Molecular architecture of inner dynein arms in situ in Chlamydomonas reinhardtii flagella

Journal of Cell Biology

Volumn 183, Issue 5, 2008, Pages 923-932

  Bui, Khanh Huy ^a   Sakakibara, Hitoshi ^b   Movassagh, Tandis ^a   Oiwa, Kazuhiro ^b,c   Ishikawa, Takashi ^a  

^a ETH ZURICH   (Switzerland)

^b NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^c UNIVERSITY OF HYOGO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; DYNEIN ADENOSINE TRIPHOSPHATASE; MUTANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; AXONEME; CHLAMYDOMONAS REINHARDTII; CRYOELECTRON TOMOGRAPHY; EUKARYOTE; FLAGELLUM; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TOMOGRAPHY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; ENZYMOLOGY; GENETICS; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

CHLAMYDOMONAS REINHARDTII; EUKARYOTA;

ANIMALS; CHLAMYDOMONAS REINHARDTII; CRYOELECTRON MICROSCOPY; DYNEIN ATPASE; ELECTRON MICROSCOPE TOMOGRAPHY; FLAGELLA; MICROTUBULES; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 58149291884     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200808050     Document Type: Article

References (46)

1. Avolio, J., A.N. Glazzard, M.E. Holwill, and P. Satir. 1986. Structures attached to doublet microtubules of cilia: computer modeling of thin-section and negative-stain stereo images. Proc. Natl. Acad. Sci. USA. 83:4804-4808.
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. Burgess, S.A., D.A. Carter, S.D. Dover, and D.M. Woolley. 1991. The inner dy-nein arm complex: compatible images from freeze-etch and thin section methods of microscopy. J. Cell Sci. 100:319-328.
4. Burgess, S.A., M.L. Walker, H. Sakakibara, P.J. Knight, and K. Oiwa. 2003. Dynein structure and power stroke. Nature. 421:715-718.
5. Burgess, S.A., M.L. Walker, H. Sakakibara, H. Oiwa, and P.J. Knight. 2004. The structure of dynein-c by negative stain electron microscopy. J. Struct. Biol. 146:205-216.
6. Dymek, E.E., and E.F. Smith. 2007. A conserved CaM- and radial spoke associated complex mediates regulation of flagellar dynein activity. J. Cell Biol. 179:515-526.
7. Frank, J., M. Radermacher, P. Penczek, J. Zhu, Y.H. Li, M. Ladjadj, and A. Leith. 1996. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116:190-199.
8. Gardner, L.C., E. O'Toole, C.A. Perrone, T. Giddings, and M.E. Porter. 1994. Components of a "dynein regulatory complex" are located at the junction between the radial spokes and the dynein arms in Chlamydomonas flagella. J. Cell Biol. 127:1311-1325.
9. Goodenough, U., and J. Heuser. 1984. Structural comparison of purified dynein proteins with in situ dynein arms. J. Mol. Biol. 180:1083-1118.
10. Goodenough, U.W., and J. Heuser. 1985. Substructure of inner dynein arms, radial spokes, and the central pair/projection complex of cilia and flagella. J. Cell Biol. 100:2008-2018.
11. Gorman, D.S., and R.P. Levine. 1965. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA. 54:1665-1669.
12. Hendrickson, T.W., C.A. Perrone, P. Griffin, K. Wuichet, J. Mueller, P. Yang, M.E. Porter, and W.S. Sale. 2004. IC138 is a WD-repeat dynein intermediate chain required for light chain assembly and regulation of flagellar bending. Mol. Biol. Cell. 15:5431-5442.
13. Heymann, J.B. 2001. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133:156-169.
14. Ishikawa, T., H. Sakakibara, and K. Oiwa. 2007. The architecture of outer dynein arms in situ. J. Mol. Biol. 368:1249-1258.
15. Johnson, K.A., and J.S. Wall. 1983. Structure and molecular weight of the dynein ATPase. J. Cell Biol. 96:669-678.
16. Kagami, O., and R. Kamiya. 1992. Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J. Cell Sci. 103:653-664.
17. Kamiya, R. 1988. Mutations at twelve independent loci result in absence of outer dynein arms in Chlamydomonas reinhardtii. J. CellBiol. 107:2253-2258.
18. Kamiya, R. 2002. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int. Rev. Cytol. 219:115-155.
19. Kamiya, R., E. Kurimoto, and E. Muto. 1991. Two types of Chlamydomonas fiagellar mutants missing different components of inner-arm dynein. J. Cell Biol. 112:441-447.
20. Kato, T., O. Kagami, T. Yagi, and R. Kamiya. 1993. Isolation of two species of Chlamydomonas reinhardtii ffagellar mutants, ida5 and ida6, that lack a newly identified heavy chain of the inner dynein arm. Cell Struct. Funct. 18:371-377.
21. Kikushima, K., and R. Kamiya. 2008. Clockwise translocation of microtubules by ffagellar inner-arm dyneins in vitro. Biophys. J. 94:4014-4019.
