Skip to main content

Advertisement

SpringerLink
Log in

Remarkable heterogeneity in myosin heavy-chain composition of the human young masseter compared with young biceps brachii

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Adult human jaw muscles differ from limb and trunk muscles in enzyme-histochemical fibre type composition. Recently, we showed that the human masseter and biceps differ in fibre type pattern already at childhood. The present study explored the myosin heavy-chain (MyHC) expression in the young masseter and biceps muscles by means of gel electrophoresis (GE) and immuno-histochemical (IHC) techniques. Plasticity in MyHC expression during life was evaluated by comparing the results with the previously reported data for adult muscles. In young masseter, GE identified MyHC-I, MyHC-IIa MyHC-IIx and small proportions of MyHC-fetal and MyHC-α cardiac. Western blots confirmed the presence of MyHC-I, MyHC-IIa and MyHC-IIx. IHC revealed in the masseter six isomyosins, MyHC-I, MyHC-IIa, MyHC-IIx, MyHC-fetal, MyHC α-cardiac and a previously not reported isoform, termed MyHC-IIx′. The majority of the masseter fibres co-expressed two to four isoforms. In the young biceps, both GE and IHC identified MyHC-I, MyHC-IIa and MyHC-IIx. MyHC-I predominated in both muscles. Young masseter showed more slow and less-fast and fetal MyHC than the adult and elderly masseter. These results provide evidence that the young masseter muscle is unique in MyHC composition, expressing MyHC-α cardiac and MyHC-fetal isoforms as well as hitherto unrecognized potential spliced isoforms of MyHC-fetal and MyHC-IIx. Differences in masseter MyHC expression between young adult and elderly suggest a shift from childhood to adulthood towards more fast contractile properties. Differences between masseter and biceps are proposed to reflect diverse evolutionary and developmental origins and confirm that the masseter and biceps present separate allotypes of muscle.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • 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  Google Scholar 

  • Berg JS, Powell BC, Cheney RE (2001) A millennial myosin census. Mol Biol Cell 12:780–794

    PubMed  CAS  Google Scholar 

  • Bredman JJ, Wessels A, Weijs WA, Korfage JA, Soffers CA, Mooman AF (1991) Demonstration of “cardiac-specific” myosin heavy chain in masticatory muscles of human and rabbit. Histochem J 23:160–170

    Article  PubMed  CAS  Google Scholar 

  • Butler-Browne G, Eriksson P-O, Laurent C, Thornell L-E (1988) Adult human masseter muscle fibres express myosin isozymes characteristic of development. Muscle Nerve 11:610–620

    Article  PubMed  CAS  Google Scholar 

  • Cho M, Webster SG, Blau HM (1993) Evidence for myoblast-extrinsic regulation of slow myosin heavy chain expression during muscle fiber formation in embryonic development. J Cell Biol 121:795–810

    Google Scholar 

  • Desjardins PR, Burkman JM, Shrager JB, Allmond LA, Stedman HH (2002) Evolutionary implications of three novel members of the human sarcomeric myosin heavy chain gene family. Mol Biol Evol 19:375–393

    Article  PubMed  CAS  Google Scholar 

  • Dubowitz V (2007) Muscle biopsy: a practical approach, vol 3. Bailliére Tindall, London, pp 47–74

    Google Scholar 

  • Ecob-Prince M, Hill M, Brown W (1989) Immunocytochemical demonstration of myosin heavy chain expression in human muscle. J Neurol Sci 91:71–78

    Google Scholar 

  • Engel A, Franzini-Armstrong C (2004) Myology: basic and Clinical, New York

  • Eriksson P-O (1982) Muscle-fibre composition of the human mandibular locomotor system: enzyme-histochemical and morphological characteristics of functionally different parts. Swed Dent J Suppl 12(Suppl):1–44

    PubMed  Google Scholar 

  • Eriksson P-O, Thornell L-E (1983) Histochemical and morphological muscle-fibre characteristics of the human masseter, the medial pterygoid and the temporal muscles. Arch Oral Biol 28:781–795

    Article  PubMed  CAS  Google Scholar 

  • Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimaraes-Camboa N, Evans SM, Tzahor E (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16:822–832

    Article  PubMed  CAS  Google Scholar 

  • Harzer W, Maricic N, Gedrange T, Lewis M, Hunt N (2010) Molecular diagnosis in orthodontics, facial, and orthognathic surgery: implications for treatment progress and relapse. Semin Orthod 16:118–127

    Article  Google Scholar 

  • Herron TJ, McDonald KS (2002) Small amounts of alpha-myosin heavy chain isoform expression significantly increase power output of rat cardiac myocyte fragments. Circ Res 90:1150–1152

    Article  PubMed  CAS  Google Scholar 

  • Hoh JF (2002) Superfast or masticatory myosin and the evolution of jaw-closing muscles of vertebrates. J Exp Biol 205:2203–2210

