Low intensity pulsed ultrasound (LIPUS) influences the multilineage differentiation of mesenchymal stem and progenitor cell lines through ROCK-Cot/Tpl2-MEK-ERK signaling pathway

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10330-10344

  Kusuyama, Joji ^a   Bandow, Kenjiro ^a   Shamoto, Mitsuo ^a   Kakimoto, Kyoko ^a   Ohnishi, Tomokazu ^a   Matsuguchi, Tetsuya ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMINERALIZATION; ENZYMES; FLOWCHARTING; GENE EXPRESSION; OSTEOBLASTS; PHOSPHORYLATION; PIGMENTS; PROTEINS; ULTRASONICS;

ADIPOGENIC DIFFERENTIATIONS; EXTRACELLULAR SIGNALS; FATTY ACID-BINDING PROTEINS; LOW-INTENSITY PULSED ULTRASOUND; MESENCHYMAL STEM CELL; OSTEOGENIC DIFFERENTIATION; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; TRANSCRIPTIONAL ACTIVITY;

CELL CULTURE;

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; FAT DROPLET; FATTY ACID BINDING PROTEIN 4; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; OSTEOCALCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE; RHO KINASE; TPL2 KINASE INHIBITOR; TRANSCRIPTION FACTOR RUNX2; TUMOR PROGRESSION LOCUS 2 KINASE; UNCLASSIFIED DRUG;

ADIPOGENESIS; ADIPOGENIC PROGENITOR CELL; ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL LINE; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; FABP4 GENE; GENE; GENE EXPRESSION; GENE INDUCTION; LOW INTENSITY PULSED ULTRASOUND; MECHANICAL STIMULATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PPARG2 GENE; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RUNX2 GENE; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION INITIATION; ULTRASOUND THERAPY;

ADIPOGENESIS; CELL DIFFERENTIATION; LIPUS; MAP KINASES (MAPKS); MECHANOTRANSDUCTION; MESENCHYMAL STEM CELLS; OSTEOGENESIS;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; ANTHRAQUINONES; AZO COMPOUNDS; CELL DIFFERENTIATION; CELL LINEAGE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FRACTURE HEALING; MAP KINASE KINASE KINASES; MESENCHYMAL STROMAL CELLS; MICE; OSTEOGENESIS; OSTEOPOROSIS; PROTO-ONCOGENE PROTEINS; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STEM CELLS; ULTRASONICS;

EID: 84898645115     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.546382     Document Type: Article

References (72)

1. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., and Marshak, D. R. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147
2. Verma, S., Rajaratnam, J. H., Denton, J., Hoyland, J. A., and Byers, R. J. (2002) Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J. Clin. Pathol. 55, 693-698
3. Nuttall, M. E., Patton, A. J., Olivera, D. L., Nadeau, D. P., and Gowen, M. (1998) Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders. J. Bone Miner. Res. 13, 371-382
4. Qiu, W., Andersen, T. E., Bollerslev, J., Mandrup, S., Abdallah, B. M., and Kassem, M. (2007) Patients with high bone mass phenotype exhibit enhanced osteoblast differentiation and inhibition of adipogenesis of human mesenchymal stem cells. J. Bone Miner. Res. 22, 1720-1731
5. Wan, Y. (2010) PPAR γ in bone homeostasis. Trends Endocrinol. Metab. 21, 722-728
6. Ji, H., Liu, Y., Zhao, X., and Zhang, M. (2011) N-Acetyl-L-cysteine enhances the osteogenic differentiation and inhibits the adipogenic differentiation through up regulation of Wnt 5a and down regulation of PPARG in bone marrow stromal cells. Biomed. Pharmacother. 65, 369-374
7. Komori, T. (2010) Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res. 339, 189-195
8. Hughes-Fulford, M. (2004) Signal transduction and mechanical stress. Sci. STKE 2004, RE12
9. Romano, C. L., Romano, D., and Logoluso, N. (2009) Low-intensity pulsed ultrasound for the treatment of bone delayed union or nonunion: a review. Ultrasound Med. Biol. 35, 529-536
10. Naruse, K., Miyauchi, A., Itoman, M., and Mikuni-Takagaki, Y. (2003) Distinct anabolic response of osteoblast to low-intensity pulsed ultrasound. J. Bone Miner. Res. 18, 360-369
11. Bandow, K., Nishikawa, Y., Ohnishi, T., Kakimoto, K., Soejima, K., Iwabuchi, S., Kuroe, K., and Matsuguchi, T. (2007) Low-intensity pulsed ultrasound (LIPUS) induces RANKL, MCP-1, and MIP-1β expression in osteoblasts through the angiotensin II type 1 receptor. J. Cell. Physiol. 211, 392-398
12. Bielby, R., Jones, E., and McGonagle, D. (2007) The role of mesenchymal stem cells in maintenance and repair of bone. Injury 38, Suppl. 1, S26-S32
13. Widmann, C., Gibson, S., Jarpe, M. B., and Johnson, G. L. (1999) Mitogenactivated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79, 143-180
14. Papachristou, D. J., Papachroni, K. K., Basdra, E. K., and Papavassiliou, A. G. (2009) Signaling networks and transcription factors regulating mechanotransduction in bone. BioEssays 31, 794-804
15. de Gusmão, C. V., Pauli, J. R., Saad, M. J., Alves, J. M., and Belangero, W. D. (2010) Low-intensity ultrasound increases FAK, ERK-1/2, and IRS-1 expression of intact rat bones in a noncumulative manner. Clin. Orthop. Relat. Res. 468, 1149-1156
16. Nakao, J., Fujii, Y., Kusuyama, J., Bandow, K., Kakimoto, K., Ohnishi, T., and Matsuguchi, T. (2014) Low-intensity pulsed ultrasound (LIPUS) inhibits LPS-induced inflammatory responses of osteoblasts through TLR4- MyD88 dissociation. Bone 58, 17-25
17. Bandow, K., Maeda, A., Kakimoto, K., Kusuyama, J., Shamoto, M., Ohnishi, T., and Matsuguchi, T. (2010) Molecular mechanisms of the inhibitory effect of lipopolysaccharide (LPS) on osteoblast differentiation. Biochem. Biophys. Res. Commun. 402, 755-761
18. Sugimoto, K., Ohata, M., Miyoshi, J., Ishizaki, H., Tsuboi, N., Masuda, A., Yoshikai, Y., Takamoto, M., Sugane, K., Matsuo, S., Shimada, Y., and Matsuguchi, T. (2004) A serine/threonine kinase, Cot/Tpl2, modulates bacterial DNA-induced IL-12 production and Th cell differentiation. J. Clin. Investig. 114, 857-866
