Advertisement

Gravitational Effects on Human Physiology

  • Yoriko Atomi
Part of the Subcellular Biochemistry book series (SCBI, volume 72)

Abstract

Physical working capacity decreases with age and also in microgravity. Regardless of age, increased physical activity can always improve the physical adaptability of the body, although the mechanisms of this adaptability are unknown. Physical exercise produces various mechanical stimuli in the body, and these stimuli may be essential for cell survival in organisms. The cytoskeleton plays an important role in maintaining cell shape and tension development, and in various molecular and/or cellular organelles involved in cellular trafficking. Both intra and extracellular stimuli send signals through the cytoskeleton to the nucleus and modulate gene expression via an intrinsic property, namely the “dynamic instability” of cytoskeletal proteins. αB-crystallin is an important chaperone for cytoskeletal proteins in muscle cells. Decreases in the levels of αB-crystallin are specifically associated with a marked decrease in muscle mass (atrophy) in a rat hindlimb suspension model that mimics muscle and bone atrophy that occurs in space and increases with passive stretch. Moreover, immunofluorescence data show complete co-localization of αB-crystallin and the tubulin/microtubule system in myoblast cells. This association was further confirmed in biochemical experiments carried out in vitro showing that αB-crystallin acts as a chaperone for heat-denatured tubulin and prevents microtubule disassembly induced by calcium. Physical activity induces the constitutive expression of αB-crystallin, which helps to maintain the homeostasis of cytoskeleton dynamics in response to gravitational forces. This relationship between chaperone expression levels and regulation of cytoskeletal dynamics observed in slow anti-gravitational muscles as well as in mammalian striated muscles, such as those in the heart, diaphragm and tongue, may have been especially essential for human evolution in particular. Elucidation of the intrinsic properties of the tubulin/microtubule and chaperone αB-crystallin protein complex systems is expected to provide valuable information for high-pressure bioscience and gravity health science.

Keywords

Cytoskeleton Dynamic instability Mechanical stress response Molecular chaperone Slow muscle 

References

  1. Agarkova I, Schoenauer R, Ehler E, Carlsson L, Carlsson E, Thornell LE, Perriard JC (2004) The molecular composition of the sarcomeric M-band correlates with muscle fiber type. Eur J Cell Biol 83:193–204PubMedCrossRefGoogle Scholar
  2. Agbulut O, Li Z, Mouly V, Butler-Browne GS (1996) Analysis of skeletal and cardiac muscle from desmin knock-out and normal mice by high resolution separation of myosin heavy-chain isoforms. Biol Cell 88:131–135PubMedCrossRefGoogle Scholar
  3. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, Mukku V, Edgerton VR (1997) Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol 273(2 Pt 1):C579–C587PubMedGoogle Scholar
  4. American Society for Gravitational and Space Research (2013) Physiological slides. American Society for Gravitational and Space Research Website. https://www.asgsr.org/index.php/education/slide-sets
  5. Appaix F, Kuznetsov AV, Usson Y, Kay L, Andrienko T, Olivares J, Kaambre T, Sikk P, Margreiter R, Saks V (2003) Possible role of cytoskeleton in intracellular arrangement and regulation of mitochondria. Exp Physiol 88:175–190PubMedCrossRefGoogle Scholar
  6. Arai H, Atomi Y (1997) Chaperone activity of αB-crystallin suppresses tubulin aggregation through complex formation. Cell Struct Funct 22:539–544PubMedCrossRefGoogle Scholar
