Skip to main content

Bases moléculaires du mouvement flagellaire

Molecular basis of axonemal movement

Resume

Au cours de l’évolution, pour pouvoir se déplacer dans le milieu qui les entoure, les cellules ont développé des structures spécialisées: les cils et les flagelles. Ces structures qui produisent des successions d’ondes symétriques ou asymétriques, contiennent la même “machinerie” interne, l’axonème.

L’axonème est composé généralement de neuf doublets de microtubules externes entourant une paire centrale de microtubules. Le battement résulte d’un phénomène actif, dû à l’attachement temporaire des dynéine-ATPases d’un doublet externe au doublet adjacent. II se produit alors un glissement entre les doublets qui est transformé en courbure par les résistances de certaines structures axonémale. Les mécanismes moléculaires impliqués dans la génération du vouvement sont les même dans les cils et les flagelles, bien que les voies de contrôle de ces mécanismes puissent être différents.

Cette revue se présente en deux parties: la première est un rappel sur la composition de l’axonème incluant les récentes découvertes aux niveaux ultrastructural et biochimique, la seconde porte sur la mécanique du battement axonémal et présente le rôle de certaines des structures ou des protéines dans la génération du battement.

Abstract

Because of their small size, cells encounter fundamentally different physical constraints when they want to move in their surrounding media than when aquatic animals want to move in water. For cells, external viscosity is the main resistance while inertia plays almost no role; then in order to move, cells will have to produce continually a force against the viscous media. During the evolution, eukaryotic cells have gained specialised structures to efficiently propel them: cilia and flagella. These thread-like appendages produce repetitive beating which consists in propagation of waves from the bottom to the tip of these structures. Cilia generally show an asymmetrical beating while flagella have a more symmetrical bend propagation. Cilia and flagella contain an almost identical internal complex machinery: the axoneme. As a consequence, the mechanisms involved in the generation of the movement are identical although the precise regulation may be different.

In this paper, the reader will find a review of the molecular organisation of the ciliary and flagellar axoneme and of the role played by some of the constituting elements on the generation of the movement.

References

  1. 1.

    AFZELUIS B.A. Int. Rev. Exp. Pathology 19: 1–43, 1979.

    Google Scholar 

  2. 2.

    Afzeluis B.A., Bellon P.L., Lanzavecchia S. etDallai R.: In: Comparative Spermatology 20 Years After: The Axoneme Studied by Computeraided analysis, B. Baccetti ed., Serono Symposia, vol. 75, Raven Press New York. 315–319, 1991.

    Google Scholar 

  3. 3.

    Asai D.J., Beckwith S.M., Kandl K.A., Keating H.H., Tjandra H., etForney J.D.: J. Cell. Sci. 107: 839–847, (1994).

    PubMed  CAS  Google Scholar 

  4. 4.

    Baccetti B.: In: Biology of Fertilization, Vol. 2: Evolution of the Sperm Cell, C.B. Metz, and A. Monroy eds. Academic Press: New York, 1–58, (1985).

    Google Scholar 

  5. 5.

    Baccetti B., Burrini A.G., Pallini V., etRenieri T.: J. Cell Biol. 88: 102–107. 1980.

    Article  Google Scholar 

  6. 6.

    Barkalow K., Avolio J, Holwill M.E.J., Hamasaki T., etSatir P. (1994): Cell. Motil. Cytoskel. 27: 299–312.

    CAS  Article  Google Scholar 

  7. 7.

    Bedford J.M., etHoskins D.D.: In: Marshall’s Physiology of Reproduction, vol. 2: The Mammalian Spermatozoon, G.E. Lamming ed. Churchill Livingstone, London. 379–569, 1990.

    Google Scholar 

  8. 8.

    Bell C.W., Fronk E., etGibbons I.R.: J. Supramol. Struct. 11: 311–317, 1979.

    PubMed  CAS  Article  Google Scholar 

  9. 9.

    Berstein M., Beech P.L., Gatz S.G., etRosenbaum J.L.: J. Cell. Biol. 125: 1113–1326, 1994.

    Google Scholar 

  10. 10.

    Bozkurt H.H., etWoolley D.M.: Cell Motil. Cytoskel., 24: 109–118. 1993.

