Abstract
Airways smooth muscle physiology and pharmacology have been extensively studied. In contrast, and probably due to the problem of obtaining enough homogenous tissue, no proper biochemical studies have been performed on even the major contractile proteins of the airways smooth muscle. For biochemical investigations avian gizzard muscle has been the most common source of smooth muscle tissue since myosin and other contractile proteins can readily be isolated and purified. Porcine stomach owing to its large muscle mass, has also been usefully employed. A higher level of endogenous, or contaminating, proteolytic activity creates problems however in obtaining some of the proteins in an undergraded state. Nevertheless, the properties of the contractile proteins in general and myosin in particular appear to be similar or identical to those of gizzard. On this basis we can assume that smooth muscle myosins share at least common major properties. In this review most of the information cited derives from studies on avian gizzard or pig stomach myosins but this should be readily applicable to myosin from airways smooth muscle.
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References
Mooseker M. A multitude of myosins. Current Biology 1993; 3: 245–8.
Elliott A, Offer G, Burridge K. Electron microscopy of myosin molecules from muscle and non-muscle sources. Proc R Soc Lond B 1976; 193: 45–53.
Trybus KM, Huiatt TW, Lowey S. A bent monomeric conformation of myosin from smooth muscle. Proc Natl Acad Sci 1982; 79: 6151–5.
Trybus KM, Lowey S. Conformational states of smooth muscle myosin. Effects of light chain phosphorylation and ionic strength. J Biol Chem 1984; 259: 8564–71.
Onishi H, Wakabayashi T. Electron microscopic studies of myosin molecules from chicken gizzard muscle I: the formation of the intramolecular loop in the myosin tail. J Biochem 1982; 92: 871–879.
Okamoto Y, Sekine T. Involvement of 17K dalton light chain of smooth muscle myosin in substrate-induced conformational change. J Biochem 1980; 87: 167–78.
Hasegawa Y, Morita F. Role of 17-kDa essential light chain isoforms of aorta smooth muscle myosin. J Biochem 1992; 111: 804–9.
Morita J-I, Takashi R, Ikebe, M. Exchange of the fluorescence-labeled 20 000-dalton light chain of smooth muscle myosin. Biochemistry 1991; 30: 9539–45.
Trybus KM, Chatman TA. Chimeric regulatory light chains as probes of smooth muscle myosin function. J Biol Chem 1993; 268: 4412–9.
Persechini A, Hartshorne DJ. Ordered phosphorylation of the two 20 000 molecular weight light chains of smooth muscle myosin. Biochemistry 1983; 22: 470–6.
Cross RA, Bardsley RG, Ledward DA, Small JV, Sobieszek A. Reversible helix-coil transition of pig stomach myosin rod. FEBS Lett 1983; 162: 189–92.
Cross RA, Bardsley RG, Ledward DA, Small JV, Sobieszek A. Conformational stability of the myosin rod. FEBS Lett. 1984; 145: 305–10.
Onishi H, Suzuki H, Nakamura K, Takahashi K, Watanabe S. Adenosine triphosphatase activity and “thick filament” formation of chicken gizzard myosin in low salt media. J Biochem 1978; 83: 835–47.
Kendrick-Jones J, Smith RC, Craig R, Citi S. Polymerization of vertebrate non-muscle and smooth muscle myosin. J Mol Biol 1987; 198: 241–52.
Suzuki H, Onishi H, Takahashi K, Watanabe S. Structure and function of chicken gizzard myosin. J Biochem 1987; 84: 1529–42.
Onishi H, Wakabayashi T, Kamata T, Watanabe S. Electron microscopic studies of myosin molecules from chicken gizzard muscle II: The effect of thiophosphorylation of the 20k-dalton light chain on the ATP-induced change in the conformation of myosin monomers. J Biochem 1983; 94: 1147–54.
Trybus KM, Lowey S. The regulatory light chain is required for folding of smooth muscle myosin. J Biol Chem 1988; 263: 16485–92.
Cross RA, Cross KE, Sobieszek A. ATP-linked monomer-polymer equilibrium of smooth muscle myosin: the free folded monomer traps ADP.Pi. EMBO J. 1986; 5: 2637–41.
Cross RA. Jackson AP, Citi S, Kendrick-Jones J, Bagshaw CR. Active site trapping of nucleotide by smooth and non-muscle myosins. J Mol Biol 1988; 203: 173–81.