  7. Arany Z, Wagner BK, Ma Y, Chinsomboon J, Laznik D, Spiegelman BM (2008) Gene expression-based screening identifies microtubule inhibitors as inducers of PGC-1α and oxidative phosphorylation. Proc Natl Acad Sci U S A 105:4721–4726PubMedCentralPubMedCrossRefGoogle Scholar
  8. Atomi Y (1980) Aerobic capacity of Japanese adult women. Doctoral Thesis, The University of TokyoGoogle Scholar
  9. Atomi Y (1992) Decreased αB-crystallin in soleus muscle atrophy and role of αB-Crystallin in muscle. Med Sport Sci 37:171–192CrossRefGoogle Scholar
  10. Atomi Y (1999) Why active life is important for health and longevity? From the studies of stress protein and mechanical stress. In: Current reviews of medical science by women, International Conference of Women Engineers and Scientists, Tokyo, 150–153Google Scholar
  11. Atomi Y, Fukunaga T, Hana H, Yamamoto Y (1987) Relationship between lactate threshold during running and relative gastrocnemius area. J Appl Physiol 63:2343–2347PubMedGoogle Scholar
  12. Atomi Y, Miyashita M (1974) Maximal aerobic power of Japanese active and sedentary adult females of different ages (20 to 62 years). Med Sci Sports 6:223–225PubMedGoogle Scholar
  13. Atomi Y, Toro K, Masuda T, Hatta H (2000) Fiber-type-specific αB-crystallin distribution and its shifts with T(3) and PTU treatments in rat hindlimb muscles. J Appl Physiol 88:1355–1364PubMedGoogle Scholar
  14. Atomi Y, Yamada S (1986) Mechanism of muscle atrophy. III. A model of muscle atrophy with the tail suspension of rat. Dept Sports Sci Univ Tokyo 20:8–12Google Scholar
  15. Atomi Y, Yamada S, Hong Y-M (1990) Dynamic expression of αB-crystallin in skeletal muscle -effects of unweighting, passive stretch and denervation. Proc Japan Acad 66B:203–208CrossRefGoogle Scholar
  16. Atomi Y, Yamada S, Nishida T (1991a) Early changes of αB-crystallin mRNA in rat skeletal muscle to mechanical tension and denervation. Biochem Biophys Res Commun 181:1323–1330PubMedCrossRefGoogle Scholar
  17. Atomi Y, Yamada S, Strohman R, Nonomura Y (1991b) αB-crystallin in skeletal muscle: purification and localization. J Biochem 110:812–822PubMedGoogle Scholar
  18. Baba M (2001) Brain and nerves in pictures: their system and mechanism of the disorder, 2nd Japanese edn. Igaku Shoin, Tokyo, 1–233Google Scholar
  19. Bandyopadhyay A, Saxena K, Kasturia N, Dalal V, Bhatt N, Rajkumar A, Maity S, Sengupta S, Chakraborty K (2012) Chemical chaperones assist intracellular folding to buffer mutational variations. Nat Chem Biol 8:238–245PubMedCentralPubMedCrossRefGoogle Scholar
  20. Bauer NG, Richter-Landsberg C (2006) The dynamic instability of microtubules is required for aggresome formation in oligodendroglial cells after proteolytic stress. J Mol Neurosci 29:153–168PubMedCrossRefGoogle Scholar
  21. Bogumil D, Dagan T (2012) Cumulative impact of chaperone-mediated folding on genome evolution. Biochemistry 51:9941–9953PubMedCrossRefGoogle Scholar
  22. Boudriau S, Vincent M, Côté CH, Rogers PA (1993) Cytoskeletal structure of skeletal muscle: identification of an intricate exosarcomeric microtubule lattice in slow- and fast-twitch muscle fibers. J Histochem Cytochem 41:1013–1021PubMedCrossRefGoogle Scholar
  23. Bramble DM, Lieberman DF (2004) Endurance running and the evolution of Homo. Nature 432:345–352PubMedCrossRefGoogle Scholar
  24. Bray D (2001) Chapter 5: Actin filaments. In: Bray D (ed) Cell movements: from molecules to motility, 2nd edn. Garland, New York, 65–80Google Scholar
  25. Brígido C, Oliveira S (2012) Most acid-tolerant chickpea mesorhizobia show induction of major chaperone genes upon acid shock. Microb Ecol 65:145–153PubMedCrossRefGoogle Scholar
  26. Bulinski JC, Gundersen GG (1991) Stabilization of post-translational modification of microtubules during cellular morphogenesis. Bioessays 13:285–293PubMedCrossRefGoogle Scholar
