Advertisement

Mechanical Stretching and Signaling Pathways in Adipogenesis

  • Yoshiyuki TanabeEmail author
  • Maki Tanji Saito
  • Koichi Nakayama
Chapter
Part of the Studies in Mechanobiology, Tissue Engineering and Biomaterials book series (SMTEB, volume 16)

Abstract

Adipogenesis is a fundamental process to develop adipose tissues via commitment of mesenchymal stem cells (MSCs) to direction of preadipocytes and production of terminally differentiated lipid-laden adipocytes. While adipose tissues play important roles for energy and metabolic homeostasis in our body, dysregulated adiposities become considerable risk factors for various metabolic and cardiovascular diseases. In view of both preventive and therapeutic aspects, clinical interventions have been mostly directed at control of adiposity such as weight control by improved balance of calorie intake and energy expenditure. Physical exercise has been considered to be an effective approach to improve the systemic energy balance; however, the effects of locally generated mechanical stress on adipose tissues that are directly or indirectly accessible by the exercise and/or massage had remained obscure. It has now become apparent that stretching and other mechanical stimuli activate various cellular signals, including matrix elasticity/stiffness and cytoskeletal control, extracellular matrix–integrin interaction, the extracellular signal-regulated protein kinase/mitogen activated protein kinase (ERK/MAPK), Rho–Rho-kinase pathway, tension-induced/inhibited proteins (TIPs), the cyclooxygenase pathway, and Wnt signaling; all of them are involved in the mechanotransduction pathways and have a significant influence on adipogenesis. The stretching shows bidirectional effects of either inhibition or stimulation on adipogenesis that is presumably depending on the strength, duration, and timing of mechanical inputs, as well as cellular statuses of differentiation. The ERK/MAPK plays a crucial role in the bidirectional outcomes, and other coexisting signals adjust and determine the commitment and adipogenic statuses of MSCs and preadipocytes. These results imply that the mechanical stimulation would modulate the adipose tissue functions through the bidirectional control of adipocyte renewal, adiposity, endocrine function of adipocytes, and fine-tuning of drug actions.

Keywords

Adipose Tissue Mesenchymal Stem Cell Focal Adhesion Kinase Mechanical Stimulus Adipocyte Differentiation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors thank Paul Langman, Ph.D. for his critical comments, discussion and advice for this manuscript. This work was partly supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan (1996–1997, 1998–1999, 2005–2007, 2010–2012), a grant from the Shizuoka Research Institute (1999–2000), and Goto Research Grant of University of Shizuoka (2003–2004).

Competing financial interests

The authors declare no competing financial interests.

References

  1. 1.
    Gesta, S., Tseng, Y.H., Kahn, C.R.: Developmental origin of fat: tracking obesity to its source. Cell 131, 242–256 (2007)Google Scholar
  2. 2.
    Gregoire, F.M., Smas, C.M., Sul, H.S.: Understanding adipocyte differentiation. Physiol. Rev. 78, 783–809 (1998)Google Scholar
  3. 3.
    Cristancho, A.G., Lazar, M.A.: Forming functional fat: a growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol. 12, 722–734 (2011)Google Scholar
  4. 4.
    Rosen, E.D., MacDougald, O.A.: Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7, 885–896 (2006)Google Scholar
  5. 5.
    Tang, Q.Q., Lane, M.D.: Adipogenesis: from stem cell to adipocyte. Ann. Rev. Biochem. 81, 715–736 (2012)Google Scholar
  6. 6.
    Park, K.W., Halperin, D.S., Tontonoz, P.: Before they were fat: adipocyte progenitors. Cell Metab. 8, 454–457 (2008)Google Scholar
  7. 7.
    Rodeheffer, M.S., Birsoy, K., Friedman, J.M.: Identification of white adipocyte progenitor cells in vivo. Cell 135, 240–249 (2008)Google Scholar
  8. 8.
    Sanchez-Gurmaches, J., Guertin, D.A.: Adipocyte lineages: Tracing back the origins of fat. Biochim. Biophys. Acta (2013). http://dx.doi.org/10.1016/j.bbadis.2013.05.027
  9. 9.
    Wang, Q.A., Tao, C., Gupta, R.K., Scherer, P.E.: Tracking adipogenesis during white adipose tissue development, expansion and regeneration. Nat. Med. 19, 1338–1344 (2013)Google Scholar
  10. 10.
    Shoham, N., Gefen, A.: Mechanotransduction in adipocytes. J. Biomech. 45, 1–8 (2012)Google Scholar
  11. 11.
    Nakayama, K., Tanabe, Y., Obara, K., Ishikawa, T.: Mechanosensitivity of pancreatic β-cells, adipocytes, and skeletal muscle cells: the therapeutic targets of metabolic syndrome. In: Kamkin, A., Lozinsky, I. (eds.), Mechanosensitivity in Cells and Tissues, vol 6. Mechanically Gated Channels and Their Regulation, pp. 379-404. Springer, Berlin (2012)Google Scholar
  12. 12.
    Liu, X., Jefcoate, C.: 2,3,7,8-tetrachlorodibenzo-p-dioxin and epidermal growth factor cooperatively suppress peroxisome proliferator-activated receptor-gamma1 stimulation and restore focal adhesion complexes during adipogenesis: selective contributions of Src, Rho, and Erk distinguish these overlapping processes in C3H10T1/2 cells. Mol. Pharmacol. 70, 1902–1915 (2006)Google Scholar
  13. 13.
