Central-pair-linked regulation of microtubule sliding by calcium in flagellar axonemes

Journal of Cell Science

Volumn 116, Issue 8, 2003, Pages 1627-1636

  Nakano, Izumi ^a   Kobayashi, Takeshi ^a,b   Yoshimura, Misako ^a   Shingyoji, Chikako ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

9+2 Structure; Dynein; Elastase; Sliding pattern; Sliding velocity

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; DYNEIN ADENOSINE TRIPHOSPHATASE; ELASTASE;

AXONEME; CALCIUM CELL LEVEL; CELL MOTION; CELL STRUCTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EUKARYOTIC FLAGELLUM; FREQUENCY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SEA URCHIN; SPERM; STRUCTURE ANALYSIS;

ANIMALS; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MICROSCOPY, ELECTRON; MICROTUBULES; PANCREATIC ELASTASE; SEA URCHINS; SPERM MOTILITY; SPERM TAIL; TIME FACTORS;

ECHINOIDEA; EUKARYOTA;

EID: 0012941446     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00336     Document Type: Review

References (39)

1. Afzelius, B. A. (1959). Electron microscopy of the sperm tail. Results obtained with a new fixative. J. Biophys. Biochem. Cytol., 5, 269-278.
2. Bannai, H., Yoshimura, M., Takahashi, K. and Shingyoji, C. (2000). Calcium regulation of microtubule sliding in reactivated sea urchin sperm flagella. J. Cell Sci., 113, 831-839.
3. Bessen, M., Fay, R. B. and Witman, G. B. (1980). Calcium control of waveform in isolated flagellar axonemes of Chlamydomonas. J. Cell Biol. 86, 446-455.
4. Brokaw, C. J. (1979). Calcium-induced asymmetrical beating of Triton-demembranated sea urchin sperm flagella. J. Cell Biol. 82, 401-411.
5. Brokaw, C. J. (1980). Elastase digestion of demembranated sperm flagella. Science. 207, 1365-1367.
6. Gibbons, B. H. and Gibbons, I. R. (1980). Calcium-induced quiescence in reactivated sea urchin sperm. J. Cell Biol. 84, 13-27.
7. Gibbons, I. R., Shingyoji, C., Murakami, A. and Takahashi, K. (1987). Spontaneous recovery after experimental manipulation of the plane of beat in sperm flagella. Nature 325, 351-352.
8. Goldstein, D. A. (1979). Calculation of the concentration of free cations and cation-ligand complexes in solution containing multiple divalent cations and ligands. Biophys. J. 26, 235-242.
9. Holwill, M. E. J. and McGregor, J. L. (1976). Effects of calcium on flagellar movement in the trypanosome Crithidia oncopelti. J. Exp. Biol. 65, 229-242.
10. Holwill, M. E. J. and Satir, P. (1994). Physical model of axonemal splitting. Cell Motil. Cytoskel. 27, 287-298.
11. Hosokawa, Y. and Miki-Noumura, T. (1987). Bending motion of Chlamydomonas axonemes after extrusion of central-pair micrombules. J. Cell Biol. 105, 1297-1301.
12. Hyams, J. S. and Borisy, G. G. (1978). Isolated flagellar apparatus of Chlamydomonas: characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro. J. Cell Sci. 33, 235-253.
13. Izumi, A. and Miki-Noumura, T. (1985). Tetrahymena cell model exhibiting Ca-dependent behavior. Cell Motil. 5, 323-331.
14. Kamiya, R. (2002). Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int. Rev. Cytol. 219, 115-155.
15. Kinoshita, S., Miki-Noumura, T. and Omoto, C. K. (1995). Regulatory role of nucleotides in axonemal function. Cell Motil. Cytoskel. 32, 46-54.
16. Mitchell, D. R. and Sale, W. S. (1999). Characterization of a Chlamydomonas insertional mutant that disrupts flagellar central pair microtubule-associated structures. J. Cell Biol. 144, 293-304.
17. Mogami, Y. and Takahashi, K. (1983). Calcium and microtubule sliding in ciliary axonemes isolated from Paramecium caudatum. J. Cell. Sci. 61, 107-121.
