Abstract
Striated craniofacial and limb muscles differ in their embryological origin, regulatory program during myogenesis, and innervation. In an attempt to explore the effects of these differences on the striated muscle phenotype in humans, the expression of myosin and myosin-associated thick filament proteins were studied at the single fiber level both in the human jaw-closing masseter muscle and in two limb muscles (biceps brachii and quadriceps femoris muscles). In the masseter, unique combinations of myosin heavy chain (MyHC) and myosin binding protein C (MyBP-C) isoforms were observed at the single fiber level. Compared to the limb muscles, the MyHC isoform expression was more complex in the masseter while the opposite was observed for MyBP-C. In limb muscles, a coordinated expression of three MyHC and three MyBP-C isoforms were observed, i.e., single fibers contained one or two MyHC isoforms, and up to three MyBP-C isoforms. Also, the relative content of the different MyBP-C isoforms correlated with the MyHC isoform expression. In the masseter, on the other hand, up to five different MyHC isoforms could be observed in the same fiber, but only one MyBP-C isoform was identified irrespective MyHC isoform expression. This MyBP-C isoform had a migration rate similar to the slow MyBP-C isoform in limb muscle fibers. In conclusion, a unique myofibrillar protein isoform expression was observed in the human masseter muscle fibers, suggesting significant differences in structural and functional properties between muscle fibers from human masseter and limb muscles.
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Ausoni S, Gorza L, Schiaffno S, Gundersen K and Lomo T (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J Neurosci 10: 153-160.
Bergström J (1962) Muscle electrolytes in man. Scand J Clin Lab Invest (Suppl. 68).
Bredman JJ, Wessels A, Weijs WA, Korfage JA, Soffers CA and Moorman AF (1991) Demonstration of 'cardiac-specific' myosin heavy chain in masticatory muscles of human and rabbit. Histochem J 23: 160-170.
Butler-Browne GS, Eriksson PO, Laurent C and Thornell LE (1988) Adult human masseter muscle fibers express myosin isozymes characteristic of development. Muscle Nerve 11: 610-620.
Dennis JE, Shimizu T, Reinach FC and Fischman DA (1984) Localization of C-protein isoforms in chicken skeletal muscle: ultrastructural detection using monoclonal antibodies. J Cell Biol 98: 1514-1522.
Ecob-Prince M, Hill M and Brown W (1989) Immunocytochemical demonstration of myosin heavy chain expression in human muscle. J Neurol Sci 91: 71-78.
Einheber S and Fischman DA (1990) Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein: an intracellular member of the immunoglobulin superfamily. Proc Natl Acad Sci USA 87: 2157-2161.
English AW, Eason J, Pol M, Schwartz G and Shirley A (1998) Different phenotypes among slow/beta myosin heavy chain-containing fibres of rabbit masseter muscle: a novel type of diversity in adult muscle. J Muscle Res Cell Motil 19: 525-535.
Eriksson PO, Eriksson A, Ringqvist M and Thornell LE (1980) The reliability of histochemical fibre typing of human necropsy muscles. Histochemistry 65: 193-205.
Furst DO, Nave R, Osborn M and Weber K (1989) Repetitive titin epitopes with a 42 nm spacing coincide in relative position with known A band striations also identified by major myosin-associated proteins. An immunoelectron-microscopical study on myofibrils. J Cell Sci 94: 119-125.
Giulian GG, Moss RL and Greaser M (1983) Improved methodology for analysis and quantitation of proteins on one-dimensional silver-stained slab gels. Anal Biochem 129: 277-287.
Hartzell HC and Glass DB (1984) Phosphorylation of purified cardiac muscle C-protein by purified cAMP-dependent and endogenous Ca2+-calmodulin-dependent protein kinases. J Biol Chem 259: 15,587-15,596.
Hill A (1950) The dimensions of animals and their muscular dynamics. Sci Prog 38: 209-230.
Hofmann PA, Greaser ML and Moss RL (1991a) C-protein limits shortening velocity of rabbit skeletal muscle fibres at low levels of Ca2+ activation. J Physiol (Lond) 439: 701-715.
Hofmann PA, Hartzell HC and Moss RL (1991b) Alterations in Ca2+ sensitive tension due to partialextraction of C-protein from rat skinned cardiac myocytes and rabbit skeletal muscle fibers. J Gen Physiol 97: 1141-1163.
Hoh JF (1992) Muscle fiber types and function. Curr Opin Rheumatol 4: 801-808.
