Skip to main content
SpringerLink
Log in

Effect of altered innervation and thyroid hormones on myosin heavy chain expression and fiber type transitions: a mini-review

  • Review
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

In this mini-review, we briefly present the data regarding the effect of extrinsic factors, i.e., innervation and thyroid hormones (TH) on myosin heavy chain genes and isoforms expression and consequently on muscle fiber type transitions. It has been well known that reduced neuromuscular activity, hyperthyroidism or mechanical unloading stimulate slow-to-fast fiber type transitions, while increased neuromuscular activity, hypothyroidism and higher mechanical loading result in fast to slow fiber type transitions. As there is a plethora of results on these topics, we focus mostly on data relevant to our experimental model of slow-to-fast muscle transformation following heterochronous intramuscular isotransplantation in rats with altered TH status.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen JL, Gruschy-Knudsen T, Sandri C, Larsson L, Schiaffino S (1999) Bed rest increases the amount of mismatched fibers in human skeletal muscle. J Appl Physiol 86:455–460

    CAS  PubMed  Google Scholar 

  • Arai M, Otsu K, MacLennan DH, Alpert NR, Periasamy M (1991) Effect of thyroid hormone on the expression of mRNA encoding sarcoplasmic reticulum proteins. Circ Res 69:266–276

    Article  CAS  PubMed  Google Scholar 

  • Arnostova P, Jedelsky PL, Soukup T, Zurmanova J (2011) Electrophoretic mobility of cardiac myosin heavy chain isoforms revisited: application of MALDI TOF/TOF analysis. J Biomed Biotechnol 2011:634253

    Article  PubMed Central  PubMed  Google Scholar 

  • Asmussen G, Soukup T (1991) Arrest of developmental conversion of type II to type I fibres after suspension hypokinesia. Histochem J 23:312–322

    Article  CAS  PubMed  Google Scholar 

  • Asmussen G, Schmalbruch I, Soukup T, Pette D (2003) Contractile properties, fiber types, and myosin isoforms in fast and slow muscles of hyperactive Japanese waltzing mice. Exp Neurol 184:758–766

    Article  PubMed  Google Scholar 

  • Ausoni S, Gorza L, Schiaffino S, Gundersen K, Lomo T (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 10:153–160

    CAS  PubMed  Google Scholar 

  • Bar A, Pette D (1988) Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett 235:153–155

    Article  CAS  PubMed  Google Scholar 

  • Beard NA, Laver DR, Dulhunty AF (2004) Calsequestrin and the calcium release channel of skeletal and cardiac muscle. Prog Biophys Mol Biol 85:33–69

    Article  CAS  PubMed  Google Scholar 

  • Berchtold MW, Brinkmeier H, Muntener M (2000) Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev 80:1215–1265

    CAS  PubMed  Google Scholar 

  • Blaauw B, Schiaffino S, Reggiani C (2013) Mechanisms modulating skeletal muscle phenotype. Compr Physiol 3:1645–1687

    Article  PubMed  Google Scholar 

  • Buller AJ, Eccles JC, Eccles RM (1960) Interactions between motoneurons and muscles in respect of the characteristic speeds of their responses. J Physiol 50:417–439

    Article  Google Scholar 

  • Buonanno A, Rosenthal N (1996) Molecular control of muscle diversity and plasticity. Dev Genet 19:95–107

    Article  CAS  PubMed  Google Scholar 

  • Caiozzo VJ, Baker MJ, Herrick RE, Tao M, Baldwin KM (1994) Effect of spaceflight on skeletal muscle: mechanical properties and myosin isoform content of a slow muscle. J Appl Physiol 76:1764–1773

    Article  CAS  PubMed  Google Scholar 

  • Caiozzo VJ, Baker MJ, Baldwin KM (1998) Novel transitions in MHC isoforms: separate and combined effects of thyroid hormone and mechanical unloading. J Appl Physiol 85:2237–2248

    CAS  PubMed  Google Scholar 

  • Caiozzo VJ, Baker MJ, Huang K, Chou H, Wu YZ, Baldwin KM (2003) Single-fiber myosin heavy chain polymorphism: how many patterns and what proportions? Am J Physiol Regul Integr Comp Physiol 285:R570–R580

