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BioMed Research International
Volume 2013 (2013), Article ID 598461, 17 pages
http://dx.doi.org/10.1155/2013/598461
Review Article

Cell Mechanosensitivity: Mechanical Properties and Interaction with Gravitational Field

State Research Center of Russian Federation Institute of Biomedical Problems, Russian Academy of Sciences, 76-a, Khoroshevskoyoe shosse, Moscow 123007, Russia

Received 7 October 2012; Revised 17 November 2012; Accepted 27 November 2012

Academic Editor: Masamitsu Yamaguchi

Copyright © 2013 I. V. Ogneva. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Ph. Carl and H. Schillers, “Elasticity measurement of living cells with an atomic force microscope: data acquisition and processing,” Pflugers Archiv European Journal of Physiology, vol. 457, no. 2, pp. 551–559, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. A. B. Mathur, A. M. Collinsworth, W. M. Reichert, W. E. Kraus, and G. A. Truskey, “Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy,” Journal of Biomechanics, vol. 34, no. 12, pp. 1545–1553, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. E. Defranchi, E. Bonaccurso, M. Tedesco et al., “Imaging and elasticity measurements of the sarcolemma of fully differentiated skeletal muscle fibres,” Microscopy Research and Technique, vol. 67, no. 1, pp. 27–35, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. A. M. Collinsworth, S. Zhang, W. E. Kraus, and G. A. Truskey, “Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation,” American Journal of Physiology, vol. 283, no. 4, pp. C1219–C1227, 2002. View at Scopus
  5. I. V. Ogneva, D. V. Lebedev, and B. S. Shenkman, “Transversal stiffness and young's modulus of single fibers from rat soleus muscle probed by atomic force microscopy,” Biophysical Journal, vol. 98, no. 3, pp. 418–424, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. I. V. Ogneva, T. M. Mirzoev, N. S. Biryukov, O. M. Veselova, and I. M. Larina, “Structure and functional characteristics of rat's left ventricle cardiomyocytes under antiorthostatic suspension of various duration and subsequent reloading,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 659869, 11 pages, 2012. View at Publisher · View at Google Scholar
  7. I. V. Ogneva and I. B. Ushakov, “The transversal stiffness of skeletal muscle fibers and cardiomyocytes in control and after simulated microgravity,” in Book ‘Atomic Force Microscopy Investigations into Biology-From Cell to Protein’, chapter 15, pp. 325–354, 2012.
  8. I. V. Ogneva, “Transversal stiffness of fibers and desmin content in leg muscles of rats under gravitational unloading of various durations,” Journal of Applied Physiology, vol. 109, no. 6, pp. 1702–1709, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. K. D. Costa, A. J. Sim, and F. C. P. Yin, “Non-Hertzian approach to analyzing mechanical properties of endothelial cells probed by atomic force microscopy,” Journal of Biomechanical Engineering, vol. 128, no. 2, pp. 176–184, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. J. C. Martens and M. Radmacher, “Softening of the actin cytoskeleton by inhibition of myosin II,” Pflugers Archiv European Journal of Physiology, vol. 456, no. 1, pp. 95–100, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Cai, J. Cai, S. Dong, H. Deng, and M. Hu, “Morphology and mechanical properties of normal lymphocyte and Jurkat revealed by atomic force microscopy,” Shengwu Gongcheng Xuebao/Chinese Journal of Biotechnology, vol. 25, no. 7, pp. 1107–1112, 2009. View at Scopus
  12. I. Dulińska, M. Targosz, W. Strojny et al., “Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy,” Journal of Biochemical and Biophysical Methods, vol. 66, no. 1–3, pp. 1–11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Lekka, M. Fornal, G. Pyka-Fościak et al., “Erythrocyte stiffness probed using atomic force microscope,” Biorheology, vol. 42, no. 4, pp. 307–317, 2005. View at Scopus