19. Bandow, K., Kusuyama, J., Shamoto, M., Kakimoto, K., Ohnishi, T., and Matsuguchi, T. (2012) LPS-induced chemokine expression in both MyD88-dependent and -independent manners is regulated by Cot/Tpl2- ERK axis in macrophages. FEBS Lett. 586, 1540-1546
20. Chiba, N., Kakimoto, K., Masuda, A., and Matsuguchi, T. (2010) Functional roles of Cot/Tpl2 in mast cell responses to lipopolysaccharide and Fc βRI-clustering. Biochem. Biophys. Res. Commun. 402, 1-6
21. Dumitru, C. D., Ceci, J. D., Tsatsanis, C., Kontoyiannis, D., Stamatakis, K., Lin, J. H., Patriotis, C., Jenkins, N. A., Copeland, N. G., Kollias, G., and Tsichlis, P. N. (2000) TNF-α induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103, 1071-1083
22. Mammoto, A., and Ingber, D. E. (2009) Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 21, 864-870
23. Amano, M., Nakayama, M., and Kaibuchi, K. (2010) Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton 67, 545-554
24. van Beekum, O., Fleskens, V., and Kalkhoven, E. (2009) Posttranslational modifications of PPAR-γ: fine-tuning the metabolic master regulator. Obesity 17, 213-219
25. Taylor, S. M., and Jones, P. A. (1979) Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17, 771-779
26. Muruganandan, S., Roman, A. A., and Sinal, C. J. (2009) Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program. Cell. Mol. Life Sci. 66, 236-253
27. Papachroni, K. K., Karatzas, D. N., Papavassiliou, K. A., Basdra, E. K., and Papavassiliou, A. G. (2009) Mechanotransduction in osteoblast regulation and bone disease. Trends Mol. Med. 15, 208-216
28. Saito, M., Soshi, S., Tanaka, T., and Fujii, K. (2004) Intensity-related differences in collagen post-translational modification in MC3T3-E1 osteoblasts after exposure to low- and high-intensity pulsed ultrasound. Bone 35, 644-655
29. Sena, K., Leven, R. M., Mazhar, K., Sumner, D. R., and Virdi, A. S. (2005) Early gene response to low-intensity pulsed ultrasound in rat osteoblastic cells. Ultrasound Med. Biol. 31, 703-708
30. Hauser, J., Hauser, M., Muhr, G., and Esenwein, S. (2009) Ultrasoundinduced modifications of cytoskeletal components in osteoblast-like SAOS-2 cells. J. Orthop. Res. 27, 286-294
31. 1 integrin and PI3K/Akt signaling pathways in mandibular osteoblasts. Exp. Cell Res. 317, 2642-2649
32. Naveiras, O., Nardi, V., Wenzel, P. L., Hauschka, P. V., Fahey, F., and Daley, G. Q. (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460, 259-263
33. Kirkland, J. L., Tchkonia, T., Pirtskhalava, T., Han, J., and Karagiannides, I. (2002) Adipogenesis and aging: does aging make fat go MAD? Exp. Gerontol. 37, 757-767
34. Wronski, T. J., and Morey, E. R. (1982) Skeletal abnormalities in rats induced by simulated weightlessness. Metab. Bone Dis. Relat. Res. 4, 69-75
35. Christodoulides, C., Lagathu, C., Sethi, J. K., and Vidal-Puig, A. (2009) Adipogenesis and WNT signalling. Trends Endocrinol. Metab. 20, 16-24
36. Tontonoz, P., Hu, E., and Spiegelman, B. M. (1994) Stimulation of adipogenesis in fibroblasts by PPAR γ2, a lipid-activated transcription factor. Cell 79, 1147-1156
37. Spiegelman, B. M. (1998) PPAR-γ: adipogenic regulator and thiazolidinedione receptor. Diabetes 47, 507-514
38. Tontonoz, P., Hu, E., Graves, R. A., Budavari, A. I., and Spiegelman, B. M. (1994) mPPARγ2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8, 1224-1234
39. Tontonoz, P., Graves, R. A., Budavari, A. I., Erdjument-Bromage, H., Lui, M., Hu, E., Tempst, P., and Spiegelman, B. M. (1994) Adipocyte-specific transcription factor ARF6 is a heterodimeric complex of two nuclear hormone receptors, PPARγ and RXRα. Nucleic Acids Res. 22, 5628-5634
