Abstract
In 1972 a “watershed” meeting took place in idyllic Cold Spring Harbor, New York. In some ways the meeting represented the end of the “classical” period of muscle investigation during which time the basic principles of muscle activation and contraction were established. The meeting also represented the opening of the contemporary era of muscle study before the explosion of molecular biology and structural biology would “super charge” the field. It also represented the beginning of many muscle workshop style meetings throughout the twentieth century and beyond. The meeting was held at the Cold Spring Harbor Laboratory and organized by Noble Laureate James D. Watson, the laboratory director, with the advice of Carolyn Cohen, John Gergely, Andrew Huxley, Hugh Huxley and Andrew Szent-Gyorgyi. In the forward to the published volume, Watson explained the purpose of the Cold Spring Harbors Symposia on Quantitative Biology and why muscle was “ripe” for selection as the 37th symposium.
Our symposium each year gives us the opportunity to seek an exploding phase of biology and to bring together most of the key practitioners. (Watson 1973. With permission Cold Spring Harbor Laboratory Press) J. D. Watson, Director, Cold Spring Harbor Laboratory 1973
J. D. Watson, Director, Cold Spring Harbor Laboratory 1973
By the early 1970s, the time of the Cold Spring Harbor Symposium on muscle contraction, it was generally accepted that the sliding filament moving crossbridge model was correct. (Huxley 1996. With permission Annual Reviews)
H. E. Huxley 1996
On the one hand was the view that the attachment-detachment cycle of A. F. Huxley (1957), plus the structural picture of H. E. Huxley (1969), plus the biochemical cycle of Lymn and Taylor (1971), plus the force-generating step of A. F. Huxley and Simmons (19171b) equaled the muscle problem solved. We found this astonishing, as we knew we were just scratching the surface of the problem. (Simmons 1992. With permission Cambridge University Press)
R. M. Simmons 1992
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Notes
- 1.
Leonard Ornstein (1964) described the theoretical aspects of the gel electrophoresis technique and Baruch Joel (B.J.) Davis (1964) described the practical application for separating serum proteins. Shapiro et al. (1967) modified the technique by adding the anionic detergent sodium dodecyl sulfate (SDS) as a denaturing substance. Weber and Osborn (1969) at Harvard University showed that SDS gel electrophoresis could separate proteins according to molecular weight in the range of 11–220 kDa.
- 2.
Other prominent bands in the gel of the myosin preparation that were found to exist in the myofibril included bands labeled B, F and H (Starr and Offer 1971). The B band was likely a M-line protein and the F band was attributed to the enzyme phosphofructokinase (Starr and Offer 1982). The H band with a molecular weight of 74 kDa was homologous to C-protein and found to exist in stripe 3 of the A band (see Footnote 3 below).
- 3.
The precise number of C-protein stripes in the A band is dependent on muscle fiber type (Bennett et al. 1986). Three isoforms of C-protein are known to exist in adult muscle: fast skeletal, slow skeletal (originally described as X-protein) and cardiac. Separate genes encode each isoform. A related protein, H-protein, smaller than C-protein in skeletal muscle is localized to the third stripe from the M-line of the A band. It is interesting to note that C-protein does not occur in stripes 1 and 2. See Flashman et al. (2004) for a review.
- 4.
Electron Tomography is a technique for obtaining detailed 3D structures of subcellular macromolecular objects. It is an extension of traditional transmission electron microscopy and uses a transmission electron microscope to collect data. In the process, a beam of electrons is passed through the sample at incremental degrees of rotation around the center of the target sample. This information is collected and used to assemble a three dimensional image of the target. Current resolutions of electron tomography systems are in the 5–20 nm range.
- 5.
Ten years after Kenneth Bailey discovered tropomyosin in vertebrates, Bailey (1957) reported the characterization of what he considered a new form of tropomyosin in invertebrates. This “invertebrate tropomyosin” is now known as paramyosin. The name paramyosin was coined by Hall et al. (1946) earlier based on electron microscopic studies of invertebrate muscle fibrils since they had some properties similar to myosin but were yet also different. Paramyosin was found to be a two chain α helical coiled coil approximately 130 nm in length, 2 nm in diameter with a molecular weight of 220 kDa (Lowey et al. 1963). Paramyosin was first determined to be in the core of invertebrate thick filaments by Szent-Gyorgyi et al. (1971). It has similarities to the myosin rod. A paramyosin core allows invertebrate thick filaments to attain large diameters containing up to a seven stranded cross-bridge helix arrangement in striated scallop muscle (Squire 1986).
- 6.
In solutions of low ionic strength LMM precipitates to form ordered aggregates called paracrystals. The paracrystals can assume different forms. Spindle shaped paracrystals were first studied in the electron microscope by Philpott and Szent-Gyorgyi (1954) who observed an axial repeat of about 40 nm. Other spindle-shaped paracrystals (tactoids) have been observed but with periodicities different from 43 nm. However, almost without exception the repeats correspond to an integral multiple of 14.3 nm. Paracrystal formation is an indicator of the ability of LMM or myosin rods to assemble properly. See Bennett (1981) for examples of paracrystals with periodicities of 43 or 14.3 nm.
- 7.
