Axoneme β-Tubulin Sequence Determines Attachment of Outer Dynein Arms

Current Biology

Volumn 18, Issue 12, 2008, Pages 911-914

  Raff, Elizabeth C ^a   Hoyle, Henry D ^a   Popodi, Ellen M ^a   Turner, F Rudolf ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

CELLBIO

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; GLYCINE; TUBULIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; AXONEME; CHEMISTRY; COMPUTER ASSISTED TOMOGRAPHY; DROSOPHILA; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN CONFORMATION; SPERMATOGENESIS; SPERMATOZOON; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; AXONEME; DROSOPHILA; DYNEINS; GLYCINE; MALE; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SPERMATOGENESIS; SPERMATOZOA; TOMOGRAPHY, X-RAY COMPUTED; TUBULIN;

EUKARYOTA;

EID: 45449095354     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2008.05.031     Document Type: Article

References (38)

1. Wickstead B., and Gull K. Dyneins across eukaryotes: A comparative genomic analysis. Traffic 8 (2007) 1708-1721
2. Takada S., and Kamiya R. Functional reconstitution of Chlamydomonas outer dynein arms from alpha-beta and gamma subunits: Requirement of a third factor. J. Cell Biol. 126 (1994) 737-745
3. Nicastro D., Schwartz C., Pierson J., Gaudette R., Porter M.E., and McIntosh J.R. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313 (2006) 944-948
4. Sui H., and Downing K.H. Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature 442 (2006) 475-478
5. Ishikawa T., Sakakibara H., and Oiwa K. The architecture of outer dynein arms in situ. J. Mol. Biol. 368 (2007) 1249-1258
6. Nogales E., Wolf S.G., and Downing K.H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391 (1998) 199-203
7. Oda T., Hirokawa N., and Kikkawa M. Three-dimensional structures of the flagellar dynein-microtubule complex by cryoelectron microscopy. J. Cell Biol. 177 (2007) 243-252
8. Meurer-Grob P., Kasparian J., and Wade R.H. Microtubule structure at improved resolution. Biochemistry 40 (2001) 8000-8008
9. Satir P. Studies on cilia. 3. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J. Cell Biol. 39 (1968) 77-94
10. Gee M.A., Heuser J.E., and Vallee R.B. An extended microtubule-binding structure within the dynein motor domain. Nature 390 (1997) 636-639
11. Audebert S., White D., Cosson J., Huitorel P., Edde B., and Gagnon C. The carboxy-terminal sequence Asp427-Glu432 of beta-tubulin plays an important function in axonemal motility. Eur. J. Biochem. 261 (1999) 48-56
12. Vent J., Wyatt T.A., Smith D.D., Banerjee A., Luduena R.F., Sisson J.H., and Hallworth R. Direct involvement of the isotype-specific C-terminus of beta tubulin in ciliary beating. J. Cell Sci. 118 (2005) 4333-4341
13. Takada S., Wilkerson C.G., Wakabayashi K., Kamiya R., and Witman G.B. The outer dynein arm-docking complex: Composition and characterization of a subunit (oda1) necessary for outer arm assembly. Mol. Biol. Cell 13 (2002) 1015-1029
14. Ushimaru Y., Konno A., Kaizu M., Ogawa K., Satoh N., and Inaba K. Association of a 66 kDa homolog of Chlamydomonas DC2, a subunit of the outer arm docking complex, with outer arm dynein of sperm flagella in the ascidian Ciona intestinalis. Zoolog. Sci. 23 (2006) 679-687
15. Freshour J., Yokoyama R., and Mitchell D.R. Chlamydomonas flagellar outer row dynein assembly protein ODA7 interacts with both outer row and I1 inner row dyneins. J. Biol. Chem. 282 (2007) 5404-5412
16. Koutoulis A., Pazour G.J., Wilkerson C.G., Inaba K., Sheng H., Takada S., and Witman G.B. The Chlamydomonas reinhardtii ODA3 gene encodes a protein of the outer dynein arm docking complex. J. Cell Biol. 137 (1997) 1069-1080
17. Wakabayashi K., Takada S., Witman G.B., and Kamiya R. Transport and arrangement of the outer-dynein-arm docking complex in the flagella of Chlamydomonas mutants that lack outer dynein arms. Cell Motil. Cytoskeleton 48 (2001) 277-286
18. Sullivan K.F. Structure and utilization of tubulin isotypes. Annu. Rev. Cell Biol. 4 (1988) 687-716
19. Fackenthal J.D., Turner F.R., and Raff E.C. Tissue-specific microtubule functions in Drosophila spermatogenesis require the β2-tubulin isotype-specific carboxy terminus. Dev. Biol. 158 (1993) 213-227
20. Hoyle H.D., Hutchens J.A., Turner F.R., and Raff E.C. Regulation of beta-tubulin function and expression in Drosophila spermatogenesis. Dev. Genet. 16 (1995) 148-170
21. Raff E.C., Fackenthal J.D., Hutchens J.A., Hoyle H.D., and Turner F.R. Microtubule architecture specified by a beta-tubulin isoform. Science 275 (1997) 70-73
22. Hoyle H.D., Turner F.R., Brunick L., and Raff E.C. Tubulin sorting during dimerization in vivo. Mol. Biol. Cell 12 (2001) 2185-2194
23. Nielsen M.G., Turner F.R., Hutchens J.A., and Raff E.C. Axoneme-specific beta-tubulin specialization: A conserved C-terminal motif specifies the central pair. Curr. Biol. 11 (2001) 529-533
24. Popodi E.M., Hoyle H.D., Turner F.R., and Raff E.C. The proximal region of the beta-tubulin C-terminal tail is sufficient for axoneme assembly. Cell Motil. Cytoskeleton 62 (2005) 48-64
25. Popodi E.M., Hoyle H.D., Turner F.R., Xu K., Kruse S., and Raff E.C. Axoneme specialization embedded in a "Generalist" beta-tubulin. Cell Motil. Cytoskeleton 65 (2008) 216-237
26. Fackenthal J.D., Hutchens J.A., Turner F.R., and Raff E.C. Structural analysis of mutations in the Drosophila β2-tubulin isoform reveals regions in the beta-tubulin molecule required for general and for tissue-specific microtubule functions. Genetics 139 (1995) 267-286
27. Fuller M.T., Caulton J.H., Hutchens J.A., Kaufman T.C., and Raff E.C. Mutations that encode partially functional beta 2 tubulin subunits have different effects on structurally different microtubule arrays. J. Cell Biol. 107 (1988) 141-152
28. Wilkerson C.G., King S.M., Koutoulis A., Pazour G.J., and Witman G.B. The 78,000 M(r) intermediate chain of Chlamydomonas outer arm dynein is a WD-repeat protein required for arm assembly. J. Cell Biol. 129 (1995) 169-178
29. Nogales E., Whittaker M., Milligan R.A., and Downing K.H. High-resolution model of the microtubule. Cell 96 (1999) 79-88
30. Vaughan S., Shaw M., and Gull K. A post-assembly structural modification to the lumen of flagellar microtubule doublets. Curr. Biol. 16 (2006) R449-R450
31. Gibbons B.H., Gibbons I.R., and Baccetti B. Structure and motility of the 9 + 0 flagellum of eel spermatozoa. J. Submicrosc. Cytol. 15 (1983) 15-20
32. Afzelius B.A., Bellon P.L., Dallai R., and Lanzavecchia S. Diversity of microtubular doublets in insect sperm tails: A computer-aided image analysis. Cell Motil. Cytoskeleton 19 (1991) 282-289
33. Hyams J.S., and Campbell C.J. Widespread absence of outer dynein arms in the spermatozoids of lower plants. Cell Biol. Int. Rep. 9 (1985) 841-848
34. Renzaglia K.S., and Garbary D.J. Motile gametes of land plants: Diversity, development, and evolution. Crit. Rev. Plant Sci. 20 (2001) 107-213
35. Rensing S.A., Lang D., Zimmer A.D., Terry A., Salamov A., Shapiro H., Nishiyama T., Perroud P.F., Lindquist E.A., Kamisugi Y., et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319 (2008) 64-69
36. Rudolph J.E., Kimble M., Hoyle H.D., Subler M.A., and Raff E.C. Three Drosophila beta-tubulin sequences: A developmentally regulated isoform (beta 3), the testis-specific isoform (beta 2), and an assembly-defective mutation of the testis-specific isoform (B2t8) reveal both an ancient divergence in metazoan isotypes and structural constraints for beta-tubulin function. Mol. Cell. Biol. 7 (1987) 2231-2242
37. Michiels F., Falkenburg D., Muller A.M., Hinz U., Otto U., Bellmann R., Glatzer K.H., Brand R., Bialojan S., and Renkawitz-Pohl R. Testis-specific beta 2 tubulins are identical in Drosophila melanogaster and D. hydei but differ from the ubiquitous beta 1 tubulin. Chromosoma 95 (1987) 387-395
38. Hoyle H.D., and Raff E.C. Two Drosophila beta tubulin isoforms are not functionally equivalent. J. Cell Biol. 111 (1990) 1009-1026