Megerman J, Lowey S. Polymerization of myosin from smooth muscle of the calf aorta. Biochemistry 1981; 20: 2099–110.
Sobieszek A, Bremel RD. Preparation and properties of vertebrate smooth-muscle myofibrils and actomyosin. Eur J Biochem 1975; 55: 49–60.
Ikebe M, Hartshorne DJ. Effects of Cap + on the conformation and enzymatic activity of smooth muscle myosin. J Biol Chem 1985; 260: 13146–53.
Ebashi S. A simple method of preparing actin-free myosin from smooth muscle. J Biochem 1976; 79: 229–31.
Sobieszek A. Vertebrate smooth muscle myosin: Enzymatic and structural properties. In: The Biochemistry of Smooth Muscle, edited by Stephens, N.L. Baltimore, MD: University Park Press, 1977: 413–43.
Eddinger T, Murphy RA. Two smooth muscle heavy chains differ in their light meromyosin fragment. Biochemistry 1988; 27: 3807–11.
Kawamoto S, Adelstein RS. The heavy chain of smooth muscle myosin is phosphorylated in aorta cells. J Biol Chem 1988; 263: 1099–102.
Yanagisawa M, Hamada Y, Katsuragawa Y, Imamura M, Mikawa T, Masaki T. Complete primary structure of vertebrate smooth muscle myosin heavy chain deduced from its complementary DNA sequence: Implications on topography and function of myosin. J Mol Biol 1987; 198: 143–57.
Nagai R, Kuroo M, Babij P, Periasamy M. Identification of two types of smooth muscle myosin heavy chain isoforms by cDNA cloning and immunoblot analysis. J Biol Chem 1989; 264: 9734–37.
Kelley CA, Adelstein RS. The 204-kDa smooth muscle myosin heavy chain is phosphorylated in intact cells by casein kinase II on a serine near the carboxyl terminus. J Biol Chem 1990; 265: 17876–82.
McLachlan AD, Karn J. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 1982; 299: 226–31.
Ikebe M, Hewett TE, Martin AF, Chen M, Hartshorne DJ. Cleavage of smooth muscle myosin heavy chain near its C-terminus by ?-chymotrypsin. Effect on the properties of myosin. J Biol Chem 1991; 266: 7030–6.
Sobieszek A, Jertschin P. Urea-glycerol-acrylamide gel electrophoresis of acidic low molecular weight proteins: rapid determination of myosin light chain phosphorylation in myosin, actomyosin and whole muscle samples. Electrophoresis 1986; 7: 417–25.
Helper DJ, Lash JA, Hathaway DR. Distribution of isoelectric variants of the 17, 000Dalton myosin light chain in mammalian smooth muscle. J Biol Chem 1988; 263: 15748–53.
Hasegawa Y, Ueda Y, Watanabe M, Morita F. Studies on amino acid sequences of two isoforms of 17-kDa essential light chain of smooth muscle myosin from porcine aorta media. J Biochem 1992; 111: 798–803.
Maita T, Chen J-I, Matsuda G. Amino-acid sequence of the 20, 000-molecular-weight light chain of chicken gizzard-muscle myosin. Eur J Biochem 1981; 117: 417–24.
Pearson RB, Jakes R, John M, Kendrick-Jones J, Kemp BE. Phosphorylation site sequence of smooth muscle myosin light chain (Mr = 20,000). FEBS Lett 1984; 168: 108–12.
Kumar CC, Mohan SR, Zavodny PJ, Narula SK, Leibowitz PJ. Characterization and differential expression of human vascular smooth muscle myosin light chain 2 isoform in nonmuscle cells. Biochemistry 1989; 28: 4027–35.
Watanabe M, Hasegawa Y, Katoh T, Morita F. Amino acid sequence of the 20-kDa regulatory light chain of porcine aorta media smooth muscle myosin. J Biochem 1992; 112: 431–2.
Weeds AG, Lowey S. Substructure of the myosin molecule. II. The light chains of myosin. J Mol Biol 1971; 61: 701–25.
Sarkar, S. Stoichiometry and sequential removal of light chains of myosin. CSHS Quant Biol 1972; 37: 14–7.