Marcel Dubuisson (1903–1974) was the director of the laboratory of general biology at the University of Liege from 1949 to 1970 during which time he studied muscle proteins by electrophoresis methods. He wrote a monograph on muscle contraction in 1954. He had a long standing interest in marine biology and founded an aquarium at the university that opened in 1962 as the “Aquarium M. Dubuisson”. His most important influence was as the rector (president) of the University of Liege from 1953 to 1971 during which time he was a strong visionary for modernization of the university. He created the oceanographic research station (STARESO) in Corsica in 1970.
- 8.
Aaron Klug (1926–) won the Nobel Prize in chemistry in 1982 for development of crystallographic electron microscopy and his structural elucidation of biologically important nucleic acid-protein complexes. Klug used methods of X-ray diffraction, electron microscopy and structural modeling to develop crystallographic electron microscopy in which a sequence of two-dimensional images of crystals taken from different angles are combined to produce three-dimensional (3D) images of the target.
- 9.
Marcus Kress died tragically in a hiking accident before this paper was published.
- 10.
In the acknowledgement section of their paper, MacLennan and Wong (1971) state that the name calsequestrin was suggested by their colleague Philip Seeman, a neuropharmacologist at the University of Toronto.
- 11.
The name phospholamban was suggested by Arnold Katz’s wife Phyllis Katz who was educated in the classics. The term is derived from “phosphate” and a Greek work which means “to receive or to seize” (Katz 1998).
- 12.
Various types of calcium channels have been discovered and characterized. The current classification includes: L-type, N-type, P/Q-type and R-types calcium channels. The evolution of this classification is reviewed by Richard W. Tsien and Curtis F. Barrett (2000–2012). Richard Tsien’s laboratory at Stanford University made major contributions in the understanding of calcium channel function.
References
Adelman MR, Taylor EW (1969) Further purification and characterization of slime mold myosin and slime mold actin. Biochemistry 8:4976–4988
Adelstein RS, Conti MA (1973) The characterization of contractile proteins from platelets and fibroblasts. Cold Spring Harb Symp Quant Biol 37:599–605
Al-Amoudi A, Chang J-J, Leforestier A, McDowall A, Salamin LM, Norlen LPO, Richter K, Blanc NS, Studer D, Dubochet J (2004) Cryo-electron microscopy of vitreous sections. EMBO J 23:3583–3588
Almers W, Fink R, Palade PT (1981) Calcium depletion in frog muscle tubules: the decline of calcium current under maintained depolarization. J Physiol 312:177–207
Amos LA (1985) Structure of muscle filaments studied by electron microscopy. Annu Rev Biophys Biophys Chem 14:291–313
Ashton FT, Weisel J, Pepe FA (1992) The myosin filament XIV backbone structure. Biophys J 61:1513–1528
Atkinson SJ, Stewart M (1991) Expression in Escherichia coli of fragments of the coiled-coil domain of rabbit myosin: influence of different regions of the molecules on aggregation and paracrystal formation. J Cell Sci 99:823–836
Bailey K (1946) Tropomyosin: a new asymmetric protein component of muscle. Nature 157:368–369
Bailey K (1957) Invertebrate tropomyosin. Biochim Biophys Acta 24:612–619
Bennett PM (1981) The structure of spindle-shaped paracrystals of light meromyosin. J Mol Biol 146:201–221
Bennett P, Craig R, Starr R, Offer G (1986) The ultrastructural location of C-protein, X-protein and H-protein in rabbit muscle. J Muscle Res Cell Motil 7:550–567
Benzonana G, Capony J-P, Pechere J-F (1972) The binding of calcium to muscular parvalbumins. Biochim Biophys Acta 278:110–116
Bettex-Galland M, Clemetson KJ (2005) First isolation of actomyosin from a non-muscle cell: first isolated platelet protein. J Thrombosis Haemost 3:834–839
Bettex-Galland M, Luscher EF (1959) Extraction of an actomyosin-like protein from human thrombocytes. Nature 184:276–277
Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107:2587–2600
Bray D (1973) Cytoplasmic actin: a comparative study. Cold Spring Harb Symp Quant Biol 37:567–571
Bray D (2001) Cell movements: from molecules to motility, 2nd edn. Garland, New York
Bremel RD, Weber A (1972) Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol 238:97–101
Bremel RD, Murray JM, Weber A (1973) Manifestations of cooperative behavior in the regulated actin filament during actin-activated ATP hydrolysis in the presence of calcium. Cold Spring Harb Symp Quant Biol 37:267–275
Brenner B, Schoenberg M, Chalovich JM, Greene LE, Eisenberg E (1982) Evidence for cross-bridge attachment in relaxed muscle at low ionic strength. Proc Natl Acad Sci U S A 79:7288–7291
Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89:1341–1378
Brown JH, Kim K-H, Jun G, Greenfield NJ, Dominguez R, Volkmann N, Hitchcock-DeGregori SE, Cohen C (2001) Deciphering the design of the tropomyosin molecule. Proc Natl Acad Sci U S A 98:8496–8501
Caspar DLD, Cohen C, Longley W (1969) Tropomyosin: crystal structure, polymorphism and molecular interactions. J Mol Biol 41:87–107
Chalovich JM (2002) Regulation of striated muscle contraction: a discussion. J Muscle Res Cell Motil 23:353–361
Chalovich JM, Eisenberg E (1982) Inhibition of actomyosin ATPase activity by troponin.tropomyosin without blocking the binding of myosin to actin. J Biol Chem 257:2432–2437
Chalovich JM, Chock PB, Eisenberg E (1981) Mechanism of action of tropomyosin*tropomyosin: inhibition of actomyosin ATPase activity without inhibition of myosin binding to actin. J Biol Chem 256:575–578
Chantler P (1982) Retreats from the steric blocking of muscle contraction. Nature 298:120–121
Cohen C (1975) The protein switch of muscle contraction. Sci Am 233:36–45
Cohen P (2002) The origins of protein phosphorylation. Nat Cell Biol 4:E127–E130
Cohen C, Holmes KC (1963) X-ray diffraction evidence for α-helical coiled-coils in native muscle. J Mol Biol 6:423–432
Cohen C, Longley W (1966) Tropomyosin paracrystals formed by divalent cations. Science 152:794–796
Cohen C, Szent-Gyorgyi AG (1957) Optical rotation and helical polypeptide chain configuration in α-proteins. J Am Chem Soc 79:248
Cohen C, Caspar DLD, Johnson JP, Nauss K, Margossian SS, Parry DAD (1973) Tropomyosin-troponin assembly. Cold Spring Harb Symp Quant Biol 37:287–297
Collins JH, Potter JD, Horn MJ, Wilshire G, Jackman N (1973) The amino acid sequence of rabbit skeletal muscle troponin C: gene replication and homology with calcium-binding proteins from carp and hake muscle. FEBS Lett 36:268–272
Costantin LL, Franzini-Armstrong C, Podolsky RJ (1965) Localization of calcium-accumulating structures in striated muscle fibers. Science 147:158–160
Craig R (1986) The structure of the contractile filaments. In: Engel AG, Banker BQ (eds) Myology. McGraw-Hill, New York, pp 73–123
Craig R, Offer G (1976) The location of C-protein in rabbit skeletal muscle. Philos Trans R Soc Lond B Biol Sci 192:451–461
Crick FHC (1953) The packing of α-helices: simple coiled-coils. Acta Cryst 6:689–697
Cummins P, Perry SV (1973) The subunits and biological activity of polymorphic forms of tropomoysin. Biochem J 133:765–777
Curtis BM, Catterall WA (1984) Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry 23:2113–2118
Davis BJ (1964) Disc electrophoresis. 2, Method and application to human serum proteins. Ann N Y Acad Sci 121:404–427
de Meis L, Vianna AL (1979) Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 48:275–292
DeRosier DJ, Klug A (1968) Reconstruction of three dimensional structures from electron micrographs. Nature 217:130–134
Dolphin AC (2006) A short history of voltage-gated calcium channels. Br J Pharmacol 147:S56–S62
Draper MH, Hodge AJ (1949) Studies on muscle with the electron microscope. 1. The ultrastructure of toad striated muscle. Austral J Exptl Biol Med Sci 27:465–504
Dubuisson M (1954) Muscular contraction. Charles C. Thomas, Springfield
Ebashi S, Kodama A (1966) Interaction of troponin with F-actin in the presence of tropomyosin. J Biochem 59:425–426
Ebashi S, Endo M, Ohtsuki I (1969) Control of muscle contraction. Q Rev Biophys 2:351–384
Egelman EH, DeRosier DJ (1983) A model for F-actin derived from image analysis of isolated filaments. J Mol Biol 166:623–629
Eisenberg E, Kielley WW (1973) Evidence for a refractory state of heavy meromyosin and subfragment-1 unable to bind to actin in the presence of ATP. Cold Spring Harb Symp Quant Biol 37:145–152
Eisenberg BR, Kuda AM (1975) Stereological analysis of mammalian skeletal muscle. II. White vastus muscle of the adult guinea pig. J Ultrastruct Res 51:176–187
Elzinga M, Collins JH (1973) The amino acid sequence of rabbit skeletal muscle actin. Cold Spring Harb Symp Quant Biol 37:1–7
Endo M (1977) Calcium release from the sarcoplasmic reticulum. Physiol Rev 57:71–108
Endo M, Nonomura Y, Masaki T, Ohtsuki I, Ebashi S (1966) Localization of native tropomyosin in relation to striation patterns. J Biochem 60:605–608
Enfield DL, Ericsson LH, Blum HE, Fischer EH, Neurath H (1975) Amino-acid sequence of parvalbumin from rabbit skeletal muscle. Proc Natl Acad Sci U S A 72:1309–1313
Fabiato A, Fabiato F (1975) Contractions induced by calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol 249:469–495
Fairhurst AS, Hasselbach W (1970) Calcium efflux from a heavy sarcotubular fraction: effects of ryanodine, caffeine and magnesium. Eur J Biochem 13:504–509
Ferguson DG, Schwartz HW, Franzini-Armstrong C (1984) Subunit structure of junctional feet in triads of skeletal muscle: a freeze-drying, rotary-shadowing study. J Cell Biol 99:1735–1742
Fischer EH (1992) Nobel lecture: protein phosphorylation and cellular regulation. nobelprize.org
Flashman E, Redwood C, Moolman-Smook J, Watkins H (2004) Cardiac myosin binding protein C: its role in physiology and disease. Circ Res 94:1279–1289
Fleckenstein A (1983) History of calcium antagonism. Circ Res 52(Suppl 1):3–16
Fleischer S (2008) Personal recollections on the discovery of the ryanodine receptors of muscle. Biochem Biophys Res Commun 369:195–207
Fleischer S, Ogunbunmi EM, Dixon MC, Fleer EAM (1985) Localization of Ca2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci U S A 82:7256–7259
Flockerzi V, Oeken H-J, Hofmann F, Pelzer D, Cavalie A, Trautwein W (1986) Purified dihydropyridine-binding site from skeletal muscle t-tubules is a functional calcium channel. Nature 323:66–68
Fosset M, Jaimovich E, Delpont E, Lazdunski M (1983) [3H]Nitrendipine receptors in skeletal muscle. Properties and preferential localization in transverse tubules. J Biol Chem 258:6086–6092
Frank G, Weeds AG (1974) The amino-acid sequence of the alkali light chains of rabbit skeletal-muscle myosin. Eur J Biochem 44:317–334
Franzini-Armstrong C (1970) Studies of the triad. I. Structures of the junction in frog twitch fibers. J Cell Biol 47:488–499
Frearson N, Focant BWW, Perry SV (1976) Phosphorylation of a light chain component of myosin from smooth muscle. FEBS Lett 63:27–32
Froehlich JP, Taylor EW (1975) Transient state kinetic studies of sarcoplasmic reticulum adenosine triphosphatase. J Biol Chem 250:2013–2021
Gerday C, Gillis JM (1976) The possible role of parvalbumins in the control of contractions. J Physiol 258:96–97P
Gilbert C, Kretzschmar KM, Wilkie DR (1973) Heat, work, and phosphocreatine splitting during muscular contraction. Cold Spring Harb Symp Quant Biol 37:613–618
Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924
Greaser ML, Gergely J (1971) Reconstitution of troponin activity from three protein components. J Biol Chem 246:4226–4233
Greaser ML, Gergely J (1973) Purification and properties of the components from troponin. J Biol Chem 248:2125–2133
Greaser ML, Yamaguchi M, Brekke C, Potter J, Gergely J (1973) Troponin subunits and their interactions. Cold Spring Harb Symp Quant Biol 37:235–244
Hall CE, Jakus MA, Schmitt FO (1946) An investigation of cross striations and myosin filaments in muscle. Biol Bull 90:32–50
Hamoir G, Konosu S (1965) Carp myogens of white and red muscles. General composition and isolation of low-molecular-weight components of abnormal amino acid composition. Biochem J 96:85–97
Hanson J, Lowy J (1963) The structure of F-actin and actin filaments isolated from muscle. J Mol Biol 6:46–60
Hanson J, Lowy J (1964) The structure of actin filaments and the origin of the axial periodicity in the I-substance of vertebrate striated muscle. Philos Trans R Soc Lond B Biol Sci 160:449–460
Hanson J, Lednev V, O’Brien EJ, Bennett PM (1973) Structure of the actin-containing filaments in vertebrate skeletal muscle. Cold Spring Harb Symp Quant Biol 37:311–318
Harrington WF, Burk M, Barton JS (1973) Association of myosin to form contractile systems. Cold Spring Harb Symp Quant Biol 37:77–85
Hartshorne DJ, Mueller H (1968) Fractionation of troponin into two distinct proteins. Biochem Biophys Res Commun 31:647–653
Haselgrove JC (1973) X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle. Cold Spring Harb Symp Quant Biol 37:341–351
Hasselbach W (1978) The reversibility of the sarcoplasmic calcium pump. Biochim Biophys Acta 515:23–53
Hatano S, Ohnuma J (1970) Purification and characterization of myosin A from the myxomycete plasmodium. Biochim Biophys Acta 205:110–120
Hatano S, Oosawa F (1966) Isolation and characterization of plasmodium actin. Biochim Biophys Acta 127:488–498
Heizmann CW, Berchtold MW, Rowlerson AM (1982) Correlation of parvalbumin concentration with relaxation speed in mammalian muscle. Proc Natl Acad Sci U S A 79:7243–7247
Henrotte JG (1955) A crystalline component of carp myogen precipitating at high ionic strength. Nature 176:1221
Hodges RS, Sodek J, Smillie LB, Jurasek L (1973) Tropomyosin: amino acid sequence and coiled-coil structure. Cold Spring Harb Symp Quant Biol 37:299–310
Hoffmann-Berling H (1954) Adenosintriphosphat als betriebsstoff von zellbewegungen. Biochim Biophys Acta 14:182–194
Hoffmann-Berling H (1960) Other mechanisms of producing movement. In: Florkin M, Mason HS (eds) Comparative biochemistry, vol 2. Academic, New York, pp 341–370
Holmes KC (1996) Muscle proteins- their actions and interactions. Curr Opin Struct Biol 6:781–789
Holmes KC (2010) 50 years of fiber diffraction. J Struct Biol 170:184–191
Holmes KC, Popp D, Gebbard W, Kabsch W (1990) Atomic model of the actin filament. Nature 347:44–49
Huxley AF, Simmons RM (1973) Mechanical transients and the origin of muscular force. Cold Spring Harb Symp Quant Biol 37:669–680
Huxley HE (1957) The double array of filaments in cross-striated muscle. J Biophys Biochem Cytol 3:631–648
Huxley HE (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 7:281–308
Huxley HE (1967) Recent X-ray diffraction and electron microscope studies of striated muscle. J Gen Physiol 50(suppl 6):71–85
Huxley HE (1969) The mechanism of muscular contraction. Science 164:1356–1366
Huxley HE (1971) Structural changes during muscle contraction. Biochem J 125:85P
Huxley HE (1973a) Structural changes in the actin- and myosin-containing filaments during contraction. Cold Spring Harb Symp Quant Biol 37:361–376
Huxley HE (1973b) Muscle 1972: progress and problems. Cold Spring Harb Symp Quant Biol 37:689–693
Huxley HE (1996) A personal view of muscle and motility mechanisms. Annu Rev Physiol 58:1–29
Huxley HE, Brown W (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol 30:383–434
Huxley HE, Holmes KC (1997) Development of synchrotron radiation as a high-intensity Source for X-ray diffraction. J Synchrotron Radiat 4:366–379
Hymel L, Inui M, Fleischer S, Schindler H (1988) Purified ryanodine receptor of skeletal muscle sarcoplasmic reticulum forms Ca2+-activated oligomeric Ca2+ channels in planar bilayers. Proc Natl Acad Sci U S A 85:441–445
Ikemoto N (1975) Transport and inhibitory Ca2+ binding sites on the ATPase enzyme isolated from the sarcoplasmic reticulum. J Biol Chem 250:7219–7224
Ikemoto N (1976) Behavior of the Ca2+ transport sites linked with the phosphorylation reaction of ATPase purified from the sarcoplasmic reticulum. J Biol Chem 251:7275–7277
Imagawa T, Smith JS, Coronado R, Campbell KP (1987) Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J Biol Chem 262:16636–16643
Inui M, Saito A, Fleischer S (1987) Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem 262:1740–1747
Ishikawa H, Bischoff R, Holtzer H (1969) Formation of arrowhead complexes with heavy meromyosin in a variety of cell-types. J Cell Biol 43:312–328
Jeacocke SA, England PJ (1980) Phosphorylation of a myofibrillar protein of Mr 150,000 in perfused rat heart, and the tentative identification of this as C-protein. FEBS Lett 122:129–132
Jenden DJ, Fairhurst AS (1959) The pharmacology of ryanodine. Pharmacol Rev 21:1–25
Johnson JD, Charlton SC, Potter JD (1979) A fluorescence stopped flow analysis of Ca2+ exchange with Troponin C. J Biol Chem 254:3497–3502
Jorgensen AO, Kalnins V, MacLennan DH (1979) Localization of sarcoplasmic reticulum proteins in rate skeletal muscle by immunofluorescence. J Cell Biol 80:372–384
Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of actin: DNAase 1 complex. Nature 347:3–44
Kachur TM, Pilgrim DB (2008) Myosin assembly, maintenance and degradation in muscle: role of the chaperone UNC-45 in myosin thick filament dynamics. Int J Mol Sci 9:186–1875
Kamm KE, Stull JT (1985) The function of myosin and myosin light chain kinase phosphorylation in smooth muscle. Annu Rev Pharmacol Toxicol 25:593–620
Katz AM (1998) Discovery of phospholamban. A personal history. Ann N Y Acad Sci 853:9–19
Kendrick-Jones J, Lehman W, Szent-Gyorgyi AG (1970) Regulation in molluscan muscles. J Mol Biol 54:313–326
Kendrick-Jones J, Szentkiralyi EM, Szent-Gyorgyi AG (1973) Myosin-linked regulatory systems: the role of the light chains. Cold Spring Harb Symp Quant Biol 37:47–53
Kensler RW, Levine RJC (1982) An electron microscopic and optical diffraction analysis of the structure of Limulus telson muscle thick filaments. J Cell Biol 92:443–451
Kensler RW, Stewart M (1983) Frog skeletal muscle thick filaments are three-stranded. J Cell Biol 96:1797–1802
Kirchberger MA, Tada M, Repke DI, Katz AM (1972) Cyclic adenosine 3′,5′-monophosphate-dependent protein kinase stimulation of calcium uptake by canine cardiac microsomes. J Mol Cell Cardiol 4:673–680
Konosu S, Hamoir G, Pechere J-F (1965) Carp myogens of white and red muscle. Properties and amino acid composition of the main low molecular-weight components of white muscle. Biochem J 96:98–112
Koretz JF, Hunt T, Taylor EW (1973) Studies on the mechanism of myosin and actomyosin ATPase. Cold Spring Harb Symp Quant Biol 37:179–184
Korn ED (2004) The discovery of unconventional myosins: serendipity or luck? J Biol Chem 279:8517–8525
Krebs EG (1992) Protein phosphorylation and cellular regulation, I. December 8, 1992. nobleprize.org
Krebs EG, Beavo JA (1979) Phosphorylation-dephosphorylation of enzymes. Annu Rev Biochem 48:923–959
Kress M, Huxley HE, Faruqi AR, Hendrix J (1986) Structural changes during activation of frog muscle studied by time-resolved X-ray diffraction. J Mol Biol 188:325–342
Kretsinger RH, Barry CD (1975) The predicted structure of the calcium binding component of troponin. Biochim Biophys Acta 405:40–52