    Sakaue, H., Ogawa, W., Nakamura, T., Mori, T., Nakamura, K., Kasuga, M.: Role of MAPK phosphatase-1 (MKP-1) in adipocyte differentiation. J. Biol. Chem. 279, 39951–39957 (2004)Google Scholar
  14. 14.
    Tanabe, Y., Koga, M., Saito, M., Matsunaga, Y., Nakayama, K.: Inhibition of adipocyte differentiation by mechanical stretching through ERK-mediated downregulation of PPARγ 2. J. Cell Sci. 117, 3605–3614 (2004)Google Scholar
  15. 15.
    Tanabe, Y., Matsunaga, Y., Saito, M., Nakayama, K.: Involvement of cyclooxygenase-2 in synergistic effect of cyclic stretching and eicosapentaenoic acid on adipocyte differentiation. J. Pharmacol. Sci. 106, 478–484 (2008)Google Scholar
  16. 16.
    Tang, Q.Q., Otto, T.C., Lane, M.D.: Mitotic clonal expansion: a synchronous process required for adipogenesis. Proc. Natl. Acad. Sci. USA 100, 44–49 (2003)Google Scholar
  17. 17.
    Kawaguchi, N., Sundberg, C., Kveiborg, M., Moghadaszadeh, B., Asmar, M., Dietrich, N., Thodeti, C.K., Nielsen, F.C., Moller, P., Mercurio, A.M., Albrechtsen, R., Wewer, U.M.: ADAM12 induces actin cytoskeleton and extracellular matrix reorganization during early adipocyte differentiation by regulating β1 integrin function. J. Cell Sci. 116, 3893–3904 (2003)Google Scholar
  18. 18.
    Lieber, J.G., Evans, R.M.: Disruption of the vimentin intermediate filament system during adipose conversion of 3T3-L1 cells inhibits lipid droplet accumulation. J. Cell Sci. 109, 3047–3058 (1996)Google Scholar
  19. 19.
    Katsumi, A., Milanini, J., Kiosses, W.B., del Pozo, M.A., Kaunas, R., Chien, S., Hahn, K.M., Schwartz, M.A.: Effects of cell tension on the small GTPase Rac. J. Cell Biol. 158, 153–164 (2002)Google Scholar
  20. 20.
    Terracio, L., Miller, B., Borg, T.K.: Effects of cyclic mechanical stimulation of the cellular components of the heart: in vitro. In Vitro Cell. Dev. Biol. 24, 53–58 (1988)Google Scholar
  21. 21.
    Tanabe, Y., Saito, M., Ueno, A., Nakamura, M., Takeishi, K., Nakayama, K.: Mechanical stretch augments PDGF receptor β expression and protein tyrosine phosphorylation in pulmonary artery tissue and smooth muscle cells. Mol. Cell. Biochem. 215, 103–113 (2000)Google Scholar
  22. 22.
    Naruse, K., Yamada, T., Sokabe, M.: Involvement of SA channels in orienting response of cultured endothelial cells to cyclic stretch. Am. J. Physiol. 274, H1532–H1538 (1998)Google Scholar
  23. 23.
    Sai, X., Naruse, K., Sokabe, M.: Activation of pp60src is critical for stretch-induced orienting response in fibroblasts. J. Cell Sci. 112, 1365–1373 (1999)Google Scholar
  24. 24.
    Wang, J.G., Miyazu, M., Matsushita, E., Sokabe, M., Naruse, K.: Uniaxial cyclic stretch induces focal adhesion kinase (FAK) tyrosine phosphorylation followed by mitogen-activated protein kinase (MAPK) activation. Biochem. Biophys. Res. Commun. 288, 356–361 (2001)Google Scholar
  25. 25.
    Yano, Y., Saito, Y., Narumiya, S., Sumpio, B.E.: Involvement of rho p21 in cyclic strain-induced tyrosine phosphorylation of focal adhesion kinase (pp125FAK), morphological changes and migration of endothelial cells. Biochem. Biophys. Res. Commun. 224, 508–515 (1996)Google Scholar
  26. 26.
    Akimoto, T., Ushida, T., Miyaki, S., Akaogi, H., Tsuchiya, K., Yan, Z., Williams, R.S., Tateishi, T.: Mechanical stretch inhibits myoblast-to-adipocyte differentiation through Wnt signaling. Biochem. Biophys. Res. Commun. 329, 381–385 (2005)Google Scholar
  27. 27.
    David, V., Martin, A., Lafage-Proust, M.H., Malaval, L., Peyroche, S., Jones, D.B., Vico, L., Guignandon, A.: Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148, 2553–2562 (2007)Google Scholar
  28. 28.
    Hanson, A.D., Marvel, S.W., Bernacki, S.H., Banes, A.J., van Aalst, J., Loboa, E.G.: Osteogenic effects of rest inserted and continuous cyclic tensile strain on hASC lines with disparate osteodifferentiation capabilities. Ann. Biomed. Eng. 37, 955–965 (2009)Google Scholar
  29. 29.
    Khayat, G., Rosenzweig, D.H., Quinn, T.M.: Low frequency mechanical stimulation inhibits adipogenic differentiation of C3H10T1/2 mesenchymal stem cells. Differentiation 83, 179–184 (2012)Google Scholar
  30. 30.
    Lee, J.S., Ha, L., Park, J.H., Lim, J.Y.: Mechanical stretch suppresses BMP4 induction of stem cell adipogenesis via upregulating ERK but not through downregulating Smad or p38. Biochem. Biophys. Res. Commun. 418, 278–283 (2012)Google Scholar
  31. 31.