  14. C. H. Hsieh, Y. H. Lin, S. Lin, J. J. Tsai-Wu, C. H. Herbert Wu, and C. C. Jiang, “Surface ultrastructure and mechanical property of human chondrocyte revealed by atomic force microscopy,” Osteoarthritis and Cartilage, vol. 16, no. 4, pp. 480–488, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Docheva, D. Padula, C. Popov, W. Mutschler, H. Clausen-Schaumann, and M. Schieker, “Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy: stem Cells,” Journal of Cellular and Molecular Medicine, vol. 12, no. 2, pp. 537–552, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Takai, K. D. Costa, A. Shaheen, C. T. Hung, and X. E. Guo, “Osteoblast elastic modulus measured by atomic force microscopy is substrate dependent,” Annals of Biomedical Engineering, vol. 33, no. 7, pp. 963–971, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. E. K. F. Yim, E. M. Darling, K. Kulangara, F. Guilak, and K. W. Leong, “Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells,” Biomaterials, vol. 31, no. 6, pp. 1299–1306, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Huang, R. D. Kamm, and R. T. Lee, “Cell mechanics and mechanotransduction: pathways, probes, and physiology,” American Journal of Physiology, vol. 287, no. 1, pp. C1–C11, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. P. F. Davies, K. A. Barbee, M. V. Volin et al., “Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction,” Annual Review of Physiology, vol. 59, pp. 527–549, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. B. P. Helmke, A. B. Rosen, and P. F. Davies, “Mapping mechanical strain of an endogenous cytoskeletal network in living endothelial cells,” Biophysical Journal, vol. 84, no. 4, pp. 2691–2699, 2003. View at Scopus
  21. B. P. Helmke, D. B. Thakker, R. D. Goldman, and P. F. Davies, “Spatiotemporal analysis of flow-induced intermediate filament displacement in living endothelial cells,” Biophysical Journal, vol. 80, no. 1, pp. 184–194, 2001. View at Scopus
  22. A. R. Bausch, F. Ziemann, A. A. Boulbitch, K. Jacobson, and E. Sackmann, “Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry,” Biophysical Journal, vol. 75, no. 4, pp. 2038–2049, 1998. View at Scopus
  23. S. Hu, J. Chen, B. Fabry et al., “Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells,” American Journal of Physiology, vol. 285, no. 5, pp. C1082–C1090, 2003. View at Scopus
  24. H. Huang, C. Y. Dong, H. S. Kwon, J. D. Sutin, R. D. Kamm, and P. T. So, “Three-dimensional cellular deformation analysis with two-photon magnetic manipulator workstation,” Biophysical Journal, vol. 82, no. 4, pp. 2211–2223, 2002. View at Publisher · View at Google Scholar
  25. N. Q. Balaban, U. S. Schwarz, D. Riveline et al., “Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates,” Nature Cell Biology, vol. 3, no. 5, pp. 466–472, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. P. P. Lehenkari and M. A. Horton, “Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy,” Biochemical and Biophysical Research Communications, vol. 259, no. 3, pp. 645–650, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. H. P. Erickson, “Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 21, pp. 10114–20118, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. J. M. Ferrer, H. Lee, J. Chen et al., “Measuring molecular rupture forces between single actin filaments and actin-binding proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 27, pp. 9221–9226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. J. T. Finer, R. M. Simmons, and J. A. Spudich, “Single myosin molecule mechanics: piconewton forces and nanometre steps,” Nature, vol. 368, no. 6467, pp. 113–119, 1994. View at Publisher · View at Google Scholar · View at Scopus
  30. T. J. Dennerll, H. C. Joshi, V. L. Steel, R. E. Buxbaum, and S. R. Heidemann, “Tension and compression in the cytoskeleton of PC-12 neurites II: quantitative measurements,” Journal of Cell Biology, vol. 107, no. 2, pp. 665–674, 1988. View at Scopus
  31. A. J. Putnam, K. Schultz, and D. J. Mooney, “Control of microtubule assembly by extracellular matrix and externally applied strain,” American Journal of Physiology, vol. 280, no. 3, pp. C556–C564, 2001. View at Scopus
  32. S. Liu, D. A. Calderwood, and M. H. Ginsberg, “Integrin cytoplasmic domain-binding proteins,” Journal of Cell Science, vol. 113, no. 20, pp. 3563–3571, 2000. View at Scopus
  33. S. Sukharev and D. P. Corey, “Mechanosensitive channels: multiplicity of families and gating paradigms,” Science's STKE, vol. 2004, no. 219, Article ID re4, 2004. View at Scopus