    PubMed  Google Scholar 

  • Hoh JF (2005) Laryngeal muscle fibre types. Acta Physiol Scand 183:133–149

    Article  PubMed  CAS  Google Scholar 

  • Hoh JF, Hughes S, Kang LHD, Rughani A, Qin H (1993) The biology of cat jaw-closing muscle cells. J Comput-Assist Microsc 5:65–70

    Google Scholar 

  • Hughes SM, Cho M, Karsch-Mizrachi I, Travis M, Silberstein L, Leinwand LA, Blau HM (1993) Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev Biol 158:183–199

    Article  PubMed  CAS  Google Scholar 

  • Kang L, Hughes S, Pettigrew J, Hoh J (1994) Jaw-specific myosin heavy chain gene expression in sheep, dog monkey, flying fox and microbat jaw-closing muscles. Basic Appl Myol 4:381–392

    Google Scholar 

  • Karsch-Mizrachi I, Travis M, Blau H, Leinwand LA (1989) Expression and DNA sequence analysis of a human embryonic skeletal muscle myosin heavy chain gene. Nucleic Acids Res 17:6167–6179

    Article  PubMed  CAS  Google Scholar 

  • Kjellgren D, Thornell L-E, Andersen J, Pedrosa-Domellöf F (2003) Myosin heavy chain isoforms in human extraocular muscles. Invest Ophthalmol Vis Sci 44:1419–1425

    Article  PubMed  Google Scholar 

  • Léger JJ (1985) Institut National de la Santé et de la Recherche Médical, Unité 249, Montpellier, France

  • Liu J-X, Eriksson P-O, Thornell L-E, Pedrosa-Domellöf F (2002) Myosin heavy chain composition of muscle spindles in human biceps brachii. J Histochem Cytochem 50:171–183

    Article  PubMed  CAS  Google Scholar 

  • Lucas CA, Hoh JF (2003) Distribution of developmental myosin heavy chains in adult rabbit extraocular muscle: identification of a novel embryonic isoform absent in fetal limb. Invest Ophthalmol Vis Sci 44:2450–2456

    Article  PubMed  Google Scholar 

  • Mahdavi V, Chambers AP, Nadal-Ginard B (1984) Cardiac alpha- and beta-myosin heavy chain genes are organized in tandem. Proc Natl Acad Sci USA 81:2626–2630

    Article  PubMed  CAS  Google Scholar 

  • McCollum MA, Sherwood CC, Vinyard CJ, Lovejoy CO, Schachat F (2006) Of muscle-bound crania and human brain evolution: the story behind the MYH16 headlines. J Hum Evol 50:232–236

    Article  PubMed  Google Scholar 

  • Monemi M, Eriksson P-O, Eriksson A, Thornell L-E (1998) Adverse changes in fibre type composition of the human masseter versus biceps brachii muscle during aging. J Neurol Sci 154:35–48

    Article  PubMed  CAS  Google Scholar 

  • Monemi M, Eriksson P-O, Kadi F, Butler-Browne GS, Thornell L-E (1999) Opposite changes in myosin heavy chain composition of human masseter and biceps brachii muscles during aging. J Muscle Res Cell Motil 20:351–361

    Article  PubMed  CAS  Google Scholar 

  • Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218

    Article  PubMed  CAS  Google Scholar 

  • Österlund C, Thornell L-E, Eriksson P-O (2011) Differences in fibre type composition between human masseter and biceps muscles in young and adults reveal unique masseter fibre type growth pattern. Anat Rec (Hoboken) 294:1158–1169

    Article  Google Scholar 

  • Oukhai K, Maricic N, Schneider M, Harzer W, Tausche E (2011) Developmental myosin heavy chain mRNA in masseter after orthognathic surgery: a preliminary study. J Craniomaxillofac Surg 39:401–406

    Article  PubMed  Google Scholar 

  • Pedrosa-Domellöf F, Eriksson P-O, Butler-Browne G, Thornell L-E (1992) Expression of alpha-cardiac myosin heavy chain in mammalian skeletal muscle. Experientia 48:491–494

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Qin H, Hsu MK, Morris BJ, Hoh JF (2002) A distinct subclass of mammalian striated myosins: structure and molecular evolution of “superfast” or masticatory myosin heavy chain. J Mol Evol 55:544–552

    Article  PubMed  CAS  Google Scholar 

  • Ringqvist M (1973) Histochemical enzyme profiles of fibres in human masseter muscles with special regard to fibres with intermediate myofibrillar ATPase reaction. J Neurol Sci 18:133–141

    Article  PubMed  CAS  Google Scholar 

  • Rossi AC, Mammucari C, Argentini C, Reggiani C, Schiaffino S (2010) Two novel/ancient myosins in mammalian skeletal muscles: MYH14/7b and MYH15 are expressed in extraocular muscles and muscle spindles. J Physiol 588:353–364