    Maul, T.M., Chew, D.W., Nieponice, A., Vorp, D.A.: Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech. Model. Mechanobiol. 10, 939–953 (2011)Google Scholar
  32. 32.
    Sen, B., Xie, Z., Case, N., Ma, M., Rubin, C., Rubin, J.: Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable β-catenin signal. Endocrinology 149, 6065–6075 (2008)Google Scholar
  33. 33.
    Turner, N.J., Jones, H.S., Davies, J.E., Canfield, A.E.: Cyclic stretch-induced TGFβ1/Smad signaling inhibits adipogenesis in umbilical cord progenitor cells. Biochem. Biophys. Res. Commun. 377, 1147–1151 (2008)Google Scholar
  34. 34.
    Yang, X., Cai, X., Wang, J., Tang, H., Yuan, Q., Gong, P., Lin, Y.: Mechanical stretch inhibits adipogenesis and stimulates osteogenesis of adipose stem cells. Cell Proliferat. 45, 158–166 (2012)Google Scholar
  35. 35.
    Hara, Y., Wakino, S., Tanabe, Y., Saito, M., Tokuyama, H., Washida, N., Tatematsu, S., Yoshioka, K., Homma, K., Hasegawa, K., Minakuchi, H., Fujimura, K., Hosoya, K., Hayashi, K., Nakayama, K., Itoh, H.: Rho and Rho-kinase activity in adipocytes contributes to a vicious cycle in obesity that may involve mechanical stretch. Sci. Signal. 4, ra3 (2011)Google Scholar
  36. 36.
    Levy, A., Enzer, S., Shoham, N., Zaretsky, U., Gefen, A.: Large, but not small sustained tensile strains stimulate adipogenesis in culture. Ann. Biomed. Eng. 40, 1052–1060 (2012)Google Scholar
  37. 37.
    Shoham, N., Gefen, A.: The influence of mechanical stretching on mitosis, growth, and adipose conversion in adipocyte cultures. Biomech. Model. Mechanobiol. 11, 1029–1045 (2012)Google Scholar
  38. 38.
    Shoham, N., Gottlieb, R., Sharabani-Yosef, O., Zaretsky, U., Benayahu, D., Gefen, A.: Static mechanical stretching accelerates lipid production in 3T3-L1 adipocytes by activating the MEK signaling pathway. Am. J. Physiol. Cell Physiol. 302, C429–C441 (2012)Google Scholar
  39. 39.
    Hossain, M.G., Iwata, T., Mizusawa, N., Shima, S.W., Okutsu, T., Ishimoto, K., Yoshimoto, K.: Compressive force inhibits adipogenesis through COX-2-mediated down-regulation of PPARγ2 and C/EBPα. J. Biosci. Bioeng. 109, 297–303 (2010)Google Scholar
  40. 40.
    Li, G., Fu, N., Yang, X., Li, M., Ba, K., Wei, X., Fu, Y., Yao, Y., Cai, X., Lin, Y.: Mechanical compressive force inhibits adipogenesis of adipose stem cells. Cell Proliferat. 46, 586–594 (2013)Google Scholar
  41. 41.
    Yanagisawa, M., Suzuki, N., Mitsui, N., Koyama, Y., Otsuka, K., Shimizu, N.: Effects of compressive force on the differentiation of pluripotent mesenchymal cells. Life Sci. 81, 405–412 (2007)Google Scholar
  42. 42.
    Hoffman, B.D., Grashoff, C., Schwartz, M.A.: Dynamic molecular processes mediate cellular mechanotransduction. Nature 475, 316–323 (2011)Google Scholar
  43. 43.
    Bishnoi, M., Kondepudi, K.K., Gupta, A., Karmase, A., Boparai, R.K.: Expression of multiple Transient Receptor Potential channel genes in murine 3T3-L1 cell lines and adipose tissue. Pharmacol. Rep. 65, 751–755 (2013)Google Scholar
  44. 44.
    Hamill, O.P., Martinac, B.: Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81, 685–740 (2001)Google Scholar
  45. 45.
    Inoue, H., Takahashi, N., Okada, Y., Konishi, M.: Volume-sensitive outwardly rectifying chloride channel in white adipocytes from normal and diabetic mice. Am. J. Physiol. Cell Physiol. 298, C900–C909 (2010)Google Scholar
  46. 46.
    Zhang, L.L., Yan LiuD., Ma, L.Q., Luo, Z.D., Cao, T.B., Zhong, J., Yan, Z.C., Wang, L.J., Zhao, Z.G., Zhu, S.J., Schrader, M., Thilo, F., Zhu, Z.M., Tepel, M.: Activation of transient receptor potential vanilloid type-1 channel prevents adipogenesis and obesity. Circ. Res. 100, 1063–1070 (2007)Google Scholar
  47. 47.
    Li, C., Xu, Q.: Mechanical stress-initiated signal transductions in vascular smooth muscle cells. Cell. Signal. 12, 435–445 (2000)Google Scholar
  48. 48.
    Zou, Y., Akazawa, H., Qin, Y., Sano, M., Takano, H., Minamino, T., Makita, N., Iwanaga, K., Zhu, W., Kudoh, S., Toko, H., Tamura, K., Kihara, M., Nagai, T., Fukamizu, A., Umemura, S., Iiri, T., Fujita, T., Komuro, I.: Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat. Cell Biol. 6, 499–506 (2004)Google Scholar
  49. 49.
    Geiger, B., Bershadsky, A.: Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell 110, 139–142 (2002)Google Scholar
  50. 50.