Kretsinger RH, Nockolds CE (1973) Carp muscle calcium-binding protein. II. Structure determination and general description. J Biol Chem 248:3313–3326
Kretsinger RH, Dangelat D, Bryan RF (1971) Crystal data for low molecular weight albumins of carp. J Mol Biol 59:213–214
Lai FA, Erickson HP, Rousseau E, Liu Q-Y, Meissner G (1988) Purification and reconstitution of the calcium release channel of skeletal muscle. Nature 331:315–319
Lehman W, Craig R (2004) The structure of the vertebrate striated muscle thin filament: a tribute to the contributions of Jean Hanson. J Muscle Res Cell Motil 25:455–466
Lehman W, Szent-Gyorgyi AG (1975) Regulation of muscular contraction. Distribution of actin control and myosin control in the animal kingdom. J Gen Physiol 66:1–30
Lehman W, Kendrick-Jones J, Szent-Gyorgyi AG (1973) Myosin-linked regulatory systems: comparative studies. Cold Spring Harb Symp Quant Biol 37:319–330
Lehman W, Craig R, Vibert P (1994) Ca2+-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction. Nature 368:65–67
Lehrer SS, Morris EP (1982) Dual effects of tropomyosin and troponin-tropomyosin on actomyosin subfragment 1 ATPase. J Biol Chem 257:8073–8080
Locker RH, Hagyard CJ (1967) Variations in the small subunits of different myosins. Arch Biochem Biophys 122:521–522
Lowey S, Holt JC (1973) An immunochemical approach to the interaction of light and heavy chains in myosin. Cold Spring Harb Symp Quant Biol 37:19–28
Lowey S, Kucera J, Holtzer A (1963) On the structure of the paramyosin molecule. J Mol Biol 7:234–244
Lowy J, Vibert PJ (1973) Studies of the low-angle X-ray pattern of a molluscan smooth muscle during tonic contraction and rigor. Cold Spring Harb Symp Quant Biol 37:353–359
Luther PK, Winkler H, Taylor K, Zoghbi ME, Craig R, Padron R, Squire JM, Liu J (2011) Direct visualization of myosin-binding protein C bridging myosin and actin filaments in intact muscle. Proc Natl Acad Sci U S A 108:11423–11428
MacLennan DH (1970) Purification and properties of an adenosine triphosphatase from sarcoplasmic reticulum. J Biol Chem 245:4508–4518
MacLennan DH, Wong PTS (1971) Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc Natl Acad Sci U S A 68:1231–1235
MacLennan DH, Yip CC, Iles GH, Seeman P (1973) Isolation of sarcoplasmic reticulum proteins. Cold Spring Harb Symp Quant Biol 37:469–477
Martonosi AN, Beeler TJ (1983) Mechanisms of Ca2+ transport by sarcoplasmic reticulum. In: Peachey LD, Adrian RH, Geiger SR (eds) Handbook of physiology: section 10, skeletal muscle. American Physiological Society, Bethesda, pp 417–485
Maruyama K, Matsubara S, Natori R, Nonomura Y, Kimura S, Ohashi K, Murakami F, Handa S, Eguchi G (1977) Connectin, an elastic protein of muscle. Characterization and function. J Biochem 82:317–337
Masaki T, Takaiti O, Ebashi S (1968) “M-substance”, a new protein constituting the M-line of myofibrils. J Biochem 64:909–910
McKillop DFA, Geeves MA (1993) Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys J 65:693–701
McLachlan AD, Karn J (1982) Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299:226–231
McLachlan AD, Stewart M (1976a) The 14-fold periodicity in alpha-tropomyosin and the interaction with actin. J Mol Biol 103:271–298
McLachlan AD, Stewart M (1976b) The troponin binding region of tropomyosin. Evidence for a site near residues 197 to 217. J Mol Biol 106:1017–1022
Meissner G (1975) Isolation and characterization of two types of sarcoplasmic reticulum vesicles. Biochim Biophys Acta 389:51–68
Milligan RA, Whittaker M, Safer D (1990) Molecular structure of F-actin and location of surface binding sites. Nature 348:217–221
Moore PB, Huxley HE, DeRosier DJ (1970) Three-dimensional reconstruction of F-actin, thin filaments and decorated thin filaments. J Mol Biol 50:279–295
Moos C (1973) Discussion: interaction of C-protein with myosin and light meromyosin. Cold Spring Harb Symp Quant Biol 37:93–95
Moos C, Mason CM, Besterman JM, Feng I-NM, Dubin JH (1978) The binding of skeletal muscle C-protein to F-actin, and its relation to the interaction of actin with myosin subfragment-1. J Mol Biol 124:571–586
O’brien EJ, Bennett PM, Hanson J (1971) Optical diffraction studies of myofibrillar structure. Philos Trans R Soc Lond B Biol Sci 261:201–208
Offer G (1973) C-protein and the periodicity in the thick filaments of vertebrate skeletal muscle. Cold Spring Harb Symp Quant Biol 37:87–93
Offer G (1974) The molecular basis of muscular contraction. In: Bull AT, Lagnado JR, Thomas JQ, Tipton KF (eds) Companion to biochemistry. Longman, London, pp 623–671
Offer G, Moos C, Starr R (1973) A new protein of the thick filaments of vertebrate skeletal myofibrils: extraction, purification and characterization. J Mol Biol 74:653–676
Ohtsuki I, Masaki T, Nonomura Y, Ebashi S (1967) Periodic distribution of troponin along the thin filament. J Biochem 61:817–819
