Geometry drives the "deviated-bending" of the bi-tubular structures of the 9+2 axoneme in the flagellum

Cell Motility and the Cytoskeleton

Volumn 59, Issue 3, 2004, Pages 153-168

  Cibert, Christian ^a   Heck, Jean Vivien ^b  

^a INSTITUT JACQUES MONOD   (France)

^b Ctr Sci et Tech du Bâtiment ^*  (France)

Author keywords

Axoneme; Deviated bending; Finite elements; Microtubule; Microtubule doublet

Indexed keywords

ARTICLE; AXONEME; CELL STRUCTURE; CYTOARCHITECTURE; FINITE ELEMENT ANALYSIS; FLAGELLUM; GEOMETRY; MICROTUBULE; PRIORITY JOURNAL;

BIOMECHANICS; CELL MOVEMENT; COMPUTER SIMULATION; ELASTICITY; FLAGELLA; MICROTUBULES; MODELS, BIOLOGICAL;

EID: 7244239096     PISSN: 08861544     EISSN: None     Source Type: Journal    
DOI: 10.1002/cm.20031     Document Type: Article

References (56)

1. Amos LA, Klug A. 1974. Arrangement of subunits in flagellar microtubules. J Cell Sci 14:523-549.
2. Brokaw, C. 1996. Microtubule sliding, bend formation, and bend propagation parameters of Ciona sperm flagella altered by viscous load. Cell Motil Cystoskeleton 33:6-21.
3. Brokaw C. 1997. Transient disruption of axonemal structure an microtubule sliding during bend propagation by Ciona sperm flagella. Cell Motil Cytoskeleton 37:346-362.
4. Brokaw C. 2002. Computer simulation of flagellar movement VIII: coordination of dynein by local curvature control can generate helical bending waves. Cell Motil Cytoskeleton 53:103-124.
5. Brokaw CJ. 1989. Direct measurements of sliding between outer doublet microtubules in swimming sperm flagella. Science 243:1593-1596.
6. Brokaw CJ, Simonick T. 1977. Mechanochemical coupling in flagellar movement. V. Effect of viscosity on movement and ATP-dephosphorylation of Triton-demembranated sea urchin spermatozoa. J Cell Sci 23:227-241.
7. Burgess S. 1995. Rigor and relaxed outer dynein arms in replicas of cryofixed motile flagella. J Mol Biol 250:52-63.
8. Camalet S, Jülicher F. 2000. Generic aspects of axonemal beating. NJ Phys 2:24.21-24.23.
9. Camalet S, Jülicher F, Prost J. 1999. Self-organized beating and swimming of internally driven filaments. Phys Rev Lett 82:1590-1593.
10. Cibert C. 2001. Elastic extension and jump of the flagellar nexin links: a theoretical mechanical cycle. Cell Motil Cytoskeleton 49:161-175.
11. Cibert C. 2002. Axonemal activity relative to the 2D/3D-waveform conversion of the flagellum. Cell Motil Cytoskeleton 51:89-111.
12. Cibert C. 2003. Entropy and information in flagellar axoneme cybernetics : a radial spokes integrative function. Cell Motil Cytoskeleton 54:296-316.
13. Cosson M-P, Carré D, Cosson J. 1984. Sperm chemotaxis in siphonophores: calcium-dependent asymetrical movement of spermatozoa induced by the attractant. J Cell Sci 68:163-181.
14. Cosson M-P, Carré D, Cosson J, Sardet C. 1983. Calcium mediates sperm chemotaxis in siphonophores. J Submicrosc Cytol 15:89-93.
15. Craveur J-C. 2001. Modélisation de structures, calcul par éléments finis. Paris: Dunod.
16. Gibbons B, Gibbons I, Baccetti B. 1983. Structure and motility of the 9 + 0 flagellum of eel spermatozoa. J Submicrosc Cytol 15:15-20.
17. Gibbons I. 1975. The molecular basis of flagellar motility in sea urchin spermatozoa. In: Inoué S, Stephens R, editors. Molecular and cellular movement. New York: Raven Press. p 207-232.
18. Gibbons I. 1981. Cilia and flagella of eukaryotes. J Cell Biol 91:107s-124s.
19. Gittes F, Mickey B, Nettleton J, Howard J. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuation in shape. J Cell Biol 120:923-934.
20. Hirakawa E, Higuchi H, Toyoshima Y. 2000. Processive movement of single 22S dynein molecule occurs only at law ATP concentrations. Proc Natl Acad Sci USA 97:2533-2537.
21. Ikeba K, Brown J, Yagi T, Norrander J, Hirono M, Eccleston E, Kamiya R, Linck R. W. 2003. Rib72, a conserved protein associated with the ribbon compartment of flagellar A-microtubules and potentially involved in the linkage between outer doublet microtubules. J Biol Chem 278:7725-7734.
22. Imai H, Shingyoji C. 2003. Effects of trypsin-digested outer-arm dynein fragments on the velocity of microtubule sliding in elastase-digested flagellar axonemes. Cell Struct Funct 28:71-86.
23. Jülicher F, Prost J. 1995. Cooperative molecular motors. Phys Rev Lett 75:2618-2621.
24. Kasas S, Kis A, Riederer B, Forro L, Dietler G, Catsicas S. 2004. Mechanical properties of microtubules explored using the finite elements method. Chem Phys Chem 5:252-257.
