The dynein regulatory complex is the nexin link and a major regulatory node in cilia and flagella

Journal of Cell Biology

Volumn 187, Issue 6, 2009, Pages 921-933

  Heuser, Thomas ^a   Raytchev, Milen ^a   Krell, Jeremy ^a   Porter, Mary E ^b   Nicastro, Daniela ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; NEXIN; UNCLASSIFIED DRUG; AXONEMAL DYNEIN; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE NEXIN;

ARTICLE; AXONEME; CELL ORGANELLE; CHLAMYDOMONAS REINHARDTII; CILIARY MOTILITY; ELECTRON TOMOGRAPHY; EUKARYOTIC FLAGELLUM; MICROTUBULE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TOMOGRAPHY; WILD TYPE; BINDING SITE; CELL MOTION; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; FLAGELLUM; GENETICS; GENOTYPE; MUTATION; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

CHLAMYDOMONAS REINHARDTII;

AXONEMAL DYNEINS; BINDING SITES; CELL MOVEMENT; CHLAMYDOMONAS REINHARDTII; CILIA; CRYOELECTRON MICROSCOPY; FLAGELLA; GENOTYPE; IMAGING, THREE-DIMENSIONAL; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, MOLECULAR; MUTATION; PHENOTYPE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 74049111826     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200908067     Document Type: Article

References (57)