  27. Calabrese V, Cornelius C, Cuzzocrea S, Iavicoli I, Rizzarelli E, Calabrese EJ (2011) Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity. Mol Aspects Med 32:279–304PubMedCrossRefGoogle Scholar
  28. Campbell WG, Gordon SE, Carlson CJ, Pattison JS, Hamilton MT, Booth FW (2001) Differential global gene expression in red and white skeletal muscle. Am J Physiol Cell Physiol 280:C763–C768PubMedGoogle Scholar
  29. Carver JA, Lindner RA, Lyon C, Canet D, Hernandez H, Dobson CM, Redfield C (2002) The interaction of the molecular chaperone α-crystallin with unfolding α-lactalbumin: a structural and kinetic spectroscopic study. J Mol Biol 318:815–827PubMedCrossRefGoogle Scholar
  30. Chang W, Webster DR, Salam AA, Gruber D, Prasad A, Eiserich JP, Bulinski JC (2002) Alteration of the C-terminal amino acid of tubulin specifically inhibits myogenic differentiation. J Biol Chem 277:30690–30698PubMedCrossRefGoogle Scholar
  31. Close RI (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129–197PubMedGoogle Scholar
  32. Dart KC, Schultz E (1989) Hindlimb suspension suppresses muscle growth and satellite cell proliferation. J Appl Physiol 67:1827–1834Google Scholar
  33. Desjardins PR, Burkman JM, Shrager JB, Allmond LA, Stedman HH (2002) Evolutionary implications of three novel members of the human sarcomeric myosin heavy chain gene family. Mol Biol Evol 19:375–393PubMedCrossRefGoogle Scholar
  34. Dubin RA, Wawrousek EF, Piatigorsky J (1989) Expression of the murine αB-crystallin gene is not restricted to the lens. Mol Cell Biol 9:1083–1091PubMedCentralPubMedCrossRefGoogle Scholar
  35. Dulhunty AF, Franzini-Armstrong C (1975) The relative contributions of the folds and caveolae to the surface membrane of frog skeletal muscle fibres at different sarcomere lengths. J Physiol 250:513–539PubMedCentralPubMedCrossRefGoogle Scholar
  36. Eason JM, Schwartz GA, Pavlath GK, English AW (2000) Sexually dimorphic expression of myosin heavy chains in the adult mouse masseter. J Appl Physiol 89:251–258PubMedGoogle Scholar
  37. Endo M (1937) Muscle weights of human lower legs related to the development. J Tokyo Med Sci 51:1177–1185Google Scholar
  38. Esnault C, Stewart A, Gualdrini F, East P, Horswell S, Matthews N, Treisman R (2014) Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev 28:943–958PubMedCentralPubMedCrossRefGoogle Scholar
  39. Féasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, Denis C (2002) Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 543(Pt 1):297–306PubMedCentralPubMedCrossRefGoogle Scholar
  40. Frankenberg NT, Lamb GD, Overgaard K, Murphy RM, Vissing K (2014) Small heat shock proteins translocate to the cytoskeleton in human skeletal muscle following eccentric exercise independently of phosphorylation. J Appl Physiol 116:1463–1472PubMedCrossRefGoogle Scholar
  41. Fujita Y, Ohto E, Katayama E, Atomi Y (2004) αB-Crystallin-coated MAP microtubule resists nocodazole and calcium-induced disassembly. J Cell Sci 117:1719–1726PubMedCrossRefGoogle Scholar
  42. Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, Kenyon C (2002) Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161:1101–1112PubMedCentralPubMedGoogle Scholar
  43. Goldman RD, Chou YH, Prahlad V, Yoon M (1999) Intermediate filaments: dynamic processes regulating their assembly, motility, and interactions with other cytoskeletal systems. FASEB J 13(Suppl 2):S261–S265PubMedGoogle Scholar
  44. Goldspink DF (1980) Physiological factors influencing protein turnover and muscle growth in mammals. In: Goldspink DF (ed) Development and specialization of skeletal muscle. Cambridge University Press, London, pp 65–89Google Scholar
  45. Gollnick PD, Sjödin B, Karlsson J, Jansson E, Saltin B (1974) Human soleus muscle: a comparison of fiber composition and enzyme activities with other leg muscles. Pflugers Arch 348:247–255PubMedCrossRefGoogle Scholar