    Higashida, C., Kiuchi, T., Akiba, Y., Mizuno, H., Maruoka, M., Narumiya, S., Mizuno, K., Watanabe, N.: F- and G-actin homeostasis regulates mechanosensitive actin nucleation by formins. Nat. Cell Biol. 15, 395–405 (2013)Google Scholar
  51. 51.
    Zuk, P.A.: The adipose-derived stem cell: looking back and looking ahead. Mol. Biol. Cell 21, 1783–1787 (2010)Google Scholar
  52. 52.
    Darling, E.M., Topel, M., Zauscher, S., Vail, T.P., Guilak, F.: Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J. Biomech. 41, 454–464 (2008)Google Scholar
  53. 53.
    Gonzalez-Cruz, R.D., Fonseca, V.C., Darling, E.M.: Cellular mechanical properties reflect the differentiation potential of adipose-derived mesenchymal stem cells. Proc. Natl. Acad. Sci. USA 109, E1523–E1529 (2012)Google Scholar
  54. 54.
    Gonzalez-Cruz, R.D., Darling, E.M.: Adipose-derived stem cell fate is predicted by cellular mechanical properties. Adipocyte 2, 87–91 (2013)Google Scholar
  55. 55.
    Engler, A.J., Sen, S., Sweeney, H.L., Discher, D.E.: Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006)Google Scholar
  56. 56.
    Cristancho, A.G., Schupp, M., Lefterova, M.I., Cao, S., Cohen, D.M., Chen, C.S., Steger, D.J., Lazar, M.A.: Repressor transcription factor 7-like 1 promotes adipogenic competency in precursor cells. Proc. Nat. Acad. Sci. USA 108, 16271–16276 (2011)Google Scholar
  57. 57.
    Watanabe, N., Kato, T., Fujita, A., Ishizaki, T., Narumiya, S.: Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat. Cell Biol. 1, 136–143 (1999)Google Scholar
  58. 58.
    Daley, W.P., Peters, S.B., Larsen, M.: Extracellular matrix dynamics in development and regenerative medicine. J. Cell Sci. 121, 255–264 (2008)Google Scholar
  59. 59.
    Spiegelman, B.M., Ginty, C.A.: Fibronectin modulation of cell shape and lipogenic gene expression in 3T3-adipocytes. Cell 35, 657–666 (1983)Google Scholar
  60. 60.
    Hynes, R.O.: Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11–25 (1992)Google Scholar
  61. 61.
    Li, S., Edgar, D., Fassler, R., Wadsworth, W., Yurchenco, P.D.: The role of laminin in embryonic cell polarization and tissue organization. Dev. Cell 4, 613–624 (2003)Google Scholar
  62. 62.
    Schlessinger, J.: Direct binding and activation of receptor tyrosine kinases by collagen. Cell 91, 869–872 (1997)Google Scholar
  63. 63.
    Bouvard, D., Brakebusch, C., Gustafsson, E., Aszodi, A., Bengtsson, T., Berna, A., Fassler, R.: Functional consequences of integrin gene mutations in mice. Circ. Res. 89, 211–223 (2001)Google Scholar
  64. 64.
    Liu, J., DeYoung, S.M., Zhang, M., Zhang, M., Cheng, A., Saltiel, A.R.: Changes in integrin expression during adipocyte differentiation. Cell Metab. 2, 165–177 (2005)Google Scholar
  65. 65.
    Iqbal, J., Zaidi, M.: Molecular regulation of mechanotransduction. Biochem. Biophys. Res. Commun. 328, 751–755 (2005)Google Scholar
  66. 66.
    Chen, N.X., Ryder, K.D., Pavalko, F.M., Turner, C.H., Burr, D.B., Qiu, J., Duncan, R.L.: Ca2+ regulates fluid shear-induced cytoskeletal reorganization and gene expression in osteoblasts. Am. J. Physiol. Cell Physiol. 278, C989–C997 (2000)Google Scholar
  67. 67.
    Ruwhof, C., van der Laarse, A.: Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways. Cardiovasc. Res. 47, 23–37 (2000)Google Scholar
  68. 68.
    Hudak, C.S., Sul, H.S.: Pref-1, a gatekeeper of adipogenesis. Front. Endocrinol. 4, 79 (2013)Google Scholar
  69. 69.
    Wang, Y., Zhao, L., Smas, C., Sul, H.S.: Pref-1 interacts with fibronectin to inhibit adipocyte differentiation. Mol. Cell. Biol. 30, 3480–3492 (2010)Google Scholar
  70. 70.
    Hall, A.: Rho GTPases and the actin cytoskeleton. Science 279, 509–514 (1998)Google Scholar
  71. 71.
    Narumiya, S.: The small GTPase Rho: cellular functions and signal transduction. J. Biochem. 120, 215–228 (1996)Google Scholar
  72. 72.
    Narumiya, S., Ishizaki, T., Watanabe, N.: Rho effectors and reorganization of actin cytoskeleton. FEBS Lett. 410, 68–72 (1997)Google Scholar
  73. 73.
    Ridley, A.J.: Stress fibres take shape. Nat. Cell Biol. 1, E64–E66 (1999)Google Scholar
  74. 74.
    Cohen, D.M., Chen, C.S.: StemBook http://www.stembook.org (ed e. StemBook). The Stem Cell Research Community, Cambridge. doi: 10.3824/stembook.3821.3826.3821 (2008)
  75. 75.
    Guilak, F., Cohen, D.M., Estes, B.T., Gimble, J.M., Liedtke, W., Chen, C.S.: Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5, 17–26 (2009)Google Scholar
  76. 76.
    McBeath, R., Pirone, D.M., Nelson, C.M., Bhadriraju, K., Chen, C.S.: Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483–495 (2004)Google Scholar
  77. 77.
