Differences in myosin composition between human oro-facial, masticatory and limb muscles: enzyme-, immunohisto-and biochemical studies

SummaryImmunohistochemistry was used to determine the myosin composition of defined fibre types of three embryologically different adult muscles, the oro-facial, masseter and limb muscles. In addition, the myosin composition in whole muscle specimens was analysed with biochemical methods. Both similarities and differences between muscles in the content of myosin heavy chains and myosin light chains were found. Nevertheless, each muscle had its own distinct identity. Our results indicated the presence of a previously undetected fast myosin heavy chain isoform in the oro-facial type II fibre population, tentatively termed ‘fast F’. The masseter contained aberrant myosin isoforms, such as foetal myosin heavy chain and α-cardiac myosin heavy chain and unique combinations of myosin heavy chain isoforms which were not found in the limb or oro-facial muscles. The type IM and IIC fibres coexpressed slow and fast A myosin heavy chains in the oro-facial and limb muscles but slow and a fast B like myosin heavy chain in the masseter. While single oro-facial and limb muscle fibres contained one or two myosin heavy chain types, single masseter fibres coexpressed up to four different myosin heavy chain isoforms. Describing the fibres according to their expression of myosin heavy chain isozymes, up to five fibre types could be distinguished in the oro-facial and limb muscles and eight in the masseter. Oro-facial and limb muscles expressed five myosin light chains, MLC1S, MLC2S, MLC1F, MLC2F and MLC3F, and the masseter four, MLC1S, MLC2S, MLC1F, and, in addition, an embryonic myosin light chain, MLCtemb, which is usually not present in normal adult skeletal muscle. These results probably reflect the way the muscles have evolved to meet the specialized functional requirements imposed upon them and are in agreement with the previously proposed concept that jaw and limb muscles belong to two distinct allotypes.

[1]  L. Leinwand,et al.  Characterization of diverse forms of myosin heavy chain expressed in adult human skeletal muscle. , 1986, Nucleic acids research.

[2]  Cellular and molecular biology of muscle development , 2022 .

[3]  D. Biral,et al.  Myosin heavy chain composition of single fibres from normal human muscle. , 1988, The Biochemical journal.

[4]  H. Eppenberger,et al.  Myosin types in human skeletal muscle fibers , 2004, Histochemistry.

[5]  R. Low,et al.  Fractional synthesis rates in vivo of skeletal-muscle myosin isoenzymes. , 1987, The Biochemical journal.

[6]  L. Gorza Identification of a novel type 2 fiber population in mammalian skeletal muscle by combined use of histochemical myosin ATPase and anti-myosin monoclonal antibodies. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[7]  N. Rubinstein,et al.  A monoclonal antibody to the embryonic myosin heavy chain of rat skeletal muscle. , 1984, The Journal of biological chemistry.

[8]  P. Schantz,et al.  Coexistence of slow and fast isoforms of contractile and regulatory proteins in human skeletal muscle fibres induced by endurance training. , 1987, Acta physiologica Scandinavica.

[9]  J. Léger,et al.  Levels of ventricular myosin fragments in human sera after myocardial infarction, determined with monoclonal antibodies to myosin heavy chains , 1985, European journal of clinical investigation.

[10]  J. Hoh,et al.  Embryonic and foetal myosins in human skeletal muscle The presence of foetal myosins in duchenne muscular dystrophy and infantile spinal muscular atrophy , 1981, Journal of the Neurological Sciences.

[11]  B. Saltin,et al.  Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. , 1990, Acta physiologica Scandinavica.

[12]  L. Thornell,et al.  Histochemical and morphological muscle-fibre characteristics of the human masseter, the medial pterygoid and the temporal muscles. , 1983, Archives of oral biology.

[13]  D. Leroith,et al.  Skeletal muscle. , 2005, Advances in experimental medicine and biology.

[14]  S. Shafiq,et al.  Characterization of a monoclonal antibody to myosin specific for mammalian and human type II muscle fibers , 1985, Journal of the Neurological Sciences.

[15]  S. Schiaffino,et al.  "Slow" myosins in vertebrate skeletal muscle. An immunofluorescence study , 1980, The Journal of cell biology.

[16]  G. Butler-Browne,et al.  Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. , 1984, Developmental biology.

[17]  R. Herrick,et al.  Time course adaptations in rat skeletal muscle isomyosins during compensatory growth and regression. , 1987, Journal of applied physiology.

[18]  F. Gros,et al.  Identification of a novel form of myosin light chain present in embryonic muscle tissue and cultured muscle cells. , 1978, Journal of molecular biology.

[19]  M. Brooke,et al.  Muscle fiber types: how many and what kind? , 1970, Archives of neurology.

[20]  G. Butler-Browne,et al.  Myosin heavy and light chain expression during human skeletal muscle development and precocious muscle maturation induced by thyroid hormone , 2004, Anatomy and Embryology.