    CAS  Article  Google Scholar 

  11. 11.

    Bray D.: Cell Movements. Garland Publishing, New York. 1992.

    Google Scholar 

  12. 12.

    Brokaw C.J.: In: Cell Movement, Vol. 1: Operation and Regulation of the Flagellar Oscillator, F.D. Warner, P. Satir, et I.R. Gibbons eds: Alan R. Liss, New York. 121–140, 1989a

    Google Scholar 

  13. 13.

    Brokaw C.J.: Science 243:1593–1596, 1989b.

    PubMed  CAS  Article  Google Scholar 

  14. 14.

    Brokaw C.J.: Cell. Motil. Cytoskel. 28: 199–204, 1994.

    CAS  Article  Google Scholar 

  15. 15.

    Burfeind, P., etHoyer-Fender, S.: Dev. Biol. 148: 195–204. 1991.

    PubMed  CAS  Article  Google Scholar 

  16. 16.

    Burns R.G., etSurridge C.D. In: Microtubules: Tubulin: Conservation and Structure, J.S. Hyams, et C.W. Lloyd, eds. Wiley-Liss, New York. 3–32, 1994.

    Google Scholar 

  17. 17.

    Carrera A., Gerton G.L., etMoss S.B.: Dev. Biol. 165: 272–284, 1994.

    PubMed  CAS  Article  Google Scholar 

  18. 18.

    Chilcote T.J., etJohnson K.A.: J. Biol. Chem. 265: 17257–17266, 1990.

    PubMed  CAS  Google Scholar 

  19. 19.

    Cosson, J Biol. Cell, 76: 319–327, 1992.

    CAS  Article  Google Scholar 

  20. 20.

    Curry A.M., Williams B.D., etRosembaum J.L.: Mol. Cell. Biol. 12: 3967–3977, 1992.

    PubMed  CAS  Google Scholar 

  21. 21.

    Deiner D.R., Ang L.H., etRosembaum J.L.: J. Cell. Biol., 123: 183–190, 1993.

    Article  Google Scholar 

  22. 22.

    Dey C.S., etBrokaw C.J.: J. Cell. Sci., 100: 815–824, 1991.

    PubMed  CAS  Google Scholar 

  23. 23.

    Feneux D., Serres C., etJouannet P.: Fertil. Steril. 44: 508–511, 1985.

    PubMed  CAS  Google Scholar 

  24. 24.

    Fox L.A., etSale W.F.: J. Cell. Biol. 105:1781–1787, 1987.

    PubMed  CAS  Article  Google Scholar 

  25. 25.

    Fox L.A., Sawin K.E., etSale W.F.: J. Cell. Sci. 107:1545–1550, 1994.

    PubMed  CAS  Google Scholar 

  26. 26.

    Gatti J.-L., King S.M., Moss A.G., etWitman G.B. J. Biol. Chem. 264: 11450–11457, 1989.

    PubMed  CAS  Google Scholar 

  27. 27.

    Gatti J.-L., King S.M., etWitman G.B.: In: Comparative Spermatology 20 Years After: The ATPases of Chlamydomonas Outer Arm Dynein Differ in Their pH and Cationic Requirements, B. Baccetti ed., Serono Symposia, vol 75, Raven Press, New York. 373–375, 1991.

    Google Scholar 

  28. 28.

    Gepner J., etHays T.S.: Proc. Natl. Acad. Sci. USA, 90: 11132–11136, 1993.

    PubMed  CAS  Article  Google Scholar 

  29. 29.

    Gibbons B.H., etGibbons I.R.: J. Cell Sci. 13: 337–357, 1973.

    PubMed  CAS  Google Scholar 

  30. 30.

    Gibbons B.H., Gibbons I.R, etBaccetti B.: J. Submicrosc. Cytol. 15: 15–20, 1983.

    PubMed  CAS  Google Scholar 

  31. 31.

    Gibbons B.H., Gibbons I.R., Mocz G., etAsai D.J.: Nature 352: 640–643, 1991.

    PubMed  CAS  Article  Google Scholar 

  32. 32.

