Skip to main content
SpringerLink
Log in

Calcitonin gene-related peptide expression at endplates of different fibre types in muscles in rat hind limbs

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Calcitonin gene-related peptide (CGRP) occurs only in some motoneurons. In this study, the presence of CGRP in motor endplates in relation to muscle fibre types was examined in slow (soleus muscle) and fast [tibialis anterior (TA) and extensor digitorum longus (EDL)] leg muscles of the rat. CGRP was detected by use of immunohistochemical methods, and staining for the mitochondrial-bound enzyme NADH-TR was used for demonstration of fibre types. The fibres showing low NADH-TR activity were interpreted as representing IIB fibres. All such fibres located in the superficial portion of TA were innervated by endplates displaying CGRP-like immunoreactivity (LI), whereas in the deep portion of TA some of these fibres lacked CGRP-LI at their endplates. Thirty per cent of the IIB fibres in EDL showed CGRP-LI at the endplates. All fibres in TA and EDL displaying high NADH-TR activity and interpreted as type-IIA fibres, lacked CGRP-LI in their motor innervation. One third of the fibres with intermediate NADH-TR activity in TA exhibited CGRP-LI at their endplates, whereas in EDL only few such fibres displayed CGRP-LI in the endplate formation. These fibres are likely to belong to type-IIX or type-I motor units. CGRP-LI was very rarely detected at the endplates in the soleus muscle. These observations show that distinct differences exist between the slow muscle, soleus, and the fast muscles, TA and EDL, but that there are also differences between the different types of fibres in TA and EDL with respect to presence of CGRP-LI at the endplates. As CGRP-LI was frequently detected at endplates of IIB fibres, it is likely that CGRP has a particular role related to the differentiation and maintenance of these fibres.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evans RM (1982) Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptides products. Nature 298:240–244

    Google Scholar 

  • Armstrong RB, Phelps RO (1984) Muscle fibre type composition of the rat hindlimb. Am J Anat 171:259–272

    Google Scholar 

  • Changeux J-P (1991) Compartmentalized transcription of acetylcholine receptor genes during motor endplate epigenesis. The New Biologist 3:413–429

    Google Scholar 

  • Close R (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129–197

    Google Scholar 

  • Fontaine B, Klarsfeld A, Hökfelt T, Changeux JP (1986) Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increasing the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci Lett 71:59–65

    Google Scholar 

  • Fontaine B, Klarsfeld A, Changeux JP (1987) Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor α-subunit mRNA levels by distinct intracellular pathways. J Cell Biol 105:1337–1342

    Google Scholar 

  • Forsgren S, Söderberg L (1987) Immunohistochemical procedures for the demonstration of peptide- and tyrosine hydroxylase-containing nerve fibers in cryostat sections of unfixed rapidly frozen tissue stored for long periods of time. Histochemistry 87:561–568

    Google Scholar 

  • 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 

  • Garcia L, Pincon-Raymond M, Romey G, Changuex J-P, Lazdunski M, Rieger F (1990) Induction of normal ultrastructure by CGRP treatment in dysgenic myotubes. Fed Eur Biochem Socs Lett 263:147–152

    Google Scholar 

  • Gauthier GF (1986) Skeletal muscle fibre types. In: Banker BQ (ed) Myology. McGraw-Hill, New York, pp 255–285

    Google Scholar 

  • Gibbins IL, Furness JB, Costa M, Macintyre I, Hillyard CJ, Girgis S (1985) Co-localisation of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57:125–130

    Google Scholar 

  • Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, Mcgregor GP, Morrison JFB, Kelly JS, Evans RM, Rosenfeld MG (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4:3101–3111

    Google Scholar 

  • Gibson SJ, Polak JM, Katagiri T, Su H, Weller RO, Brownell DB, Holland S, Hughes JT, Kikuyama S, Ball J, Bloom SR, Steiner TJ, De Belleroche J, Clifford Rose F (1988a) A comparison of the distributions of eight peptides in spinal cord from normal controls and cases of motor neurone disease with special reference to Onufs nucleus. Brain Res 474:255–278