  34. R. Maroto, A. Raso, T. G. Wood, A. Kurosky, B. Martinac, and O. P. Hamill, “TRPC1 forms the stretch-activated cation channel in vertebrate cells,” Nature Cell Biology, vol. 7, no. 2, pp. 179–185, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Sukharev, M. Betanzos, C. S. Chiang, and H. Robert Guy, “The gating mechanism of the large mechanosensitive channel MscL,” Nature, vol. 409, no. 6821, pp. 720–724, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Howard and S. Bechstedt, “Hypothesis: a helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors,” Current Biology, vol. 14, no. 6, pp. R224–R226, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. O. P. Hamill and B. Martinac, “Molecular basis of mechanotransduction in living cells,” Physiological Reviews, vol. 81, no. 2, pp. 685–740, 2001. View at Scopus
  38. G. Chang, R. H. Spencer, A. T. Lee, M. T. Barclay, and D. C. Rees, “Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel,” Science, vol. 282, no. 5397, pp. 2220–2226, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Gullingsrud, D. Kosztin, and K. Schulten, “Structural determinants of MscL gating studied by molecular dynamics simulations,” Biophysical Journal, vol. 80, no. 5, pp. 2074–2081, 2001. View at Scopus
  40. E. Perozo, D. M. Cortes, P. Sompornpisut, A. Kloda, and B. Martinac, “Open channel structure of MscL and the gating mechanism of mechanosensitive channels,” Nature, vol. 418, no. 6901, pp. 942–948, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Arnadottir and M. Chalfie, “Eukaryotic mechanosensitive channels,” Annual Review of Biophysics, vol. 39, pp. 111–137, 2010. View at Publisher · View at Google Scholar
  42. C. Montell, “The TRP superfamily of cation channels,” Science's STKE, vol. 2005, no. 272, Article ID re3, 2005. View at Scopus
  43. J. A. Stiber, Y. Tang, T. Li, and P. B. Rosenberg, “Cytoskeletal regulation of TRPC channels in the cardiorenal system,” Current Hypertension Reports, vol. 14, no. 6, pp. 492–497, 2012. View at Publisher · View at Google Scholar
  44. F. Lesage and M. Lazdunski, “Molecular and functional properties of two-pore-domain potassium channels,” American Journal of Physiology, vol. 279, no. 5, pp. F793–F801, 2000. View at Scopus
  45. M. Althaus, R. Bogdan, W. G. Clauss, and M. Fronius, “Mechano-sensitivity of epithelial sodium channels (ENaCs): laminar shear stress increases ion channel open probability,” FASEB Journal, vol. 21, no. 10, pp. 2389–2399, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. L. M. Satlin, S. Sheng, C. B. Woda, and T. R. Kleyman, “Epithelial Na+ channels are regulated by flow,” American Journal of Physiology, vol. 280, no. 6, pp. F1010–F1018, 2001. View at Scopus
  47. M. D. Carattino, S. Sheng, and T. R. Kleyman, “Epithelial Na+ channels are activated by Laminar shear stress,” Journal of Biological Chemistry, vol. 279, no. 6, pp. 4120–4126, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. W. Liu, S. Xu, C. Woda, P. Kim, S. Weinbaum, and L. M. Satlin, “Effect of flow and stretch on the [Ca2+]i response of principal and intercalated cells in cortical collecting duct,” American Journal of Physiology, vol. 285, no. 5, pp. F998–F1012, 2003. View at Scopus
  49. R. Tarran, B. Button, M. Picher et al., “Normal and cystic fibrosis airway surface liquid homeostasis: the effects of phasic shear stress and viral infections,” Journal of Biological Chemistry, vol. 280, pp. 35751–35759, 2005. View at Publisher · View at Google Scholar
  50. H. A. Drummond, D. Gebremedhin, and D. R. Harder, “Degenerin/epithelial Na+ channel proteins: components of a vascular mechanosensor,” Hypertension, vol. 44, no. 5, pp. 643–648, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. H. A. Drummond, M. J. Welsh, and F. M. Abboud, “ENaC subunits are molecular components of the arterial baroreceptor complex,” Annals of the New York Academy of Sciences, vol. 940, pp. 42–47, 2001. View at Scopus