Okamota Y, Sekine T, Grammer J, Yount RG. The essential light chains constitute part of the active site of smooth muscle myosin. Nature 1986; 324: 78–80.
Flicker PF, Wallimann T, Vibert P. Electron microscopy of scallop myosin. Location of regulatory light chains. J Mol Biol 1983; 169: 723–41.
Szentkiralyi EM. Tryptic digestion of scallop Sl: evidence for a complex between the two light chains and a heavy-chain peptide. J Muscle Res Cell Motil 1984; 5: 147–64.
Sellers JR, Harvey EV. Localization of a light-chain binding site on smooth muscle myosin revealed by light-chain overlay of sodium dodecyl sulfate-polyacrylamide electrophoresis gels. J Biol Chem 1984; 259: 14203–7.
Onishi H, Maita T, Matsuda G, Fujiwara K. Interaction between the heavy and the regulatory light chains in smooth muscle myosin subfragment 1. Biochemistry 1992; 31: 1201–10.
Lowey S. Myosin: molecule and filament. In: Biological Macromolecules, vol.V, part A “Subunits in Biological Systems”, edited by Timasheff, SN, Fasman, GD. New York: Marcel Dekker, 1971; 201–59.
Redowicz MJ, Sobieszek A, Strzelecka-Golaszewska H. Conformational transitions within the head and the head-rod junction in smooth muscle myosin studied with a limited proteolysis method. Eur J Biochem 1990; 192: 601–8.
Sobieszek A. Calmodulin antagonist action in smooth-muscle myosin phosphorylation. Different mechanisms for trifluoperazine and calmidazolium inhibition. Biochem J 1989; 262: 215–23.
Ikebe M, Hartshorne DJ. Proteolysis of smooth muscle myosin by Staphylococcus aureus protease: preparation of heavy meromyosin and subfragment 1 with intact 20,000-dalton light chains. Biochemistry 1985; 24: 2380–7.
Adelstein RS, Eisenberg E. Regulation and kinetics of the actin-myosin-ATP interaction. Ann Rev Biochem 1980; 49: 921–56.
Eisenberg E, Hill TL. Muscle contraction and free energy transduction in biological systems. Science 1985; 227: 999–1006.
Simmons RM. Testing time for muscle. Current Biology 1992; 2: 373–5.
Sobieszek A. Smooth muscle myosin as a calmodulin binding protein. Affinity increase on filament assembly. J Muscle Res Cell Motil 1990; 11: 114–24.
Sobieszek A. Regulation of smooth-muscle myosin-light-chain-kinase. Steady state kinetic studies of the reaction mechanism. Eur J Biochem 1991; 199: 735–43.
Jakes R, Northrop F, Kendrick-Jones J. Calcium binding regions of myosin ‘regulatory’ light chains. FEBS Lett 1976; 70: 229–34.
Cole HA, Griffiths HS, Patchell VB, Perry SV. Two-site phosphorylation of the phosphorylatable light chain (20-kDa light chain) of chicken gizzard myosin. FEBS Lett 1985; 180: 165–9.
Ikebe M, Hartshorne DJ. Phosphorylation of smooth muscle myosin at two distinct sites by myosin light chain kinase. J Biol Chem 1985; 260: 10027–31.
Ikebe M, Hartshorne DJ, Elzinga M. Identification, phosphorylation, and dephosphorylation of a second site for myosin light chain kinase on the 20, 000-dalton light chain of smooth muscle myosin. J Biol Chem 1986; 261: 36–9.
Tanaka T, Sobue K, Owada MK, Hakura A. Linear relationship between diphosphorylation of 20 kDa light chain of gizzard myosin and the actin-activated myosin ATPase activity. Biochem Biophys Res Comm 1985; 131: 987–93.
Tanaka T, Yamazaki K, Sobue K. Correlation between multiple phosphorylation of gizzard myosin light chain and actin-activated myosin ATPase activity. J Biochem 1985; 97: 1823–6.
Noiman ES. Phosphorylation of smooth muscle myosin light chains by cAMP-dependent protein kinase. J Biol Chem 1980; 255: 11067–70.
Tashiro Y, Matsumura S, Murakami N, Kumon A. The phosphorylation site for casein kinase II on 20, 000-Da light chain of gizzard myosin. Arch Biochem Biophys 1984; 233: 540–6.
