Abstract
The structure of the thin, actin-containing filament of muscle is both highly conserved across a broad range of muscle types and is now well understood. The structure of the thick, myosin-containing filaments of striated muscle are quite variable and remained comparatively unknown until recently, particularly in the arrangement of the myosin tails. John Squire played a major role not only in our understanding of thin filament structure and function but also in the structure of the thick filaments. Long before much was known about the structure and composition of muscle thick filaments, he proposed a general model for how myosin filaments were constructed. His role in our current understanding the structure of striated muscle thick filaments and the extent through which his predictions have held true is the topic of this review.
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References
AL-Khayat HA, Hudson L, Reedy MK, Irving TC, Squire JM (2003) Myosin head configuration in relaxed insect flight muscle: X-ray modelled resting crossbridges in a pre-powerstroke state are poised for actin binding. Biophys J 85:1063–1079. https://doi.org/10.1016/S0006-3495(03)74545-7
Al-Khayat HA, Kensler RW, Squire JM, Marston SB, Morris EP (2013) Atomic model of the human cardiac muscle myosin filament. Proc Natl Acad Sci U S A 110:318–323. https://doi.org/10.1073/pnas.1212708110
Bear RS, Selby CC (1956) The structure of paramyosin fibrils according to x-ray diffraction. J Biophys Biochem Cytol 2:55–69. https://doi.org/10.1083/jcb.2.1.55
Beinbrech G, Ashton FT, Pepe FA (1988) Invertebrate myosin filament: subfilament arrangement in the wall of tubular filaments of insect flight muscles. J Mol Biol 201:557–565. https://doi.org/10.1016/0022-2836(88)90637-7
Bullard B, Luke B, Winkelman L (1973) The paramyosin of insect flight muscle. J Mol Biol 75:359–367. https://doi.org/10.1016/0022-2836(73)90026-0
Chew MW, Squire JM (1995) Packing of alpha-helical coiled-coil myosin rods in vertebrate muscle thick filaments. J Struct Biol 115:233–249. https://doi.org/10.1006/jsbi.1995.1048
Craig R, Megerman J (1977) Assembly of smooth muscle myosin into side-polar filaments. J Cell Biol 75:990–996. https://doi.org/10.1083/jcb.75.3.990
Crowther RA, Padron R, Craig R (1985) Arrangement of the heads of myosin in relaxed thick filaments from tarantula muscle. J Mol Biol 184:429–439. https://doi.org/10.1016/0022-2836(85)90292-x
Daneshparvar N, Taylor DW, O’Leary TS, Rahmani H, Abbasiyeganeh F, Previs MJ, Taylor KA (2020) CryoEM structure of Drosophila flight muscle thick filaments at 7 a resolution. Life Sci Alliance 3:e202000823. https://doi.org/10.26508/lsa.202000823
Egelman EH (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85:225–234. https://doi.org/10.1016/s0304-3991(00)00062-0
Elzinga M, Collins JH (1977) Amino acid sequence of a myosin fragment that contains SH-1, SH-2, and ntau-methylhistidine. Proc Natl Acad Sci U S A 74:4281–4284. https://doi.org/10.1073/pnas.74.10.4281
Haselgrove JC (1975) X-ray evidence for conformational changes in the myosin filaments of vertebrate striated muscle. J Mol Biol 92:113–143. https://doi.org/10.1016/0022-2836(75)90094-7
Hu Z, Taylor DW, Reedy MK, Edwards RJ, Taylor KA (2016) Structure of myosin filaments from relaxed Lethocerus flight muscle by cryo-EM at 6 Å resolution. Sci Adv 2:e1600058. https://doi.org/10.1126/sciadv.1600058
Hu Z, Taylor DW, Edwards RJ, Taylor KA (2017) Coupling between myosin head conformation and the thick filament backbone structure. J Struct Biol 200:334–342. https://doi.org/10.1016/j.jsb.2017.09.009
Huszar G, Elzinga M (1971) Amino acid sequence around the single 3-methylhistidine residue in rabbit skeletal muscle myosin. Biochemistry 10:229–236. https://doi.org/10.1021/bi00778a006
Huxley HE (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 7:281–308. https://doi.org/10.1016/s0022-2836(63)80008-x
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. https://doi.org/10.1016/s0022-2836(67)80046-9
Huxley HE (1969) The mechanism of muscular contraction. Science 164:1356–1365. https://doi.org/10.1126/science.164.3886.1356
Kendrick-Jones J, Cohen C, Szent-Gyorgyi AG, Longley W (1969) Paramyosin: molecular length and assembly. Science 163:1196–1198. https://doi.org/10.1126/science.163.3872.1196
Levine RJ, Elfvin M, Dewey MM, Walcott B (1976) Paramyosin in invertebrate muscles. II. Content in relation to structure and function. J Cell Biol 71:273–279. https://doi.org/10.1083/jcb.71.1.273
Li J, Rahmani H, Abbasi Yeganeh F, Rastegarpouyani H, Taylor DW, Wood NB, Previs MJ, Iwamoto H, Taylor KA (2023) Structure of the flight muscle thick filament from the Bumble Bee, Bombus ignitus, at 6 Å resolution. Int J Mol Sci 24:377
Lowey S, Slayter HS, Weeds AG, Baker H (1969) Substructure of the myosin molecule. I. Subfragments of myosin by enzymic degradation. J Mol Biol 42:1–29. https://doi.org/10.1016/0022-2836(69)90483-5
Mackenzie JM Jr, Epstein HF (1980) Paramyosin is necessary for determination of nematode thick filament length in vivo. Cell 22:747–755. https://doi.org/10.1016/0092-8674(80)90551-6
MacLeod AR, Karn J, Brenner S (1981) Molecular analysis of the unc-54 myosin heavy-chain gene of Caenorhabditis elegans. Nature 291:386–390. https://doi.org/10.1038/291386a0
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. https://doi.org/10.1038/299226a0
Miller A, Tregear RT (1972) Structure of insect fibrillar flight muscle in the presence and absence of ATP. J Mol Biol 70:85–104
Morris EP, Squire JM, Fuller GW (1991) The 4-stranded helical arrangement of myosin heads on insect (Lethocerus) flight muscle thick filaments. J Struct Biol 107:237–249. https://doi.org/10.1016/10478477(91)90049-3
Offer G, Moos C, Starr R (1973) A new protein of the thick filaments of vertebrate skeletal myofibrils. Extractions, purification and characterization. J Mol Biol 74:653–676. https://doi.org/10.1016/0022-2836(73)90055-7
Onishi H, Suzuki H, Nakamura K, Takahashi K, Watanabe S (1978) Adenosine triphosphatase activity and “thick filament” formation of chicken gizzard myosin in low salt media. J Biochem 83:835–847. https://doi.org/10.1093/oxfordjournals.jbchem.a131980
Patel SR, Saide JD (2005) Stretchin-klp, a novel Drosophila indirect flight muscle protein, has both myosin dependent and independent isoforms. J Muscle Res Cell Motil 26:213–224. https://doi.org/10.1007/s10974-005-9012-y
Pepe FA (1967) The myosin filament. I. Structural organization from antibody staining observed in electron microscopy. J Mol Biol 27:203–225. https://doi.org/10.1016/0022-2836(67)90016-2
Pepe FA, Drucker B (1972) The myosin filament. IV. Observation of the internal structural arrangement. J Cell Biol 52:255–260. https://doi.org/10.1083/jcb.52.2.255
Qiu F, Brendel S, Cunha PM, Astola N, Song B, Furlong EE, Leonard KR, Bullard B (2005) Myofilin, a protein in the thick filaments of insect muscle. J Cell Sci 118:1527–1536. https://doi.org/10.1242/jcs.02281
Rahmani H, Daneshparvar N, Hu Z, Taylor D, Edwards RJ, Taylor KA (2019) A Complete Atomic Model for Lethocerus Flight Muscle Myosin Filament. Biophys J 116, 160a. doi: https://doi.org/10.1016/j.bpj.2018.11.888
Rahmani H, Ma W, Hu Z, Daneshparvar N, Taylor DW, McCammon JA, Irving TC, Edwards RJ, Taylor KA (2021) The myosin II coiled-coil domain atomic structure in its native environment. Proc Natl Acad Sci U S A 118:e202415111. https://doi.org/10.1073/pnas.2024151118
Reedy MK, Holmes KC, Tregear RT (1965) Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature 207:1276–1280
Reedy MK (1968) Ultrastructure of insect flight muscle. I. Screw sense and structural grouping in the rigor cross-bridge lattice. J Mol Biol 31:155–176. https://doi.org/10.1016/0022-2836(68)90437-3
Reedy MC, Bullard B, Vigoreaux JO (2000) Flightin is essential for thick filament assembly and sarcomere stability in Drosophila flight muscles. J Cell Biol 151:1483–1500. https://doi.org/10.1083/jcb.151.7.1483
Rice RV, McManus GM, Devine OF, Somlyo AP (1971) Regular organization of thick filaments in mammalian smooth muscle. Nat New Biol 231:242–243. https://doi.org/10.1038/newbio231242a0
Schmitz H, Ashton FT, Pepe FA, Beinbrech G (1993) Invertebrate myosin filament: parallel subfilament arrangement in the wall of solid filaments from the honeybee, Apis mellifica. Tissue Cell 25:111–119
Small JV, Squire JM (1972) Structural basis of contraction in vertebrate smooth muscle. J Mol Biol 67:117–149. https://doi.org/10.1016/0022-2836(72)90390-7
Small JV (1977) Studies on isolated smooth muscle cells: the contractile apparatus. J Cell Sci 24:327–349. https://doi.org/10.1242/jcs.24.1.327
Sobieszek IJ, Sobieszek A (2022) Myosin assembly of smooth muscle: from ribbons and side polarity to a row polar helical model. J Muscle Res Cell Motil 43:113–133. https://doi.org/10.1007/s10974-022-09622-4