  52. N. L. Jernigan and H. A. Drummond, “Vascular ENaC proteins are required for renal myogenic constriction,” American Journal of Physiology, vol. 289, no. 4, pp. F891–F901, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. H. A. Drummond, F. M. Abboud, and M. J. Welsh, “Localization of β and γ subunits of ENaC in sensory nerve endings in the rat foot pad,” Brain Research, vol. 884, no. 1-2, pp. 1–12, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. H. T. Ma, R. L. Patterson, D. B. Van Rossum, L. Birnbaumer, K. Mikoshiba, and D. L. Gill, “Requirement of the inositol trisphosphate receptor for activation of store-operated Ca2+ channels,” Science, vol. 287, no. 5458, pp. 1647–1651, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. J. R. Holda and L. A. Blatter, “Capacitative calcium entry is inhibited in vascular endothelial cells by disruption of cytoskeletal microfilaments,” FEBS Letters, vol. 403, no. 2, pp. 191–196, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Schatten, M. L. Lewis, and A. Chakrabarti, “Spaceflight and clinorotation cause cytoskeleton and mitochondria changes and increases in apoptosis in cultured cells,” Acta Astronautica, vol. 49, no. 3–10, pp. 399–418, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Devarajan, D. A. Scaramuzzino, and J. S. Morrow, “Ankyrin binds to two distinct cytoplasmic domains of Na,K-ATPase α subunit,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 8, pp. 2965–2969, 1994. View at Scopus
  58. Y. Srinivasan, L. Elmer, J. Davis, V. Bennett, and K. Angelides, “Ankyrin and spectrin associate with voltage-dependent sodium channels in brain,” Nature, vol. 333, no. 6169, pp. 177–180, 1988. View at Scopus
  59. D. J. Benos, M. S. Awayda, I. I. Ismailov, and J. P. Johnson, “Structure and function of amiloride-sensitive Na+ channels,” Journal of Membrane Biology, vol. 143, no. 1, pp. 1–18, 1995. View at Scopus
  60. Y. A. Negulyaev, E. A. Vedernikova, and A. V. Maximov, “Disruption of actin filaments increases the activity of sodium- conducting channels in human myeloid leukemia cells,” Molecular Biology of the Cell, vol. 7, no. 12, pp. 1857–1864, 1996. View at Scopus
  61. A. V. Maximov, E. A. Vedernikova, H. Hinssen, S. Y. Khaitlina, and Y. A. Negulyaev, “Ca-dependent regulation of Na+-selective channels via actin cytoskeleton modification in leukemia cells,” FEBS Letters, vol. 412, no. 1, pp. 94–96, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. A. V. Maximov, E. A. Vedernikova, and N. YuA, “F-actin network regulates the activity of Na+-selective channels in human myeloid leukemia cells. The role of plasma gelsolin and intracellular calcium,” Biophysical Journal, vol. 72, no. 2, part 2, p. A.226, 1997.
  63. T. Harder and K. Simons, “Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation,” European Journal of Immunology, vol. 29, no. 2, pp. 556–562, 1999. View at Publisher · View at Google Scholar
  64. D. A. Brown and E. London, “Structure and function of sphingolipid- and cholesterol-rich membrane rafts,” Journal of Biological Chemistry, vol. 275, no. 23, pp. 17221–17224, 2000. View at Publisher · View at Google Scholar
  65. T. Nebl, K. N. Pestonjamasp, J. D. Leszyk, J. L. Crowley, S. W. Oh, and E. J. Luna, “Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes,” Journal of Biological Chemistry, vol. 277, no. 45, pp. 43399–43409, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. D. A. Brown, “Lipid rafts, detergent-resistant membranes, and raft targeting signals,” Physiology, vol. 21, no. 6, pp. 430–439, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. I. Levitan, A. E. Christian, T. N. Tulenko, and G. H. Rothblat, “Membrane cholesterol content modulates activation of volume-regulated anion current in bovine endothelial cells,” Journal of General Physiology, vol. 115, no. 4, pp. 405–416, 2000. View at Publisher · View at Google Scholar · View at Scopus
  68. V. G. Shlyonsky, F. Mies, and S. Sariban-Sohraby, “Epithelial sodium channel activity in detergent-resistant membrane microdomains,” American Journal of Physiology, vol. 284, no. 1, pp. F182–F188, 2003. View at Scopus
  69. M. Edidin, “The state of lipid rafts: from model membranes to cells,” Annual Review of Biophysics and Biomolecular Structure, vol. 32, pp. 257–283, 2003. View at Publisher · View at Google Scholar
  70. A. V. Sudarikova, Y. A. Negulyaev, and E. A. Morachevskaya, “Cholesterol depletion affects mechanosensitive channel gating coupled with F-actin rearrangement,” Proceedings of the Physical Society, pp. 95–96, 2006.