    PubMed  Google Scholar 

  • d’Albis A, Butler-Browne G (1993) The hormonal control of myosin isoform expression in skeletal muscle of mammals: a review. BAM 3:7–16

    Google Scholar 

  • DeNardi C, Ausoni S, Moretti P, Gorza L, Velleca M, Buckingham M, Schiaffino S (1993) Type 2X-myosin heavy chain is coded by a muscle fiber type-specific and developmentally regulated gene. J Cell Biol 123:823–835

    Article  CAS  PubMed  Google Scholar 

  • Devor ST, White TP (1995) Myosin heavy chain phenotype in regenerating skeletal muscle is affected by thyroid hormone. Med Sci Sports Exerc 27:674–681

    Article  CAS  PubMed  Google Scholar 

  • Devor ST, White TP (1996) Myosin heavy chain of immature soleus muscle grafts adapts to hyperthyroidism more than to physical activity. J Appl Physiol 80:789–794

    CAS  PubMed  Google Scholar 

  • Diffee GM, Haddad F, Herrick RE, Baldwin KM (1991) Control of myosin heavy chain expression: interaction of hypothyroidism and hindlimb suspension. Am J Physiol 261:C1099–C1106

    CAS  PubMed  Google Scholar 

  • Donovan CM, Faulkner JA (1987) Plasticity of skeletal muscle: regenerating fibers adapt more rapidly than surviving fibers. J Appl Physiol 62:2507–2511

    CAS  PubMed  Google Scholar 

  • Gambke B, Lyons GE, Haselgrove J, Kelly AM, Rubinstein NA (1983) Thyroidal and neural control of myosin transitions during development of rat fast and slow muscles. FEBS Lett 156:335–339

    Article  CAS  PubMed  Google Scholar 

  • Gunning P, Hardeman E (1991) Multiple mechanisms regulate muscle fiber diversity. FASEB J 5:3064–3070

    CAS  PubMed  Google Scholar 

  • Hamalainen N, Pette D (1996) Slow-to-fast transitions in myosin expression of rat soleus muscle by phasic high-frequency stimulation. FEBS Lett 399:220–222

    Article  CAS  PubMed  Google Scholar 

  • Harvey CB, Williams GR (2002) Mechanism of thyroid hormone action. Thyroid 12:441–446 (Review)

    Article  CAS  PubMed  Google Scholar 

  • Hennig R, Lomo T (1985) Firing patterns of motor units in normal rats. Nature 314:164–166

    Article  CAS  PubMed  Google Scholar 

  • Hoh JF (1991) Myogenic regulation of mammalian skeletal muscle fibres. News Physiol Sci 6:1–6

    CAS  PubMed  Google Scholar 

  • Hudecova S, Vadaszova A, Soukup T, Krizanova O (2004) Effect of thyroid hormones on the gene expression of calcium transport systems in rat muscles. Life Sci 75:923–931

    Article  CAS  PubMed  Google Scholar 

  • Ianuzzo CD, Hamilton N, Li B (1991) Competitive control of myosin expression: hypertrophy vs. hyperthyroidism. J Appl Physiol 70:2328–2330

    CAS  PubMed  Google Scholar 

  • Izumo S, Nadal-Ginard B, Mahdavi V (1986) All members of the MHC multigene family respond to thyroid hormone in a highly tissue-specific manner. Science 231:597–600

    Article  CAS  PubMed  Google Scholar 

  • Jirmanova I, Soukup T (1995) Critical period in muscle spindle regeneration in grafts of developing rat muscles. Anat Embryol (Berl) 192:283–291

    Article  CAS  Google Scholar 

  • Jirmanova I, Soukup T (2001) Early changes in extrafusal and intrafusal muscle fibers following heterochronous isotransplantation. Acta Neuropathol 102:473–484

    CAS  PubMed  Google Scholar 

  • Kirschbaum BJ, Kucher HB, Termin A, Kelly AM, Pette D (1990) Antagonistic effects of chronic low frequency stimulation and thyroid hormone on myosin expression in rat fast-twitch muscle. J Biol Chem 265:13974–13980