    Article  PubMed  CAS  Google Scholar 

  • Rowlerson A, Pope B, Murray R, Weeds A (1981) A novel myosin present in cat jaw-closing muscles. J Muscle Res Cell Motil 2:415–438

    Article  CAS  Google Scholar 

  • Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138:2401–2415

    Article  PubMed  CAS  Google Scholar 

  • Sawchak JA, Leung B, Shafiq SA (1985) Characterization of a monoclonal antibody to myosin specific for mammalian and human type II muscle fibers. J Neurol Sci 69:247–254

    Article  PubMed  CAS  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, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lomo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Nielson K (1984) Scaling: why animal size is so important. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Sewry CA, Uziyel Y, Torelli S, Buchanan S, Sorokin L, Cohen J, Watt DJ (1998) Differential labelling of laminin alpha 2 in muscle and neural tissue of dy/dy mice: are there isoforms of the laminin alpha 2 chain? Neuropathol Appl Neurobiol 24:66–72

    PubMed  CAS  Google Scholar 

  • Silberstein L, Webster SG, Travis M, Blau HM (1986) Developmental progression of myosin gene expression in cultured muscle cells. Cell 46:1075–1081

    Article  PubMed  CAS  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

    PubMed  Google Scholar 

  • Soussi-Yanicostas N, Barbet J, Laurent-Winter C, Barton P, Butler-Browne GS (1990) Transition of myosin isozymes during development of human masseter muscle: persistence of developmental isoforms during postnatal stage. Development 108:239–249

    PubMed  CAS  Google Scholar 

  • Stål P, Eriksson P-O, Schiaffino S, Butler-Browne GS, Thornell L-E (1994) Differences in myosin composition between human orofacial, masticatory and limb muscles: enzyme-, immunohist- and biochemical-studies. J Muscle Res Cell Motil 15:517–534

    Article  PubMed  Google Scholar 

  • Stedman HH, Kozyak BW, Nelson A, Thesier DM, Su LT, Low DW, Bridges CR, Shrager JB, Minugh-Purvis N, Mitchell MA (2004) Myosin gene mutation correlates with anatomical changes in the human lineage. Nature 428:415–418

    Article  PubMed  CAS  Google Scholar 

  • Sternberger LA (1979) The unlabeled antibody (PAP) method, introduction. J Histochem Cytochem 27:1657

    Article  PubMed  CAS  Google Scholar 

  • Swynghedauw B (1986) Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Physiol Rev 66:710–771

    PubMed  CAS  Google Scholar 

  • Talmadge RJ, Roy RR (1993) Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 75:2337–2340

    PubMed  CAS  Google Scholar 

  • Thornell L-E, Billeter R, Eriksson P-O, Ringqvist M (1984) Heterogenous distribution of myosin in human masticatory muscle fibres as shown by immunocytochemistry. Archs oral Biol 29:1–5

    Article  CAS  Google Scholar 

  • Thornell L-E, Grove B, Pedrosa F, Butler-Browne G, Dhoot G, Fischman D (1989) Expression of slow tonic myosin in muscle spindle fibres early in mammalian development. In: Stockdale F, Kedes I (eds) Molecular biology of muscle development. Alan R Liss, New York, pp 471–480

  • Walro JM, Kucera J (1999) Why adult mammalian intrafusal and extrafusal fibers contain different myosin heavy-chain isoforms. Trends Neurosci 22:180–184

    Article  PubMed  CAS  Google Scholar 

  • Weiss A, Schiaffino S, Leinwand LA (1999) Comparative sequence analysis of the complete human sarcomeric myosin heavy chain family: implications for functioanl diversity. J Mol Biol 290:61–75

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Mrs. Inga Johansson for excellent technical assistance and associate professor Albert Crenshaw for English revision and valuable comments. This work was supported by grants from the Department of Odontology, Umeå University, Västerbotten County Council and the Swedish Dental Society.

Author information

Authors and Affiliations

  1. Department of Odontology, Clinical Oral Physiology, Umeå University, 901 87, Umeå, Sweden

    Catharina Österlund & Per-Olof Eriksson

  2. Integrative Medical Biology, Section of Anatomy Umeå University, Umeå, Sweden

    Mona Lindström & Lars-Eric Thornell

Authors
  1. Catharina Österlund
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mona Lindström
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lars-Eric Thornell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Per-Olof Eriksson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Per-Olof Eriksson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Österlund, C., Lindström, M., Thornell, LE. et al. Remarkable heterogeneity in myosin heavy-chain composition of the human young masseter compared with young biceps brachii. Histochem Cell Biol 138, 669–682 (2012). https://doi.org/10.1007/s00418-012-0985-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-012-0985-5

Keywords

Search

Navigation