  71. E. A. Morachevskaya, A. V. Sudarikova, and Y. A. Negulyaev, “Mechanosensitive channel activity and F-actin organization in cholesterol-depleted human leukaemia cells,” Cell Biology International, vol. 31, no. 4, pp. 374–381, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Jalali, M. A. Del Pozo, K. D. Chen et al., “Integrin-mediated mechanotransduction requires its dynamic interaction with specific extracellular matrix (ECM) ligands,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 9, pp. 1042–1046, 2001. View at Scopus
  73. P. J. Butler, T. C. Tsou, J. Y. Li, S. Usami, and S. Chien, “Rate sensitivity of shear-induced changes in the lateral diffusion of endothelial cell membrane lipids: a role for membrane perturbation in shear-induced MAPK activation,” The FASEB Journal, vol. 16, no. 2, pp. 216–218, 2002. View at Scopus
  74. A. J. Maniotis, C. S. Chen, and D. E. Ingber, “Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 3, pp. 849–854, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. D. J. Odde, L. Ma, A. H. Briggs, A. DeMarco, and M. W. Kirschner, “Microtubule bending and breaking in living fibroblast cells,” Journal of Cell Science, vol. 112, no. 19, pp. 3283–3288, 1999. View at Scopus
  76. D. Craig, A. Krammer, K. Schulten, and V. Vogel, “Comparison of the early stages of forced unfolding for fibronectin type III modules,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 10, pp. 5590–5595, 2001. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Gao, D. Craig, V. Vogel, and K. Schulten, “Identifying unfolding intermediates of FN-III10 by steered molecular dynamics,” Journal of Molecular Biology, vol. 323, no. 5, pp. 939–950, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. V. Vogel, W. E. Thomas, D. W. Craig, A. Krammer, and G. Baneyx, “Structural insights into the mechanical regulation of molecular recognition sites,” Trends in Biotechnology, vol. 19, no. 10, pp. 416–423, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. B. Geiger, A. Bershadsky, R. Pankov, and K. M. Yamada, “Transmembrane extracellular matrix-cytoskeleton crosstalk,” Nature Reviews Molecular Cell Biology, vol. 2, no. 11, pp. 793–805, 2001. View at Publisher · View at Google Scholar · View at Scopus
  80. M. E. Chicurel, R. H. Singer, C. J. Meyer, and D. E. Ingber, “Integrin binding and mechanical tension induce movement of mRNA and ribosomes to focal adhesions,” Nature, vol. 392, no. 6677, pp. 730–733, 1998. View at Publisher · View at Google Scholar · View at Scopus
  81. C. Zhong, M. Chrzanowska-Wodnicka, J. Brown, A. Shaub, A. M. Belkin, and K. Burridge, “Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly,” Journal of Cell Biology, vol. 141, no. 2, pp. 539–551, 1998. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Sawada and M. P. Sheetz, “Force transduction by Triton cytoskeletons,” Journal of Cell Biology, vol. 156, no. 4, pp. 609–615, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. D. E. Ingber, “Cellular mechanotransduction: putting all the pieces together again,” FASEB Journal, vol. 20, no. 7, pp. 811–827, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. C. Vera, R. Skelton, F. Bossens, and L. A. Sung, “3-D nanomechanics of an erythrocyte junctional complex in equibiaxial and anisotropic deformations,” Annals of Biomedical Engineering, vol. 33, no. 10, pp. 1387–1404, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. G. Albrecht-Buehler, “The simulation of microgravity conditions on the ground,” ASGSB Bulletin, vol. 5, no. 2, pp. 3–10, 1992. View at Scopus
  86. A. Cogoli, “Gravitational physiology of human immune cells: a review of in vivo, ex vivo and in vitro studies,” Journal of Gravitational Physiology, vol. 3, no. 1, pp. 1–9, 1996. View at Scopus
  87. S. J. Pardo, M. J. Patel, M. C. Sykes et al., “Simulated microgravity using the Random Positioning Machine inhibits differentiation and alters gene expression profiles of 2T3 preosteoblasts,” American Journal of Physiology, vol. 288, no. 6, pp. C1211–C1221, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. J. G. Gershovich, N. A. Konstantinova, P. M. Gershovich, and L. B. Buravkova, “The effects of prolonged gravity vector randomization on differentiation of precursour cells in vitro,” Journal of Gravitational Physiology, vol. 14, no. 1, pp. P133–134, 2007. View at Scopus
  89. L. B. Buravkova, Y. A. Romanov, N. A. Konstantinova, S. V. Buravkov, Y. G. Gershovich, and I. A. Grivennikov, “Cultured stem cells are sensitive to gravity changes,” Acta Astronautica, vol. 63, no. 5-6, pp. 603–608, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. P. M. Gershovich, J. G. Gershovich, and L. B. Buravkova, “Simulated microgravity alters actin cytoskeleton and integrin-mediated focal adhesions of cultured human mesenchymal stromal cells,” in Life in Space for Life on Earth, fra, July 2008. View at Scopus
  91. D. Sarkar, T. Nagaya, K. Koga, and H. Seo, “Culture in vector-averaged gravity environment in a clinostat results in detachment of osteoblastic ROS 17/2.8 cells,” Environmental Medicine, vol. 43, no. 1, pp. 22–24, 1999. View at Scopus
  92. B. M. Uva, M. A. Masini, M. Sturla et al., “Clinorotation-induced weightlessness influences the cytoskeleton of glial cells in culture,” Brain Research, vol. 934, no. 2, pp. 132–139, 2002. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Gaboyard, M. P. Blanchard, C. Travo, M. Viso, A. Sans, and J. Lehouelleur, “Weightlessness affects cytoskeleton of rat utricular hair cells during maturation in vitro,” NeuroReport, vol. 13, no. 16, pp. 2139–2142, 2002. View at Publisher · View at Google Scholar · View at Scopus
  94. P. A. Plett, R. Abonour, S. M. Frankovitz, and C. M. Orschell, “Impact of modeled microgravity on migration, differentiation, and cell cycle control of primitive human hematopoietic progenitor cells,” Experimental Hematology, vol. 32, no. 8, pp. 773–781, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. M. A. Kacena, P. Todd, and W. J. Landis, “Osteoblasts subjected to spaceflight and simulated space shuttle launch conditions,” In Vitro Cellular & Developmental Biology, vol. 39, no. 10, pp. 454–459, 2004.