    CAS  PubMed  Google Scholar 

  • Kopecká K, Zacharova G, Smerdu V, Soukup T (2014) Slow to fast muscle transformation following heterochronous isotransplantation is influenced by host thyroid hormone status. Histochem Cell Biol. doi:10.1007/s00418-014-1247-5

    PubMed  Google Scholar 

  • Kraemer WJ, Staron RS, Gordon SE, Volek JS, Koziris LP, Duncan ND, Nindl BC, Gomez AL, Marx JO, Fry AC, Murray JD (2000) The effects of 10 days of spaceflight on the shuttle Endeavor on predominantly fast-twitch muscles in the rat. Histochem Cell Biol 114:349–355

    CAS  PubMed  Google Scholar 

  • Larsson L, Li X, Teresi A, Salviati G (1994) Effects of thyroid hormone on fast- and slow-twitch skeletal muscles in young and old rats. J Physiol 481(Pt 1):149–161

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lucas CA, Kang LH, Hoh JF (2000) Monospecific antibodies against the three mammalian fast limb myosin heavy chains. Biochem Biophys Res Commun 272:303–308

    Article  CAS  PubMed  Google Scholar 

  • Novak P, Soukup T (2011) Calsequestrin distribution, structure and function, its role in normal and pathological situations and the effect of thyroid hormones. Physiol Res 60:439–452

    CAS  PubMed  Google Scholar 

  • Novak P, Zacharova G, Soukup T (2010) Individual, age and sex differences in fiber type composition of slow and fast muscles of adult Lewis rats: comparison with other rat strains. Physiol Res 59:783–801

    CAS  PubMed  Google Scholar 

  • Pette D (2002) The adaptive potential of skeletal muscle fibers. Can J Appl Physiol 27:423–448

    Article  PubMed  Google Scholar 

  • Pette D, Staron RS (1997) Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 170:143–223

    Article  CAS  PubMed  Google Scholar 

  • Pette D, Staron RS (2000) Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50:500–509

    Article  CAS  PubMed  Google Scholar 

  • Pette D, Staron RS (2001) Transitions of muscle fiber phenotypic profiles. Histochem Cell Biol 115:359–372

    CAS  PubMed  Google Scholar 

  • Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115–202

    Article  CAS  PubMed  Google Scholar 

  • Rauchova H, Mracek T, Novak P, Vokurkova M, Soukup T (2011) Glycerol-3-phosphate dehydrogenase expression and oxygen consumption in liver mitochondria of female and male rats with chronic alteration of thyroid status. Horm Metab Res 43:43–47

    Article  CAS  PubMed  Google Scholar 

  • Rauchova H, Vokurkova M, Pavelka S, Behuliak M, Tribulova N, Soukup T (2013) N-3 polyunsaturated fatty acids supplementation does not affect changes of lipid metabolism induced in rats by altered thyroid status. Horm Metab Res 45:507–512

    Article  CAS  PubMed  Google Scholar 

  • Ricny J, Soukup T (2011) Comparison of new ELISA method with established SDS-PAGE method for determination of muscle myosin heavy chain isoforms. Physiol Res 60:899–904

    CAS  PubMed  Google Scholar 

  • Schiaffino S (2010) Fibre types in skeletal muscle: a personal account. Acta Physiol (Oxf) 199:451–463

    Article  CAS  Google Scholar 

  • Schiaffino S, Reggiani C (1994) Myosin isoforms in mammalian skeletal muscle. J Appl Physiol 77:493–501

    CAS  PubMed  Google Scholar 

  • Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76:371–423

    CAS  PubMed  Google Scholar 

  • Schiaffino S, Reggiani C (2011) Fiber types in mammalian skeletal muscles. Physiol Rev 91:1447–1531

    Article  CAS  PubMed  Google Scholar 

  • Schiaffino S, Hanzlikova V, Pierobon S (1970) Relations between structure and function in rat skeletal muscle fibers. J Cell Biol 47:107–119

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Simonides WS, van Hardeveld C (2008) Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid 18:205–216. doi:10.1089/thy.2007.0256 (Review)

    Article  CAS  PubMed  Google Scholar 

  • Smerdu V, Cvetko E (2013) Myosin heavy chain-2b transcripts and isoform are expressed in human laryngeal muscles. Cells Tissues Organs 198:75–86

