Basal sliding and the mechanics of oscillation in a mammalian sperm flagellum

Biophysical Journal

Volumn 87, Issue 6, 2004, Pages 3934-3944

  Vernon, Geraint G ^a   Woolley, David M ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CHINCHILLA; ELECTRON MICROSCOPY; FLAGELLUM; MICROSCOPY; MICROTUBULE; NONHUMAN; OSCILLATION; SHEAR RATE; SPERM; SPERMATOZOON MOTILITY; VIDEORECORDING;

ANIMALIA; MAMMALIA;

EID: 10044246306     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.042648     Document Type: Article

References (51)

1. Baccetti, B., B. H. Gibbons, and I. R. Gibbons. 1989. Bidirectional swimming in spermatozoa of Tephritid flies. J. Submicrosc. Cytol. Pathol. 21:619-625.
2. Bozkurt, H. H., and D. M. Woolley. 1993. Morphology of nexin links in relation to interdoublet sliding in the sperm flagellum. Cell Motil. Cytoskeleton. 24:109-118.
3. Brokaw, C. J. 1982. Models for oscillation and bend propagation by flagella. Symp. Soc. Exp. Biol. 35:313-338.
4. Brokaw, C. J. 1985. Computer simulation of flagellar movement. VI. Simple curvature-controlled models are incompletely specified. Biophys. J. 48:633-642.
5. Brokaw, C. J. 1989. Operation and regulation of the flagellar oscillator. In Cell Movement, Vol. 1. The Dynein ATPases. F. D. Warner, P. Satir, and I. R. Gibbons editors. Alan R. Liss, New York. 267-279.
6. Brokaw, C. J. 1991. Microtubule sliding in swimming sperm flagella: direct and indirect measurements on sea urchin and tunicate spermatozoa. J. Cell Biol. 114:1201-1215.
7. Brokaw, C. J. 1996. Microtubule sliding, bend initiation, and bend propagation parameters of Ciona sperm flagella altered by viscous load. Cell Motil. Cytoskeleton. 33:6-21.
8. Brokaw, C. J. 1997. Transient disruptions of axonemal structure and microtubule sliding during bend propagation by Ciona sperm flagella. Cell Motil. Cytoskeleton. 37:346-362.
9. Douglas, G. J., and M. E. J. Holwill. 1972. Behaviour of flagella isolated from Crithidia oncopelti. J. Mechanochem. Cell Motil. 1:213-223.
10. Eshel, D., and I. R. Gibbons. 1989. External mechanical control of the timing of bend initiation in sea urchin sperm flagella. Cell Motil. Cytoskeleton. 14:416-423.
11. Eshel, D., C. Shingyoji, K. Yoshimura, B. H. Gibbons, I. R. Gibbons, and K. Takahashi. 1990. Transient behaviour of sea urchin sperm flagella following an abrupt change in beat frequency. J. Exp. Biol. 152:441-451.
12. Eshel, D., C. Shingyoji, K. Yoshimura, I. R. Gibbons, and K. Takahashi. 1992. The phase of sperm flagellar beating is not conserved over a brief imposed interruption. Exp. Cell Res. 202:552-555.
13. Fawcett, D. W. 1975. The mammalian spermatozoon. Dev. Biol. 44:394-436.
14. Fawcett, D. W., and D. M. Phillips. 1969. The fine structure and development of the neck region of the mammalian spermatozoon: Anat. Rec. S 165:153-184.
15. Gibbons, I. R. 1961. The relationship between the fine structure and direction of beat in gill cilia of a lamelli branch mollusc. J. Biophys. Biochem. Cytol. 11:179-205.
16. Gibbons, I. R. 1974. Mechanisms of flagellar motility. In The Functional Anatomy of the Spermatozoon. B. A. Afzelius, editor. Pergamon, Oxford and New York. 127-140.
17. Gibbons, I. R. 1982. Sliding and bending in sea urchin sperm flagella. Symp. Soc. Exp. Biol. 35:225-287.
18. Goldstein, S. F. 1977. Asymmetric waveforms in echinoderm sperm flagella. J. Exp. Biol. 71:157-170.
19. Goldstein, S. F. 1981. Motility of basal fragments of sea urchin sperm flagella. J. Cell Sci. 50:65-77.
20. Hamasaki, M., M. Wakimoto, T. Maehara, and H. Matsuo. 1994. Three-dimensional structures of the neck region of the hamster spermatozoa in the caudal epididymis. Arch. Histol. Cytol. 57:59-65.
21. Holwill, M. E. J., and J. L. McGregor. 1976. Effects of calcium on flagellar movement in the trypanosome Crithidia oncopelti. J. Exp. Biol. 65:229-242.
22. Ishijima, S., S. A. Ishijima, and B. A. Afzelius. 1994. Movement of Myzostomum spermatozoa: calcium ion regulation of swimming direction. Cell Motil. Cytoskeleton. 28:135-142.
23. Iwashita, T., and C. Öura. 1980. A three-dimensional analysis of the capitellum and striated columns in the sperm neck region of the mouse. Okajimas Folia Anat. Jpn. 56:361-382.
