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Histochemistry and Cell Biology

, Volume 131, Issue 2, pp 197–206 | Cite as

Expression of nestin, desmin and vimentin in intact and regenerating muscle spindles of rat hind limb skeletal muscles

  • Dana Čížková
  • Tomáš SoukupEmail author
  • Jaroslav Mokrý
Original Paper

Abstract

We describe the expression and distribution patterns of nestin, desmin and vimentin in intact and regenerating muscle spindles of the rat hind limb skeletal muscles. Regeneration was induced by intramuscular isotransplantation of extensor digitorum longus (EDL) or soleus muscles from 15-day-old rats into the EDL muscle of adult female inbred Lewis rats. The host muscles with grafts were excised after 7-, 16-, 21- and 29-day survival and immunohistochemically stained. Nestin expression in intact spindles in host muscles was restricted to Schwann cells of sensory and motor nerves. In transplanted muscles, however, nestin expression was also found in regenerating “spindle fibers”, 7 and 16 days after grafting. From the 21st day onwards, the regenerated spindle fibers were devoid of nestin immunoreactivity. Desmin was detected in spindle fibers at all developmental stages in regenerating as well as in intact spindles. Vimentin was expressed in cells of the outer and inner capsules of all muscle spindles and in newly formed myoblasts and myotubes of regenerating spindles 7 days after grafting. Our results show that the expression pattern of these intermediate filaments in regenerating spindle fibers corresponds to that found in regenerating extrafusal fibers, which supports our earlier suggestion that they resemble small-diameter extrafusal fibers.

Keywords

Intermediate filaments Muscle spindle regeneration Skeletal muscle transplantation Rat muscle spindles Rat hind limb 

Notes

Acknowledgments

The authors thank Mrs. Helena Rückerová, Mrs. Hana Hollerová, Mrs. Magda Kudrnová and Ms. Jana Kudrnáčová for their skillful technical assistance. This work was supported by the following grant projects: 304/08/0329 and 304/08/0256 from the Grant Agency of the Czech Republic, MSM0021620820 from the Ministry of Education of the Czech Republic, MYORES LSH-CT-2004-511978 and by the Research project AV0Z 50110509.

