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Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle

Nature volume 299, pages 226–231 (1982)Cite this article

Abstract

The amino acid sequence of the rod portion of nematode myosin, deduced from the sequence of the unc-54 heavy chain gene of Caenorhabditis elegans, is highly repetitive and has the characteristics of an α-helical coiled coil. The molecular surface contains alternate clusters of positive and negative charge. Interactions between charge clusters on adjacent molecules could account for the observed spacings of the myosin cross-bridges in muscle. Calculations also suggest that the N-terminal third of the rod is only loosely associated with the thick filament backbone. Bending of the rod near the end of this region could allow the N-terminal section to act as a hinged arm during muscle contraction.

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References

  1. Huxley, H. E. in Fibrous Proteins: Scientific Industrial and Medical Aspects Vol. 1 (eds Parry, D. A. D. & Creamer, L. K.) 71–95 (Academic, New York, 1979).

    Google Scholar 

  2. Squire, J. M. The structural Basis of Muscular Contraction (Plenum, New York, 1981).

    Book  Google Scholar 

  3. Huxley, H. E. & Hanson, J. Nature 173, 973–976 (1954).

    Article  ADS  CAS  Google Scholar 

  4. Huxley, A. F. & Niedergerke, R. Nature 173, 971–972 (1954).

    Article  ADS  CAS  Google Scholar 

  5. Lowey, S., Slayter, H. S., Weeds, A. & Baker, H. J. molec. Biol. 42, 1–29 (1969).

    Article  CAS  Google Scholar 

  6. Lowey, S. in Fibrous Proteins: Scientific Industrial and Medical Aspects (eds Parry, D. A. D. & Creamer, L. K.) 1–26 (Academic, New York, 1979).

    Google Scholar 

  7. Elliott, A. & Offer, G. J. molec. Biol. 123, 505–519 (1978).

    Article  CAS  Google Scholar 

  8. Craig, R. W. J. molec. Biol. 109, 69–81 (1977).

    Article  CAS  Google Scholar 

  9. Sjostrom, M. & Squire, J. M. J. molec. Biol. 109, 49–68 (1977).

    Article  CAS  Google Scholar 

  10. Huxley, H. E. & Brown, W. J. molec. Biol. 30, 383–434 (1967).

    Article  CAS  Google Scholar 

  11. Miller, A. & Tregear, R. T. J. molec. Biol. 70, 85–104 (1972).

    Article  CAS  Google Scholar 

  12. Wray, J. S. Nature 277, 37–40 (1979).

    Article  ADS  CAS  Google Scholar 

  13. Offer, G. & Elliott, A. Nature 271, 325–329 (1978).

    Article  ADS  CAS  Google Scholar 

  14. Weeds, A. & Pope, B. J. molec. Biol. 111, 129–157 (1977).

    Article  CAS  Google Scholar 

  15. Pepe, F. A. J. molec. Biol. 27, 227–236 (1967).

    Article  CAS  Google Scholar 

  16. MacLeod, A. R., Waterston, R. H., Fishpool, R. M. & Brenner, S. J. molec. Biol. 114, 133–140 (1977).

    Article  CAS  Google Scholar 

  17. Karn, J., Brenner, S., Barnett, L. & Cesareni, G. Proc. natn. Acad. Sci. U.S.A. 77, 5172–5176 (1980).

    Article  ADS  CAS  Google Scholar 

  18. MacLeod, A. R., Karn, J. & Brenner, S. Nature 291, 386–390 (1981).

    Article  ADS  CAS  Google Scholar 

  19. Karn, J., McLachlan, A. D. & Barnett, L. in Molecular and Cellular Control of Muscle Development (eds Epstein, H. F., Garrels, J. I., Kaufman, S. J. & Pearson, M. L.) (Cold Spring Harbor Laboratory, New York, in the press).

  20. Elzinga, M. & Collins, J. H. Proc. natn. Acad. Sci. U.S.A. 74, 4281–4284 (1977).

    Article  ADS  CAS  Google Scholar 

  21. Trus, B. L. & Elzinga, M. in Structural Aspects of Recognition & Assembly in Biological Macromolecules Vol. 1 (eds Balaban, M., Sussman, J. L., Traub, W. & Yonath, A.) 361 (International Science Services, Tel-Aviv, 1981).