Edelman AM, Lin W-H, Osterhout DJ, Bennett MK, Kennedy MB, Krebs EG. Phosphorylation of smooth muscle myosin by type II Ca2+/calmodulin-dependent protein kinase. Mol Cell Biochem 1990; 97: 87–98.
Endo T, Naka M, Hidaka H. Ca2+-phospholipid dependent phosphorylation of smooth muscle myosin. Biochem Biophys Res Commun 1982; 105: 942–8.
Nishikawa M, Hidaka H, Adelstein RS. Phosphorylation of smooth muscle heavy meromyosin by calcium-activated, phospholipid-dependent protein kinase. The effect of actin-activated MgATPase activity. J Biol Chem 1983; 258: 14069–72.
Suzuki H, Kamata T, Onishi H, Watanabe S. Adenosine triphosphate-induced reversible change in the conformation of chicken gizzard myosin and heavy meromyosin. J Biochem 1982; 91: 1699–705.
Ikebe M, Hinkins S, Hartshorne DJ. Correlation of enzymatic properties and conformation of smooth muscle myosin. Biochemistry 1983; 22: 4580–7.
Ikebe M, Kortez J, Hartshorne DJ. Effects of phosphorylation of light chain residues threonine 18 and serine 19 on the properties and conformation of smooth muscle myosin. J Biol Chem 1988; 263: 6432–7.
Cross RA. Smooth muscle contraction. What is 105 myosin for? J Muscle Res Cell Motil 1988; 9: 108–10.
Sobieszek A. Cross-bridges on self-assembled smooth muscle myosin filaments. J Mol Biol 1972; 70: 741–4.
Shoenberg CF, Needham DM. A study of the mechanism of contraction in vertebrate smooth muscle. Biol Rev 1976; 51: 53–104.
Small JV, Sobieszek A. The contractile apparatus of smooth muscle. Int Rev Cytol 1980; 64: 241–306.
Somlyo AV, Butler TM, Bond M, Somlyo AP. Myosin filaments have non-phosphorylated light chains in relaxed smooth muscle. Nature 1981; 294: 567–570.
Tsukita S, Usukura J, Ishikawa H. Myosin filaments in smooth muscle cells of the guinea pig taenia coli: a freeze-substitution study. Eur J Cell Biol 1982; 28: 195–201.
Huxley HE, Brown W. The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol 1967; 30: 383–434.
Lowy J, Poulsen FR, Vibert PJ. Myosin filaments in vertebrate smooth muscle. Nature 1970; 225: 1053–4.
Shoenberg CF, Haselgrove JC. Filaments and ribbons in vertebrate smooth muscle. Nature 1974; 249: 152–4.
Huxley HE. Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 1963; 7: 281–308.
Kammer B. Synthetic myosin filaments from vertebrate smooth muscle. J Mol Biol 1969; 39: 257–64.
Hinssen H, D’Haese J, Small JV, Sobieszek A. Mode of filament assembly of myosins from muscle and nonmuscle cells. J Ultrastruct Res 1978; 64: 282–302.
Craig R, Megerman J. Assembly of smooth muscle myosin into side-polar filaments. J Cell Biol 1977; 75: 990–6.
Small JV, Squire JM. Structural basis of contraction in vertebrate smooth muscle. J Mol Biol 1972; 67: 117–49.
Cooke PH, Fay FS, Craig R. Myosin filaments isolated from skinned amphibian smooth muscle cells are side-polar. J Muscle Res Cell Motil 1989; 10: 206–20.
Atkinson SJ, Stewart M. Molecular basis of myosin assembly: Coiled-coil interactions and the role of charge periodicities. J Cell Sci 98 Suppl 1991; 14: 7–10.
Atkinson SJ, Stewart M. Expression in Escherichia coli of fragments of the coiled-coil rod domain of rabbit myosin: influence of different regions of the molecule on aggregation and paracrystal formation. J Cell Sci 1991; 99: 823–36.
Cross RA, Hodge TP, Kendrick-Jones J. Self-assembly pathway of nonsarcomeric myosin II. J Cell Sci 98 Suppl 1991; 14: 17–21.
Chalovich JM. Actin mediated regulation of muscle contraction. Pharmacol Ther 1992; 55: 95–148.
Persechini A, Hartshorne DJ. Phosphorylation of smooth muscle myosin: evidence for cooperativity between the myosin heads. Science 1981; 213: 1383–5.