    Gibbons I.R., Asai D.J., Tang W-J.Y., etGibbons B.H.: Biol. Cell 76: 303–309, 1992.

    PubMed  CAS  Article  Google Scholar 

  33. 33.

    Goodenough U.W., etHeuser J.E.: In: Cell Movement Vol. 1: Structure of the Soluble and In-Situ Ciliary Dyneins Visualized by Quick-Freeze Deep-Etch microscopy, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York. 121–140, 1989.

    Google Scholar 

  34. 34.

    Greer K., etRosenbaum, J.L.: In: Cell Movement, Vol. 2: Post-translational Modifications of Tubulin, F.D. Warner, et J.R. MacIntoch eds. Alan R. Liss, New York. 47–66, 1989.

    Google Scholar 

  35. 35.

    Hamasaki T., Barkalow K., Richmond J., etSatir P.: Proc. Natl. Acad. Sci. USA 88: 7978–7922. 1991.

    Article  Google Scholar 

  36. 36.

    Henkel, R., Stalf T., Mertens, N., Miska, W., etSchill, W.-B.: Int. J. Androl. 17: 68–73, 1994.

    PubMed  CAS  Article  Google Scholar 

  37. 37.

    Holwill M.E.: In: Cell Movement, Vol. 1: Biophysical Properties of the Sliding Filement Mechanism, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York. 61–75, 1989.

    Google Scholar 

  38. 38.

    Horst C.J., etWitman G.B.: J. Cell. Biol. 120: 733–741, 1993.

    PubMed  CAS  Article  Google Scholar 

  39. 39.

    Huang B., Ramanis Z., Piperno G., etLuck D.J.L.: J. Cell. Biol. 88: 80–88, 1981.

    PubMed  CAS  Article  Google Scholar 

  40. 40.

    Ishijima S., Sekiguchi K., etHiramoto Y.: Cell. Motil. Cytoskel. 9: 264–270, 1988.

    Article  Google Scholar 

  41. 41.

    Johnson K.A., etWall J.S.: J. Cell. Biol. 96: 669–678, 1983.

    PubMed  CAS  Article  Google Scholar 

  42. 42.

    Johnson K.A., Haas M.A., etRosenbaum J.L.: J. Cell. Sci. 107: 1551–1556, 1994.

    PubMed  CAS  Google Scholar 

  43. 43.

    Jouannet P., Escalier D., Serres C., etDavid G.: J. Submicrosc. Cytol. 15: 67–71, 1983.

    PubMed  CAS  Google Scholar 

  44. 44.

    Kagami O., etKamiya R.: Eur. J. Biochem. 187: 441–446, 1990.

    Article  Google Scholar 

  45. 45.

    Kagami O., etKamiya R.: J. Cell. Sci. 103: 653–664, 1992.

    CAS  Google Scholar 

  46. 46.

    Kamiya, R., etHasegawa, E.: Exp. Cell Res. 173: 229–304, 1987.

    Article  Google Scholar 

  47. 47.

    Kamiya R., Kurimoto E., Sakakibara H., etOkagaki T.: In Cell Movement, Vol. 1: A Genetic Approach to the Function of Inner and Outer Arm Dyneins, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York. 209–218, 1989.

    Google Scholar 

  48. 48.

    Kamiya R., Kurimoto E., etMuto E.: J. Cell. Biol. 112: 441–447, 1991.

    PubMed  CAS  Article  Google Scholar 

  49. 49.

    King S.M., etWitman G.B.: In: Cell Movement, Vol. 1: Molecular Structure of Chlamydomonas Outer Arm Dyneins, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York, 61–75, 1989.

    Google Scholar 

  50. 50.

    King S.M., Gatti J.-L., Moss A.G., etWitman G.B.: Cell Motil. Cytoskel. 16: 266–278, 1990.

    CAS  Article  Google Scholar 

  51. 51.

    King S.M., Wilkerson C.G., etWitman G.B.: J. Biol. Chem. 266: 8401–8407, 1990.

    Google Scholar 

  52. 52.

    King S.M., etWitman G.B.: J. Biol. Chem. 269: 5452–5457, 1994.

    PubMed  CAS  Google Scholar 

  53. 53.

