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Neomyogenesis in neonatally de-efferented and postnatally denervated rat muscle spindles

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Abstract

The ultrastructure of muscle spindles de-efferented by the extirpation of the lumbosacral spinal cord at the age of 2 days and subsequently deprived of their sensory innervation by the section of the sciatic nerve at 3–4 weeks of age was studied in serial sections of 2-month-old rat hindlimb muscles. De-efferentation leaves the primary sensory neurons and their peripheral axons intact and capable of inducing the muscle spindle morphogenesis during the critical period of their development. In de-efferented and subsequently denervated muscle spindles, new supernumerary intrafusal muscle profiles (SIPs) appeared in the muscle spindle A region. They were formed in intimate spatial relation with the original intrafusal muscle fibres (IMFs) predominantly from activated satellite cells derived from both nuclear bag (larger diameter) and nuclear chain fibres. SIPs, however, lacked the typical nuclear accumulations, as well as other ultrastructural distinctions present in control IMFs. The majority of differentiated SIPs separated from original IMFs, whereas the less differentiated SIPs were usually closely apposed to the surface of the parent IMFs and both were covered by the common basal lamina. In some spindles, the original IMFs and/or new SIPs at different stages of their differentiation were found together and they formed clusters of variable shape and composition. In the majority of clusters, all profiles seemed to be isolated along their entire length, although in few clusters, occasional cytoplasmic connections of variable length between intrafusal profiles were found. This result is important for the interpretation of the forthcoming study of expression of muscle spindle-specific myosin heavy chain isoforms in denervated SIPs in rat muscle spindles gradually deprived of their motor and sensory innervation.

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References

  1. Arendt K-W, Asmussen G (1976) Die Muskelspindeln im denervierten und reinnervierten M. soleus der Ratte. II. Veränderungen an den extra-und intrafusalen Muskelfasern. Anat Anz 140:254–266

    Google Scholar 

  2. Barker D (1974) The morphology of muscle receptors. In: Hunt CC (ed) Handbook of sensory physiology, vol III/2. Springer, Berlin Heidelberg New York

    Google Scholar 

  3. Barker D, Banks RW (1986) The muscle spindle. In: Engel AG, Banker BQ (eds) Myology. McGraw-Hill, New York, pp 309–341

    Google Scholar 

  4. Boyd IA (1980) The isolated mammalian muscle spindle. Trends Neurosci 3:256–265

    Google Scholar 

  5. Copray JCVM, Brouwer N (1994) Selective expression of neurotrophin-3 mRNA in muscle spindles of the rat. Neuroscience (in press)

  6. Dieler R, Schröder JM (1990) Increase of elastic fibers in muscle spindles of rats following single or repeated denervation with or without reinnervation. Virchows Arch [A] 417:213–221

    Google Scholar 

  7. Forsgren S, Bergh A, Carlsson E, Thornell L-E (1992) Studies on the distribution of calcitonin gene-related peptide-like and substance P-like immunoreactivities in rat hind limb muscles. Histochem J 24:345–353

    Google Scholar 

  8. Gutmann E, Zelená J (1962) Morphological changes in the denervated muscle. In: Gutmann E (ed) The denervated muscle. House Czech Acad Sci, Prague, pp 55–75

    Google Scholar 

  9. Hník P, Soukup T, Arutyunyan R, Ujec E (1977) Response to stretch of proprioceptors in adult rat muscles de-efferented at birth. Pflügers Arch 368:129–133

    Google Scholar 

  10. Kucera J, Walro JM (1988) The effect of neonatal deafferentation or deefferentation on myosin heavy chain expression in intrafusal muscle fibers of the rat. Histochemistry 90:151–160

    Google Scholar 

  11. Kucera J, Walro JM (1990) Origin of intrafusal fibers in the rat. Histochemistry 93:567–580

    Google Scholar 

  12. Kucera J, Walro JM (1990) Treatment with beta bungarotoxin blocks muscle spindle formation in fetal rats. Development 110:483–489

    Google Scholar 

  13. Kucera J, Walro JM, Reichler J (1988) Innervation of developing intrafusal muscle fibers in the rat. Am J Anat 183:344–358

    Google Scholar 

  14. Kucera J, Walro JM, Reichler J (1993) Differential effects of neonatal denervation on intrafusal muscle fibers in the rat. Anat Embryol 187:397–408

    Google Scholar 

  15. Landon DN (1972) The fine structure of the equatorial regions of developing muscle spindles in the rat. J Neurocytol 1:189–210

    Google Scholar 

  16. Landon DN (1982) Skeletal muscle-normal pathology, development and innervation. In: Mastaglia FL, Walton J (eds) Skeletal muscle pathology. Churchill Livingstone, London, pp 1–87

