Axoneme structure from motile cilia

Cold Spring Harbor Perspectives in Biology

Volumn 9, Issue 1, 2017, Pages

  Ishikawa, Takashi ^a,b  

^a PAUL SCHERRER INSTITUTE   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; PROTEIN;

ANIMAL; AXONEME; CHLAMYDOMONAS; CILIUM; ELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY; X RAY CRYSTALLOGRAPHY;

ANIMALS; AXONEME; CHLAMYDOMONAS; CILIA; CRYSTALLOGRAPHY, X-RAY; DYNEINS; MICROSCOPY, ELECTRON; PROTEINS;

EID: 85009063935     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a028076     Document Type: Article

References (97)

1. Avolio J, Lebduska S, Sati P. 1984. Dynein arm substructure and the orientation of arm-microtubule attachments. J Mol Biol 173: 389-401.
2. Awata J, Takada S, Standley C, Lechtreck KF, Bellvé KD, Pazour GJ, Fogarty KE, Witman GB. 2014. NPHP4 controls ciliary trafficking of membrane proteins and large soluble proteins at the transition zone. J Cell Sci 127: 4714-4727.
3. Berns MW, Rattner JB, Brenner S, Meredith S. 1977. The role of the centriolar region in animal cell mitosis. A laser microbeam study. J Cell Biol 72: 351-367.
4. Bower R, Tritschler D, Vanderwaal K, Perrone CA, Mueller J, Fox L, Sale WS, Porter ME. 2013. The N-DRC forms a conserved biochemical complex that maintains outer doublet alignment and limits microtubule sliding in motile axonemes. Mol Biol Cell 24: 1134-1152.
5. Bui KH, Ishikawa T. 2013. 3D structural analysis of flagella/ cilia by cryo-electron tomography. Methods Enzymol 524: 305-323.
6. Bui KH, Sakakibara H, Movassagh T, Oiwa K, Ishikawa T. 2008.Molecular architecture of inner dynein arms in situ in Chlamydomonas reinhardtii flagella. J Cell Biol 183: 923-932.
7. Bui KH, Sakakibara H, Movassagh T, Oiwa K, Ishikawa T. 2009. Asymmetry of inner dynein arms and inter-doublet links in Chlamydomonas flagella. JCell Biol 186: 437-446.
8. Bui KH, Yagi T, Yamamoto R, Kamiya R, Ishikawa T. 2012. Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. J Cell Biol 198: 913-925.
9. Carter AP, Cho C, Jin L, Vale RD. 2011. Crystal structure of the dynein motor domain. Science 331: 1159-1165.
10. Chrétien D, Wade RH. 1991. New data on the microtubule surface lattice. Biol Cell 71: 161-174.
11. Dallai R. 2014. Overview on spermatogenesis and sperm structure of Hexapoda. Arthropod Struct Dev 43: 257-290.
12. Diener DR, Yang P, Geimer S, Cole DG, Sale WS, Rosenbaum JL. 2011. Sequential assembly of flagellar radial spokes. Cytoskeleton (Hoboken) 68: 389-400.
13. Diener DR, Lupetti P, Rosenbaum JL. 2015. Proteomic analysis of isolated ciliary transition zones reveals the presence of ESCRT proteins. Curr Biol 25: 379-384.
14. Doroquez DB, Berciu C, Anderson JR, Sengupta P, Nicastro D. 2014. A high-resolution morphological and ultrastructural map of anterior sensory cilia and glia in Caenorhabditis elegans. eLife 3: e01948.
15. Dougherty GW, Loges NT, Klinkenbusch JA, Olbrich H, Pennekamp P, Menchen T, Raidt J, Wallmeier J, Werner C, Westermann C, et al. 2016. DNAH11 localization in the proximal region of respiratory cilia defines distinct outer dynein arm complexes. Am J Respir Cell Mol Biol doi: 10.1165/rcmb.2015-0353OC.
16. Ebersold WT, Levine RP, Levine EE, Olmsted MA. 1962. Linkage maps in Chlamydomonas reinhardi. Genetics 47: 531-543.
17. Fliegauf M, Olbrich H, Horvath J, Wildhaber JH, Zariwala MA, Kennedy M, Knowles MR, Omran H. 2005. Mislocalization of DNAH5 and DNAH9 in respiratory cells frompatientswith primary ciliary dyskinesia. AmJ Respir Crit Care Med 171: 1343-1349.
18. Fliegauf M, Benzing T, Omran H. 2007. When cilia go bad: Cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8: 880-893.
19. Gardner LC, O’Toole E, Perrone CA, Giddings T, Porter ME. 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.
20. Gilliam JC, Chang JT, Sandoval IM, Zhang Y, Li T, Pittler SJ, Chiu W, Wensel TG. 2012. Three-dimensional architecture of the rod sensory cilium and its disruption in retinal neurodegeneration. Cell 151: 1029-1041.
21. Goodenough U, Heuser J. 1984. Structural comparison of purified dynein proteins with in situ dynein arms. J Mol Biol 180: 1083-1118.
22. Goodenough UW, Heuser JE. 1985a. Outer and inner dynein arms of cilia and flagella. Cell 41: 341-342.
23. Goodenough UW, Heuser JE. 1985b. Substructure of inner dynein arms, radial spokes, and the central pair/projection complex of cilia and flagella. J Cell Biol 100: 2008-2018.
24. Guichard P, Desfosses A, Maheshwari A, Hachet V, Dietrich C, Brune A, Ishikawa T, Sachse C, Gönczy P. 2012. Cartwheel architecture of Trichonympha basal body. Science 337: 553.
25. Hayashi S, Shingyoji C. 2008. Mechanism of flagellar oscillation-bending-induced switching of dynein activity in elastase-treated axonemes of sea urchin sperm. J Cell Sci 121: 2833-2843.
26. Heuser T, Raytchev M, Krell J, Porter ME, Nicastro D. 2009. The dynein regulatory complex is the nexin link and a major regulatory node in cilia and flagella. J Cell Biol 187: 921-933.
27. Heuser T, Barber CF, Lin J, Krell J, Rebesco M, Porter ME, Nicastro D. 2012. Cryoelectron tomography reveals doublet-specific structures and unique interactions in the I1 dynein. Proc Natl Acad Sci 109: E2067-E2076.
28. Hoops HJ, Witman GB. 1983. Outer doublet heterogeneity reveals structural polarity related to beat direction in Chlamydomonas flagella. J Cell Biol 97: 902-908.
29. Huang B, Piperno G, Ramanis Z, Luck DJ. 1981. Radial spokes of Chlamydomonas flagella: Genetic analysis of assembly and function. J Cell Biol 88: 80-88.
30. Ikeda K, Brown JA, Yagi T, Norrander JM, Hirono M, Eccleston E, Kamiya R, Linck RW. 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.
31. Inaba K. 2015. Calcium sensors of ciliary outer arm dynein: Functions and phylogenetic considerations for eukaryotic evolution. Cilia 4: 6.
32. Ishikawa T. 2015. