Summary
Many fibrous proteins have repeating sequence motifs that are associated with macromolecular interactions. We discuss here some of these motifs in a-helical coiled-coils found in muscle and cytoskeletal proteins. The motifs are most conveniently detected and analysed using Fourier methods which, if the data is appropriately scaled, can also be used to assess the statistical significance of a particular feature. Tropomyosin has a repeating motif in its acidic residues that occurs every 19.7 residues and which is associated with the interaction between tropomyosin and actin that plays a key role in the regulation of contraction in vertebrate skeletal muscle. The tails of myosin molecules have a pattern of alternating positive and negative zones that repeats every 28 residues and which is important in the interactions between myosin tails that result in the formation of thick filaments. Electron microscopy of 2-dimensional crystals of proteolytic fragments of myosin rod showed the coiled-coil pitch was near 14.3 nm and also indicated the likely interaction geometry between coiled-coils in thick filaments. The assembly of intermediate filament proteins also seems to involve the complementation of alternating zones of charge in an analogous way to that seen with myosin. The actual assembly of intermediate filament proteins appears to involve the formation of molecular dimers (that is, two molecules or four chains) often referred to as “tetramers”. We have been able to produce paracrystals from fragments of glial fibrillary acidic protein (the intermediate filament type present in astrocytes) that we have produced by recombinant DNA methods. These paracrystals indicated that the two molecules within a tetramer overlap their N- termini by approximately 33 nm, which would be consistent with models of intermediate filament structure proposed on the basis of X-ray diffraction data.
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References
Aebi U, Fowler WE, Rew P, Sun T-T (1983) The fibrillar structure of keratin filaments unravelled. J Cell Biol. 97: 1131–1143.
Caspar DLD, Cohen C, Longley W (1969) Tropomyosin crystal structure, polymorphism and molecular interactions. J Mol Biol. 41: 87–107.
Conway, JF, Parry, DAD (1988) Intermediate filament structure: 3. Analysis of sequence homologies. Internat J Biol Macromol 10: 79–98.
Crick FHC (1953) The Fourier transform of a coiled coil. Acta Crystallogr. 6: 685–689.
Fraser RDB, MacRae TP (1973) Conformation in Fibrous Proteins, Academic Press, New York.
Fraser RDB, MacRae TP, Suzuki E, Parry DAD (1985) Intermediate filament structure: 2. molecular interactions in the filament. Internat J Biol Macromol 7: 258–274.
Geisler N, Weber K (1982) The amino acid sequence of chicken muscle desmin provides a common structural model for intermediate filament proteins. EMBO J. 1: 1649–1656.
Kaufmann E, Weber K, Geisler N (1985) Intermediate filament forming ability of desmin derivatives lacking either the amino-terminal 67 or the carboxy-terminal 27 residues. J Mol Biol. 185: 733–742.
McLachlan AD (1978) Coiled-coil conformation and sequence regularities in the helical regions of alpha-keratin. J Mol Biol. 124: 279–304.
McLachlan AD, Kam J (1982) Periodic charge distributions in the myosin rod amino acid sequence match crossbridge spacings in muscle. Nature (London), 299: 226–231.
McLachlan AD, Stewart M (1975) Tropomyosin coiled-coil interactions. J Mol Biol. 97: 293–304.
McLachlan AD, Stewart M (1976) The 14-fold periodicity in tropomyosin. J Mol Biol. 103: 271–298.
McLachlan AD, Stewart M (1982) Periodic charge distribution in the intermediate filament proteins desmin and vimentin. J Mol Biol. 162: 693–698.
Parry DAD (1981) Structure of rabbit skeletal myosin. Analysis of the amino acid sequences of two fragments of the rod region. J Mol Biol. 153: 495–464.
Pany DAD, Crewther WG, Fraser RDB, MacRae TP (1977) Structure of alpha-keratin: structural implications of the amino acid sequences of type I and type II chain segments. J Mol Biol. 113: 449–454.
Phillips GN, Fillers JP, Cohen C (1986) Tropomyosin crystal structure and muscle regulation. J Mol Biol. 192: 111–131.
Phillips GN, Cohen C, Stewart M (1987) Preliminary X-ray diffraction studies and analysis of molecular packing in a new crystalline form of tropomyosin. J Mol Biol. 195: 219–223.
Quinlan RA, Franke WW (1982) Heteropolymer filament of desmin and vimentin in vascular smooth muscle tissue and cultured baby hamster kidney cells demonstrated by chemical crosslinking. Proc Natl Acad Sci USA. 79: 3452–3456.
Quinlan RA, Stewart M (1987) Crystalline tubes of myosin subfragment-2 showing the coiled-coil and molecular interaction geometry. J Cell Biol. 105: 403–415.
Quinlan RA, Hatzfeld M, Franke WW, Lustig A, Schulthess T, Engel J (1986) Characterisation of dimer subunits of intermediate filament proteins. J Mol Biol. 192: 337–349.
Soellner P, Quinlan RA, Franke WW (1985) Identification of a distinct soluble subunit of an intermediate filament protein: tetrameric vimentin from living cells. Proc Natl Acad Sci USA. 82: 7929–7933.
Stewart M (1975) Tropomyosin: no stagger between chains. FEBS Letters 53: 5–7.
Stewart M (1982) Chain register in myosin rod. FEBS Letters 140: 210–212.
Stewart M (1988) Introduction to the computer image processing of electron micrographs of two- dimensionally ordered biological material. J EM Tech., 9: 301–324.
Stewart M, Kensler RW (1986) The arrangement of myosin heads in relaxed thick filaments from frog skeletal muscle. J Mol Biol. 192: 831–851.
Stewart M, McLachlan AD (1975) 14 actin-binding sites on tropomyosin? Nature (London), 257: 331–333.
Stewart M, Kensler RW, Levine RJC (1985) Three-dimensional reconstruction of thick filaments from Limulus and scorpion muscle. J Cell Biol. 101: 402–411.
Stewart M, McLachlan AD, Calladine CR (1987) A model to account for the elastic element in muscle crossbridges in terms of a bending myosin rod. Proc Roy Soc London, Ser B. 229: 381–413.
Stone D & Smillie LB (1978). The amino acid sequence of rabbit skeletal alpha-tropomyosin. J Biol Chem. 253: 37–1148.
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Stewart, M., Quinlan, R.A., Moir, R.D., Clarke, S.R., Atkinson, S.J. (1989). The Role of Repeating Sequence Motifs in Interactions Between α-Helical Coiled-Coils such as Myosin, Tropomyosin and Intermediate-Filament Proteins. In: Aebi, U., Engel, J. (eds) Cytoskeletal and Extracellular Proteins. Springer Series in Biophysics, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-73925-5_29
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DOI: https://doi.org/10.1007/978-3-642-73925-5_29
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