Ornstein L (1964) Disc electrophoresis. 1, Background and theory. Ann N Y Acad Sci 121:321–349
Parry DAD (1981) Structure of rabbit skeletal myosin. Analysis of the amino acid sequences of two fragments from the rod region. J Mol Biol 153:459–464
Parry DAD, Squire JM (1973) Structural role of tropomyosin in muscle regulation: analysis of the X-ray diffraction patterns from relaxed and contracting muscles. J Mol Biol 75:33–55
Pauling L, Corey RB, Branson HR (1951) The structure of proteins: two hydrogen-bonded helical configuration of the polypeptide chain. Proc Natl Acad Sci U S A 37:205–211
Pechere J-F (1968) Muscular parvalbumins as homologous proteins. Comp Biochem Physiol 24:289–295
Pechere J-F, Capony J-P, Ryden L (1971) The primary structure of the major parvalbumin from Hake muscle. Isolation and general properties of the protein. Eur J Biochem 23:421–428
Pechere J-F, Derancourt J, Haiech J (1977) The participation of parvalbumins in the activation-relaxation cycle of vertebrate fast skeletal-muscle. FEBS Lett 75111–114
Pepe FA (1967) The myosin filament. I. Structural organization from antibody-staining in electron microscopy. J Mol Biol 27:203–225
Pepe FA (1973) The myosin filament: immunochemical and ultrastructural approaches to molecular organization. Cold Spring Harb Symp Quant Biol 37:97–108
Pepe FA, Drucker B (1975) The myosin filament. III. C-protein. J Mol Biol 88:609–617
Permyakov EA, Kretsinger RH (2011) Calcium binding proteins. Wiley, Hoboken
Perrie WT, Smillie LB, Perry SV (1973a) A phosphorylated light chain component of myosin from skeletal muscle. Cold Spring Harb Symp Quant Biol 37:17–18
Perrie WT, Smillie LB, Perry SV (1973b) A phosphorylated light-chain component of myosin from skeletal muscle. Biochem J 135:151–164
Pessah IN, Francini AO, Scales DJ, Waterhouse AL, Casida JE (1986) Calcium-ryanodine receptor complex: solubilization and partial characterization from skeletal muscle junctional sarcoplasmic reticulum vesicles. J Biol Chem 261:8643–8648
Phillips GN, Filler JP, Cohen C (1986) Tropomyosin crystal structure and muscle regulation. J Mol Biol 192:111–131
Philpott DE, Szent-Gyorgyi AG (1954) The structure of light-meromyosin: an electron microscopic study. Biochim Biophys Acta 15:165–173
Pollard TD, Korn ED (1973a) The “contractile” proteins of Acanthamoeba castellanii. Cold Spring Harb Symp Quant Biol 37:573–583
Pollard TD, Korn ED (1973b) Acanthamoeba myosin: I. Isolation from Acanthamoeba castellanii of an enzyme similar to myosin. J Biol Chem 248:4682–4690
Pollard TD, Korn ED (1973c) Acanthamoeba myosin: II. Interaction with actin and with a new cofactor protein required for activation of Mg2+ adenosine triphosphatase activity. J Biol Chem 248:4691–4697
Poole KJV, Lorenz M, Evans G, Rosenbaum G, Pirani A, Craig R, Tobacman LS, Lehman W, Holmes KC (2006) A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fibre diagrams from non-overlap muscle. J Struct Biol 155:273–284
Potter JD, Gergely J (1974) Troponin, tropomyosin, and actin interactions in the Ca2+ regulation of muscle contraction. Biochemistry 13:2697–2703
Potter JD, Gergely J (1975) The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J Biol Chem 250:4628–4633
Rayment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, Holmes KC, Milligan R (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, Holden HM (1993b) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261:50–58
Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720
Rosemblatt M, Hidalgo C, Vergara C, Ikemoto N (1981) Immunological and biochemical properties of transverse tubule membranes isolated from rabbit skeletal muscle. J Biol Chem 256:8140–8148
Saito A, Seiler S, Chu A, Fleischer S (1984) Preparation and morphology of sarcoplasmic reticulum terminal cisternae from skeletal muscle. J Cell Biol 99:875–885
Sanchez JA, Stefani E (1978) Inward calcium current in twitch muscle fibres of the frog. J Physiol 283197–209
Schneider MF, Chandler WK (1973) Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242:244–246
Schwartz LM, McCleskey EW, Almers W (1985) Dihydropyridine receptors in muscle are voltage-dependent but most are not functional calcium channels. Nature 314:747–751
Sellers JR (1999) Myosins, 2nd edn. Oxford University Press, Oxford
Seymour J, O’Brien EJ (1980) The position of tropomyosin in muscle thin filaments. Nature 83:680–682
Shapiro A, Vinuela E, Maizel JV (1967) Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem Biophys Res Commun 28:815–820
Sheterline P, Clayton J, Sparrow JC (1998) Actin, 4th edn. Oxford University Press, Oxford
Simmons RM (1992) A. F. Huxley’s research on muscle. In: Simmons RM (ed) Muscular contraction. Cambridge University Press, Cambridge, pp 19–42