1. Böttcher, B., S.A. Wynne, and R.A. Crowther. 1997. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature. 386:88-91. doi:10.1038/386088a0
2. Bower, R., K. VanderWaal, E. O'Toole, L. Fox, C. Perrone, J. Mueller, M. Wirschell, R. Kamiya, W.S. Sale, and M.E. Porter. 2009. IC138 defines a subdomain at the base of the I1 dynein that regulates microtubule sliding and flagellar motility. Mol. Biol. Cell. 20:3055-3063. doi:10.1091/mbc.E09- 04-0277
3. 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. doi:10.1002/cm.970240204
4. Brokaw, C.J., and R. Kamiya. 1987. Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motil. Cytoskeleton. 8:68-75. doi:10.1002/cm.970080110
5. Brokaw, C.J., and D.J.L. Luck. 1985. Bending patterns of chlamydomonas flagella: III. A radial spoke head deficient mutant and a central pair deficient mutant. Cell Motil. 5:195-208. doi:10.1002/cm.970050303
6. Brokaw, C.J., D.J. Luck, and B. Huang. 1982. Analysis of the movement of Chlamydomonas flagella: the function of the radial-spoke system is revealed by comparison of wild-type and mutant flagella. J. Cell Biol. 92:722-732. doi:10.1083/jcb.92.3.722
7. Bui, K.H., H. Sakakibara, T. Movassagh, K. Oiwa, and T. Ishikawa. 2008. Molecular architecture of inner dynein arms in situ in Chlamydomonas reinhardtii flagella. J. Cell Biol. 183:923-932. doi:10.1083/jcb. 200808050
8. Colantonio, J.R., J. Vermot, D. Wu, A.D. Langenbacher, S. Fraser, J.N. Chen, and K.L. Hill. 2009. The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear. Nature. 457:205-209. doi:10.1038/nature07520
9. 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. doi:10.1083/jcb.200703107
10. Fliegauf, M., T. Benzing, and H. Omran. 2007. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8:880-893. doi:10.1038/nrm2278
11. 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. doi:10.1083/jcb.127.5.1311
12. Gibbons, B.H., B. Baccetti, and I.R. Gibbons. 1985. Live and reactivated motility in the 9+0 flagellum of Anguilla sperm. Cell Motil. 5:333-350. doi:10.1002/cm.970050406
13. Gibbons, I.R. 1963. Studies on the protein components of cilia from Tetrahymena pyriformis. Proc. Natl. Acad. Sci. USA. 50:1002-1010. doi:10.1073/pnas.50.5.1002
14. Harris, E.H., D.B. Stern, and G.B. Witman. 2009. The Chlamydomonas Sourcebook. Second edition. Academic Press, Oxford, UK. 2000 pp.
15. Huang, B., Z. Ramanis, and D.J. Luck. 1982. Suppressor mutations in Chlamydomonas reveal a regulatory mechanism for Flagellar function. Cell. 28:115-124. doi:10.1016/0092-8674(82)90381-6
16. Ishikawa, T., H. Sakakibara, and K. Oiwa. 2007. The architecture of outer dynein arms in situ. J. Mol. Biol. 368:1249-1258. doi:10.1016/j.jmb. 2007.02.072
17. 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. doi:10.1006/jsbi.1996.0013
18. Linck, R.W., and R.E. Stephens. 2007. Functional protofilament numbering of ciliary, flagellar, and centriolar microtubules. Cell Motil. Cytoskeleton. 64:489-495. doi:10.1002/cm.20202
19. Lindemann, C.B., L.J. Macauley, and K.A. Lesich. 2005. The counterbend phenomenon in dynein-disabled rat sperm flagella and what it reveals about the interdoublet elasticity. Biophys. J. 89:1165-1174. doi:10.1529/biophysj. 105.060681
20. Mastronarde, D.N. 2005. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152:36-51. doi:10.1016/j.jsb.2005.07.007
21. 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 flagella of Chlamydomonas. J. Cell Biol. 118:1145-1162. doi:10.1083/jcb.118.5.1145
22. McIntosh, R., D. Nicastro, and D. Mastronarde. 2005. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 15:43-51. doi:10.1016/j.tcb.2004.11.009
23. Minoura, I., T. Yagi, and R. Kamiya. 1999. Direct measurement of interdoublet elasticity in flagellar axonemes. Cell Struct. Funct. 24:27-33. doi:10.1247/csf.24.27
24. Mitchell, D.R. 2009. The flagellar central pair apparatus. In The Chlamydomonas Sourcebook: Cell Motility and Behavior, vol. 3. Second edition. E.H. Harris, D.B. Stern, and G.B. Witman, editors. Academic Press, Oxford, UK. 235-252.
25. Nicastro, D., J.R. McIntosh, and W. Baumeister. 2005. 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc. Natl. Acad. Sci. USA. 102:15889-15894. doi:10.1073/pnas.0508274102
26. 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. doi:10.1126/science.1128618
27. Olson, G.E., and R.W. Linck. 1977. Observations of the structural components of flagellar axonemes and central pair microtubules from rat sperm. J. Ultrastruct. Res. 61:21-43. doi:10.1016/S0022-5320(77)90004-1
28. 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. doi:10.1002/jcc.20084
29. Piperno, G. 1995. Regulation of dynein activity within Chlamydomonas flagella. Cell Motil. Cytoskeleton. 32:103-105. doi:10.1002/cm.970320206
30. 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. doi:10.1083/jcb.118.6.1455
31. 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. doi:10.1083/jcb.125.5.1109