Ikebe M, Ogihara S, Tonomura Y. Nonlinear dependence of actin-activated Mg2+-ATPase activity on the extent of phosphorylation of gizzard myosin and Hmeromyosin. J Biochem 1982; 91: 1809–12.
Sellers JR, Chock PB, Adelstein RS. The apparently negatively cooperative phosphorylation of smooth muscle myosin at low ionic strength is related to its filamentous state. J Biol Chem 1983; 258: 14181–8.
Sobieszek A. MgATPase activity of vertebrate smooth muscle actomyosin: stimulation by tropomyosin is modified by myosin phosphorylation and its conformational state. In: Regulation and Contraction of Smooth Muscle, edited by Siegman, M.J., Somlyo, A.P. and Stephens, N.L. New York: Alan R. Liss, Inc., 1987; 159–81.
Trybus KM, Lowey S. Mechanism of smooth muscle myosin phosphorylation. J Biol Chem 1985; 260: 15988–95.
Reisler E, Smith C, Seegan G. Myosin minifilaments. J Mol Biol 1980; 143: 129–45.
Ebashi S. Regulation of muscle contraction. Proc R Soc Lond B 1980; 207: 259–86.
Sobieszek A, Small JV. Regulation of the actin-myosin interaction in vertebrate smooth muscle: activation via a myosin light chain kinase and effect of tropomyosin. J Mol Biol 1977; 112: 559–76.
Sobieszek A. Steady-state kinetic studies on the actin-activation of skeletal muscle meromyosin subfragments. Effects of skeletal, smooth and non-muscle tropomyosins. J Mol Biol 1982; 157: 275–86.
Cooke R, Morales MF. Interaction of globular actin with myosin subfragments. J Mol Biol 1971; 60: 249–61.
Applegate D, Pardee JD. Actin-facilitated assembly of smooth muscle myosin induces formation of actomyosin fibrils. J Cell Biol 1992; 117: 1223–30.
Kamm KE, Stull JT. Regulation of smooth muscle contractile elements by second messengers. Ann Rev Physiol 1989; 51: 299–313.
Kamm KE, Hsu L-C, Kubota Y, Stull JT. Phosphorylation of smooth muscle myosin heavy and light chains. Effects of phorbol dibutyrate and agonists. J Biol Chem 1989; 264: 21223–9.
Itoh T, Ikebe M, Kargacin GJ, Hartshorne DJ, Kemp BE, Fay FS. Effects of modulators of myosin light-chain kinase activity in single smooth muscle cells. Nature 1989; 338: 164–7.
Sellers JR. Mechanism of the phosphorylation-dependent regulation of smooth muscle heavy meromyosin. J Biol Chem 1985; 260: 15815–9.
Sellers JR, Eisenberg E, Adelstein RS. The binding of smooth muscle heavy meromyosin to actin in the presence of ATP. J Biol Chem 1982; 257: 13880–3.
Greene LE, Sellers JR. Effect of phosphorylation on the binding of smooth muscle heavy meromyosin. ADP to actin. J Biol Chem 1987; 262: 4177–81.
Trybus KM. Filamentous smooth muscle myosin is regulated by phosphorylation. J Cell Biol 1989; 109: 2887–94.
Marston SB. The regulation of smooth muscle contractile proteins. Prog Biophys Mol Biol 1982; 41: 1–41.
Sobieszek A, Small JV. Myosin-linked calcium regulation in vertebrate smooth muscle. J Mol Biol 1976; 102: 75–92.
Strzelecka-Golaszewska H, Sobieszek A. Activation of smooth muscle myosin by smooth and skeletal muscle actins. FEBS Lett 1981; 134: 197–202.
Ikebe M, Morita J. Identification of the sequence of the regulatory light chain required for the phosphorylation-dependent regulation of actomyosin. J Biol Chem 1991; 266: 21339–42.
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Sobieszek, A. (1994). Smooth Muscle Myosin: Molecule Conformation, Filament Assembly and Associated Regulatory Enzymes. In: Raeburn, D., Giembycz, M.A. (eds) Airways Smooth Muscle: Biochemical Control of Contraction and Relaxation. Respiratory Pharmacology and Pharmacotherapy. Birkhäuser, Basel. https://doi.org/10.1007/978-3-0348-7681-0_1
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