[21]  A. Moorman,et al.  Demonstration of ‘cardiac-specific’ myosin heavy chain in masticatory muscles of human and rabbit , 1991, The Histochemical Journal.

[22]  G. Butler-Browne,et al.  Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. , 1994, Developmental biology.

[23]  K. Trybus,et al.  Skeletal muscle myosin light chains are essential for physiological speeds of shortening , 1993, Nature.

[24]  G. Butler-Browne,et al.  Immunohistochemical characterization of human masseter muscle spindles , 1994, Muscle & nerve.

[25]  D. Pette,et al.  Cellular and molecular diversities of mammalian skeletal muscle fibers. , 1990, Reviews of physiology, biochemistry and pharmacology.

[26]  D. Pette,et al.  Correlation between myofibrillar ATPase activity and myosin heavy chain composition in rabbit muscle fibers , 2004, Histochemistry.

[27]  R. Herrick,et al.  Subunit composition of rodent isomyosins and their distribution in hindlimb skeletal muscles. , 1987, Journal of applied physiology.

[28]  G. Butler-Browne,et al.  Adult human masseter muscle fibers express myosin isozymes characteristic of development , 1988, Muscle & nerve.

[29]  D. Pette,et al.  Three fast myosin heavy chains in adult rat skeletal muscle , 1988, FEBS letters.

[30]  G. Butler-Browne,et al.  Three myosin heavy-chain isozymes appear sequentially in rat muscle development , 1981, Nature.

[31]  C. Heizmann,et al.  Analysis of myosin light and heavy chain types in single human skeletal muscle fibers. , 1981, European journal of biochemistry.

[32]  Kristian Gundersen,et al.  Three myosin heavy chain isoforms in type 2 skeletal muscle fibres , 1989, Journal of Muscle Research & Cell Motility.

[33]  S. Schiaffino,et al.  Fibre types in extraocular muscles: a new myosin isoform in the fast fibres , 1987, Journal of Muscle Research & Cell Motility.

[34]  L. Thornell,et al.  Enzyme-histochemical and morphological characteristics of muscle fibre types in the human buccinator and orbicularis oris. , 1990, Archives of oral biology.

[35]  R. Staron Correlation between myofibrillar ATPase activity and myosin heavy chain composition in single human muscle fibers , 2004, Histochemistry.

[36]  A Eriksson,et al.  Enzyme-histochemical differences in fibre-type between the human major and minor zygomatic and the first dorsal interosseus muscles. , 1987, Archives of oral biology.

[37]  R. Staron,et al.  Histochemical, biochemical, and ultrastructural analyses of single human muscle fibers, with special reference to the C-fiber population. , 1992, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[38]  J. Hoh,et al.  Three Hierarchies in Skeletal Muscle Fibre Classification Allotype, Isotype and Phenotype , 1991 .

[39]  G. Butler-Browne,et al.  Immunocytochemical characterisation of two generations of fibers during the development of the human quadriceps muscle , 1991, Mechanisms of Development.

[40]  Myofibrillar and Cytoskeletal Proteins in Human Muscle Spindles , 1988 .

[41]  S. Schiaffino,et al.  "SLOW" MYOSINS IN VERTEBRATE SKELETAL MUSCLE , 1980 .

[42]  S. Schiaffino,et al.  "Fast" isomyosins and fiber types in mammalian skeletal muscle. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[43]  M. Ringqvist Fiber types in human masticatory muscles. Relation to function. , 1974, Scandinavian journal of dental research.

[44]  C. Catani,et al.  A sensitive SDS-PAGE method separating myosin heavy chain isoforms of rat skeletal muscles reveals the heterogeneous nature of the embryonic myosin. , 1983, Biochemical and biophysical research communications.

[45]  L. Thornell,et al.  The reliability of histochemical fibre typing of human necropsy muscles , 2004, Histochemistry.

[46]  G. Butler-Browne,et al.  Expression of alpha-cardiac myosin heavy chain in mammalian skeletal muscle , 1992, Experientia.

[47]  P. O’Farrell High resolution two-dimensional electrophoresis of proteins. , 1975, The Journal of biological chemistry.

[48]  G. Butler-Browne,et al.  Co-expression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular musculature , 1985, The Journal of cell biology.

[49]  J. Hoh,et al.  Myosin isoenzymes in fast‐twitch and slow‐twitch muscles of normal and dystrophic mice. , 1983, The Journal of physiology.

[50]  S. Schiaffino,et al.  Fetal myosin immunoreactivity in human dystrophic muscle , 1986, Muscle & nerve.

[51]  R. Billeter,et al.  Heterogeneous distribution of myosin in human masticatory muscle fibres as shown by immunocytochemistry. , 1984, Archives of oral biology.