Hook P, Sriramoju V and Larsson L (2001) Effects of aging on actin sliding speed on myosin from single mouse, rat and human skeletal muscle cells. Am J Physiol Cell Physiol 280: C782-C788.
Hughes SM, Cho M, Karsch-Mizrachi I, Travis M, Silberstein L, Leinwand LA and Blau HM (1993) Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev Biol 158: 183-199.
Larsson L and Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol (Lond) 472: 595-614.
Larsson L, Greaser M and Moss RL (1993) Extraction of C-protein eliminates the delayed overshoot of isometric tension due to stretch of mammalian muscles. Biophys J 64: A253.
Larsson L, Li X, Teresi A and Salviati G (1994) Effects of thyroid hormone on fast-and slow-twitch skeletal muscles in young and old rats. J Physiol (Lond) 481: 149-161.
Leger JO, Bouvagnet P, Pau B, Roncucci R and Leger JJ (1985) Levels of ventricular myosin fragments in human sera after myocardialinfarctio n, determined with monoclonal antibodies to myosin heavy chains. Eur J Clin Invest 15: 422-429.
McCormick KM, Baldwin KM and Schachat F (1994) Coordinate changes in C protein and myosin expression during skeletal muscle hypertrophy. Am J Physiol 267: C443-C449.
Monemi M, Eriksson PO, Dubail I, Butler-Browne GS and Thornell LE (1996) Fetalmyosin heavy chain increases in human masseter muscle during aging. FEBS Lett 386: 87-90.
Monemi M, Eriksson PO, Kadi F, Butler-Browne GS and Thornell LE (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.
Morris TJ, Brandon CA, Horton MJ, Carlson DS and Sciote JJ (2001) Maximum shortening velocity and myosin heavy-chain isoform expression in human masseter muscle fibers. J Dent Res 80: 1845-1848.
Moss RL, Diee GM and Greaser ML (1995) Contractile properties of skeletal muscle fibers in relation to myofibrillar protein isoforms. Rev Physiol Biochem Pharmacol 126: 1-63.
Pette D and Staron RS (2001) Transitions of muscle fiber phenotypic profiles. Histochem Cell Biol 115: 359-372.
Pol-Rodriguez MM, Schwartz GA and English AW (2001) Posttranslational phosphorylation of the slow/beta myosin heavy chain isoform in adult rabbit masseter muscle. J Muscle Res Cell Motil 22: 513-519.
Rayment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, Holmes KC and Milligan RA (1993a) Structure of the actin-myosin complex and its implications for muscle contraction. Science 261: 58-65.
Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G and Holden HM (1993b) Three-dimensionalstructur e of myosin subfragment-1: a molecular motor. Science 261: 50-58.
Rome LC, Sosnicki AA and Goble DO (1990) Maximum velocity of shortening of three fibre types from horse soleus muscle: implications for scaling with body size. J Physiol (Lond) 431: 173-185.
Schiaffno S and Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76: 371-423.
Schiaffno S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K and Lomo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10: 197-205.
Stål P, Eriksson PO, Schiaffno S, Butler-Browne GS and Thornell LE (1994) Differences in myosin composition between human orofacial, masticatory and limb muscles: enzyme-, immunohisto-and biochemicalstudies. J Muscle Res Cell Motil 15: 517-534.
Stål P, Yu F, Thornell LE and Larsson L (1998) Single human masseter fibres contain unique combinations of myofibrillar proteins. J Dent Res 77: 877.
Staron RS (1997) Human skeletal muscle fiber types: delineation, development, and distribution. Can J Appl Physiol 22: 307-327.
Tajbakhsh S, Rocancourt D, Cossu G and Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89: 127-138.
Takano-Ohmuro H, Goldfine SM, Kojima T, Obinata T and Fischman DA (1989) Size and charge heterogeneity of C-protein isoforms in avian skeletal muscle. Expression of six different isoforms in chicken muscle. J Muscle Res Cell Motil 10: 369-378.
Towbin H, Staehelin T and Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
Uddhammar A, Rantapaa Dahlqvist S, Hedberg B and Thornell LE (1998) Deltoid muscle in patients with polymyalgia rheumatica. J Rheumatol 25: 1344-1351.
Winegrad S (1999) Cardiac myosin binding protein C. Circ Res 84: 1117-1126.
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Yu, F., Stål, P., Thornell, LE. et al. Human single masseter muscle fibers contain unique combinations of myosin and myosin binding protein C isoforms. J Muscle Res Cell Motil 23, 317–326 (2002). https://doi.org/10.1023/A:1022061706126
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DOI: https://doi.org/10.1023/A:1022061706126