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The Role of Spinal Cord Motoneurons in the Mechanisms of Development of Low-Gravity Motor Syndrome

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We summarize here the results obtained from studies of the effects of gravitational unloading on the spinal system controlling the structure and function of the muscle apparatus. Important roles in the development of low-gravity motor syndrome were found for: the process of axon demyelination due to reductions in the expression of genes responsible for the synthesis of myelin proteins, decreases in the activity of one of the key enzymes of the cholinergic system, i.e., choline acetyltransferase, changes in the kinetics of quantum and non-quantum transmitter secretion processes, impairments to the autoregulation of acetylcholine release from motor nerve endings via the presynaptic cholinoreceptor system, and slowing of the axonal transport of substances in motoneurons innervating the postural musculature. In addition, signs of the activation of neuroprotective mechanisms were observed in simulations of low gravity (increased expression of heat shock proteins Hsp25 and Hsp70), preventing the development of motoneuron and glial cell apoptosis in the spinal cord.

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References

  1. G. N. Gevlich, L. S. Grigor’eva, and I. B. Kozlovskaya, “Assessment of skeletal muscle tone by recording transverse rigidity,” Kosm. Biol. Aviakosm. Med., No. 5, 86–89 (1989).

  2. A. M. Genin, A. I. Il’in, A. S. Kaplanskii, et al., “Bioethics rules for studies on humans and animals in aviation, space, and marine medicine,” Kosm. Biol. Aviakosm. Med., 35, No. 4, 14–20 (2001).

    CAS  Google Scholar 

  3. E. A. Il’in and V. E. Novikov, “A stand for simulating the physiological effects of weightlessness in laboratory experiments on rats,” Kosm. Biol., 14, No. 3, 79–80 (1980).

    Google Scholar 

  4. R. R. Islamov, A. A. Rizvanov, O. V. Tyapkina, et al., “Whole-genome studies of gene expression in the lumbar segment of the spinal cord in mice during simulation of the effects of weightlessness,” Dokl. Akad. Nauk., 439, No. 3, 1–5 (2011).

    Google Scholar 

  5. A. V. Kirenskaya, I. B. Kozlovskaya, and M. G. Sirota, “Effects of immersion hypokinesia on the characteristics of rhythmic activity of motor units in the soleus muscle,” Fiziol. Chelov., No. 12, 617–632 (1986).

  6. A. I. Malomuzh and E. E. Nikol’skii, “Nonquantum transmitter release: myth or reality?” Usp. Fiziol. Nauk., 41, No. 2, 27–43 (2010).

    PubMed  CAS  Google Scholar 

  7. E. E. Nikol’skii, “Effects of carbachol on miniature endplate potentials and currents in rat skeletal muscle,” Neirofiziologiya, 14, No. 2, 185–189 (1982).

    Google Scholar 

  8. N. P. Rezvyakov, and E. E. Nikol’skii, “Changes in the properties of fast and slow muscles in rats in crossed reinnervation,” Fiziol. Zh. SSSR, 64, No. 8, 1117–1123 (1978).

    CAS  Google Scholar 

  9. I. V. Saenko, D. G. Saenko, and I. B. Kozlovskaya, “Effects of 120-day antiorthostatic hypokinesia on the characteristics of tendon reflexes,” Aviakosm. Ekol. Med., 34, No. 4, 13–18 (2000).

    CAS  Google Scholar 

  10. O. V. Tyapkina, E. A. Bukharaeva, and E. E. Nikol’skii, “Effects of support unloading on the efficiency of the modulation of transmitter secretion via the autoreceptor system,” Biofizika, 51, No. 5, 827–832 (2006).

    CAS  Google Scholar 

  11. O. V. Tyapkina, L. F. Nurullin, P. N. Rezvyakov, et al., “Impairments to myelination in the central nervous system as a possible mechanism of development of low-gravity motor syndrome,” Biofizika, 57, No. 5, 876–879 (2012).

    Google Scholar 

  12. J. L. Aguirre, L. I. Plotkin, S. S. Stewart, et al., “Osteocyte apoptosis is induced by weightlessness in mice and precedes osteoclast recruitment and bone loss,” J. Bone Miner. Res., 2, No. 4, 605–615 (2006).

    Article  Google Scholar 

  13. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Anal. Biochem., 72, 248–254 (1976).

    Article  PubMed  CAS  Google Scholar 

  14. A. Brown, “Axonal transport of membranous and nonmembranous cargoes: a unified perspective,” J. Cell Biol., 160, 817–821 (2003).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  15. P. de Monasterio-Schrader, O. Jahn, S. Tenzer, et al., “Systematic approaches to central nervous system myelin,” Cell. Mol. Life Sci., 69, No. 7, 2879–2894 (2012).