    Frost, J.A., Steen, H., Shapiro, P., Lewis, T., Ahn, N., Shaw, P.E., Cobb, M.H.: Cross-cascade activation of ERKs and ternary complex factors by Rho family proteins. EMBO J. 16, 6426–6438 (1997)Google Scholar
  78. 78.
    Roskoski Jr, R.: ERK1/2 MAP kinases: structure, function, and regulation. Pharmacol. Res. 66, 105–143 (2012)Google Scholar
  79. 79.
    Sadoshima, J., Izumo, S.: Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. EMBO J. 12, 1681–1692 (1993)Google Scholar
  80. 80.
    Chien, S., Li, S., Shyy, Y.J.: Effects of mechanical forces on signal transduction and gene expression in endothelial cells. Hypertension 31, 162–169 (1998)Google Scholar
  81. 81.
    Li, C., Hu, Y., Mayr, M., Xu, Q.: Cyclic strain stress-induced mitogen-activated protein kinase (MAPK) phosphatase 1 expression in vascular smooth muscle cells is regulated by Ras/Rac-MAPK pathways. J. Biol. Chem. 274, 25273–25280 (1999)Google Scholar
  82. 82.
    Ingram, A.J., Ly, H., Thai, K., Kang, M., Scholey, J.W.: Activation of mesangial cell signaling cascades in response to mechanical strain. Kidney Int. 55, 476–485 (1999)Google Scholar
  83. 83.
    Jansen, J.H., Weyts, F.A., Westbroek, I., Jahr, H., Chiba, H., Pols, H.A., Verhaar, J.A., van Leeuwen, J.P., Weinans, H.: Stretch-induced phosphorylation of ERK1/2 depends on differentiation stage of osteoblasts. J. Cell. Biochem. 93, 542–551 (2004)Google Scholar
  84. 84.
    Wang, J.G., Miyazu, M., Xiang, P., Li, S.N., Sokabe, M., Naruse, K.: Stretch-induced cell proliferation is mediated by FAK-MAPK pathway. Life Sci. 76, 2817–2825 (2005)Google Scholar
  85. 85.
    Hata, M., Naruse, K., Ozawa, S., Kobayashi, Y., Nakamura, N., Kojima, N., Omi, M., Katanosaka, Y., Nishikawa, T., Naruse, K., Tanaka, Y., Matsubara, T.: Mechanical stretch increases the proliferation while inhibiting the osteogenic differentiation in dental pulp stem cells. Tissue Eng. Part A 19, 625–633 (2013)Google Scholar
  86. 86.
    Schmelter, M., Ateghang, B., Helmig, S., Wartenberg, M., Sauer, H.: Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J. 20, 1182–1184 (2006)Google Scholar
  87. 87.
    Bost, F., Caron, L., Marchetti, I., Dani, C., Le Marchand-Brustel, Y., Binetruy, B.: Retinoic acid activation of the ERK pathway is required for embryonic stem cell commitment into the adipocyte lineage. Biochem. J. 361, 621–627 (2002)Google Scholar
  88. 88.
    Klemm, D.J., Leitner, J.W., Watson, P., Nesterova, A., Reusch, J.E., Goalstone, M.L., Draznin, B.: Insulin-induced adipocyte differentiation. Activation of CREB rescues adipogenesis from the arrest caused by inhibition of prenylation. J. Biol. Chem. 276, 28430–28435 (2001)Google Scholar
  89. 89.
    Machinal-Quelin, F., Dieudonne, M.N., Leneveu, M.C., Pecquery, R., Giudicelli, Y.: Proadipogenic effect of leptin on rat preadipocytes in vitro: activation of MAPK and STAT3 signaling pathways. Am. J. Physiol. Cell Physiol. 282, C853–C863 (2002)Google Scholar
  90. 90.
    Park, B.H., Qiang, L., Farmer, S.R.: Phosphorylation of C/EBPβ at a consensus extracellular signal-regulated kinase/glycogen synthase kinase 3 site is required for the induction of adiponectin gene expression during the differentiation of mouse fibroblasts into adipocytes. Mol. Cell. Biol. 24, 8671–8680 (2004)Google Scholar
  91. 91.
    Prusty, D., Park, B.H., Davis, K.E., Farmer, S.R.: 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 (2002)Google Scholar
  92. 92.
    Zhang, B., Berger, J., Zhou, G., Elbrecht, A., Biswas, S., White-Carrington, S., Szalkowski, D., Moller, D.E.: Insulin- and mitogen-activated protein kinase-mediated phosphorylation and activation of peroxisome proliferator-activated receptor γ. J. Biol. Chem. 271, 31771–31774 (1996)Google Scholar
  93. 93.
    de Mora, Font J., Porras, A., Ahn, N., Santos, E.: Mitogen-activated protein kinase activation is not necessary for, but antagonizes, 3T3-L1 adipocytic differentiation. Mol. Cell. Biol. 17, 6068–6075 (1997)Google Scholar
  94. 94.
    Hu, E., Kim, J.B., Sarraf, P., Spiegelman, B.M.: Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARγ. Science 274, 2100–2103 (1996)Google Scholar
  95. 95.
    Kim, S.W., Muise, A.M., Lyons, P.J., Ro, H.S.: Regulation of adipogenesis by a transcriptional repressor that modulates MAPK activation. J. Biol. Chem. 276, 10199–10206 (2001)Google Scholar
  96. 96.