    Google Scholar 

  • Gibson SJ, Polak JM, Giaid A, Hamid QA, Kar S, Jones PM, Denny P, Legon S, Amara SG, Craig RK, Bloom SR, Penketh RJA, Rodek C, Ibrahim NBN, Dawson A (1988b) Calcitonin gene-related peptide messenger RNA is expressed in sensory neurones of the dorsal root ganglia and also in spinal motoneurones in man and rat. Neurosci Lett 91:283–288

    Google Scholar 

  • Gorza L (1990) Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies. J Histochem Cytochem 38:257–265

    Google Scholar 

  • Hietanen M, Pelto-Huikko M, Rechardt L (1990) Immunocytochemical study of the relations of acetylcholinesterase, enkephalin-, substance P-, choline acetyltransferase- and calcitonin gene-related peptide-immunoreactive structures in the ventral horn of rat spinal cord. Histochemistry 93:473–477

    Google Scholar 

  • Jinnai K, Chihara K, Kanda F, Tada K, Fujita T (1989) Calcitonin gene-related peptide enhances spontaneous acetylcholine release from the rat motor nerve terminal. Neurosci Lett 103:64–68

    Google Scholar 

  • Kugelberg E (1973) Properties of the rat hind-limb motor units. In: Desmedt JE (ed) New developments in electromyography and clinical neurophysiology. Karger, Basel, pp 2–13

    Google Scholar 

  • Kugelberg E, Lindegren B (1979) Transmission and contraction fatigue of rat motor units in relation to succinate dehydrogenase activity of motor unit fibres. J Physiol (Lond) 288:285–300

    Google Scholar 

  • Larsson L (1992) Is the motor unit uniform? Acta Physiol Scand 144:143–154

    Google Scholar 

  • Larsson L, Edström L, Lindegren B, Gorza L, Schiaffino S (1991) Myosin heavy chain composition and enzyme-histochemical and physiological properties of a novel fast-twitch motor unit type. Am J Physiol 261:C93–101

    Google Scholar 

  • Laufer R, Changeux JP (1987) Calcitonin gene-related peptide elevates cyclic AMP levels in chick skeletal muscle; possible neurotrophic role for a coexisting neuronal messenger. EMBO J 6:901–906

    Google Scholar 

  • Li J-Y, Dahlström AB (1992) Development of calcitonin gene-related peptide, chromogranin A, and synaptic vesicle markers in rat motor endplates, studied using immunofluorescence and confocal laser scanning. Muscle Nerve 15:984–992

    Google Scholar 

  • Lundberg JM, Franco-Cereceda A, Hua X, Hökfelt T, Fischer JA (1985) Coexistence of substance P and calcitonin gene-related peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. Eur J Pharmacol 108:315–319

    Google Scholar 

  • Matteoli M, Balbi S, Sala C, Chini B, Cimino M, Vitadello M, Fumagalli G (1990) Developmentally regulated expression of calcitonin gene-related peptide at mammalian neuromuscular junction. J Mol Neurosci 2:175–184

    Google Scholar 

  • Mora M, Marchi M, Polak JM, Gibson SJ, Cornelio F (1989) Calcitonin gene-related peptide immunoreactivity at the human neuromuscular junction. Brain Res 492:404–407

    Google Scholar 

  • Mulle C, Benoit P, Pinset C, Roa M, Changeux JP (1988) Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci USA 85:5728–5732

    Google Scholar 

  • New HV, Mudge AW (1986) Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809–811

    Google Scholar 

  • Newton BW, Unger J, Hamill RW (1990) Calcitonin gene-related peptide and somatostatin immunoreactivity in the rat lumbar spinal cord: sexually dimorphic aspects. Neuroscience 37:471–489

    Google Scholar 

  • Ohhashi T, Jacobowitz DM (1988) Effects of calcitonin gene-related peptide on neuromuscular transmission in the isolated rat diaphragm. Peptides 9:613–617

