Abstract
Cell body size and succinate dehydrogenase activity of motoneurons in the dorsolateral region of the ventral horn in the lumbar and cervical segments of the mouse spinal cord were assessed after long-term exposure to microgravity and compared with those of ground-based controls. Mice were housed in a mouse drawer system on the International Space Station for 13 weeks. The mice were transported to the International Space Station by the Space Shuttle Discovery and returned to Earth by the Space Shuttle Atlantis. No changes in the cell body size of motoneurons were observed in either segment after exposure to microgravity, but succinate dehydrogenase activity of small-sized (<300 μm2) gamma and medium-sized (300–700 μm2) alpha motoneurons, which have higher succinate dehydrogenase activity than large-sized (>700 μm2) alpha motoneurons, in both segments was lower than that of ground-based controls. We concluded that exposure to microgravity for longer than 3 months induced decreased succinate dehydrogenase activity of both gamma and slow-type alpha motoneurons. In particular, the decreased succinate dehydrogenase activity of gamma motoneurons was observed only after long-term exposure to microgravity.
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Abbreviations
- FOXO1:
-
Forkhead box-containing protein O1
- GC:
-
Ground-based control
- HSP:
-
Heat shock protein
- MDS:
-
Mice drawer system
- MHC:
-
Myosin heavy chain
- OD:
-
Optical density
- PGC-1α:
-
Peroxisome proliferator-activated receptor γ coactivator-1α
- SDH:
-
Succinate dehydrogenase
- SF:
-
Spaceflight
- STS:
-
Space transportation system
References
Hori A, Ishihara A, Kobayashi S, Ibata Y (1998) Immunohistochemical classification of skeletal muscle fibers. Acta Histochem Cytochem 31:375–384
Ohira Y (2000) Neuromuscular adaptation to microgravity environment. Jpn J Physiol 50:303–314
Ishihara A, Fujino H, Nagatomo F, Takeda I, Ohira Y (2008) Gene expression levels of heat shock proteins in the soleus and plantaris muscles of rats after hindlimb suspension or spaceflight. J Physiol Sci 58:413–417
McHanwell S, Biscoe TJ (1981) The localization of motoneurons supplying the hindlimb muscles of the mouse. Philos Trans R Soc Lond B Biol Sci 293:477–508
Nicolopoulos-Stournaras S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:75–85
Burke RE, Dum RP, Fleshman JW, Glenn LL, Lev-Tov A, O’Donovan MJ, Pinter MJ (1982) A HRP study of the relation between cell size and motor unit type in cat ankle extensor motoneurons. J Comp Neurol 209:17–28
Sickles DW, Oblak TG (1984) Metabolic variation among α-motoneurons innervating different muscle-fiber types I. Oxidative enzyme activity. J Neurophysiol 51:529–537
Ishihara A, Roy RR, Edgerton VR (1995) Succinate dehydrogenase activity and soma size of motoneurons innervating different portions of the rat tibialis anterior. Neuroscience 68:813–822
Ishihara A, Hayashi S, Roy RR, Tamada Y, Yokoyama C, Ohira Y, Edgerton VR, Ibata Y (1997) Mitochondrial density of ventral horn neurons in the rat spinal cord. Acta Anat 160:248–253
Ishihara A, Ohira Y, Roy RR, Nagaoka S, Sekiguchi C, Hinds WE, Edgerton VR (1996) Influence of spaceflight on succinate dehydrogenase activity and soma size of rat ventral horn neurons. Acta Anat 157:303–308
Ishihara A, Ohira Y, Roy RR, Nagaoka S, Sekiguchi C, Hinds WE, Edgerton VR (2000) Comparison of the response of motoneurons innervating perineal and hind limb muscles to spaceflight and recovery. Muscle Nerve 23:753–762
Ishihara A, Ohira Y, Roy RR, Nagaoka S, Sekiguchi C, Hinds WE, Edgerton VR (2002) Succinate dehydrogenase activity in rat dorsolateral ventral horn motoneurons at L6 after spaceflight and recovery. J Grav Physiol 9:39–48
Ishihara A, Yamashiro J, Matsumoto A, Higashibata A, Ishioka N, Shimazu T, Ohira Y (2006) Comparison of cell body size and oxidative enzyme activity in motoneurons between the cervical and lumbar segments in the rat spinal cord after spaceflight and recovery. Neurochem Res 31:411–415
Ishihara A, Taguchi S, Araki H, Nishihira Y (1991) Retrograde neuronal labeling of motoneurons in the rat by fluorescent tracers, and quantitative analysis of oxidative enzyme activity in labeled neurons. Neurosci Lett 124:141–143
Nagatomo F, Ishihara A, Ohira Y (2009) Effects of hindlimb unloading at early postnatal growth on cell body size in spinal motoneurons innervating soleus muscle of rats. Int J Devl Neurosci 27:21–26