18. Naitoh, Y. and Kaneko, H. (1972). Reactivated Triton-extracted models of Paramecium: modification of ciliary movement by calcium ions. Science 176, 523-524.
19. Okagaki, T. and Kamiya, R. (1986). Microtubule sliding in mutant Chlamydomonas axonemes devoid of outer or inner dynein arms. J. Cell Biol. 103, 1895-1902.
20. Omoto, C. K. and Brokaw, C. J. (1985). Bending patterns of Chlamydomonas flagella: II. Calcium effects on reactivated Chlamydomonas flagella. Cell Motil. 5, 53-60.
21. Omoto, C. K., Yagi, T., Kurimoto, E. and Kamiya, R. (1996). Ability of paralyzed flagella mutants of Chlamydomonas to move. Cell Motil. Cytoskel. 33, 88-94.
22. Omoto, C. K., Gibbons, I. R., Kamiya, R., Shingyoji, C., Takahashi, K. and Witman, G. B. (1999). Rotation of the central pair microtubules in eukaryotic flagella. Mol. Biol. Cell 10, 1-4.
23. Porter, M. E. and Sale, W. S. (2000). The 9+2 axoneme anchors multiple inner arm dyneins and a network of kinase and phosphatases that control motility. J. Cell Biol. 151, F37-F42.
24. Roush-Gaillard, A., Diener, D. R., Rosenbaum, J. L. and Sale, W. S. (2001). Flagellar radial spoke protein 3 is an A-kinase anchoring protein (AKAP). J. Cell Biol. 153, 443-448.
25. 2+-induced asymmetry of active microtubule sliding in sea urchin sperm tails. J. Cell Biol. 102, 2042-2052.
26. Shingyoji, C. and Takahashi, K. (1995). Cyclical bending movements induced locally by successive iontophoretic application of ATP to an elastase-treated flagellar axoneme. J. Cell. Sci. 108, 1359-1369.
27. Shingyoji, C., Higuchi, H., Yoshimura, M., Katayama, E. and Yanagida, T. (1998). Dynein arms are oscillating force generators. Nature 393, 711-714.
28. Smith, E. F. (2002a). Regulation of flagellar dynein by the axonemal central apparatus. Cell Motil. Cytoskel. 52, 33-42.
29. Smith, E. F. (2002b). Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol. BIol. Cell 13, 3303-3313.
30. Smith, E. F. and Lefebvre, P. A. (1997). The role of central apparatus components in flagellar motility and microtubule assembly. Cell Motil. Cytoskel. 38, 1-8.
31. Summers, K. E. and Gibbons, I. R. (1971). Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc. Natl. Acad. Sci. USA 68, 3092-3096.
32. Takahashi, K., Shingyoji, C. and Kamimura, S. (1982). Microtubule sliding in reactivated flagella. Symp. Soc. Exp. Biol. 35, 159-177
33. Takahashi, K., Shingyoji, C., Katada, J., Eshel, D. and Gibbons, I. R. (1991). Polarity in spontaneous unwinding after prior rotation of the flagellar beat plane in sea-urchin spermatozoa. J Cell Sci. 98, 183-189.
34. Vale, R. D. and Toyoshima, Y. Y. (1989). Microtubule translocation properties of intact and proteolytically digested dyneins from Tetrahymena cilia. J. Cell Biol. 108, 2327-2334.
35. 2+-dependent waveform conversion in the flagellar axoneme of Chlamydomonas mutants lacking the central-pair/radial spoke system. Cell Motil. Cytoskel. 38, 22-28.
36. Walter, M. F. and Satir, P. (1979). Calcium does not inhibit active sliding of microtubules from mussel gill cilia. Nature 278, 69-70.
37. Witman, G. B., Plummer, J. and Sander, G. (1978). Chlamydomonas flagellar mutants lacking radial spokes and central tubules. J. Cell Biol. 76, 729-747.
38. Yang, P., Fox, L., Colbran, R. J. and Sale, W. S. (2000). Protein phosphatases PP1 and PP2A are located in distinct positions in the Chlamydomonas flagellar axoneme. J. Cell Sci. 113, 91-102.
39. Yoshimura, M. and Shingyoji, C. (1999). Effects of the central pair apparatus on microtubule sliding velocity in sea urchin sperm flagella. Cell Struct. Funct. 24, 43-54.