    Kurimoto E., etKamiya R.: Cell Motil. Cytoskel. 19: 275–281, 1991.

    CAS  Article  Google Scholar 

  54. 54.

    Lieberman S.J., Wasco W., Macleod J., Paupard M.-C. etOrr G.A.: J. Cell. Biol. 107: 1809–1816, 1988.

    PubMed  CAS  Article  Google Scholar 

  55. 55.

    Lindemann C.B., etKanous K.S.: Arch. Androl. 23: 1–22, 1990.

    Article  Google Scholar 

  56. 56.

    Lindemann C.B., Orlando A., etKanous K.S.: J. Cell Sci. 102: 249–260, 1992.

    PubMed  CAS  Google Scholar 

  57. 57.

    Lindemann C.B.: Cell Motil. Cytoskel. 29: 141–154, 1994.

    CAS  Article  Google Scholar 

  58. 58.

    Luck, D.J.L.: J. Cell. Biol. 98: 789–794, 1984.

    PubMed  CAS  Article  Google Scholar 

  59. 59.

    Marchese-Ragona S.P., etJohnson K.A.: Electron Microsc. Rev. 1: 141–153, 1988.

    PubMed  CAS  Google Scholar 

  60. 60.

    Mastronarde D.N., O’Toole E.T., McDonald K.L., McIntoch J.R., etPorter M.E.: J. Cell. Biol. 118: 1145–1162, 1992.

    PubMed  CAS  Article  Google Scholar 

  61. 61.

    Mendelkow E., etMendelkow E.M.: Curr. Opin. Struct. Biol. 4: 171–179, 1994.

    Article  Google Scholar 

  62. 62.

    Merlino G.T., Stahle C., Linton R., Mahon K.A., etWillingham M.C.: Genes & Dev. 5: 1395–1406, 1991.

    CAS  Article  Google Scholar 

  63. 63.

    Mitchell D.R., etRosenbaum J.L.: J. Cell. Biol. 100: 1228–1234, 1985.

    PubMed  CAS  Article  Google Scholar 

  64. 64.

    Mitchell D.R, etRosenbaum J.L.: Cell Motil. Cytoskel. 6: 510–520, 1986.

    CAS  Article  Google Scholar 

  65. 65.

    Mitchell D.R., etKang Y.: J. Cell. Biol. 113: 835–842, 1991.

    PubMed  CAS  Article  Google Scholar 

  66. 66.

    Mitchell D.R., etKang Y.: J. Cell. Sci. 105: 1069–1078, 1993.

    PubMed  CAS  Google Scholar 

  67. 67.

    Mitchell D.R., etBrown K.S.: J. Cell. Sci., 107: 635–644, 1994.

    PubMed  CAS  Google Scholar 

  68. 68.

    Moss A.G., Gatti J.-L., etWitman G.B.: J. Cell. Biol. 118: 1177–1188, 1992 (a).

    PubMed  CAS  Article  Google Scholar 

  69. 69.

    Moss A.G., Sale W.S., Fox L.A., etWitman G.B.: J. Cell. Biol. 118: 1189–1200, 1992 (b).

    PubMed  CAS  Article  Google Scholar 

  70. 70.

    Multigner L., Gagnon J., Van Dorsselaer A. etJob D.: Nature 360: 33–39, 1992.

    PubMed  CAS  Article  Google Scholar 

  71. 71.

    Muto E., Kamiya R., etTsukita S.: J. Cell Sci., 99: 57–66, 1991.

    Google Scholar 

  72. 72.

    Norrander J.M., etLink R.W.: In: Microtubules: Tektins, J.S. Hyams et Lloyd C.W. eds. Wiley-Liss, New York. p 201–220 1994

    Google Scholar 

  73. 73.

    Ogawa K.: Nature, 352: 643–645, 1991.

    PubMed  CAS  Article  Google Scholar 

  74. 74.

    Olson G.E. In: The Spermatozoon: Isolation of the Fibrous Sheath and Perforatorium of Rat Spermatozoa, D.W. Fawcett et J.M. Bedford eds, Urban-Schwarzenberg, Baltimore, p 395–400, 1979

    Google Scholar 

  75. 75.