40. Vidal-Puig, A. J., Considine, R. V., Jimenez-Liñan, M., Werman, A., Pories, W. J., Caro, J. F., and Flier, J. S. (1997) Peroxisome proliferator-activated receptor gene expression in human tissues. Effects of obesity, weight loss, and regulation by insulin and glucocorticoids. J. Clin. Investig. 99, 2416-2422
41. Luconi, M., Cantini, G., and Serio, M. (2010) Peroxisome proliferatoractivated receptor γ (PPARγ): is the genomic activity the only answer? Steroids 75, 585-594
42. Hu, E., Kim, J. B., Sarraf, P., and Spiegelman, B. M. (1996) Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARγ. Science 274, 2100-2103
43. Adams, M., Reginato, M. J., Shao, D., Lazar, M. A., and Chatterjee, V. K. (1997) Transcriptional activation by peroxisome proliferator-activated receptor γ is inhibited by phosphorylation at a consensus mitogen-activated protein kinase site. J. Biol. Chem. 272, 5128-5132
44. Diradourian, C., Girard, J., and Pégorier, J. P. (2005) Phosphorylation of PPARs: from molecular characterization to physiological relevance. Biochimie 87, 33-38
45. Komori, T. (2006) Regulation of osteoblast differentiation by transcription factors. J. Cell. Biochem. 99, 1233-1239
46. Hong, J. H., Hwang, E. S., McManus, M. T., Amsterdam, A., Tian, Y., Kalmukova, R., Mueller, E., Benjamin, T., Spiegelman, B. M., Sharp, P. A., Hopkins, N., and Yaffe, M. B. (2005) TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309, 1074-1078
47. Calo, E., Quintero-Estades, J. A., Danielian, P. S., Nedelcu, S., Berman, S. D., and Lees, J. A. (2010) Rb regulates fate choice and lineage commitment in vivo. Nature 466, 1110-1114
48. Nishikawa, K., Nakashima, T., Takeda, S., Isogai, M., Hamada, M., Kimura, A., Kodama, T., Yamaguchi, A., Owen, M. J., Takahashi, S., and Takayanagi, H. (2010) Maf promotes osteoblast differentiation in mice by mediating the age-related switch in mesenchymal cell differentiation. J. Clin. Investig. 120, 3455-3465
49. Hu, E., Tontonoz, P., and Spiegelman, B. M. (1995) Transdifferentiation of myoblasts by the adipogenic transcription factors PPARγ and C/EBPα. Proc. Natl. Acad. Sci. U.S.A. 92, 9856-9860
50. Yin, J., Jin, X., Beck, S., Kang, D. H., Hong, Z., Li, Z., Jin, Y., Zhang, Q., Choi, Y. J., Kim, S. C., and Kim, H. (2010) In vitro myogenic and adipogenic differentiation model of genetically engineered bovine embryonic fibro- blast cell lines. Biotechnol. Lett. 32, 195-202
51. Miyaoka, Y., Tanaka, M., Naiki, T., and Miyajima, A. (2006) OncostatinM inhibits adipogenesis through the RAS/ERK and STAT5 signaling pathways. J. Biol. Chem. 281, 37913-37920
52. Than, A., Cheng, Y., Foh, L. C., Leow, M. K., Lim, S. C., Chuah, Y. J., Kang, Y., and Chen, P. (2012) Apelin inhibits adipogenesis and lipolysis through distinct molecular pathways. Mol. Cell. Endocrinol. 362, 227-241
53. Prusty, D., Park, B. H., Davis, K. E., and Farmer, S. R. (2002) Activation of MEK/ERK signaling promotes adipogenesis by enhancing peroxisome proliferator-activated receptor γ(PPARγ) and C/EBPα gene expression during the differentiation of 3T3-L1 preadipocytes. J. Biol. Chem. 277, 46226-46232
54. Bost, F., Caron, L., Marchetti, I., Dani, C., Le Marchand-Brustel, Y., and Binétruy, B. (2002) Retinoic acid activation of the ERK pathway is required for embryonic stem cell commitment into the adipocyte lineage. Biochem. J. 361, 621-627