    Article  CAS  PubMed  Google Scholar 

  • Smerdu V, Eržen I (2001) Dynamic nature of fibre-type specific expression of myosin heavy chain transcripts in 14 different human skeletal muscles. J Muscle Res Cell Motil 22:647–655

    Article  CAS  PubMed  Google Scholar 

  • Smerdu V, Soukup T (2008) Demonstration of myosin heavy chain isoforms in rat and humans: the specificity of seven available monoclonal antibodies used in immunohistochemical and immunoblotting methods. Eur J Histochem 52:179–190

    Article  PubMed  Google Scholar 

  • Snoj-Cvetko E, Smerdu V, Sketelj J, Dolenc I, D’Albis A, Janmot C, Erzen I (1996) Adaptive range of myosin heavy chain expression in regenerating soleus is broader than in mature muscle. J Muscle Res Cell Motil 17:401–409

    Article  CAS  PubMed  Google Scholar 

  • Soukup T (2014) Effects of long-term thyroid hormone level alterations, n-3 polyunsaturated fatty acid supplementation and statin administration in rats. Physiol Res 63(Suppl 1):S119–S131

    CAS  PubMed  Google Scholar 

  • Soukup T (2015) Alterations of thyroid status preserve proportions between myosin heavy chain mRNAs, protein isoforms and fiber types revealed in the slow and fast muscles of euthyroid rats. Physiol Res 63(1):1–8 (in press)

  • Soukup T, Jirmanova I (2000) Regulation of myosin expression in developing and regenerating extrafusal and intrafusal muscle fibers with special emphasis on the role of thyroid hormones. Physiol Res 49:617–633

    CAS  PubMed  Google Scholar 

  • Soukup T, Zacharova G, Smerdu V, Jirmanova I (2001) Body, heart, thyroid gland and skeletal muscle weight changes in rats with altered thyroid status. Physiol Res 50:619–626

    CAS  PubMed  Google Scholar 

  • Soukup T, Zacharova G, Smerdu V (2002) Fibre type composition of soleus and extensor digitorum longus muscles in normal female inbred Lewis rats. Acta Histochem 104:399–405

    Article  PubMed  Google Scholar 

  • Soukup T, Smerdu V, Zacharova G (2009) Fiber type composition of unoperated rat soleus and extensor digitorum longus muscles after unilateral isotransplantation of a foreign muscle in long-term experiments. Physiol Res 58:253–262

    CAS  PubMed  Google Scholar 

  • Soukup T, Sulimenko V, Markova V, Kopecka K, Zacharova G, Palecek J (2012) Expression of the skeletal calsequestrin isoform in normal and regenerated skeletal muscles and in the hearts of rats with altered thyroid status. Physiol Res 61:575–586

    CAS  PubMed  Google Scholar 

  • Staron RS, Herman JR, Schuenke MD (2012) Misclassification of hybrid fast fibers in resistance-trained human skeletal muscle using histochemical and immunohistochemical methods. J Strength Cond Res 26:2616–2622

    Article  PubMed  Google Scholar 

  • Stephenson GM (2001) Hybrid skeletal muscle fibres: a rare or common phenomenon? Clin Exp Pharmacol Physiol 28:692–702 (Review)

    Article  CAS  PubMed  Google Scholar 

  • Stevens L, Sultan KR, Peuker H, Gohlsch B, Mounier Y, Pette D (1999) Time-dependent changes in myosin heavy chain mRNA and protein isoforms in unloaded soleus muscle of rat. Am J Physiol 277:C1044–C1049

    CAS  PubMed  Google Scholar 

  • Talmadge RJ (2000) Myosin heavy chain isoform expression following reduced neuromuscular activity: potential regulatory mechanisms. Muscle Nerve 23:661–679

    Article  CAS  PubMed  Google Scholar 

  • Tian LM, Feng DP (1990) The interaction of thyroidectomy with spinal cord transaction or cross-innervation in their effects on muscle phenotypic characteristics. Chin J Physiol Sci 6:1–12

    Google Scholar 

  • Tribulova N, Knezl V, Shainberg A, Seki S, Soukup T (2010) Thyroid hormones and cardiac arrhythmias. Vascul Pharmacol 52:102–112