  96. Z. Q. Dai, R. Wang, S. K. Ling, Y. M. Wan, and Y. H. Li, “Simulated microgravity inhibits the proliferation and osteogenesis of rat bone marrow mesenchymal stem cells,” Cell Proliferation, vol. 40, no. 5, pp. 671–684, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. N. A. Konstantinova, L. B. Buravkova, E. S. Manuilova, and I. A. Grivennikov, “The effects of gravity vector randomization on mouse embryonic stem cells in vitro,” Journal of Gravitational Physiology, vol. 13, no. 1, pp. 149–150, 2006.
  98. M. Zayzafoon, W. E. Gathings, and J. M. McDonald, “Modeled microgravity inhibits osteogenic differentiation of human mesenchymal stem cells and increases adipogenesis,” Endocrinology, vol. 145, no. 5, pp. 2421–2432, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. V. E. Meyers, M. Zayzafoon, J. T. Douglas, and J. M. McDonald, “RhoA and cytoskeletal disruption mediate reduced osteoblastogenesis and enhanced adipogenesis of human mesenchymal stem cells in modeled microgravity,” Journal of Bone and Mineral Research, vol. 20, no. 10, pp. 1858–1866, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. V. E. Meyers, M. Zayzafoon, S. R. Gonda, W. E. Gathings, and J. M. McDonald, “Modeled microgravity disrupts collagen I/integrin signaling during osteoblastic differentiation of human mesenchymal stem cells,” Journal of Cellular Biochemistry, vol. 93, no. 4, pp. 697–707, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. L. Yuge, T. Kajiume, H. Tahara et al., “Microgravity potentiates stem cell proliferation while sustaining the capability of differentiation,” Stem Cells and Development, vol. 15, no. 6, pp. 921–929, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. M. J. Patel, W. Liu, M. C. Sykes et al., “Identification of mechanosensitive genes in osteoblasts by comparative microarray studies using the rotating wall vessel and the Random Positioning Machine,” Journal of Cellular Biochemistry, vol. 101, no. 3, pp. 587–599, 2007. View at Publisher · View at Google Scholar · View at Scopus
  103. Z. Pan, J. Yang, C. Guo et al., “Effects of hindlimb unloading on ex vivo growth and osteogenic/adipogenic potentials of bone marrow-derived mesenchymal stem cells in rats,” Stem Cells and Development, vol. 17, no. 4, pp. 795–804, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. Y. Huang, Z. Q. Dai, S. K. Ling, H. Y. Zhang, Y. M. Wan, and Y. H. Li, “Gravity, a regulation factor in the differentiation of rat bone marrow mesenchymal stem cells,” Journal of Biomedical Science, vol. 16, no. 1, p. 87, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. R. Sordella, W. Jiang, G. C. Chen, M. Curto, and J. Settleman, “Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis,” Cell, vol. 113, no. 2, pp. 147–158, 2003. View at Publisher · View at Google Scholar · View at Scopus
  106. R. McBeath, D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen, “Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment,” Developmental Cell, vol. 6, no. 4, pp. 483–495, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. F. W. Booth and J. R. Kelso, “Effect of hind limb immobilization on contractile and histochemical properties of skeletal muscle,” Pflugers Archiv European Journal of Physiology, vol. 342, no. 3, pp. 231–238, 1973. View at Scopus
  108. D. Desplanches, M. H. Mayet, E. I. Ilyina-Kakueva, B. Sempore, and R. Flandrois, “Skeletal muscle adaptation in rats flown on Cosmos 1667,” Journal of Applied Physiology, vol. 68, no. 1, pp. 48–52, 1990. View at Scopus
  109. Y. Capetanaki, R. J. Bloch, A. Kouloumenta, M. Mavroidis, and S. Psarras, “Muscle intermediate filaments and their links to membranes and membranous organelles,” Experimental Cell Research, vol. 313, no. 10, pp. 2063–2076, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. G. T. Waites, I. R. Graham, P. Jackson et al., “Mutually exclusive splicing of calcium-binding domain exons in chick α- actinin,” Journal of Biological Chemistry, vol. 267, no. 9, pp. 6263–6271, 1992. View at Scopus
  111. K. Lee, Y. S. Lee, M. Lee, M. Yamashita, and I. Choi, “Mechanics and fatigability of the rat soleus muscle during early reloading,” Yonsei Medical Journal, vol. 45, no. 4, pp. 690–702, 2004. View at Scopus
  112. K. S. McDonald and R. H. Fitts, “Effect of hindlimb unloading on rat soleus fiber force, stiffness, and calcium sensitivity,” Journal of Applied Physiology, vol. 79, no. 5, pp. 1796–1802, 1995. View at Scopus
  113. W. E. Thornton, T. P. Moore, and S. L. Pool, “Fluid shifts in weightlessness,” Aviation, Space, and Environmental Medicine, vol. 58, no. 9, pp. A86–A90, 1987.