    Google Scholar 

  17. Milburn A (1973) The early development of muscle spindles in the rat. J Cell Sci 12:175–195

    Google Scholar 

  18. Ovalle WK (1971) Fine structure of rat intrafusal muscle fibers. The polar region. J Cell Biol 51:83–103

    Google Scholar 

  19. Ovalle WK (1972) Fine structure of rat intrafusal muscle fibres. The equatorial region. J Cell Biol 52:382–396

    Google Scholar 

  20. Pedrosa F, Thornell L-E (1990) Expression of myosin heavy chain isoforms in developing rat muscle spindles. Histochemistry 94:231–244

    Google Scholar 

  21. Pedrosa-Domellöf F, Soukup T, Thornell L-E (1991) Rat muscle spindle immunocytochemistry revisited. Histochemistry 96:327–338

    Google Scholar 

  22. Santini H, Ibata Y (1971) The fine structure of thin unmyelinated axons within muscle spindles. Brain Res 33:279–287

    Google Scholar 

  23. Schiaffino S, Pierobon-Bormioli S (1976) Morphogenesis of rat muscle spindles after nerve lesion during early postnatal development. J Neurocytol 5:319–336

    Google Scholar 

  24. Schmalbruch H (1985) Skeletal Muscle. Springer-Verlag, Berlin Heidelberg New York Tokyo

    Google Scholar 

  25. Schröder JM (1974) The fine structure of de-and reinnervated muscle spindles. I. The increase, atrophy and ‘hypertrophy’ of intrafusal muscle fibers. Acta Neuropathol (Berl) 30:109–128

    Google Scholar 

  26. Schröder JM (1974) The fine structure of de-and reinnervated muscle spindles. II. Regenerated sensory and motor nerve terminals. Acta Neuropathol (Berl) 30:129–144

    Google Scholar 

  27. Schröder JM, Kemme PT, Scholz L (1979) The fine structure of denervated and reinnervated muscle spindles, morphometric study of intrafusal muscle fibers. Acta Neuropathol (Berl) 46: 95–106

    Google Scholar 

  28. Soukup T (1976) Intrafusal fibre types in rat limb muscle spindles. Morphological and histochemical characteristics. Histochemistry 47:43–57

    Google Scholar 

  29. Soukup T, Pedrosa F, Thornell L-E (1990) Influence of neonatal motor denervation on expression of myosin heavy chain isoforms in rat muscle spindles. Histochemistry 94:245–256

    Google Scholar 

  30. Soukup T, Pedrosa-Domellöf F, Thornell L-E (1993) Differentiation of supernumerary fibres in neonatally de-efferented rat muscle spindles. Differentiation 53:35–43

    Google Scholar 

  31. Soukup T, Novotová M, Pedrosa-Domellöf F, Thornell L-E (1993) Neoformation of intrafusal fibres in rat muscle spindles de-efferented at birth and denervated at 4 weeks. Physiol Res 42:8P

    Google Scholar 

  32. Soukup T, Pedrosa-Domellöf F, Thornell L-E (1994) Expression of myosin heavy chain isoforms and myogenesis of intrafusal fibres in the rat muscle spindles. Microsc Res Tech (in press)

  33. Soukup T, Zelená J, Zachařová G, Novotová M, Pedrosa-Domellöf F, Thornell L-E (1994) Myogenesis of intrafusal fibres in rat muscle spindles. J Muscle Res Cell Motil 15:192

    Google Scholar 

  34. Soukup T, Novotová M, Thornell L-E (1994) Expression of myosin heavy chains in denervated adult rat intrafusal fibres. Physiol Res 43:21P

    Google Scholar 

  35. Tower SS (1932) Atrophy and degeneration in the muscle spindle. Brain 55:77–89

    Google Scholar 

  36. Werner JK (1973) Duration of normal innervation required for complete differentiation of muscle spindles in newborn rats. Exp Neurol 41:214–217

    Google Scholar 

  37. Zelená J (1957) The morphogenetic influence of innervation on the ontogenetic development of muscle spindles. J Embryol Exp Morphol 5:283–292

    Google Scholar 

  38. Zelená J (1976) The role of sensory innervation in the development of mechanoreceptors. Prog Brain Res 43:59–64

    Google Scholar 

  39. Zelená J (1994) Nerves and Mechanoreceptors. Chapman and Hall, London

    Google Scholar 

  40. Zelená J, Soukup T (1973) Development of muscle spindles deprived of fusimotor innervation. Z Zellforsch 144:435–452

    Google Scholar 

  41. Zelená J, Soukup T (1974) The differentiation of intrafusal types in rat muscle spindles after motor denervation. Cell Tissue Res 153:115–136

    Google Scholar 

  42. Zelená J, Soukup T (1975) Ultrastructural changes of developing muscle spindles after denervation. Folia Morphol 23:275–277

    Google Scholar 

  43. Zelená J, Soukup T (1993) Increase in the number of intrafusal muscle fibres in rat muscles after neonatal motor denervation. Neuroscience 52:207–218

    Google Scholar 

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Novotová, M., Soukup, T. Neomyogenesis in neonatally de-efferented and postnatally denervated rat muscle spindles. Acta Neuropathol 89, 85–95 (1995). https://doi.org/10.1007/BF00294263

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  • DOI: https://doi.org/10.1007/BF00294263

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