32. Porter, M.E., and W.S. Sale. 2000. The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J. Cell Biol. 151:37-42. doi:10.1083/jcb.151.5.37
33. Quillin, M.L., and B.W. Matthews. 2000. Accurate calculation of the density of proteins. Acta Crystallogr. D Biol. Crystallogr. 56:791-794. doi:10.1107/S090744490000679X
34. Ralston, K.S., and K.L. Hill. 2006. Trypanin, a component of the flagellar Dynein regulatory complex, is essential in bloodstream form African trypanosomes. PLoS Pathog. 2:e101. doi:10.1371/journal.ppat.0020101
35. 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. doi:10.1083/jcb.200303019
36. Rupp, G., E. O'Toole, L.C. Gardner, B.F. Mitchell, and M.E. Porter. 1996. The sup-pf-2 mutations of Chlamydomonas alter the activity of the outer dynein arms by modification of the γ-dynein heavy chain. J. Cell Biol. 135:1853-1865. doi:10.1083/jcb.135.6.1853
37. Sale, W.S., and P. Satir. 1977. Direction of active sliding of microtubules in Tetrahymena cilia. Proc. Natl. Acad. Sci. USA. 74:2045-2049. doi:10.1073/pnas.74.5.2045
38. Satir, P. 1968. Studies on cilia. 3. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J. Cell Biol. 39:77-94. doi:10.1083/jcb.39.1.77
39. Satir, P. 1985. Switching mechanisms in the control of ciliary motility. In Modern Cell Biology. P. Satir, editor. Alan R. Liss, Inc., New York. 1-46.
40. Smith, E.F. 2002. Regulation of flagellar dynein by the axonemal central apparatus. Cell Motil. Cytoskeleton. 52:33-42. doi:10.1002/cm.10031
41. Smith, E.F., and W.S. Sale. 1992. Regulation of dynein-driven microtubule sliding by the radial spokes in flagella. Science. 257:1557-1559. doi:10.1126/science.1387971
42. Smith, E.F., and P. Yang. 2004. The radial spokes and central apparatus: mechano-chemical transducers that regulate flagellar motility. Cell Motil. Cytoskeleton. 57:8-17. doi:10.1002/cm.10155
43. Sui, H., and K.H. Downing. 2006. Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature. 442:475-478. doi:10.1038/nature04816
44. Summers, K.E., and I.R. Gibbons. 1971. Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc. Natl. Acad. Sci. USA. 68:3092-3096. doi:10.1073/pnas.68.12.3092
45. Warner, F.D. 1976. Ciliary inter-microtubule bridges. J. Cell Sci. 20:101-114.
46. Wirschell, M., D. Nicastro, M.E. Porter, and W.S. Sale. 2009a. The regulation of axonemal bending. In The Chlamydomonas Sourcebook: Cell Motility and Behavior, vol. 3. Second edition. E.H. Harris, D.B. Stern, and G.B. Witman, editors. Academic Press, Oxford, UK. 253-282.
47. Wirschell, M., C. Yang, P. Yang, L. Fox, H.-A. Yanagisawa, R. Kamiya, G.B. Witman, M.E. Porter, and W.S. Sale. 2009b. IC97 is a novel intermediate chain of I1 dynein that interacts with tubulin and regulates interdoublet sliding. Mol. Biol. Cell. 20:3044-3054. doi:10.1091/mbc.E09-04-0276
48. Witman, G.B., K. Carlson, J. Berliner, and J.L. Rosenbaum. 1972. Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes, and mastigonemes. J. Cell Biol. 54:507-539. doi:10.1083/jcb.54.3.507
49. Witman, G.B., J. Plummer, and G. Sander. 1978. Chlamydomonas flagellar mutants lacking radial spokes and central tubules. Structure, composition, and function of specific axonemal components. J. Cell Biol. 76:729-747. doi:10.1083/jcb.76.3.729
50. Woolley, D.M. 1997. Studies on the eel sperm flagellum. I. The structure of the inner dynein arm complex. J. Cell Sci. 110:85-94.
51. Woolley, D.M. 1998a. Studies on the eel sperm flagellum. 2. The kinematics of normal motility. Cell Motil. Cytoskeleton. 39:233-245. doi:10.1002/(SICI)1097-0169(1998)39:3<233::AID-CM6>3.0.CO;2-5
52. Woolley, D.M. 1998b. Studies on the eel sperm flagellum. 3. Vibratile motility and rotatory bending. Cell Motil. Cytoskeleton. 39:246-255. doi:10.1002/(SICI)1097-0169(1998)39:3<246::AID-CM7>3.0.CO;2-2
53. Woolley, D.M., and G.G. Vernon. 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.
54. Xiong, Q., M.K. Morphew, C.L. Schwartz, A.H. Hoenger, and D.N. Mastronarde. 2009. CTF determination and correction for low dose tomographic tilt series. J. Struct. Biol. 168:378-387. doi:10.1016/j.jsb.2009.08.016
55. Yanagisawa, H.A., and R. Kamiya. 2004. A tektin homologue is decreased in Chlamydomonas mutants lacking an axonemal inner-arm dynein. Mol. Biol. Cell. 15:2105-2115. doi:10.1091/mbc.E03-11-0854
56. Yang, P., D.R. Diener, C. Yang, T. Kohno, G.J. Pazour, J.M. Dienes, N.S. Agrin, S.M. King, W.S. Sale, R. Kamiya, et al. 2006. Radial spoke proteins of Chlamydomonas flagella. J. Cell Sci. 119:1165-1174. doi:10.1242/jcs.02811
57. Yeh, S.D., Y.J. Chen, A.C. Chang, R. Ray, B.R. She, W.S. Lee, H.S. Chiang, S.N. Cohen, and S. Lin-Chao. 2002. Isolation and properties of Gas8, a growth arrest-specific gene regulated during male gametogenesis to produce a protein associated with the sperm motility apparatus. J. Biol. Chem. 277:6311-6317. doi:10.1074/jbc.M106941200