25. Kis A, Kasas S, Babic B, Kulik AJ, Benoît W, Briggs GAD, Schönenberger C, Casticas S, Forro L. 2002. Nanomechanics of microtubules. Phys Rev Lett 89:1-4.
26. Lindemann C. 1994. A "geometric clutch" hypothesis to explain oscillations of the axoneme of cilia and flagella. J Theoret Biol 168:175-189.
27. Lindemann C. 2002. Geometric clutch model version 3: the role of the inner and outer dyneins in the ciliary beat. Cell Motil Cytoskeleton 52:242-254.
28. Lindemann C. 2003. Structural-functional relationships of the dynein, spokes, and central-pair projections predicted from an analysis of the forces acting within a flagellum. Biophys J 84:4115-4126.
29. Lindemann C, Hunt A. 2003. Does axonemal dynein push, pull or oscillate ? Cell Motil Cytoskeleton 56:237-244.
30. Lindemann C, Kanous K. 1997. A model for flagellar motility. Int Rev Cytol 173:1-72.
31. Machemer H. 1974. Ciliary activity and metachronism in protozoa. In: Sleigh MA, editor. Cilia and flagella. New York: Academic Press. p 199-286.
32. Meurer-Grob P, Kasparian J, Wade R. 2001. Microtubule structure at improved resolution. Biochemistry 40:8000-8008.
33. Minoura I, Yagi T, Kamiya R. 1999. Direct measurement of interdoublet elasticity in flagellar axonemes. Cell Struct Funct 24:27-33.
34. Mitchell D. 2003a. Orientation of the central pair complex during flagellar bend formation in Chlamydomonas. Cell Motil Cytoskeleton 56:120-129.
35. Mitchell D. 2003b. Reconstruction of the projection periodicity and surface architecture of the flagellar central pair complex. Cell Motil Cytoskeleton 55:188-199.
36. Nojima D, Linck RW, Egelman E. 1995. At least one of the protofilaments in flagellar microtubules is not composed of tubulin. Curr Biol 5:158-167.
37. Norrander J, Perrone C, Amos LA, Linck RW. 1996. Structural comparison of tektins adn evidence for their determination of complex spacings in flagellar microtubules. J Mol Biol 257:385-397.
38. Omoto C, Gibbons I, Kamiya R, Shingyoji C, Takahashi K, Witman G. 1999. Rotation of the central pair microtubules in eukaryotic flagella. Mol Biol Cell 10:1-4.
39. Prensier G, Vivier E, Goldstein S, Schrevel J. 1980. Motile flagellum with a "3 + 0" ultrastructure. Science 207:1493-1494.
40. Sakato M, King S. 2004. Design and regulation of AAA+ microtubule motor dynein. J Struct Biol 146:58-71.
41. Schoutens J. 1994. Prediction of elastic properties of sperm flagella. J Theoret Biol 171:163-177.
42. Schrevel J, Besse C. 1975. A functional flagella with a 6 + 0 pattern. J Cell Biol 66:492-507.
43. Shingyoji C, Higuchi H, Yoshimura M, Katayama R, Yanagida T. 1998. Dynein arms are oscillating force generators. Nature 293:711-714.
44. Sleigh M. 1991. Mechanism of flagella: propulsion. A biologist's view of the relation between structure, motion and fluid mechanics. Protoplasma 164:45-53.
45. Smith E. 2002. Regulation of flagellar dynein by the axonemal central apparatus. Cell Modi Cytoskeleton 52:33-42.
46. Smith E, Yang P. 2004. The radial spokes and central apparatus: Mechano-chemical transducers that regulate flagellar motility. Cell Motil Cytoskeleton 57:8-17.
47. Sugino K, Naitoh Y. 1982. Simulated cross-bridge patterns corresponding to ciliary beating in Paramecium. Nature 295:609-611.
48. Wargo MJ, Smith E. 2003. Asymmetry of the central apparatus defines the location of active microtubule sliding in Chlamidomonas flagella. Proc Natl Acad Sci USA 100:137-142.
49. Warner F. 1979. Cilia and flagella : microtubule sliding and regulated motion. In: Roberts K, Hyams J, editors. Microtubules. New York: Academic Press, Inc. p 359-380.
50. Warner F. 1983. Organization of interdoublet links in Tetrahymena cilia. Cell Motil 3:321-332.
51. Warner FD. 1976a. Ciliary inter-microtubule bridges. J Cell Sci 20:101-114.
52. Warner FD. 1976b. Cross-bridge mechanism in ciliary motility: the sliding-bending conversion. In: Goldman R, Pollard T, Rosenbaum J, editors. Cell motility. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 891-914.
53. Wolgemuth C, Powers T, Goldstein, R. 2000. Twirling and whirling : viscous dynamics of rotating elastic filaments. Phys Rev Lett 84:1623-1626.
54. Woolley D, Vernon G. 1999. Alternating torsions in a living "9+2" flagellum. Proc R Soc Lond B 266:1271-1275.
55. Woolley D, Vernon G. 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.
56. Zanetti N, Mitchell D, Warner F. 1979. Effects of divalent cations on dynein cross bridging and ciliary microtubule sliding. J Cell Biol 80:573-588.