    Kimura, I., Konishi, M., Asaki, T., Furukawa, N., Ukai, K., Mori, M., Hirasawa, A., Tsujimoto, G., Ohta, M., Itoh, N., Fujimoto, M.: Neudesin, an extracellular heme-binding protein, suppresses adipogenesis in 3T3-L1 cells via the MAPK cascade. Biochem. Biophys. Res. Commun. 381, 75–80 (2009)Google Scholar
  97. 97.
    Shimba, S., Wada, T., Tezuka, M.: Arylhydrocarbon receptor (AhR) is involved in negative regulation of adipose differentiation in 3T3-L1 cells: AhR inhibits adipose differentiation independently of dioxin. J. Cell Sci. 114, 2809–2817 (2001)Google Scholar
  98. 98.
    Ueno, T., Fujimori, K.: Novel suppression mechanism operating in early phase of adipogenesis by positive feedback loop for enhancement of cyclooxygenase-2 expression through prostaglandin F2α receptor mediated activation of MEK/ERK-CREB cascade. FEBS J. 278, 2901–2912 (2011)Google Scholar
  99. 99.
    Tang, Q.Q., Gronborg, M., Huang, H., Kim, J.W., Otto, T.C., Pandey, A., Lane, M.D.: Sequential phosphorylation of CCAAT enhancer-binding protein β by MAPK and glycogen synthase kinase 3β is required for adipogenesis. Proc. Natl. Acad. Sci. USA 102, 9766–9771 (2005)Google Scholar
  100. 100.
    Adams, M., Reginato, M.J., Shao, D., Lazar, M.A., Chatterjee, V.K.: 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 (1997)Google Scholar
  101. 101.
    Camp, H.S., Tafuri, S.R.: Regulation of peroxisome proliferator-activated receptor γ activity by mitogen-activated protein kinase. J. Biol. Chem. 272, 10811–10816 (1997)Google Scholar
  102. 102.
    Chan, G.K., Deckelbaum, R.A., Bolivar, I., Goltzman, D., Karaplis, A.C.: PTHrP inhibits adipocyte differentiation by down-regulating PPAR γ activity via a MAPK-dependent pathway. Endocrinology 142, 4900–4909 (2001)Google Scholar
  103. 103.
    Reginato, M.J., Krakow, S.L., Bailey, S.T., Lazar, M.A.: Prostaglandins promote and block adipogenesis through opposing effects on peroxisome proliferator-activated receptor γ. J. Biol. Chem. 273, 1855–1858 (1998)Google Scholar
  104. 104.
    Burgermeister, E., Chuderland, D., Hanoch, T., Meyer, M., Liscovitch, M., Seger, R.: Interaction with MEK causes nuclear export and downregulation of peroxisome proliferator-activated receptor γ. Mol. Cell. Biol. 27, 803–817 (2007)Google Scholar
  105. 105.
    Burgermeister, E., Seger, R.: MAPK kinases as nucleo-cytoplasmic shuttles for PPARγ. Cell Cycle 6, 1539–1548 (2007)Google Scholar
  106. 106.
    Hornberger, T.A., Armstrong, D.D., Koh, T.J., Burkholder, T.J., Esser, K.A.: Intracellular signaling specificity in response to uniaxial versus multiaxial stretch: implications for mechanotransduction. Am. J. Physiol. Cell Physiol. 288, C185–C194 (2005)Google Scholar
  107. 107.
    Vassaux, G., Gaillard, D., Ailhaud, G., Negrel, R.: Prostacyclin is a specific effector of adipose cell differentiation. Its dual role as a cAMP- and Ca2+-elevating agent. J. Biol. Chem. 267, 11092–11097 (1992)Google Scholar
  108. 108.
    Miller, C.W., Casimir, D.A., Ntambi, J.M.: The mechanism of inhibition of 3T3-L1 preadipocyte differentiation by prostaglandin F2α. Endocrinology 137, 5641–5650 (1996)Google Scholar
  109. 109.
    Tsuboi, H., Sugimoto, Y., Kainoh, T., Ichikawa, A.: Prostanoid EP4 receptor is involved in suppression of 3T3-L1 adipocyte differentiation. Biochem. Biophys. Res. Commun. 322, 1066–1072 (2004)Google Scholar
  110. 110.
    Petersen, R.K., Jorgensen, C., Rustan, A.C., Froyland, L., Muller-Decker, K., Furstenberger, G., Berge, R.K., Kristiansen, K., Madsen, L.: Arachidonic acid-dependent inhibition of adipocyte differentiation requires PKA activity and is associated with sustained expression of cyclooxygenases. J. Lipid Res. 44, 2320–2330 (2003)Google Scholar
  111. 111.
    Inazumi, T., Shirata, N., Morimoto, K., Takano, H., Segi-Nishida, E., Sugimoto, Y.: Prostaglandin E2-EP4 signaling suppresses adipocyte differentiation in mouse embryonic fibroblasts via an autocrine mechanism. J. Lipid Res. 52, 1500–1508 (2011)Google Scholar
  112. 112.
    Fain, J.N., Ballou, L.R., Bahouth, S.W.: Obesity is induced in mice heterozygous for cyclooxygenase-2. Prostag. Other Lipid Mediat. 65, 199–209 (2001)Google Scholar
  113. 113.
    Amma, H., Naruse, K., Ishiguro, N., Sokabe, M.: Involvement of reactive oxygen species in cyclic stretch-induced NF-κB activation in human fibroblast cells. Br. J. Pharmacol. 145, 364–373 (2005)Google Scholar
  114. 114.
    Copland, I.B., Reynaud, D., Pace-Asciak, C., Post, M.: Mechanotransduction of stretch-induced prostanoid release by fetal lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L487–L495 (2006)Google Scholar
  115. 115.