  46. Goyal RK, Kumar V, Shukla V, Mattoo R, Liu Y, Chung SH, Giovannoni JJ, Mattoo AK (2012) Features of a unique intronless cluster of class I small heat shock protein genes in tandem with box C/D snoRNA genes on chromosome 6 in tomato (Solanum lycopersicum). Planta 235:453–471PubMedCrossRefGoogle Scholar
  47. Gros PA, Tenaillon O (2009) Selection for chaperone-like mediated genetic robustness at low mutation rate: impact of drift, epistasis and complexity. Genetics 182(2):555–564PubMedCentralPubMedCrossRefGoogle Scholar
  48. Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 11:81–94PubMedCrossRefGoogle Scholar
  49. Gundersen GG, Khawaja S, Bulinski JC (1989) Generation of a stable, posttranslationally modified microtubule array is an early event in myogenic differentiation. J Cell Biol 109:2275–2288PubMedCrossRefGoogle Scholar
  50. Gyoeva FK, Gelfand VI (1991) Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353:445–448PubMedCrossRefGoogle Scholar
  51. Healy EF, Little C, King PJ (2014) A model for small heat shock protein inhibition of polyglutamine aggregation. Cell Biochem Biophys 69:275–281PubMedCrossRefGoogle Scholar
  52. Hishiya A, Takayama S (2008) Molecular chaperones as regulators of cell death. Oncogene 27:6489–6506PubMedCrossRefGoogle Scholar
  53. Hochberg GK, Ecroyd H, Liu C, Cox D, Cascio D, Sawaya MR, Collier MP, Stroud J, Carver JA, Baldwin AJ, Robinson CV, Eisenberg DS, Benesch JL, Laganowsky A (2014) The structured core domain of αB-crystallin can prevent amyloid fibrillation and associated toxicity. Proc Natl Acad Sci U S A 111:E1562–E1570PubMedCentralPubMedCrossRefGoogle Scholar
  54. Hoson T, Matsumoto S, Soga K, Wakabayashi K (2010) Cortical microtubules are responsible for gravity resistance in plants. Plant Signal Behav 5:752–754PubMedCentralPubMedCrossRefGoogle Scholar
  55. Houck SA, Landsbury A, Clark JI, Quinlan RA (2011) Multiple sites in αB-crystallin modulate its interactions with desmin filaments assembled in vitro. PLoS One 6:e25859PubMedCentralPubMedCrossRefGoogle Scholar
  56. Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300:1142–1145PubMedCrossRefGoogle Scholar
  57. Iki T, Yoshikawa M, Nishikiori M, Jaudal MC, Matsumoto-Yokoyama E, Mitsuhara I, Meshi T, Ishikawa M (2010) In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol Cell 39:282–291PubMedCrossRefGoogle Scholar
  58. Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104:613–627PubMedGoogle Scholar
  59. Ingber DE (1997) Tensegrity: the architectural basis of cellular mechanotransduction. Annu Rev Physiol 59:575–599PubMedCrossRefGoogle Scholar
  60. Iwaki T, Kume-Iwaki A, Goldman JE (1990) Cellular distribution of αB-crystallin in non-lenticular tissues. J Histochem Cytochem 38:31–39PubMedCrossRefGoogle Scholar
  61. Jee H, Sakurai T, Kawada S, Ishii N, Atomi Y (2009) Significant roles of microtubules in mature striated muscle deduced from the correlation between tubulin and its molecular chaperone αB-crystallin in rat muscles. J Physiol Sci 59:149–155PubMedCrossRefGoogle Scholar
  62. Karakesisoglou I, Yang Y, Fuchs E (2000) An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J Cell Biol 149:195–208PubMedCentralPubMedCrossRefGoogle Scholar
  63. Kim BS, Kim MY, Leem YH (2011) Hippocampal neuronal death induced by kainic acid and restraint stress is suppressed by exercise. Neuroscience 194:291–301PubMedCrossRefGoogle Scholar
  64. Kirschner MW (1980) Implications of treadmilling for the stability and polarity of actin and tubulin polymers in vivo. J Cell Biol 86:330–334PubMedCrossRefGoogle Scholar
  65. Koh TJ, Escobedo J (2004) Cytoskeletal disruption and small heat shock protein translocation immediately after lengthening contractions. Am J Physiol Cell Physiol 286:C713–C722PubMedCrossRefGoogle Scholar