    Google Scholar 

  22. Mahdavi, U., Periasamy, M. & Nadal-Ginard, B. Nature 297, 659–664 (1982).

    Article  ADS  CAS  Google Scholar 

  23. McLachlan, A. D. Int. J. quant. Chem. 12, Suppl. 1. 371–385 (1977).

    Google Scholar 

  24. Crick, F. H. C. Acta crystalloqr. 6, 689–697 (1953).

    Article  CAS  Google Scholar 

  25. Wilson, I. A., Skehel, J. J. & Wiley, D. C. Nature 289, 366–373 (1981).

    Article  ADS  CAS  Google Scholar 

  26. Geisler, N. & Weber, C. Proc. natn. Acad. Sci. U.S.A. 78, 4120–4123 (1981).

    Article  ADS  CAS  Google Scholar 

  27. Stone, D., Sodek, J., Johnson, P. & Smillie, L. B. Proc. 9th FEBS Meet. Budapest 31, 125–136 (1975).

  28. McLachlan, A. D. & Stewart, M. J. molec. Biol. 103, 271–298 (1976).

    Article  CAS  Google Scholar 

  29. Parry, D. A. D. J. molec. Biol. 120, 545–551 (1978).

    Article  CAS  Google Scholar 

  30. Doolittle, R. F., Goldbaum, D. M. & Doolittle, L. R. J. molec. Biol. 120, 311–326 (1978).

    Article  CAS  Google Scholar 

  31. Parry, D. A. D., Crewther, W. G., Fraser, R. D. B. & MacRae, T. P. J. molec. Biol. 113, 449–454 (1977).

    Article  CAS  Google Scholar 

  32. McLachlan, A. D. & Stewart, M. J. molec. Biol. 98, 293–304 (1975).

    Article  CAS  Google Scholar 

  33. Parry, D. A. D. in Fibrous Proteins: Scientific Industrial and Medical Aspects Vol. 1 (eds Parry, D. A. D. & Creamer, L. K.) 393–427 (Academic, New York, 1979).

    Google Scholar 

  34. Capony, J. P. & Elzinga, M. Biophys. J. 33, 148a (1981).

    Google Scholar 

  35. Hoffmann, H., Fietzek, P. P. & Kuhn, H. J. molec. Biol. 141, 293–314 (1980).

    Article  Google Scholar 

  36. McLachlan, A. D., Stewart, M. & Smillie, L. B. J. molec. Biol. 98, 281–291 (1975).

    Article  CAS  Google Scholar 

  37. Parry, D. A. D. J. molec. Biol. 153, 459–464 (1981).

    Article  CAS  Google Scholar 

  38. Elzinga, M. & Trus, B. L. in Methods in Peptide and Protein Sequence Analysis (ed. Birr, Chr.) 213–224 (Elsevier, Amsterdam, 1980).

    Google Scholar 

  39. Phillips, G. N., Fillers, J. P. & Cohen, C. Biophys. J. 32, 485–502 (1980).

    Article  ADS  CAS  Google Scholar 

  40. Elliott, A. & Lowy, J. J. molec. Biol. 53, 181–203 (1970).

    Article  CAS  Google Scholar 

  41. Cohen, C. & Holmes, K. C. J. molec. Biol. 6, 423–432 (1963).

    Article  CAS  Google Scholar 

  42. Hulmes, D. J. S., Miller, A., Parry, D. A. D., Piez, K. A. & Woodhead-Galloway, J. J. molec. Biol. 79, 137–148 (1973).

    Article  CAS  Google Scholar 

  43. Fraser, R. D. B. & MacRae, T. P. Conformation in Fibrous Proteins (Academic, New York, 1973).

    Google Scholar 

  44. Takahashi, K. J. Biochem. Japan 83, 905–908 (1978).

    Article  CAS  Google Scholar 

  45. Lu, R. C. & Wong, A. Biophys. J. 37, 52a (1982).

    Google Scholar 

  46. Lu, R. C. Proc. natn. Acad. Sci. U.S.A. 77, 2010–2013 (1980).

    Article  ADS  CAS  Google Scholar 

  47. Ueno, H. & Harrington, W. F. Proc. natn. Acad. Sci. U.S.A. 78, 6101–6105 (1981).

    Article  ADS  CAS  Google Scholar 

  48. Bennett, P. M. J. molec. Biol. 146, 201–221 (1981).

    Article  CAS  Google Scholar 

  49. Katsura, I. & Noda, H. J. Biochem. Japan 73, 257–268 (1973).

    CAS  Google Scholar 

  50. Cohen, C., Szent-Györgyi, A. G. & Kendrick-Jones, J. J. molec. Biol. 56, 223–237 (1971).

    Article  CAS  Google Scholar 

  51. Bloomer, A. C., Champness, J. N., Bricogne, G., Staden, R. & Klug, A. Nature 276, 362–368 (1978).

    Article  ADS  CAS  Google Scholar 

  52. Stewart, M. & McLachlan, A. D. J. molec. Biol. 103, 251–269 (1976).

    Article  CAS  Google Scholar 

Download references

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  1. Laboratory of Molecular Biology, University Postgraduate Medical School, Hills Road, Cambridge, CB2 2QH, UK

    Andrew D. McLachlan & Jonathan Karn

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  1. Andrew D. McLachlan
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  2. Jonathan Karn
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McLachlan, A., Karn, J. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature 299, 226–231 (1982). https://doi.org/10.1038/299226a0

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