  114. D. E. Watenpaugh and A. R. Hargens, “The cardiovascular system in microgravity,” in Handbook of Physiology. Environmental Physiology, vol. 1, part 3, chapter 29, pp. 631–674, American Physiological Society, Bethesda, Md, USA, 4th edition, 1996.
  115. J. V. Nixon, R. G. Murray, C. Bryant et al., “Early cardiovascular adaptation to simulated zero gravity,” Journal of Applied Physiology, vol. 46, no. 3, pp. 541–548, 1979.
  116. M. W. Bungo, D. J. Goldwater, R. L. Popp, and H. Sandler, “Echocardiographic evaluation of space shuttle crewmembers,” Journal of Applied Physiology, vol. 62, no. 1, pp. 278–283, 1987. View at Scopus
  117. J. B. Charles and C. M. Lathers, “Cardiovascular adaptation to spaceflight,” Journal of Clinical Pharmacology, vol. 31, pp. 1010–1023, 1991.
  118. E. Morey-Holton, R. K. Globus, A. Kaplansky, and G. Durnova, “The hindlimb unloading rat model: literature overview, technique update and comparison with space flight data,” Advances in Space Biology and Medicine, vol. 10, pp. 7–40, 2005. View at Publisher · View at Google Scholar · View at Scopus
  119. C. P. Ingalls, G. L. Warren, and R. B. Armstrong, “Intracellular Ca2+ transients in mouse soleus muscle after hindlimb unloading and reloading,” Journal of Applied Physiology, vol. 87, no. 1, pp. 386–390, 1999. View at Scopus
  120. C. P. Ingalls, J. C. Wenke, and R. B. Armstrong, “Time course changes in [Ca2+]i, force, and protein content in hindlimb-suspended mouse soleus muscles,” Aviation Space and Environmental Medicine, vol. 72, no. 5, pp. 471–476, 2001. View at Scopus
  121. I. V. Ogneva, V. A. Kurushin, E. G. Altaeva, E. V. Ponomareva, and B. S. Shenkman, “Effect of short-term gravitational unloading on rat and mongolian gerbil muscles,” Journal of Muscle Research and Cell Motility, vol. 30, no. 7-8, pp. 261–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  122. D. L. Enns, T. Raastad, I. Ugelstad, and A. N. Belcastro, “Calpain/calpastatin activities and substrate depletion patterns during hindlimb unweighting and reweighting in skeletal muscle,” European Journal of Applied Physiology, vol. 100, no. 4, pp. 445–455, 2007. View at Publisher · View at Google Scholar · View at Scopus
  123. E. G. Altaeva, L. A. Lysenko, N. P. Kantserova, N. N. Nemova, and B. S. Shenkman, “The basal calcium level in fibers of the rat soleus muscle under gravitational unloading: the mechanisms of its increase and the role in calpain activation,” Doklady Biological Sciences, vol. 433, no. 1, pp. 241–243, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. I. V. Ogneva, “Transversal stiffness and beta-actin and alpha-actinin-4 content of the m. Soleus fibers in the conditions of a 3-day reloading after 14-day gravitational unloading,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 393405, 7 pages, 2011. View at Publisher · View at Google Scholar
  125. T. Parr, G. T. Waites, B. Patel, D. B. Millake, and D. R. Critchley, “A chick skeletal-muscle α-actinin gene gives rise to two alternatively spliced isoforms which differ in the EF-hand Ca2+-binding domain,” European Journal of Biochemistry, vol. 210, no. 3, pp. 801–809, 1992. View at Publisher · View at Google Scholar · View at Scopus
  126. C. Velez, A. E. Aranega, J. C. Prados, C. Melguizo, L. Alvarez, and A. Aranega, “Basic fibroblast and platelet-derived growth factors as modulators of actin and α-actinin in chick myocardiocytes during development,” Proceedings of the Society for Experimental Biology and Medicine, vol. 210, no. 1, pp. 57–63, 1995. View at Scopus