    Fujishiro, T., Nishikawa, T., Shibanuma, N., Akisue, T., Takikawa, S., Yamamoto, T., Yoshiya, S., Kurosaka, M.: Effect of cyclic mechanical stretch and titanium particles on prostaglandin E2 production by human macrophages in vitro. J. Biomed. Mater. Res. Part A 68, 531–536 (2004)Google Scholar
  116. 116.
    Martineau, L.C., McVeigh, L.I., Jasmin, B.J., Kennedy, C.R.: p38 MAP kinase mediates mechanically induced COX-2 and PG EP4 receptor expression in podocytes: implications for the actin cytoskeleton. Am. J. Physiol. Renal Physiol. 286, F693–F701 (2004)Google Scholar
  117. 117.
    Park, J.M., Yang, T., Arend, L.J., Schnermann, J.B., Peters, C.A., Freeman, M.R., Briggs, J.P.: Obstruction stimulates COX-2 expression in bladder smooth muscle cells via increased mechanical stretch. Am. J. Physiol. Renal Physiol. 276, F129–F136 (1999)Google Scholar
  118. 118.
    Sooranna, S.R., Lee, Y., Kim, L.U., Mohan, A.R., Bennett, P.R., Johnson, M.R.: Mechanical stretch activates type 2 cyclooxygenase via activator protein-1 transcription factor in human myometrial cells. Mol. Hum. Reprod. 10, 109–113 (2004)Google Scholar
  119. 119.
    Mohan, A.R., Sooranna, S.R., Lindstrom, T.M., Johnson, M.R., Bennett, P.R.: The effect of mechanical stretch on cyclooxygenase type 2 expression and activator protein-1 and nuclear factor-kappaB activity in human amnion cells. Endocrinology 148, 1850–1857 (2007)Google Scholar
  120. 120.
    Tazawa, R., Xu, X.M., Wu, K.K., Wang, L.H.: Characterization of the genomic structure, chromosomal location and promoter of human prostaglandin H synthase-2 gene. Biochem. Biophys. Res. Commun. 203, 190–199 (1994)Google Scholar
  121. 121.
    Bhattacharya, S., Patel, R., Sen, N., Quadri, S., Parthasarathi, K., Bhattacharya, J.: Dual signaling by the αvβ3-integrin activates cytosolic PLA2 in bovine pulmonary artery endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L1049–L1056 (2001)Google Scholar
  122. 122.
    Bilkovski, R., Schulte, D.M., Oberhauser, F., Gomolka, M., Udelhoven, M., Hettich, M.M., Roth, B., Heidenreich, A., Gutschow, C., Krone, W., Laudes, M.: Role of WNT-5a in the determination of human mesenchymal stem cells into preadipocytes. J. Biol. Chem. 285, 6170–6178 (2010)Google Scholar
  123. 123.
    Kang, S., Bennett, C.N., Gerin, I., Rapp, L.A., Hankenson, K.D., Macdougald, O.A.: Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein α and peroxisome proliferator-activated receptor γ. J. Biol. Chem. 282, 14515–14524 (2007)Google Scholar
  124. 124.
    Santos, A., Bakker, A.D., de Blieck-Hogervorst, J.M., Klein-Nulend, J.: WNT5A induces osteogenic differentiation of human adipose stem cells via rho-associated kinase ROCK. Cytotherapy 12, 924–932 (2010)Google Scholar
  125. 125.
    Ross, S.E., Hemati, N., Longo, K.A., Bennett, C.N., Lucas, P.C., Erickson, R.L., MacDougald, O.A.: Inhibition of adipogenesis by Wnt signaling. Science 289, 950–953 (2000)Google Scholar
  126. 126.
    Day, T.F., Guo, X., Garrett-Beal, L., Yang, Y.: Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 8, 739–750 (2005)Google Scholar
  127. 127.
    Hill, T.P., Spater, D., Taketo, M.M., Birchmeier, W., Hartmann, C.: Canonical Wnt/β-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 8, 727–738 (2005)Google Scholar
  128. 128.
    Bennett, C.N., Ross, S.E., Longo, K.A., Bajnok, L., Hemati, N., Johnson, K.W., Harrison, S.D., MacDougald, O.A.: Regulation of Wnt signaling during adipogenesis. J. Biol. Chem. 277, 30998-31004Google Scholar
  129. 129.
    Kanazawa, A., Tsukada, S., Kamiyama, M., Yanagimoto, T., Nakajima, M., Maeda, S.: Wnt5b partially inhibits canonical Wnt/β-catenin signaling pathway and promotes adipogenesis in 3T3-L1 preadipocytes. Biochem. Biophys. Res. Commun. 330, 505–510 (2005)Google Scholar
  130. 130.
    Nishizuka, M., Koyanagi, A., Osada, S., Imagawa, M.: Wnt4 and Wnt5a promote adipocyte differentiation. FEBS Lett. 582, 3201–3205 (2008)Google Scholar
  131. 131.
    van Tienen, F.H., Laeremans, H., van der Kallen, C.J., Smeets, H.J.: Wnt5b stimulates adipogenesis by activating PPARγ, and inhibiting the β-catenin dependent Wnt signaling pathway together with Wnt5a. Biochem. Biophys. Res. Commun. 387, 207–211 (2009)Google Scholar
  132. 132.