    Article  PubMed  CAS  Google Scholar 

  16. L. De Doncker, M. Kasri, and M. Falempin, “Soleus motoneuron excitability after rat hindlimb unloading using histology and a new physiological approach to record a neurographic analogue of the H-reflex,” Exp. Neurol., 201, 368–374 (2006).

    Article  Google Scholar 

  17. R. Ferreira, M. J. Neuparth, R. Vitorino, et al., “Evidences of apoptosis during the early phases of soleus muscle atrophy in hindlimb suspended mice,” Physiol. Res., 57, No. 4, 601–611 (2008).

    PubMed  CAS  Google Scholar 

  18. E. Gallasch, M. Moser, T. Kenner, et al., “Investigation of tremor in microgravity,” in: Health from Space Research, ASM, Vienna (1992), Vol. 7, pp. 85–107.

  19. A. I. Grigoriev and I. B. Kozlovskaya, “Physiological reactions to muscle loading under conditions of long-term hypogravity,” Physiologist, 30, No. 1, 76–77 (1991).

    Google Scholar 

  20. A. Ishihara, J. Yamashiro, A. Matsumoto, et al., “Comparison of cell body size and oxidative enzyme activity in motoneurons between the cervical and lumbar segments in the rat spinal cord after space flight and recovery,” Neurochem. Res., 31, 411–415 (2006).

    Article  PubMed  CAS  Google Scholar 

  21. A. H. Ishihara, H. Naitoh, H. Araki, and Y. Nishihara, “Soma size and oxidative enzyme activity of motoneurons supplying the fast twitch and slow twitch muscle in the rat,” Brain Res., 446, 195–198 (1988).

    Article  PubMed  CAS  Google Scholar 

  22. R. R. Islamov, E. A. Mishagina, O. V. Tyapkina, et al., “Mechanisms of spinal motoneurons survival in rats under simulated hypogravity on earth,” Acta Astronaut., 68, 1469–1477 (2011).

    Article  Google Scholar 

  23. Yu. A. Koryak, “Contractile properties of the human triceps surae in simulated weightlessness,” Eur. J. Appl. Physiol., 70, 344–350 (1995).

    Article  CAS  Google Scholar 

  24. I. B. Kozlovskaya, I. Dmitrieva, L. Grigorieva, et al., “Studies in real and simulated weightlessness. Gravitational mechanisms in real and simulated weightlessness,” in: Stance and Motions, V. S. Gurfinkel et al. (eds.), Plenum, New York (1988), pp. 37–48.

    Chapter  Google Scholar 

  25. I. B. Kozlovskaya and A. V. Kirenskaya, “Mechanisms of disorders of the characteristics of fine movements in long-term hypokinesia,” Neurosci. Behav. Physiol., 34, No. 7, 747–754 (2004).

    Article  PubMed  CAS  Google Scholar 

  26. I. B. Kozlovskaya, Y. V. Kreydich, V. S. Oganov, and O. P. Kozerenko, “Pathophysiology of motor function in prolonged manned space flights,” Acta Astronaut, 8, 1059–1072 (1981).

    Article  PubMed  CAS  Google Scholar 

  27. Y. Kumei, S. Morita, H. Nakamura, et al., “Coinduction of GTP cyclohydrolase I and inducible NO synthase in rat osteoblasts during space flight: apoptotic and self-protective response?” Ann. N.Y. Acad. Sci., 1010, 481–485 (2003).

    Article  PubMed  CAS  Google Scholar 

  28. M. D. Miyamoto and R. L. Volle, “Enhancement by carbachol of transmitter release from motor nerve terminals,” Proc. Natl. Acad. Sci. USA, 71, 1489–1492 (1974).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  29. E. R. Morey-Holton and K. Globus, Hindlimb unloading rodent model: technical aspects,” J. Appl. Physiol., 92, 1367–1377 (2002).

    Article  PubMed  CAS  Google Scholar 

  30. Mouse Genomes Project, www.sanger.ac.uk/modelorgs/mousegemones/.

  31. F. Nagamoto, A. Ishihara, and Y. Ohira, “Effects of hindlimb unloading at early postnatal growth on cell body size in spinal motoneurons innervating soleus muscle of rats,” Int. J. Dev. Sci., 27, No. 1, 21–26 (2009).

    Google Scholar 

  32. M. V. Narici, B. Kayser, P. Barattini, and P. Cerretelli, “Changes in electrically evoked skeletal muscle contractions during 17-day spaceflight and bed rest,” Int. J. Sports Med., 8, No. 4, 290–292 (1997).

