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. 1974 Dec 1;63(3):970–985. doi: 10.1083/jcb.63.3.970

PROPERTIES OF FLAGELLAR "RIGOR WAVES" FORMED BY ABRUPT REMOVAL OF ADENOSINE TRIPHOSPHATE FROM ACTIVELY SWIMMING SEA URCHIN SPERM

Barbara H Gibbons 1, I R Gibbons 1
PMCID: PMC2109359  PMID: 4215820

Abstract

Sea urchin sperm were demembranated and reactivated with a solution containing 0.04% Triton X-100 and 0.03 mM ATP. The ATP concentration was then lowered abruptly by diluting the sperm suspension 50-fold into reactivating solution containing no ATP. The flagella of the sperm in the diluted suspension were not motile, but they were bent into a variety of stationary rigor wave forms closely resembling the wave forms occurring at different stages of the flagellar bending cycle during normal movement. The form of these rigor waves was unchanged upon storage for several hours in the presence of dithiothreitol and EDTA. Addition of 1 µM ATP induced slow relaxation of the waves, with most of the sperm becoming partially straightened over a period of about 30 min; somewhat higher concentrations gave a more rapid and complete relaxation. Concentrations of ATP above 10 µM induced resumption of normal beating movements. Addition of ITP, GTP, or GDP (up to 1 mM) produced no relaxation of the rigor waves. Digestion with trypsin to an extent sufficient to disrupt the radial spokes and the nexin links caused no change in the rigor wave forms, suggesting that these wave forms could be maintained by the dynein cross-bridges between the outer doublet tubules of the flagellar axoneme. Study of the effects of viscous shear on the rigor wave axonemes has shown that they are resistant to distortion by bending, although they can be twisted relatively easily.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aiello E., Sleigh M. A. The metachronal wave of lateral cilia of Mytilus edulis. J Cell Biol. 1972 Sep;54(3):493–506. doi: 10.1083/jcb.54.3.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen R. D. A reinvestigation of cross-sections of cilia. J Cell Biol. 1968 Jun;37(3):825–831. doi: 10.1083/jcb.37.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bedford J. M., Calvin H., Cooper G. W. The maturation of spermatozoa in the human epididymis. J Reprod Fertil Suppl. 1973 Jul;18:199–213. [PubMed] [Google Scholar]
  4. Brokaw C. J. Effects of increased viscosity on the movements of some invertebrate spermatozoa. J Exp Biol. 1966 Aug;45(1):113–139. doi: 10.1242/jeb.45.1.113. [DOI] [PubMed] [Google Scholar]
  5. Brokaw C. J. Flagellar movement: a sliding filament model. Science. 1972 Nov 3;178(4060):455–462. doi: 10.1126/science.178.4060.455. [DOI] [PubMed] [Google Scholar]
  6. Brokaw C. J., Gibbons I. R. Localized activation of bending in proximal, medial and distal regions of sea-urchin sperm flagella. J Cell Sci. 1973 Jul;13(1):1–10. doi: 10.1242/jcs.13.1.1. [DOI] [PubMed] [Google Scholar]
  7. GIBBONS I. R., GRIMSTONE A. V. On flagellar structure in certain flagellates. J Biophys Biochem Cytol. 1960 Jul;7:697–716. doi: 10.1083/jcb.7.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gibbons B. H., Gibbons I. R. Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100. J Cell Biol. 1972 Jul;54(1):75–97. doi: 10.1083/jcb.54.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gibbons B. H., Gibbons I. R. The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm. J Cell Sci. 1973 Sep;13(2):337–357. doi: 10.1242/jcs.13.2.337. [DOI] [PubMed] [Google Scholar]
  10. Gibbons I. R., Fronk E. Some properties of bound and soluble dynein from sea urchin sperm flagella. J Cell Biol. 1972 Aug;54(2):365–381. doi: 10.1083/jcb.54.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Huxley H. E. The structural basis of muscular contraction. Proc R Soc Lond B Biol Sci. 1971 Jun 29;178(1051):131–149. doi: 10.1098/rspb.1971.0057. [DOI] [PubMed] [Google Scholar]
  12. Kincaid H. L., Jr, Gibbons B. H., Gibbons I. R. The salt-extractable fraction of dynein from sea urchin sperm flagella: an analysis by gel electrophoresis and by adenosine triphosphatase activity. J Supramol Struct. 1973;1(6):461–470. doi: 10.1002/jss.400010603. [DOI] [PubMed] [Google Scholar]
  13. Lindemann C. B., Rudd W. G., Rikmenspoel R. The stiffness of the flagella of impaled bull sperm. Biophys J. 1973 May;13(5):437–448. doi: 10.1016/S0006-3495(73)85997-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lymn R. W., Taylor E. W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry. 1971 Dec 7;10(25):4617–4624. doi: 10.1021/bi00801a004. [DOI] [PubMed] [Google Scholar]
  15. Olmsted J. B., Borisy G. G. Microtubules. Annu Rev Biochem. 1973;42:507–540. doi: 10.1146/annurev.bi.42.070173.002451. [DOI] [PubMed] [Google Scholar]
  16. SATIR P. STUDIES ON CILIA. THE FIXATION OF THE METACHRONAL WAVE. J Cell Biol. 1963 Aug;18:345–365. doi: 10.1083/jcb.18.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Satir P. Studies on cilia. 3. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J Cell Biol. 1968 Oct;39(1):77–94. doi: 10.1083/jcb.39.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Summers K. E., Gibbons I. R. Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3092–3096. doi: 10.1073/pnas.68.12.3092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Summers K. E., Gibbons I. R. Effects of trypsin digestion on flagellar structures and their relationship to motility. J Cell Biol. 1973 Sep;58(3):618–629. doi: 10.1083/jcb.58.3.618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Taylor E. W. Chemistry of muscle contraction. Annu Rev Biochem. 1972;41(10):577–616. doi: 10.1146/annurev.bi.41.070172.003045. [DOI] [PubMed] [Google Scholar]
  21. Zobel C. R. Effect of solution composition and proteolysis on the conformation of axonemal components. J Cell Biol. 1973 Dec;59(3):573–594. doi: 10.1083/jcb.59.3.573. [DOI] [PMC free article] [PubMed] [Google Scholar]

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