  127. S. Goffart, A. Franko, C. S. Clemen, and R. J. Wiesner, “α-Actinin 4 and BAT1 interaction with the Cytochrome c promoter upon skeletal muscle differentiation,” Current Genetics, vol. 49, no. 2, pp. 125–135, 2006. View at Publisher · View at Google Scholar · View at Scopus
  128. M. J. F. Broderick and S. J. Winder, “Towards a complete atomic structure of spectrin family proteins,” Journal of Structural Biology, vol. 137, no. 1-2, pp. 184–193, 2002. View at Publisher · View at Google Scholar
  129. H. Youssoufian, M. McAfee, and D. J. Kwiatkowski, “Cloning and chromosomal localization of the human cytoskeletal α-actinin gene reveals linkage to the β-spectrin gene,” American Journal of Human Genetics, vol. 47, no. 1, pp. 62–72, 1990. View at Scopus
  130. M. D. Baron, M. D. Davison, P. Jones, and D. R. Critchley, “The structure and function of alpha-actinin,” Biochemical Society Transactions, vol. 15, no. 5, pp. 796–798, 1987. View at Scopus
  131. K. Honda, T. Yamada, R. Endo et al., “Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion,” Journal of Cell Biology, vol. 140, no. 6, pp. 1383–1393, 1998. View at Publisher · View at Google Scholar · View at Scopus
  132. Y. Capetanaki and D. J. Milner, “Desmin cytoskeleton in muscle integrity and function,” Sub-Cellular Biochemistry, vol. 31, pp. 463–495, 1998. View at Scopus
  133. D. J. Milner, M. Mavroidis, N. Weisleder, and Y. Capetanaki, “Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function,” Journal of Cell Biology, vol. 150, no. 6, pp. 1283–1297, 2000. View at Publisher · View at Google Scholar · View at Scopus
  134. T. M. Mirzoev, N. S. Biryukov, O. M. Veselova, I. M. Larina, B. S. Shenkman, and I. V. Ogneva, “Parameters of fibers cell respiration and desmin content in rat soleus muscle at early stages of gravitational unloading,” Biophysics, vol. 57, no. 3, pp. 509–514, 2012.
  135. T. M. Mirzoev, N. S. Biryukov, O. M. Veselova, I. M. Larina, B. S. Shenkman, and I. V. Ogneva, “Content of desmin and energy substrates and cell respiration of the rat's m. soleus fibers under 3- and 7-day reloading after 14-day unloading,” Aviakosmicheskaia i Ekologicheskaia Meditsina, vol. 46, no. 1, pp. 41–45, 2012.
  136. D. A. Krieger, C. A. Tate, J. McMillin-Wood, and F. W. Booth, “Populations of rat skeletal muscle mitochondria after exercise and immobilization,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 48, no. 1, pp. 23–28, 1980. View at Scopus
  137. I. N. Belozerova, T. L. Nemirovskaya, and B. S. Shenkman, “Structural and metabolic profile of rhesus monkey m. vastus lateralis after spaceflight,” Journal of Gravitational Physiology, vol. 7, no. 1, pp. S55–58, 2000. View at Scopus
  138. A. X. Bigard, E. Boehm, V. Veksler, P. Mateo, K. Anflous, and R. Ventura-Clapier, “Muscle unloading induces slow to fast transitions in myofibrillar but not mitochondrial properties. Relevance to skeletal muscle abnormalities in heart failure,” Journal of Molecular and Cellular Cardiology, vol. 30, no. 11, pp. 2391–2401, 1998. View at Publisher · View at Google Scholar · View at Scopus
  139. V. A. Saks, A. Kuznetsov, T. Andrienko et al., “Heterogeneity of ADP diffusion and regulation of respiration in cardiac cells,” Biophysical Journal, vol. 84, no. 5, pp. 3436–3456, 2003. View at Scopus
  140. T. Kunishima, “Ultrastructural and biochemical enzymatic properties of right ventricular muscles during hindlimb suspension in rats,” Nihon Seirigaku Zasshi, vol. 55, no. 4, pp. 153–164, 1993.