    Article  CAS  PubMed  Google Scholar 

  • Vadaszova A, Zacharova G, Machacova K, Jirmanova I, Soukup T (2004) Influence of thyroid status on the differentiation of slow and fast muscle phenotypes. Physiol Res 53(Suppl 1):S57–S61

    PubMed  Google Scholar 

  • Vadaszova A, Hudecova S, Krizanova O, Soukup T (2006a) Levels of myosin heavy chain mRNA transcripts and content of protein isoforms in the slow soleus muscle of 7 month-old rats with altered thyroid status. Physiol Res 55:221–225

    CAS  PubMed  Google Scholar 

  • Vadaszova A, Hudecova S, Krizanova O, Soukup T (2006b) Levels of myosin heavy chain mRNA transcripts and protein isoforms in the fast extensor digitorum longus muscle of 7-month-old rats with chronic thyroid status alterations. Physiol Res 55:707–710

    CAS  PubMed  Google Scholar 

  • Vadaszova-Soukup A, Soukup T (2007) Dual role of thyroid hormones in rat soleus muscle MyHC isoform expression. Physiol Res 56:833–836

    CAS  PubMed  Google Scholar 

  • Weiss A, McDonough D, Wertman B, Acakpo-Satchivi L, Montgomery K, Kucherlapati R, Leinwand L, Krauter K (1999) Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc Natl Acad Sci USA 96:2958–2963

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yen PM (2001) Physiological and molecular basis of thyroid hormone action. Physiol Rev 81:1097–1142

    CAS  PubMed  Google Scholar 

  • Yoon SJ, Seiler SH, Kucherlapati R, Leinwand L (1992) Organization of the human skeletal myosin heavy chain gene cluster. Proc Natl Acad Sci USA 89:12078–12082

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu F, Degens H, Larsson L (1999) The influence of thyroid hormone on myosin isoform composition and shortening velocity of single skeletal muscle fibres with special reference to ageing and gender. Acta Physiol Scand 167:313–316

    Article  CAS  PubMed  Google Scholar 

  • Zacharova G, Kubinova L (1995) Stereological methods based on point counting and unbiased counting frames for two-dimensional measurements in muscles: comparison with manual and image analysis methods. J Muscle Res Cell Motil 16:295–302

    Article  CAS  PubMed  Google Scholar 

  • Zacharova G, Knotkova-Urbancova H, Hnik P, Soukup T (1997) Nociceptive atrophy of the rat soleus muscle induced by bone fracture: a morphometric study. J Appl Physiol 82:552–557

    Article  CAS  PubMed  Google Scholar 

  • Zacharova G, Vadaszova A, Smerdu V, Asmussen G, Soukup T (2005) The effect of a unilateral muscle transplantation on the muscle fiber type and the MyHC isoform content in unoperated hind limb slow and fast muscles of the inbred Lewis rats. Physiol Res 54:691–696

    CAS  PubMed  Google Scholar 

  • Zurmanova J, Soukup T (2013) Comparison of myosin heavy chain mRNAs, protein isoforms and fiber type proportions in the rat slow and fast muscles. Physiol Res 62:445–453

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by MYORES LSH-CT-2004-511978, MSCT CR LH12058 and 7AMB14SK123, the Czech-Slovenian Intergovernmental S&T Co-operation Program Grant, Slovenian Research Agency (P3-0043) and by Research Project RVO: 67985823 (AV0Z 50110509).

Author information

Authors and Affiliations

  1. Institute of Physiology, Academy of Sciences of the Czech Republic, v.v.i., Vídeňská 1083, 142 20, Prague, Czech Republic

    Tomáš Soukup

  2. Faculty of Medicine, Institute of Anatomy, University in Ljubljana, Ljubljana, Slovenia

    Vika Smerdu

Authors
  1. Tomáš Soukup
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vika Smerdu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomáš Soukup.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soukup, T., Smerdu, V. Effect of altered innervation and thyroid hormones on myosin heavy chain expression and fiber type transitions: a mini-review. Histochem Cell Biol 143, 123–130 (2015). https://doi.org/10.1007/s00418-014-1276-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-014-1276-0

Keywords

Search

Navigation