  66. Korfage JA, Van Eijden TM (1999) Regional differences in fibre type composition in the human temporalis muscle. J Anat 194:355–362PubMedCentralPubMedCrossRefGoogle Scholar
  67. Labbadia J, Morimoto RI (2014) Proteostasis and longevity: when does aging really begin? F1000Prime Rep 6:7Google Scholar
  68. Ladner JT, Barshis DJ, Palumbi SR (2012) Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol Biol 12:217PubMedCentralPubMedCrossRefGoogle Scholar
  69. Lagisz M, Hector KL, Nakagawa S (2013) Life extension after heat shock exposure: assessing meta-analytic evidence for hormesis. Ageing Res Rev 12:653–660PubMedCrossRefGoogle Scholar
  70. Laskey RA, Honda BM, Mills AD, Finch JT (1978) Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275:416–420PubMedCrossRefGoogle Scholar
  71. Lazarides E (1981) Intermediate filaments – chemical heterogeneity in differentiation. Cell 23:649–650PubMedCrossRefGoogle Scholar
  72. Lele TP, Thodeti CK, Ingber DE (2006) Forced meets chemistry: analysis of mechanochemical conversion in focal adhesions using fluorescence recovery after photobleaching. J Cell Biochem 97:1175–1183PubMedCrossRefGoogle Scholar
  73. Leung CL, Sun D, Zheng M, Knowles DR, Liem RK (1999) Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 147:1275–1286PubMedCentralPubMedCrossRefGoogle Scholar
  74. Li K, Jiang T, Yu B, Wang L, Gao C, Ma C, Xu P, Ma Y (2012) Transcription elongation factor GreA has functional chaperone activity. PLoS One 7:e47521PubMedCentralPubMedCrossRefGoogle Scholar
  75. Li R, Gundersen GG (2008) Beyond polymer polarity: how the cytoskeleton builds a polarized cell. Nat Rev Mol Cell Biol 9:860–873PubMedCrossRefGoogle Scholar
  76. Liao G, Gundersen GG (1998) Kinesin is a candidate for cross- bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J Biol Chem 273:9797–9803PubMedCrossRefGoogle Scholar
  77. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM (2002) Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres. Nature 418:797–801PubMedCrossRefGoogle Scholar
  78. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ, Rustgi A, Fuchs SY, Diehl JA (2006) Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF (FBX4-αB crystallin) complex. Mol Cell 24:355–366PubMedCentralPubMedCrossRefGoogle Scholar
  79. McElhinny AS, Perry CN, Witt CC, Labeit S, Gregorio CC (2004) Muscle-specific RING finger-2 (MURF-2) is important for microtubule, intermediate filament and sarcomeric M-line maintenance in striated muscle development. J Cell Sci 117:3175–3188PubMedCrossRefGoogle Scholar
  80. Maruyama K, Natori R, Nonomura Y (1976) New elastic protein from muscle. Nature 262:58–60PubMedCrossRefGoogle Scholar
  81. Mendez R, Fritsche M, Porto M, Bastolla U (2010) Mutation bias favors protein folding stability in the evolution of small populations. PLoS Comput Biol 6:e1000767PubMedCentralPubMedCrossRefGoogle Scholar
  82. Mitchison T, Kirschner M (1984) Dynamic instability of micro-tubule growth. Nature 312:237–242PubMedCrossRefGoogle Scholar
  83. Morey ER (1979) Spaceflight and bone turnover: correlation with a new rat model of weightlessness. BioSci 29:168–172CrossRefGoogle Scholar
  84. Mozdziak PE, Troung Q, Macius A, Schultz E (1998) Hindlimb suspension reduces muscle regeneration. Eur J Appl Physiol Occup Physiol 78:136–140PubMedCrossRefGoogle Scholar
  85. Musacchia XJ, Steffen JM, Fell RD (1988) Disuse atrophy of skeletal muscle: animal models. Exerc Sport Sci Rev 16:61–87PubMedCrossRefGoogle Scholar
  86. Nakata T, Nishina Y, Yorifuji H (2001) Cytoplasmic gamma actin as a Z-disc protein. Biochem Biophys Res Commun 286:156–163PubMedCrossRefGoogle Scholar
  87. Nicholl RA, Quinlan RA (1994) Chaperone activity of α-crystallins modulates intermediate filament assembly. EMBO J 13:945–953PubMedCentralPubMedGoogle Scholar
  88. Nicogossian AE, Huntoon CL, Pool SL (1989) Space physiology and medicine, 2nd edn. Lea and Febiger, PhiladelphiaGoogle Scholar