References

  1. Aarimaa V, Kaariainen M, Vaittinen S, Tanner J, Jarvinen T, Best T, Kalimo H (2004) Restoration of myofiber continuity after transection injury in the rat soleus. Neuromuscul Disord 14:421–428PubMedCrossRefGoogle Scholar
  2. Autilio-Gambetti L, Sipple J, Sudilovsky O, Gambetti P (1982) Intermediate filaments of Schwann cells. J Neurochem 38:774–780PubMedCrossRefGoogle Scholar
  3. Barbet JP, Thornell LE, Butler-Browne GS (1991) Immunocytochemical characterisation of two generations of fibers during the development of the human quadriceps muscle. Mech Dev 35:3–11PubMedCrossRefGoogle Scholar
  4. Barker D, Banks RW (2004) The muscle spindle. In: Engel AG, Franzini-Armstrong C (eds) Myology: basic and clinical. McGraw-Hill Inc, New York, pp 489–510Google Scholar
  5. Bignami A, Dahl D (1984) Early appearance of desmin, the muscle-type intermediate filament protein, in the rat embryo. J Histochem Cytochem 32:473–476PubMedGoogle Scholar
  6. Boyd IA (1980) The isolated mammalian muscle spindle. Trends Neurosci 3:258–265CrossRefGoogle Scholar
  7. Carlsson L, Li Z, Paulin D, Thornell LE (1999) Nestin is expressed during development and in myotendinous and neuromuscular junctions in wild type and desmin knock-out mice. Exp Cell Res 251:213–223PubMedCrossRefGoogle Scholar
  8. Chiu FC, Sacchi RS, Claudio L, Kobayashi S, Suzuki K (1988) Coexpression of glial fibrillary acidic protein and vimentin in the central and peripheral nervous systems of the twitcher mutant. Glia 1:105–112PubMedCrossRefGoogle Scholar
  9. Čížková D, Soukup T, Mokrý J (2008) Nestin expression reflects formation, revascularization and reinnervation of new myofibers in the regenerating rat hind limb skeletal muscles. Cells Tissues Organs DOI: 10.1159/000142161
  10. Colucci-Guyon E, Portier MM, Dunia I, Paulin D, Pournin S, Babinet C (1994) Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79:679–694PubMedCrossRefGoogle Scholar
  11. Diwan FH, Milburn A (1986) The effects of temporary ischaemia on rat muscle spindles. J Embryol Exp Morphol 92:223–254PubMedGoogle Scholar
  12. Franke WW, Schmid E, Osborn M, Weber K (1978) Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc Natl Acad Sci USA 75:5034–5038PubMedCrossRefGoogle Scholar
  13. Friedman B, Zaremba S, Hockfield S (1990) Monoclonal antibody rat 401 recognizes Schwann cells in mature and developing peripheral nerve. J Comp Neurol 295:43–51PubMedCrossRefGoogle Scholar
  14. Fürst DO, Osborn M, Weber K (1989) Myogenesis in the mouse embryo: differential onset of expression of myogenic proteins and the involvement of titin in myofibril assembly. J Cell Biol 109:517–527PubMedCrossRefGoogle Scholar
  15. Gabbiani G, Schmid E, Winter S, Chaponnier C, de Ckhastonay C, Vandekerckhove J, Weber K, Franke WW (1981) Vascular smooth muscle cells differ from other smooth muscle cells: predominance of vimentin filaments and a specific alpha-type actin. Proc Natl Acad Sci USA 78:298–302PubMedCrossRefGoogle Scholar
  16. Hirose T, Scheithauer BW, Sano T (1998) Perineurial malignant peripheral nerve sheath tumor (MPNST): a clinicopathologic, immunohistochemical, and ultrastructural study of seven cases. Am J Surg Pathol 22:1368–1378PubMedCrossRefGoogle Scholar
  17. Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310–3328PubMedGoogle Scholar
  18. Ivaska J, Pallari HM, Nevo J, Eriksson JE (2007) Novel functions of vimentin in cell adhesion, migration, and signaling. Exp Cell Res 13:2050–2062CrossRefGoogle Scholar
  19. James NT, Meek GA (1971) The blood supply of rat muscle spindles. J Anat 110:165Google Scholar
  20. Jirmanová I, Soukup T (1995) Critical period in muscle spindle regeneration in grafts of developing rat muscles. Anat Embryol 192:283–291PubMedCrossRefGoogle Scholar
  21. Jirmanová I, Soukup T (2001) Early changes in extrafusal and intrafusal muscle fibers following heterochronous isotransplantation. Acta Neuropathol 102:473–484PubMedGoogle Scholar
  22. Kachinsky AM, Dominov JA, Miller JB (1994) Myogenesis and the intermediate filament protein, nestin. Dev Biol 165:216–228PubMedCrossRefGoogle Scholar
  23. Kida S, Yamashima T, Kubota T, Ito H, Yamamoto S (1988) A light and electron microscopic and immunohistochemical study of human arachnoid villi. J Neurosurg 69:429–435PubMedCrossRefGoogle Scholar
  24. Lendahl U, Zimmerman LB, McKay RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell 23:585–595CrossRefGoogle Scholar
  25. Li Z, Mericskay M, Agbulut O, Butler-Browne G, Carlsson L, Thornell LE, Babinet C, Paulin D (1997) Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol 139:129–144PubMedCrossRefGoogle Scholar
  26. Merrillees NC (1960) The fine structure of muscle spindles in the lumbrical muscles of the rat. J Biophys Biochem Cytol 7:725–742PubMedCrossRefGoogle Scholar
  27. Michalczyk K, Ziman M (2005) Nestin structure and predicted function in cellular cytoskeletal organisation. Histol Histopathol 20:665–671PubMedGoogle Scholar
  28. Milburn A (1976) The effect of the local anaesthetic bupivacaine on the muscle spindle of rat. J Neurocytol 5:425–446PubMedCrossRefGoogle Scholar