    Omoto C.K., etWitman G.B.: Nature 288: 708–710 1981.

    Article  Google Scholar 

  76. 76.

    Otter T.: In: Cell Movement, Vol. 1: Calmodulin and the Control of Flagellar Movement, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York. p 281–298, 1989

    Google Scholar 

  77. 77.

    Paschal B.M., Mikami A., Pfister K.K., etVallee R.B.: J. Cell. Biol. 118: 1133–1143, 1992.

    PubMed  CAS  Article  Google Scholar 

  78. 78.

    Paturle-Lafanechere L., Manier M., Trigault N., Pirollet F., Mazarguil H., etJob D: J. Cell Sci. 107: 1529–1543, 1994.

    PubMed  CAS  Google Scholar 

  79. 79.

    Peirera A., etGoldstein L.S.B.: In: Microtubules: The Kinesin Superfamily, J.S. Hyams et Lloyd C.W. eds. Wiley-Liss, New York. p 229–249, 1994.

    Google Scholar 

  80. 80.

    Pilder S.H., Olds-Clarke P., Phillips D.M., etSilver L.M.: Dev. Biol. 159: 631–642, 1993.

    PubMed  CAS  Article  Google Scholar 

  81. 81.

    Piperno G.: Cell Motil. Cytoskel. 17: 147–149, 1990.

    CAS  Article  Google Scholar 

  82. 82.

    Piperno G., etLuck, D.J.L.: J. Biol. Chem., 254: 2187–219, 1990.

    Google Scholar 

  83. 83.

    Piperno G., Ramanis, Z., Smith, E.F., etSale, W.S.: J. Cell. Biol. 110: 379–389, 1990.

    PubMed  CAS  Article  Google Scholar 

  84. 84.

    Piperno G., etRamanis Z.: J. Cell. Biol. 112: 701–709, 1991.

    PubMed  CAS  Article  Google Scholar 

  85. 85.

    Piperno G., Mead C., LeDizet M., etMoscatelli A.: J. Cell. Biol. 125: 1109–1117, 1994.

    PubMed  CAS  Article  Google Scholar 

  86. 86.

    Porter M.E., etJohnson K.A.: J. Biol. Chem. 258: 6575–658, 1983.

    PubMed  CAS  Google Scholar 

  87. 87.

    Porter M.E., Power J., etDutcher S.K.: J. Cell. Biol. 118: 1163–1176, 1992.

    PubMed  CAS  Article  Google Scholar 

  88. 88.

    Porter, M.E., Knott, J.A., Gardner, L.C., Mitchell, D.R., etDutcher S.K.: J. Cell. Biol. 126, 1495–1507, 1994.

    PubMed  CAS  Article  Google Scholar 

  89. 89.

    Sakakibara H., Mitchell D.R., etKamiya R.: J. Cell. Biol. 113: 615–622, 1991.

    PubMed  CAS  Article  Google Scholar 

  90. 90.

    Sakakibara H., Takada S., King S.M., Witman G.B. etKamiya R.: J. Cell. Biol. 122: 653–661 1993.

    PubMed  CAS  Article  Google Scholar 

  91. 91.

    Sale W.S.: J. Cell. Biol. 102: 2042–2052, 1986.

    PubMed  CAS  Article  Google Scholar 

  92. 92.

    Sale W.S., Fox L.A., etMilgram S.L.: In: Cell Movement, Vol. 1: Composition and Organization of the Inner Row Dynein Arms, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York. p 89–102, 1989.

    Google Scholar 

  93. 93.

    Satir P.: Comp. Biochem. Phys. 94A: 351–357, 1989.

    Google Scholar 

  94. 94.

    Serres C., Feneux D., etJouannet P.: Cell Motil. Cytoskel. 6: 68–76, 1986.

    CAS  Article  Google Scholar 

  95. 95.

    Smith, E.F., etSale, W.S. (1991): Cell Motil. Cytoskel., 18: 258–268.

    CAS  Article  Google Scholar 

  96. 96.

    Smith E.F., etSale W.S: Science 257:1557–1559, 1992.

    PubMed  CAS  Article  Google Scholar 

  97. 97.