55. Liedert, A., Kaspar, D., Blakytny, R., Claes, L., and Ignatius, A. (2006) Signal transduction pathways involved in mechanotransduction in bone cells. Biochem. Biophys. Res. Commun. 349, 1-5
56. Wang, B., Du, T., Wang, Y., Yang, C., Zhang, S., and Cao, X. (2011) Focal adhesion kinase signaling pathway is involved in mechanotransduction in MG-63 cells. Biochem. Biophys. Res. Commun. 410, 671-676
57. Hsu, H. J., Lee, C. F., Locke, A., Vanderzyl, S. Q., and Kaunas, R. (2010) Stretch-induced stress fiber remodeling and the activations of JNK and ERK depend on mechanical strain rate, but not FAK. PLoS One 5, e12470
58. Harris, I. S., Zhang, S., Treskov, I., Kovacs, A., Weinheimer, C., and Muslin, A. J. (2004) Raf-1 kinase is required for cardiac hypertrophy and cardiomyocyte survival in response to pressure overload. Circulation 110, 718-723
59. Kawamura, S., Miyamoto, S., and Brown, J. H. (2003) Initiation and transduction of stretch-induced RhoA and Rac1 activation through caveolae: cytoskeletal regulation of ERK translocation. J. Biol. Chem. 278, 31111-31117
60. Chao, J. T., and Davis, M. J. (2011) The roles of integrins in mediating the effects of mechanical force and growth factors on blood vessels in hypertension. Curr. Hypertens. Rep. 13, 421-429
61. Storch, U., Mederos y Schnitzler, M., and Gudermann, T. (2012) G protein- mediated stretch reception. Am. J. Physiol. Heart Circ. Physiol. 302, H1241-H1249
62. Puklin-Faucher, E., and Sheetz, M. P. (2009) The mechanical integrin cycle. J. Cell Sci. 122, 179-186
63. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K., and Chen, C. S. (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495
64. Rodríguez, J. P., González, M., Ríos, S., and Cambiazo, V. (2004) Cytoskeletal organization of human mesenchymal stem cells (MSC) changes during their osteogenic differentiation. J. Cell. Biochem. 93, 721-731
65. Liao, J. K., Seto, M., and Noma, K. (2007) Rho kinase (ROCK) inhibitors. J. Cardiovasc. Pharmacol. 50, 17-24
66. Amano, M., Fukata, Y., and Kaibuchi, K. (2000) Regulation and functions of Rho-associated kinase. Exp. Cell Res. 261, 44-51
67. Zhao, Y., Lv, M., Lin, H., Cui, Y., Wei, X., Qin, Y., Kohama, K., and Gao, Y. (2013) Rho-associated protein kinase isoforms stimulate proliferation of vascular smooth muscle cells through ERK and induction of cyclin D1 and PCNA. Biochem. Biophys. Res. Commun. 432, 488-493
68. Sarasa-Renedo, A., Tunç-Civelek, V., and Chiquet, M. (2006) Role of RhoA/ROCK-dependent actin contractility in the induction of tenascin-C by cyclic tensile strain. Exp. Cell Res. 312, 1361-1370
69. Chapados, R., Abe, K., Ihida-Stansbury, K., McKean, D., Gates, A. T., Kern, M., Merklinger, S., Elliott, J., Plant, A., Shimokawa, H., and Jones, P. L. (2006) ROCK controls matrix synthesis in vascular smooth muscle cells: coupling vasoconstriction to vascular remodeling. Circ. Res. 99, 837-844
70. Xu, B., Song, G., Ju, Y., Li, X., Song, Y., and Watanabe, S. (2012) RhoA/ ROCK, cytoskeletal dynamics, and focal adhesion kinase are required for mechanical stretch-induced tenogenic differentiation of human mesenchymal stem cells. J. Cell. Physiol. 227, 2722-2729
71. Appleton, C. T., Usmani, S. E., Mort, J. S., and Beier, F. (2010) Rho/ROCK and MEK/ERK activation by transforming growth factor-β induces articular cartilage degradation. Lab. Invest. 90, 20-30
72. Hodges, R. R., Guilbert, E., Shatos, M. A., Natarajan, V., and Dartt, D. A. (2011) Phospholipase D1, but not D2, regulates protein secretion via Rho/ ROCK in a Ras/Raf-independent, MEK-dependent manner in rat lacrimal gland. Invest. Ophthalmol. Vis. Sci. 52, 2199-2210