Nagatomo F, Ishihara A, Sudoh M, Ohira Y (2009) Growth-related changes in motoneuron properties of rats are not influenced by chronic exposure to 2-G. J Grav Physiol 16:17–25
Swett JE, Wikholm RP, Blanks RHI, Swett AL, Conley LC (1986) Motoneurons of the rat sciatic nerve. Exp Neurol 93:227–252
Ishihara A, Ohira Y, Tanaka M, Nishikawa W, Ishioka N, Higashibata A, Izumi R, Shimazu T, Ibata Y (2001) Cell body size and succinate dehydrogenase activity of spinal motoneurons innervating the soleus muscle in mice, rats, and cats. Neurochem Res 26:1301–1304
Ishihara A, Oishi Y, Roy RR, Edgerton VR (1997) Influence of two weeks of non-weight bearing on rat soleus motoneurons and muscle fibers. Aviat Space Environ Med 68:421–425
Roy RR, Ishihara A, Kim JA, Lee M, Fox K, Edgerton VR (1999) Metabolic and morphological stability of motoneurons in response to chronically elevated neuromuscular activity. Neuroscience 92:361–366
Roy RR, Ishihara A, Moran MM, Wade CE, Edgerton VR (2001) No effect of hypergravity on adult rat ventral horn neuron size or SDH activity. Aviat Space Environ Med 72:1107–1112
Roy RR, Matsumoto A, Zhong H, Ishihara A, Edgerton VR (2007) Rat α- and γ-motoneuron soma size and succinate dehydrogenase activity are independent of neuromuscular activity level. Muscle Nerve 36:234–241
Ishihara A, Hori A, Roy RR, Oishi Y, Talmadge RJ, Ohira Y, Kobayashi S, Edgerton VR (1997) Perineal muscles and their innervation: metabolic and functional significance of the motor unit. Acta Anat 159:156–166
Matsumoto A, Nagatomo F, Mori A, Ohira Y, Ishihara A (2007) Cell size and oxidative enzyme activity of rat biceps brachii and triceps brachii muscles. J Physiol Sci 57:311–316
Ishihara A, Roy RR, Edgerton VR (1995) Succinate dehydrogenase activity and soma size relationships among cat dorsal root ganglion neurons. Brain Res 676:212–218
Ishihara A, Roy RR, Edgerton VR (1996) Comparison of succinate dehydrogenase activity and soma size relationships among neurons in dorsal root ganglia of rats and cats. Brain Res 716:183–186
Ishihara A, Ohira Y, Roy RR, Nagaoka S, Sekiguchi C, Hinds WE, Edgerton VR (1997) Effects of 14 days of spaceflight and nine days of recovery on cell body size and succinate dehydrogenase activity of rat dorsal root ganglion neurons. Neuroscience 81:275–279
Nakatani T, Nakashima T, Kita T, Hirofuji C, Itoh K, Itoh M, Ishihara A (1999) Succinate dehydrogenase activities of fibers in the rat extensor digitorum longus, soleus, and cardiac muscles. Arch Histol Cytol 62:393–399
Nakatani T, Nakashima T, Kita T, Hirofuji C, Itoh K, Itoh M, Ishihara A (2000) Cell size and oxidative enzyme activity of different types of fibers in different regions of the rat plantaris and tibialis anterior muscles. Jpn J Physiol 50:413–418
Nakatani T, Nakashima T, Kita T, Ishihara A (2003) Cell size and oxidative enzyme activity of type-identified fibers in rat hindlimb muscles: a review. Acta Histochem Cytochem 36:105–114
Sandonà D, Desaphy J-F, Camerino GM, Bianchini E, Ciciliot S, Danieli-Betto D, Dobrowolny G, Furlan S, Germinario E, Goto K, Gutsmann M, Kawano F, Nakai N, Ohira T, Ohno Y, Picard A, Salanova M, Schiffl G, Blottner D, Musarò A, Ohira Y, Betto R, Conte D, Schiaffino S (2012) Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission. PLoS ONE 7:e33232
Ishihara A, Kawano F, Ishioka N, Oishi H, Higashibata A, Shimazu T, Ohira Y (2004) Effects of running exercise during recovery from hindlimb unloading on soleus muscle fibers and their spinal motoneurons in rats. Neurosci Res 48:119–127
Nagatomo F, Fujino H, Kondo H, Suzuki H, Kouzaki M, Takeda I, Ishihara A (2011) PGC-1α and FOXO1 mRNA levels and fiber characteristics of the soleus and plantaris muscles in rats after hindlimb unloading. Histol Histopathol 26:1545–1553
Acknowledgments
We graciously thank the Alcatel-Alenia Space and the Italian Space Agency. This study was supported by a grant from the Japan Aerospace Exploration Agency.
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All authors declare no competing interest.
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Ishihara, A., Nagatomo, F., Fujino, H. et al. Decreased Succinate Dehydrogenase Activity of Gamma and Alpha Motoneurons in Mouse Spinal Cords Following 13 Weeks of Exposure to Microgravity. Neurochem Res 38, 2160–2167 (2013). https://doi.org/10.1007/s11064-013-1124-y
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DOI: https://doi.org/10.1007/s11064-013-1124-y