    Smith E.F., etSale W.S.: In: Microtubules: Mechanisms of Flagellar Movement, J.S. HYAMS et C.W. LLOYD eds, WILEY-LISS, New York. p 381–392, 1994.

    Google Scholar 

  98. 98.

    STEPHENS R.E.: In: Molecules and Cell Movement: Structural Chemistry of the Axoneme, S. INOUE et R.E. STEPHENS eds, RAVEN Press, New York. p 181–206, 1975.

    Google Scholar 

  99. 99.

    Stephens R.E., etPrior G.: J. Cell. Sci. 103: 999–1012, 1992.

    PubMed  CAS  Google Scholar 

  100. 100.

    Tadaka S, etKamiya, R.: J. Cell. Biol., 126: 737–745, 1994.

    Article  Google Scholar 

  101. 101.

    Tamm S.L., etTerasaki M.: J. Cell. Biol. 125: 1127–1135, 1994.

    PubMed  CAS  Article  Google Scholar 

  102. 102.

    Tang W.-J.Y., Bell C.W., Sale W.S. etGibbons I.R.: J. Biol. Chem. 262: 17728–17734, 1982.

    Google Scholar 

  103. 103.

    Vale R., etToyoshima Y.Y.: Cell 52: 459–469, 1988.

    PubMed  CAS  Article  Google Scholar 

  104. 104.

    Vale R., etToyoshima Y.Y.: J. Cell Biol. 108: 2327–2334, 1989.

    PubMed  CAS  Article  Google Scholar 

  105. 105.

    Vera J.C., Brito M., Zuvic T., etBurzio L.O.: J. Biol. Chem. 259: 5970–5977, 1984.

    PubMed  CAS  Google Scholar 

  106. 106.

    Wada S., Okuno M., Nakamura K.-I., etMohri H.: Biol. Cell 76, 311–317, 1992.

    CAS  Article  Google Scholar 

  107. 107.

    Walczak C.E. etNelson D.L.: J. Cell. Sci. 106: 1369–1376, 1993.

    PubMed  CAS  Google Scholar 

  108. 108.

    Walther Z., Vashishtha M., etHall J.L.: J. Cell. Biol.126: 175–188, 1994.

    PubMed  CAS  Article  Google Scholar 

  109. 109.

    Wilkerson C.G., King S.M., etWitman G.B.: J. Cell Sci. 107: 497–506, 1994.

    PubMed  CAS  Google Scholar 

  110. 110.

    Williams B.D., Curry A.M., etRosembaum J.L.: J. Cell. Biol. 109: 235–245, 1989.

    PubMed  CAS  Article  Google Scholar 

  111. 111.

    Witman G.B.: In: Cell Movement, Vol. 1: Composition and Molecular Organization of the Dyneins, F.D. Warner, P. Satir, et I.R. Gibbons eds. Alan R. Liss, New York. p 25–35, 1989.

    Google Scholar 

  112. 112.

    Witman G.B.: In: Ciliary and Flagellar Membranes: Introduction to Cilia and Flagella, R.A. BLOODGOOD ed. PLENUM PRESS, New York. p 1–30, 1990.

    Google Scholar 

  113. 113.

    Witman G.B., Plummer J., etSander, G.: J. Cell. Biol. 76: 729–747, 1978.

    PubMed  CAS  Article  Google Scholar 

  114. 114.

    Witman G.B., Wilkerson C.G., etKing S.M.: In: Microtubules: The Biochemistry, Genetics, and Molecular Biology of Flagellar dynein, J.S. HYAMS et C.W. LLOYD eds, WILEY-LISS, New York. Wiley-Liss New York. p 229–249, 1994.

    Google Scholar 

  115. 115.

    Yokota E., etMabuchi I.: J. Cell Sci. 107: 345–351, 1994.

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to J-L Gatti.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gatti, J., Dacheux, J. Bases moléculaires du mouvement flagellaire. Androl. 5, 15–30 (1995). https://doi.org/10.1007/BF03034299

Download citation

Mots clés

  • flagelles
  • cils
  • dyneines
  • battement flagellaire
  • spermatozoïdes

Key words

  • axoneme
  • dynein
  • cilia
  • flagella
  • spermatozoa
  • movement