    Takada, I., Mihara, M., Suzawa, M., Ohtake, F., Kobayashi, S., Igarashi, M., Youn, M.Y., Takeyama, K., Nakamura, T., Mezaki, Y., Takezawa, S., Yogiashi, Y., Kitagawa, H., Yamada, G., Takada, S., Minami, Y., Shibuya, H., Matsumoto, K., Kato, S.: A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-γ transactivation. Nat. Cell Biol. 9, 1273–1285 (2007)Google Scholar
  133. 133.
    Jakkaraju, S., Zhe, X., Pan, D., Choudhury, R., Schuger, L.: TIPs are tension-responsive proteins involved in myogenic versus adipogenic differentiation. Dev. Cell 9, 39–49 (2005)Google Scholar
  134. 134.
    Badri, K.R., Zhou, Y., Dhru, U., Aramgam, S., Schuger, L.: Effects of the SANT domain of tension-induced/inhibited proteins (TIPs), novel partners of the histone acetyltransferase p300, on p300 activity and TIP-6-induced adipogenesis. Mol. Cell. Biol. 28, 6358–6372 (2008)Google Scholar
  135. 135.
    Azain, M.J.: Role of fatty acids in adipocyte growth and development. J. Anim. Sci. 82, 916–924 (2004)Google Scholar
  136. 136.
    Holub, D.J., Holub, B.J.: Omega-3 fatty acids from fish oils and cardiovascular disease. Mol. Cell. Biochem. 263, 217–225 (2004)Google Scholar
  137. 137.
    Kris-Etherton, P.M., Harris, W.S., Appel, L.J.: Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106, 2747–2757 (2002)Google Scholar
  138. 138.
    Nestel, P.J.: Effects of N-3 fatty acids on lipid metabolism. Annu. Rev. Nutr. 10, 149–167 (1990)Google Scholar
  139. 139.
    Storlien, L.H., Kriketos, A.D., Calvert, G.D., Baur, L.A., Jenkins, A.B.: Fatty acids, triglycerides and syndromes of insulin resistance. Prosta. Leukotr. Ess. 57, 379–385 (1997)Google Scholar
  140. 140.
    Mater, M.K., Pan, D., Bergen, W.G., Jump, D.B.: Arachidonic acid inhibits lipogenic gene expression in 3T3-L1 adipocytes through a prostanoid pathway. J. Lipid Res. 39, 1327–1334 (1998)Google Scholar
  141. 141.
    Raclot, T., Groscolas, R., Langin, D., Ferre, P.: Site-specific regulation of gene expression by n-3 polyunsaturated fatty acids in rat white adipose tissues. J. Lipid Res. 38, 1963–1972 (1997)Google Scholar
  142. 142.
    Manickam, E., Sinclair, A.J., Cameron-Smith, D.: Suppressive actions of eicosapentaenoic acid on lipid droplet formation in 3T3-L1 adipocytes. Lipids Health Dis. 9, 57 (2010)Google Scholar
  143. 143.
    Smith, W.L.: Cyclooxygenases, peroxide tone and the allure of fish oil. Curr. Opin. Cell Biol. 17, 174–182 (2005)Google Scholar
  144. 144.
    Hirafuji, M., Machida, T., Hamaue, N., Minami, M.: Cardiovascular protective effects of n-3 polyunsaturated fatty acids with special emphasis on docosahexaenoic acid. J. Pharmacol. Sci. 92, 308–316 (2003)Google Scholar
  145. 145.
    Frith, J.E., Mills, R.J., Cooper-White, J.J.: Lateral spacing of adhesion peptides influences human mesenchymal stem cell behaviour. J. Cell Sci. 125, 317–327 (2012)Google Scholar
  146. 146.
    Lin, Y.T., Tang, C.H., Chuang, W.J., Wang, S.M., Huang, T.F., Fu, W.M.: Inhibition of adipogenesis by RGD-dependent disintegrin. Biochem. Pharmacol. 70, 1469–1478 (2005)Google Scholar
  147. 147.
    Wang, X., Yan, C., Ye, K., He, Y., Li, Z., Ding, J.: Effect of RGD nanospacing on differentiation of stem cells. Biomaterials 34, 2865–2874 (2013)Google Scholar
  148. 148.
    Wakino, S., Okada, Y., VanHook, A.M.: Science signaling podcast: 25 January 2011. Sci. Signal. 4, pc2 (2011)Google Scholar
  149. 149.
    Rubin, C.T., Capilla, E., Luu, Y.K., Busa, B., Crawford, H., Nolan, D.J., Mittal, V., Rosen, C.J., Pessin, J.E., Judex, S.: Adipogenesis is inhibited by brief, daily exposure to high-frequency, extremely low-magnitude mechanical signals. Proc. Nat. Acad. Sci. USA 104, 17879–17884 (2007)Google Scholar
  150. 150.
    Marques, M.A., Combes, M., Roussel, B., Vidal-Dupont, L., Thalamas, C., Lafontan, M., Viguerie, N.: Impact of a mechanical massage on gene expression profile and lipid mobilization in female gluteofemoral adipose tissue. Obes. Facts 4, 121–129 (2011)Google Scholar
  151. 151.
    Kim, D., Rath, O., Kolch, W., Cho, K.H.: A hidden oncogenic positive feedback loop caused by crosstalk between Wnt and ERK pathways. Oncogene 26, 4571–4579 (2007)Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Yoshiyuki Tanabe
    • 1
    Email author
  • Maki Tanji Saito
    • 1
  • Koichi Nakayama
    • 1
    • 2
  1. 1.Department of Molecular and Cellular Pharmacology, School of Pharmaceutical SciencesIwate Medical UniversityIwateJapan
  2. 2.The Professor Emeritus, School of Pharmaceutical SciencesUniversity of ShizuokaShizuokaJapan

Personalised recommendations