24. Kaneda, Y. 1965. Movement of sperm tail of frog. J. Fac. Sci. Tokyo Zool. 10:427-440.
25. Kamimura, S., and R. Kamiya. 1989. High-frequency nanometre-scale vibration in 'quiescent' flagellar axonemes. Nature. 340:476-478.
26. Kamiya, R., and T. Okagaki. 1986. Cyclical bending of two outer-doublet microtubules in frayed axonemes of Chlamydomonas. Cell Motil. Cytoskeleton. 6:580-585.
27. Kinosita, H., and T. Kamada. 1939. Movement of abfrontal cilia of Mytilus. Jap. J. Zool. 8:291-310.
28. Lindemann, C. B. 1996. Functional significance of the outer dense fibres of mammalian sperm examined by computer simulations with geometric clutch model. Cell Motil. Cytoskeleton. 34:258-270.
29. Lindemann, C. B., and I. R. Gibbons. 1975. Adenosine triphosphate-induced motility and sliding of filaments in mammalian sperm extracted with Triton X-100. J. Cell Biol. 65:147-162.
30. Machemer, H. 1974. Ciliary activity and metachronism in protozoa. In Cilia and Flagella. M. A. Sleigh, editor. Academic Press, London and New York. 199-286.
31. Murakami, A. 1963. Analysis of metachronal coordination in ciliary pads of Mytilus gill. J. Fac. Sci. Tokyo Zool. 10:23-35.
32. Okuno, M., and Y. Hiramoto. 1976. Mechanical stimulation of starfish sperm flagella. J. Exp. Biol. 65:401-413.
33. 2+-induced asymmetry of active microtubule sliding in sea urchin sperm tails. J. Cell Biol. 102:2042-2052.
34. Satir, P. 1968. Studies on cilia. III. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J. Cell Biol. 39:77-94.
35. Shingyoji, C., I. R. Gibbons, A. Murakami, and K. Takahashi. 1991. Effect of imposed head vibration on the stability and waveform of flagellar beating in sea urchin spermatozoa. J. Exp. Biol. 156:63-80.
36. Shingyoji, C., H. Higuchi, M. Yoshimura, E. Katayama, and T. Yanagida. 1998. Dynein arms are oscillating force generators. Nature. 393:711-714.
37. Shingyoji, C., and K. Takahashi. 1995. Cyclical bending movements induced locally by successive iontophoretic application of ATP to an elastase-treated flagellar axoneme. J. Cell Sci. 108:1359-1369.
38. Shingyoji, C., K. Yoshimura, D. Eshel, K. Takahashi, and I. R. Gibbons. 1995. Effect of beat frequency on the velocity of microtubule sliding in reactivated sea urchin sperm flagellar under imposed head vibration. J. Exp. Biol. 198:645-653.
39. Stommel,.E. W. 1986. Mechanical stimulation activates beating in calcium-arrested lateral cilia of Mytilus edulis gill. J. Muscle Res. Cell Motil. 7:237-244.
40. Tamm, S. L. 1983. Motility and mechanosensitivity of macrocilia in the ctenophore Beroë. Nature. 305:430-433.
41. Tani, T., and S. Kamimura. 1998. Reactivation of sea urchin sperm flagella induced by rapid photolysis of caged ATP. J. Exp. Biol. 201:1493-1503.
42. Thurm, U. 1968. Steps in the transducer process of mechanoreceptors. Symp. Zool. Soc. Lond. 23:199-216.
43. Vernon, G. G., and D. M. Woolley. 2002. Microtubule displacements at the tips of living flagella. Cell Motil. Cytoskeleton. 52:151-160.
44. Wais-Steider, J., and P. Satir. 1979. Effect of vanadate on gill cilia: switching mechanism in ciliary beat. J. Supramol. Struct. 11:339-347.
45. Warner, F. D., and P. Satir. 1974. The structural basis of ciliary bend formation. J. Cell Biol. 63:35-63.
46. Woolley, D. M. 2003. Motility of spermatozoa at surfaces. Reproduction. 126:259-270.
47. Woolley, D. M., and H. H. Bozkurt. 1995. The distal sperm flagellum: its potential for motility after separation from the basal structures. J. Exp. Biol. 198:1469-1481.
48. Woolley, D. M., and D. W. Fawcett. 1973. The degeneration and disappearance of the centrioles during the development of the rat spermatozoon. Anat. Rec. 177:289-302.
49. Woolley, D. M., and G. G. Vernon. 2001. A study of helical and planar waves on sea urchin sperm flagella, with a theory of how they are generated. J. Exp. Biol. 204:1333-1345.
50. Woolley, D. M., and G. G. Vemon. 2002. Functional state of the axonemal dyneins during flagellar bend propagation. Biophys. J. 83:2162-2169.
51. Zamboni, L., and M. Stefanini. 1971. The fine structure of the neck of mammalian spermatozoa. Anat. Rec. 169:155-172.