22. King, S.M., and R. Kamiya. 2008. Axonemal dyneins: assembly, structure, and force generation. In Chlamydomonas Sourcebook, Vol. 3. Cell Motility and Behavior. G. Witman, editor. Elsevier Press, Amsterdam. In press.
23. Kotani, N., H. Sakakibara, S.A. Burgess, H. Kojima, and K. Oiwa. 2007. Mechanical properties of inner-arm dynein-f (dynein I1) studied with in vitro motility assays. Biophys. J. 93:886-894.
24. Kremer, J.R., D.N. Mastronarde, and J.R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
25. LeDizet, M., and G. Piperno. 1995. The light chain p28 associates with a subset of inner dynein arm heavy chains in Chlamydomonas axonemes. Mol. Biol. Cell. 6:697-711.
26. Lupetti, P., S. Lanzavecchia, D. Mercati, F. Cantele, R. Dallai, and C. Mencarelli. 2005. Three-dimensional reconstruction of axonemal outer dynein arms in situ by electron tomography. Cell Motil. Cytoskeleton. 62:69-83.
27. Mastronarde, D.N. 1997. Dual-axis tomography: an approach with alignment methods that preserve resolution. J. Struct. Biol. 120:343-352.
28. Mastronarde, D.N., E.T. O'Toole, K.L. McDonald, J.R. McIntosh, and M.E. Porter. 1992. Arrangement of inner dynein arms in wild-type and mutant fiagella of Chlamydomonas. J. Cell Biol. 118:1145-1162.
29. Nicastro, D., J.R. McIntosh, and W. Baumeister. 2005. 3D structure of eukaryotic fiagella in a quiescent state revealed by cryo-electron tomography. Proc. Natl. Acad. Sci. USA. 102:15889-15894.
30. Nicastro, D., C. Schwartz, J. Pierson, R. Gaudette, M.E. Porter, and J.R. McIntosh. 2006. The molecular architecture of axonemes revealed by cryoelectron tomography. Science. 313:944-948.
31. Nickell, S., F. Förster, A. Linaroudis, W.D. Net, F. Beck, R. Hegerl, W. Baumeister, and J.M. Plitzko. 2005. TOM software toolbox: acquisition and analysis for electron tomography. J. Struct. Biol. 149:227-234.
32. Oda, T., N. Hirokawa, and M. Kikkawa. 2007. Three-dimensional structures of the flagellar dynein-microtubule complex by cryoelectron microscopy. J. CellBiol. 177:243-252.
33. Perrone, C.A., S.H. Myster, R. Bower, E.T. O'Toole, and M.E. Porter. 2000. Insights into the structural organization of the I1 inner arm dynein from a domain analysis of the 1beta dynein heavy chain. Mol. Biol. Cell. 11:2297-2313.
34. Pettersen, E.F., T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin. 2004. UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
35. Piperno, G., Z. Ramanis, E.F. Smith, and W.S. Sale. 1990. Three distinct inner dynein arms in Chlamydomonas flagella: molecular composition and location in the axoneme. J. Cell Biol. 110:379-389.
36. Piperno, G., K. Mead, and W. Shestak. 1992. The inner dynein arms I2 interact with a "dynein regulatory complex" in Chlamydomonas flagella. J. Cell Biol. 118:1455-1463.
37. Piperno, G., K. Mead, M. LeDizet, and A. Moscatelli. 1994. Mutations in the "dynein regulatory complex" alter the ATP-insensitive binding sites for inner arm dyneins in Chlamydomonas axonemes. J. Cell Biol. 125:1109-1117.
38. Porter, M.E. 1996. Axonemal dyneins: assembly, organization, and regulation. Curr. Opin. Cell Biol. 8:10-17.
39. Porter, M.E., J. Power, and S.K. Dutcher. 1992. Extragenic suppressors of paralyzed flagellar mutations in Chlamydomonas reinhardtii identify loci that alter the inner dynein arms. J. Cell Biol. 118:1163-1176.
40. Rupp, G., and M.E. Porter. 2003. A subunit of the dynein regulatory complex in Chlamydomonas is a homologue of a growth arrest-specific gene product. J. Cell Biol. 162:47-57.
41. Samso, M., and M.P. Koonce. 2004. 25 angstrom resolution structure of a cyto-plasmic dynein motor reveals a seven-member palnar ring. J. Mol. Biol. 340:1059-1072.
42. Taylor, H.C., P. Satir, and M.E. Holwill. 1999. Assessment of inner dynein arm structure and possible function in ciliary and flagellar axonemes. Cell Motil. Cytoskeleton. 43:167-177.
43. Wirschell, M., T. Hendrickson, and W.S. Sale. 2007. Keeping and eye on I1: I1 dynein as a model for flagella dynein assembly and regulation. Cell Motil. Cytoskeleton. 64:569-579.
44. Witman, G.B. 1986. Isolation of Chlamydomonas flagella and flagellar axonemes. Methods Enzymol. 134:280-290.
45. Yagi, T., I. Minoura, A. Fujiwara, R. Saito, T. Yasunaga, M. Hirono, and R. Kamiya. 2005. An axonemal dynein particularly important for flagellar movement at high viscosity. Implications from a new Chlamydomonas mutant deficient in the dynein heavy chain gene DHC9. J. Biol. Chem. 280:41412-41420.
46. Yanagisawa, H.A., and R. Kamiya. 2001. Association between actin and light chains in Chlamydomonas flagellar inner-arm dyneins. Biochem. Biophys. Res. Commun. 288:443-447.