    Article  Google Scholar 

  33. I. V. Ogneva, B. S. Shenkman, and I. B. Kozlovskaya, “The contents of desmin and α-actinin-1 in the human soleus muscle after seven-day ‘dry’ immersion,” Dokl. Biol. Sci., 436, 20–22 (2011).

    Article  PubMed  CAS  Google Scholar 

  34. I. V. Polyakov, V. I. Droyshev, and I. B. Krasnov, “Morphological changes in spinal cord and intervertebral ganglia of rats exposed to different gravity levels,” Physiologist, 34, No. 1, 187–188 (1991).

    Google Scholar 

  35. K. D. Pruitt, T. Tatusova, and D. R. Maglott, “NCBI reference samples (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins,” Nucl. Acids Res., 35, (Database Issue), D61–D65 (2007).

  36. M. F. Reschke, D. J. Anderson, and J. L. Homick, “Vestibulo-spinal response modification as determined with the H-reflex during the Spacelab-1 flight,” Exp. Brain Res., 2, 367–379 (1986).

    Google Scholar 

  37. R. R. Roy, J. A. Hodgson, J. Aragon, et al., “Recruitment of the Rhesus soleus and medial gastrocnemius before, during and after spaceflight,” J. Gravit. Physiol., 3, No. 1, 11–15 (1996).

    PubMed  CAS  Google Scholar 

  38. R. R. Roy, A. Matsumoto, H. Zhong, et al., “Rat α- and γ-motoneuron soma size and succinate dehydrogenase activity are independent of neuromuscular activity level,” Musc. Nerve, 36, 234–241 (2007).

    Article  Google Scholar 

  39. D. Ruegg, I. Sayenko, T. Kakebeeke, et al., “Effects of long-term hypokinesia on spinal mechanisms’ state,” in: Proc. Symp. Hypokinesia, Moscow (1997), p. 65.

  40. I. Sayenko, D. Sayenko, and I. Kozlovskaya, “Comparative analysis of the stretch reflexes chromosomes in human under conditions of real and simulated microgravity,” in: Proc. 9th Int. Symp. Motor Control, Varna, Bulgaria (2000), p. 42.

  41. H. Schatten, M. L. Lewis, and A. Chakrabarti, “Spaceflight and clinorotation cause cytoskeleton and mitochondria changes and increases in apoptosis in cultured cells,” Acta. Astronaut., 49, No. 3–10, 399–418 (2001).

    Article  PubMed  CAS  Google Scholar 

  42. R. Smith, H. Chung, S. Rundquist, et al., “Cholinergic neuronal defect without cell loss in Huntington’s disease,” Hum. Mol. Genet., 15, No. 21, 3119–3131 (2006).

    Article  PubMed  CAS  Google Scholar 

  43. S. Thesleff, “Functional aspects of quantal and non-quantal release of acetylcholine at the neuromuscular junction,” Prog. Brain Res., 84, 93–99 (1990).

    Article  PubMed  CAS  Google Scholar 

  44. N. Treffort, G. Dubreucq, M. H. Canu, et al., “Variations in amino acid neurotransmitters in the rat ventral spinal cord after hindlimb unloading,” Neurosci. Lett., 403, 147–150 (2006).

    Article  PubMed  CAS  Google Scholar 

  45. B. M. Uva, F. Strollo, F. Ricci, et al., “Morpho-functional alterations in testicular and nervous cells submitted to modelled microgravity,” J. Endocrinol. Invest., 28, No. 11, 84–91 (2005).

    PubMed  CAS  Google Scholar 

  46. F. Vyskocil, A. I. Malomouzh, and E. E. Nikolsky, “Non-quantal acetylcholine release at the neuromuscular junction,” Physiol. Res., 58, 763–784 (2009).

    PubMed  CAS  Google Scholar 

  47. W. Wu, L. Li, L. W. Yick, et al., “GDNF and BDNF alter the expression of neuronal NOS, c-Jun, and p75 and prevent motoneuron death following spinal root avulsion in adult rats,” J. Neurotrauma, 20, No. 6, 603–612 (2003).

    Article  PubMed  Google Scholar 

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Correspondence to R. R. Islamov.

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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 99, No. 3, pp. 281–293, March, 2013.

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Islamov, R.R., Tyapkina, O.V., Nikol’skii, E.E. et al. The Role of Spinal Cord Motoneurons in the Mechanisms of Development of Low-Gravity Motor Syndrome. Neurosci Behav Physi 45, 96–103 (2015). https://doi.org/10.1007/s11055-014-0045-9

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