Somlyo AP, Devine CE, Somlyo AV (1971a) Thick filaments in unstretched mammalian smooth muscle. Nat New Biol 233:218–219
Somlyo AP, Somlyo AV, Devine CE, Rice RV (1971b) Aggregation of thick filaments into ribbons in mammalian smooth muscle. Nat New Biol 231:243–246. https://doi.org/10.1038/newbio231243a0
Squire JM (1971) General model for the structure of all myosin-containing filaments. Nature 233:457–462. https://doi.org/10.1038/233457a0
Squire JM (1972) General model of myosin filament structure. II. Myosin filaments and cross-bridge interactions in vertebrate striated and insect flight muscles. J Mol Biol 72:125–138. https://doi.org/10.1016/0022-2836(72)90074-5
Squire JM (1973) General model of myosin filament structure. 3. Molecular packing arrangements in myosin filaments. J Mol Biol 77:291–323. https://doi.org/10.1016/0022-2836(73)90337-9
Squire JM (1975) Muscle filament structure and muscle contraction. Annu Rev Biophys Bioeng 4:137–163. https://doi.org/10.1146/annurev.bb.04.060175.001033
Stewart M, Kensler RW, Levine RJ (1981a) Structure of Limulus telson muscle thick filaments. J Mol Biol 153:781–790. https://doi.org/10.1016/0022-2836(81)90418-6
Stewart M, Ashton FT, Lieberson R, Pepe FA (1981b) The myosin filament. IX. Determination of subfilament positions by computer processing of electron micrographs. J Mol Biol 153:381–392. https://doi.org/10.1016/0022-2836(81)90284-9
Stewart M, Kensler RW, Levine RJ (1985) Three-dimensional reconstruction of thick filaments from Limulus and scorpion muscle. J Cell Biol 101:402–411
Stewart M, Kensler RW (1986) Arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol 192:831–851
Sulbaran G, Alamo L, Pinto A, Marquez G, Mendez F, Padron R, Craig R (2015) An invertebrate smooth muscle with striated muscle myosin filaments. Proc Natl Acad Sci U S A 112:E5660–5668. https://doi.org/10.1073/pnas.1513439112
Tonino P, Kiss B, Strom J, Methawasin M, Smith JE 3rd, Kolb J, Labeit S, Granzier H (2017) The giant protein titin regulates the length of the striated muscle thick filament. Nat Commun 8:1041. https://doi.org/10.1038/s41467-017-01144-9
Trybus KM (1991) Assembly of cytoplasmic and smooth muscle myosin. Curr Opin Cell Biol 3:105–111
Tskhovrebova L, Trinick J (2017) Titin and Nebulin in Thick and thin filament length regulation. Subcell Biochem 82:285–318. https://doi.org/10.1007/978-3-319-49674-0_10
Vibert P, Craig R (1983) Electron microscopy and image analysis of myosin filaments from scallop striated muscle. J Mol Biol 165:303–320. https://doi.org/10.1016/s0022-2836(83)80259-9
Vibert P (1992) Helical reconstruction of frozen-hydrated scallop myosin filaments. J Mol Biol 223:661–671
Vigoreaux JO, Saide JD, Valgeirsdottir K, Pardue ML (1993) Flightin, a novel myofibrillar protein of Drosophila stretch-activated muscles. J Cell Biol 121:587–598. https://doi.org/10.1083/jcb.121.3.587
Wendt T, Taylor D, Trybus KM, Taylor K (2001) Three-dimensional image reconstruction of dephosphorylated smooth muscle heavy meromyosin reveals asymmetry in the interaction between myosin heads and placement of subfragment 2. Proc Natl Acad Sci U S A 98:4361–4366. https://doi.org/10.1073/pnas.071051098
Woodhead JL, Zhao FQ, Craig R, Egelman EH, Alamo L, Padron R (2005) Atomic model of a myosin filament in the relaxed state. Nature 436:1195–1199. https://doi.org/10.1038/nature03920
Wray JS (1979) Structure of the backbone in myosin filaments of muscle. Nature 277:37–40. https://doi.org/10.1038/277037a0
Zhao FQ, Craig R, Woodhead JL (2009) Head-head interaction characterizes the relaxed state of Limulus muscle myosin filaments. J Mol Biol 385:423–431. https://doi.org/10.1016/j.jmb.2008.10.038
Zoghbi ME, Woodhead JL, Moss RL, Craig R (2008) Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc Natl Acad Sci U S A 105:2386–2390. https://doi.org/10.1073/pnas.0708912105
Acknowledgements
The authors work on insect flight muscle structure has been supported by NIH grants R01 GM030598 and R35 GM139616. We thank Ms Jiawei Li for the use of Fig. 4d.
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Taylor, K.A. John Squire and the myosin thick filament structure in muscle. J Muscle Res Cell Motil 44, 143–152 (2023). https://doi.org/10.1007/s10974-023-09646-4
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DOI: https://doi.org/10.1007/s10974-023-09646-4