  89. Niwa M, Jaaro-Peled H, Tankou S, Seshadri S, Hikida T, Matsumoto Y, Cascella NG, Kano S, Ozaki N, Nabeshima T, Sawa A (2013) Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 339:335–339PubMedCentralPubMedCrossRefGoogle Scholar
  90. Ohto-Fujita E, Fujita Y, Atomi Y (2007) Analysis of the αB-crystallin domain responsible for inhibiting tubulin aggregation. Cell Stress Chaperones 12:163–171PubMedCentralPubMedCrossRefGoogle Scholar
  91. Ousman SS, Tomooka BH, van Noort JM, Wawrousek EF, O'Connor KC, Hafler DA, Sobel RA, Robinson WH, Steinman L (2007) Protective and therapeutic role for αB-crystallin in autoimmune demyelination. Nature 448:474–479PubMedCrossRefGoogle Scholar
  92. Papaseit C, Pochon N, Tabony J (2000) Microtubule self-organization is gravity-dependent. Proc Natl Acad Sci U S A 97:8364–8368PubMedCentralPubMedCrossRefGoogle Scholar
  93. Paulsen G, Lauritzen F, Bayer ML, Kalhovde JM, Ugelstad I, Owe SG, Hallén J, Bergersen LH, Raastad T (2009) Subcellular movement and expression of HSP27, αB-crystallin, and HSP70 after two bouts of eccentric exercise in humans. J Appl Physiol 107:570–582PubMedCrossRefGoogle Scholar
  94. Pedersen BK (2013) Muscle as a secretory organ. Compr Physiol J 3:1337–1362Google Scholar
  95. Quinlan JA, Ellis RJ (2013) Chaperones: needed for both the good times and the bad times. Philos Trans R Soc Lond B Biol Sci 368:e0091Google Scholar
  96. Ralston E, Lu Z, Ploug T (1999) The organization of the Golgi complex and microtubules in skeletal muscle is fiber type-dependent. J Neurosci 19:10694–10705PubMedGoogle Scholar
  97. Ralston E, Ploug T, Kalhovde J, Lomo T (2001) Golgi complex, endoplasmic reticulum exit sites, and microtubules in skeletal muscle fibers are organized by patterned activity. J Neurosci 21:875–883PubMedGoogle Scholar
  98. Ruoslahti E (1997) Stretching is good for a cell. Science 276:1345–1346PubMedCrossRefGoogle Scholar
  99. Sakurai T, Fujita Y, Ohto E, Oguro A, Atomi Y (2005) The decrease of the cytoskeleton tubulin follows the decrease of the associating molecular chaperone αB-crystallin in unloaded soleus muscle atrophy without stretch. FASEB J 19:1199–1201PubMedGoogle Scholar
  100. Satake T, Atomi Y, Okajima Y (1987) Effect of physical activity in daily life on muscle weight and relative weight of the M. triceps surae. J Phys Fitness Jpn 36:25–30Google Scholar
  101. Schmidt RF ed., Uchizono K et al. transl. (1988) Fundamentals of neurophysiology, 2nd Japanese edn. Kinpodo, Kyoto, pp 1–325Google Scholar
  102. Schoenauer R, Lange S, Hirschy A, Ehler E, Perriard JC, Agarkova I (2008) Myomesin 3, a novel structural component of the M-band in striated muscle. J Mol Biol 376:338–351PubMedCrossRefGoogle Scholar
  103. Shao W, Zhang SZ, Tang M, Zhang XH, Zhou Z, Yin YQ, Zhou QB, Huang YY, Liu YJ, Wawrousek E, Chen T, Li SB, Xu M, Zhou JN, Hu G, Zhou JW (2013) Suppression of neuroinflammation by astrocytic dopamine D2 receptors via αB-crystallin. Nature 494:90–94PubMedCrossRefGoogle Scholar
  104. Sheldon KL, Maldonado EN, Lemasters JJ, Rostovtseva TK, Bezrukov SM (2011) Phosphorylation of voltage-dependent anion channel by serine/threonine kinases governs its interaction with tubulin. PLoS One 6:e25539PubMedCentralPubMedCrossRefGoogle Scholar
  105. Singh BN, Rao KS, Ramakrishna T, Rangaraj N, Rao CM (2007) Association of αB-crystallin, a small heat shock protein, with actin: role in modulating actin filament dynamics in vivo. J Mol Biol 366:756–767PubMedCrossRefGoogle Scholar
  106. Sjöström M, Kidman S, Larsén KH, Angquist KA (1982) Z- and M-band appearance in different histochemically defined types of human skeletal muscle fibers. J Histochem Cytochem 30:1–11PubMedCrossRefGoogle Scholar