    Google Scholar 

  • Popper P, Micevych PE (1989) Localization of calcitonin gene-related peptide and its receptors in a striated muscle. Brain Res 496:180–186

    Google Scholar 

  • Pullen AH (1977) The distribution and relative sizes of three histochemical fibre types in the rat tibialis anterior muscle? J Anat 123:1–19

    Google Scholar 

  • Ranatunga KW, Thomas PE (1990) Correlation between shortening velocity, force-velocity relation and histochemical fibre-type composition in rat mucles. J Muscle Res Cell Motil 11:240–250

    Google Scholar 

  • Rodrigo J, Polak JM, Terenghi G, Cervantes C, Ghatei MA, Mulderry PK, Bloom SR (1985) Calcitonin gene-related peptide immunoreactive sensory and motor nerves of the mammalian palate. Histochemistry 82:67–74

    Google Scholar 

  • Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 304:129–135

    Google Scholar 

  • Scarpelli DG, Hess R, Pearse AGE (1958) The cytochemical localization of oxidative enzymes. J Biophys Biochem Cytol 4:747–751

    Google Scholar 

  • Schmalbruch H (1985) Muscle fibre types in mammalian muscles. In: Schmalbruch H (ed) Skeletal Muscle. Springer, Berlin, pp 159–204

    Google Scholar 

  • Takami K, Kawai Y, Shiosaka S, Lee Y, Girgis S, Hillyard CJ, Macintyre I, Emson PC, Tohyama M (1985a) Immunohistochemical evidence for the coexistence of calcitonin gene-related peptide- and choline acetyltransferase-like immunoreactivity in neurons of the rat hypoglossal, facial and ambiguus nuclei. Brain Res 328:386–389

    Google Scholar 

  • Takami K, Kawai Y, Uchida S, Tohyama M, Shiotani Y, Yoshida H, Emson PC, Girgis S, Hillyard CJ, Macintyre I (1985b) Effect of calcitonin gene-related peptide on contraction of striated muscle in the mouse. Neurosci Lett 60:227–230

    Google Scholar 

  • Thornell L-E, Eriksson A, Edström L (1983) Intermediate filaments in human myopathies. In: Dowben RM, Shay JW (eds) Cell and muscle motility, vol 4. Plenum Press, New York, pp 85–136

    Google Scholar 

  • Uchida S, Yamamoto H, Iio S, Matsumoto N, Wang XB, Yonehara N, Imai Y, Inoki R, Yoshida H (1990) Release of calcitonin gene-related peptide-like immunoreactive substance from neuromuscular junction by nerve excitation and its action on striated muscle. J Neurochem 54:100–1003

    Google Scholar 

  • Villar MJ, Huchet M, Hökfelt T, Changeux JP, Fahrenkrug J, Brown JC (1988) Existence and coexistence of calcitonin gene-related peptide-, vasoactive intestinal polypeptide- and somatostatin-like immunoreactivities in spinal cord motoneurons of developing embryos and post-hatch chicks. Neurosci Lett 86:114–118

    Google Scholar 

  • Villar MJ, Roa M, Huchet M, Hökfelt T, Changeux J-P, Fahrenkrug J, Brown JC, Epstein M, Hersch L (1989) Immunoreactive calcitonin gene-related peptide, vasoactive intestinal polypeptide and somatostatin in developing chicken spinal cord motoneurons. Distribution and role in regulation of cAMP in cultured muscle cells. Eur J Neurosci 1:269–287

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, University of Umeå, S-901 87, Umeå, Sweden

    Sture Forsgren, Anna Bergh, Eva Carlsson & Lars-Eric Thornell

Authors
  1. Sture Forsgren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Bergh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Carlsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lars-Eric Thornell
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forsgren, S., Bergh, A., Carlsson, E. et al. Calcitonin gene-related peptide expression at endplates of different fibre types in muscles in rat hind limbs. Cell Tissue Res 274, 439–446 (1993). https://doi.org/10.1007/BF00314540

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00314540

Key words

Search

Navigation