostructured hydroxyapatite and analysis of human osteoblastic cellular response J. Biomed. Mater. Res. A 82 2007 1022 1032 (Pubitemid 47312918)
56. C.A. Gregory, W.G. Gunn, A. Peister, and D.J. Prockop An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction Anal. Biochem. 329 2004 77 84
57. R.K. Jaiswal, N. Jaiswal, S.P. Bruder, G. Mbalaviele, D.R. Marshak, and M.F. Pittenger Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase J. Biol. Chem. 275 2000 9645 9652
58. K.J. Cowan, and K.B. Storey Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress J. Exp. Biol. 206 2003 1107 1115
59. Y. Hu, E. Chan, S.X. Wang, and B. Li Activation of p38 mitogen-activated protein kinase is required for osteoblast differentiation Endocrinology 144 2003 2068 2074
60. J.M. Kyriakis, and J. Avruch Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation Physiol. Rev. 81 2001 807 869
61. N. Matsuda, N. Morita, K. Matsuda, and M. Watanabe Proliferation and differentiation of human osteoblastic cells associated with differential activation of MAP kinases in response to epidermal growth factor, hypoxia, and mechanical stress in vitro Biochem. Biophys. Res. Commun. 249 1998 350 354
62. K. Bandow, Y. Nishikawa, T. Ohnishi, K. Kakimoto, K. Soejima, S. Iwabuchi, K. Kuroe, and T. Matsuguchi Low-intensity pulsed ultrasound (LIPUS) induces RANKL, MCP-1, and MIP-1beta expression in osteoblasts through the angiotensin II type 1 receptor J. Cell Physiol. 211 2007 392 398
63. K. Bandow, Y. Nishikawa, T. Ohnishi, K. Kakimoto, K. Soejima, S. Iwabuchi, K. Kuroe, and T. Matsuguchi Low-intensity pulsed ultrasound (LIPUS) induces RANKL, MCP-1, and MIP-1 beta expression in osteoblasts through the angiotensin II type 1 receptor J. Cell Physiol. 211 2007 392 398
64. M. Caivano, and P. Cohen Role of mitogen-activated protein kinase cascades in mediating lipopolysaccharide-stimulated induction of cyclooxygenase-2 and IL-1 beta in RAW264 macrophages J. Immunol. 164 2000 3018 3025
65. J.L. Dean, M. Brook, A.R. Clark, and J. Saklatvala p38 mitogen-activated protein kinase regulates cyclooxygenase-2 mRNA stability and transcription in lipopolysaccharide-treated human monocytes J. Biol. Chem. 274 1999 264 269
66. K. Subbaramaiah, J.C. Hart, L. Norton, and A.J. Dannenberg Microtubule-interfering agents stimulate the transcription of cyclooxygenase-2. Evidence for involvement of ERK1/2 AND p38 mitogen-activated protein kinase pathways J. Biol. Chem. 275 2000 14838 14845
67. M. Murakami, H. Naraba, T. Tanioka, N. Semmyo, Y. Nakatani, F. Kojima, T. Ikeda, M. Fueki, A. Ueno, S. Oh, and I. Kudo Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2 J. Biol. Chem. 275 2000 32783 32792
68. L.G. Raisz, C.C. Pilbeam, and P.M. Fall Prostaglandins: mechanisms of action and regulation of production in bone Osteoporos. Int. 3 Suppl. 1 1993 136 140
69. F. Ushikubi, E. Segi, Y. Sugimoto, T. Murata, T. Matsuoka, T. Kobayashi, H. Hizaki, K. Tuboi, M. Katsuyama, A. Ichikawa, T. Tanaka, N. Yoshida, and S. Narumiya Impaired febrile response in mice lacking the prostaglandin E receptor subtype EP3 Nature 395 1998 281 284
70. J. Unsworth, S. Kaneez, S. Harris, J. Ridgway, S. Fenwick, D. Chenery, and A. Harrison Pulsed low intensity ultrasound enhances mineralisation in preosteoblast cells Ultrasound Med. Biol. 33 2007 1468 1474
71. C.H. Tang, R.S. Yang, T.H. Huang, D.Y. Lu, W.J. Chuang, T.F. Huang, and W.M. Fu Ultrasound stimulates cyclooxygenase-2 expression and increases bone formation through integrin, focal adhesion kinase, phosphatidylinositol 3-kinase, and Akt pathway in osteoblasts Mol. Pharmacol. 69 2006 2047 2057