  29. Mokrý J, Čížková D, Filip S, Ehrmann J, Osterreicher J, Kolář Z, English D (2004) Nestin expression by newly formed human blood vessels. Stem Cells Dev 13:658–664PubMedCrossRefGoogle Scholar
  30. Novotová M, Soukup T (1995) Neomyogenesis in neonatally de-efferented and postnatally denervated rat muscle spindles. Acta Neuropathol 89:85–95PubMedCrossRefGoogle Scholar
  31. Peltonen J, Jaakkola S, Virtanen I, Pelliniemi L (1987) Perineurial cells in culture. An immunocytochemical and electron microscopic study. Lab Invest 57:480–488PubMedGoogle Scholar
  32. Rogers SL (1982) Muscle spindle formation and differentiation in regenerating rat muscle grafts. Dev Biol 94:265–283PubMedCrossRefGoogle Scholar
  33. Rogers SL, Carlson BM (1981) A quantitative assessment of muscle spindle formation in reinnervated and non-reinnervated grafts of the rat extensor digitorum longus muscle. Neuroscience 6:87–94PubMedCrossRefGoogle Scholar
  34. Sarlomo-Rikala M, Tsujimura T, Lendahl U, Miettinen M (2002) Patterns of nestin and other intermediate filament expression distinguish between gastrointestinal stromal tumors, leiomyomas and schwannomas. APMIS 110:499–507PubMedCrossRefGoogle Scholar
  35. Sejersen T, Lendahl U (1993) Transient expression of the intermediate filament nestin during skeletal muscle development. J Cell Sci 106:1291–1300PubMedGoogle Scholar
  36. Shimada S, Tsuzuki T, Kuroda M, Nagasaka T, Hara K, Takahashi E, Hayakawa S, Ono K, Maeda N, Mori N, Illei PB (2007) Nestin expression as a new marker in malignant peripheral nerve sheath tumors. Pathol Int 57:60–67PubMedCrossRefGoogle Scholar
  37. Sjoberg G, Jiang WQ, Ringertz NR, Lendahl U, Sejersen T (1994) Colocalization of nestin and vimentin/desmin in skeletal muscle cells demonstrated by three-dimensional fluorescence digital imaging microscopy. Exp Cell Res 214:447–458PubMedCrossRefGoogle Scholar
  38. Soukup T (1976) Intrafusal fibre types in rat limb muscle spindles. Morphological and histochemical characteristics. Histochemistry 47:43–57PubMedCrossRefGoogle Scholar
  39. Soukup T (1988) Regeneration of muscle spindles in grafted extensor digitorum longus of the rat. In: Hník P, Soukup T, Vejsada R, Zelená J (eds) Mechanoreceptors––development structure and function. Plenum Press, New York, pp 111–116Google Scholar
  40. Soukup T, Pedrosa F, Thornell LE (1990) Rat intrafusal fibres regenerated after autotransplantation of the EDL muscle do not express their typical myosin heavy chain isoenzymes in the absence of sensory innervation. In: Maréchal G, Carraro U (eds) Muscle and Motility. Intercept Ltd, Andover, pp 105–110Google Scholar
  41. Soukup T, Pedrosa-Domellöf F, Thornell LE (1995) Expression of myosin heavy chain isoforms and myogenesis of intrafusal fibres in the rat muscle spindles. Microsc Res Tech 30:390–407PubMedCrossRefGoogle Scholar
  42. Soukup T, Novotová M (2000) Ultrastructure and innervation of regenerated intrafusal muscle fibres in heterochronous isografts of the fast rat muscle. Acta Neuropathol 100:435–444PubMedCrossRefGoogle Scholar
  43. Soukup T, Thornell L-E (1997) Expression of myosin heavy chain isoforms in regenerated muscle spindle fibres after muscle grafting in young and adult rats––plasticity of intrafusal satellite cells. Differentiation 62:179–186PubMedCrossRefGoogle Scholar
  44. Triantafyllou A (2007) Immunohistochemical characterization of capsular cells in neuromuscular spindles of the neck. J Oral Pathol Med 36:501–504PubMedGoogle Scholar
  45. Vaittinen S, Lukka R, Sahlgren C, Rantanen J, Hurme T, Lendahl U, Eriksson JE, Kalimo H (1999) Specific and innervation-regulated expression of the intermediate filament protein nestin at neuromuscular and myotendinous junctions in skeletal muscle. Am J Pathol 154:591–600PubMedGoogle Scholar
  46. Vaittinen S, Lukka R, Sahlgren C, Hurme T, Rantanen J, Lendahl U, Eriksson JE, Kalimo H (2001) The expression of intermediate filament protein nestin as related to vimentin and desmin in regenerating skeletal muscle. J Neuropathol Exp Neurol 60:588–597PubMedGoogle Scholar
  47. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM (2004) Nestin expression––a property of multi-lineage progenitor cells? Cell Mol Life Sci 61:2510–2522PubMedCrossRefGoogle Scholar
  48. Yamashima T, Tachibana O, Nitta H, Yamaguchi N, Yamashita J (1989) Ultrastructural immunogold labelling of vimentin filaments on postembedding ultrathin sections of arachnoid villi and meningiomas. Histol Histopathol 4:47–53PubMedGoogle Scholar
  49. Zelená J, Soukup T (1993) Increase in the number of intrafusal muscle fibres in rat muscles after neonatal motor denervation. Neuroscience 52:207–218PubMedCrossRefGoogle Scholar
  50. Zelená J (1994) Nerves and mechanoreceptors. Chapman and Hall, London, pp 1–355Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Dana Čížková
    • 1
  • Tomáš Soukup
    • 2
    Email author
  • Jaroslav Mokrý
    • 1
  1. 1.Department of Histology and Embryology, Faculty of Medicine in Hradec KraloveCharles University in PragueHradec Králové, 500 38Czech Republic
  2. 2.Institute of PhysiologyAcademy of Sciences of the Czech RepublicPrague 4Czech Republic

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