Simmons RM, Szent-Gyorgyi AG (1985) A mechanical study of regulation in the striated adductor muscle of the scallop. J Physiol 358:47–64
Sobieszek A (1977) Vertebrate smooth muscle myosin. In: Stephens NL (ed) The biochemistry of smooth muscle. University Park Press, Baltimore, pp 413–443
Sohn RL, Vikstrom KL, Strauss M, Cohen C, Szent-Gyorgyi AG, Leinwand LA (1997) A 29 residue region of the sarcomeric myosin rod is necessary for filament formation. J Mol Biol 266:317–330
Spudich JA (1973) Effects of cytochalasin B on actin filaments. Cold Spring Harb Symp Quant Biol 37:585–593
Spudich JA, Huxley HE, Finch JT (1972) Regulation of skeletal muscle contraction. II. Structural studies of the interaction of the tropomyosin-troponin complex with actin. J Mol Biol 72:619–632
Squire JM (1971) General model for the structure of all myosin-containing filaments. Nature 233:457–462
Squire JM (1972) General model of myosin filament structure. II. Myosin filaments and cross-bridge interactions in vertebrate striated and insect flight muscle. J Mol Biol 72:125–138
Squire JM (1981) The structural basis of muscular contraction. Plenum, New York
Squire JM (1986) Muscle: design, diversity, and disease. Benjamin/Cummings, Menlo Park
Squire JM (1994) The actomyosin interaction—shedding light on structural events: ‘Plus ca change, plus c’est la meme chose’. J Muscle Res Cell Motil 15:227–231
Starr R, Offer G (1971) Polypeptide chains of intermediate molecular weight in myosin preparations. FEBS Lett 15:40–44
Starr R, Offer G (1978) The interaction of C-protein with heavy meromyosin and subfragment-2. Biochem J 171:813–816
Starr R, Offer G (1982) Preparation of C-protein, H-protein, X-protein and phosphofructokinase. In: Frederiksen DW, Cunningham LW (eds) Methods in enzymology, vol 85, Part B, Structural and contractile proteins. Academic, New York, pp 130–138
Stone D, Smillie LB (1978) The amino acid sequence of rabbit skeletal α-tropomyosin. The NH2-terminal half and complete sequence. J Biol Chem 253:1137–1144
Stull JT, Kamm KE, Vandenboom R (2011) Myosin light chain kinase and the role of myosin light chain phosphorylation in skeletal muscle. Arch Biochem Biophys 510:120–128
Sumbilla C, Cavagna M, Zhong L, Ma H, Lewis D, Farrance I, Inesi G (1999) Comparison of SERCA1 and SERCA2a expressed in COS-1 cells and cardiac myocytes. Am J Physiol 277:H2381–H2391
Szent-Gyorgyi AG (1975) Introductory remarks. In: Inoue S, Stephens RE (eds) Molecules and cell movement, vol 30, Society of General Physiologists. Raven, New York, pp 335–338
Szent-Gyorgyi AG (2007) Regulation by myosin: how calcium regulates some myosins: past and present. Adv Exp Med Biol 592:253–264
Szent-Gyorgyi AG, Cohen C, Kendrick-Jones J (1971) Paramyosin and the filaments of molluscan “catch” muscles. II. Native filaments: isolation and characterization. J Mol Biol 56:239–258
Szent-Gyorgyi AG, Szentkiralyi EM, Kendrick-Jones J (1973) The light chains of scallop myosin as regulatory subunits. J Mol Biol 74:179–203
Taylor EW (2001) 1999 E. B. Wilson lecture: the cell as molecular machine. Mol Biol Cell 12:251–254
Taylor KA, Amos LA (1981) A new model for the geometry of the binding of myosin crossbridges to muscle thin filaments. J Mol Biol 147:297–324
Tsien RW, Barrett CF (2000–2012) A brief history of calcium channel discovery. NCBI Bookshelf ID: NBK6465. National Library of Medicine, National Institutes of Health, Madame Curie Bioscience Database [Internet]. Landes Bioscience, Austin
Vibert P, Craig R, Lehman W (1997) Steric-model for activation of muscle thin filaments. J Mol Biol 266:8–14
Wang K, McClure J, Tu A (1979) Titin: major myofibrillar components of striated muscle. Proc Natl Acad Sci 76:3698–3702
Watson JD (1973) Foreword. Cold Spring Harb Symp Quant Biol 37:xvii
Weber HH (1958) The motility of muscle and cells. Harvard University Press, Cambridge
Weber K, Osborn M (1969) The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem 244:4406–4412
Weeds AG, Frank G (1973) Structural studies on the light chains of myosin. Cold Spring Harb Symp Quant Biol 37:9–14
Weisberg A, Winegrad S (1996) Alteration of myosin cross bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proc Natl Acad Sci 93:8999–9003
Woledge RC (1973) In vitro calorimetric studies relating to the interpretation of muscle heat experiments. Cold Spring Harb Symp Quant Biol 37:629–634
Woodhead JL, Zhao F-Q, Craig R, Egelman EH, Alamo L, Padron R (2005) Atomic model of a myosin filament in the relaxed state. Nature 436:1195–1199
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Rall, J.A. (2014). 1972 Cold Spring Harbor Symposia on Quantitative Biology: The Mechanism of Muscle Contraction—Problem Solved?. In: Mechanism of Muscular Contraction. Perspectives in Physiology. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2007-5_6
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