  107. Skoyles JR (2006) Human balance, the evolution of bipedalism and dysequilibrium syndrome. Med Hypotheses 66:1060–1068PubMedCrossRefGoogle Scholar
  108. Song S, Landsbury A, Dahm R, Liu Y, Zhang Q, Quinlan RA (2009) Functions of the intermediate filament cytoskeleton in the eye lens. J Clin Invest 119:1837–1848PubMedCentralPubMedCrossRefGoogle Scholar
  109. Spencer JA, Eliazer S, Ilaria RL, Richardson JA, Olson EN (2000) Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J Cell Biol 150:771–784PubMedCentralPubMedCrossRefGoogle Scholar
  110. Stecyk JA, Couturier CS, Fagernes CE, Ellefsen S, Nilsson GE (2012) Quantification of heat shock protein mRNA expression in warm and cold anoxic turtles (Trachemys scripta) using an external RNA control for normalization. Genom Proteom 7:59–72Google Scholar
  111. Steinman L (2009) A molecular trio in relapse and remission in multiple sclerosis. Nat Rev Immunol 9:440–447PubMedCrossRefGoogle Scholar
  112. Tabony J, Job D (1990) Spatial structures in microtubular solutions requiring a sustained energy source. Nature 346:448–451PubMedCrossRefGoogle Scholar
  113. Tabony J, Glade N, Papaseit C, Demongeot J (2002) Microtubule self-organisation and its gravity dependence. Adv Space Biol Med 8:19–58PubMedCrossRefGoogle Scholar
  114. Tabony J, Rigotti N, Glade N, Cortès S (2007) Effect of weightlessness on colloidal particle transport and segregation in self-organising microtubule preparations. Biophys Chem 127:172–180PubMedCrossRefGoogle Scholar
  115. Tanaka H, DeSouza CA, Seals DR (1998) Arterial stiffness and hormone replacement use in healthy postmenopausal women. J Gerontol 53:M344–M346CrossRefGoogle Scholar
  116. Tepp K, Mado K, Varikmaa M, Klepinin A, Timohhina N, Shevchuk I, Chekulayev V, Kuznetsov AV, Guzun R, Kaambre T (2014) The role of tubulin in the mitochondrial metabolism and arrangement in muscle cells. J Bioenerg Biomembr 46:421–434PubMedCrossRefGoogle Scholar
  117. Thomason DB, Booth FW (1990) Atrophy of the soleus muscle by hindlimb unweighting. J Appl Physiol 68:1–12PubMedCrossRefGoogle Scholar
  118. Thomason DB, Riggs RB, Booth FW (1989) Protein metabolism and β-myosin heavy-chain mRNA in unweighted soleus muscle. Am J Physiol 257:R300–R305PubMedGoogle Scholar
  119. Treisman R (1995) Journey to the surface of the cell: Fos regulation and the SRE. EMBO J 14:4905–4913PubMedCentralPubMedGoogle Scholar
  120. Treisman R (2013) Shedding light on nuclear actin dynamics and function. Trends Biochem Sci 38:376–377PubMedCrossRefGoogle Scholar
  121. Tsai YL, Chiang YR, Narberhaus F, Baron C, Lai EM (2010) The small heat-shock protein HspL is a VirB8 chaperone promoting type IV secretion-mediated DNA transfer. J Biol Chem 285:19757–19766PubMedCentralPubMedCrossRefGoogle Scholar
  122. Wang W, Sreekumar PG, Valluripalli V, Shi P, Wang J, Lin YA, Cui H, Kannan R, Hinton DR, MacKay JA (2014) Protein polymer nanoparticles engineered as chaperones protect against apoptosis in human retinal pigment epithelial cells. J Control Release 191:4–14PubMedCentralPubMedCrossRefGoogle Scholar
  123. Waterman-Storer CM, Salmon ED (1997) Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 139:417–434PubMedCentralPubMedCrossRefGoogle Scholar
  124. Webster KA (2003) Serine phosphorylation and suppression of apoptosis by the small heat shock protein αB-crystallin. Circ Res 92:130–132PubMedCrossRefGoogle Scholar
  125. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725–727PubMedCrossRefGoogle Scholar
  126. Zimmerman SD, Mccormick RJ, Vadlamudi RK, Thomas DP (1993) Age and training alter collagen characteristics in fast- and slow-twitch rat limb muscle. J Appl Physiol 75:1670–1674PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.204 Research Center for Science and TechnologyTokyo University of Agriculture and TechnologyKoganei-shiJapan

Personalised recommendations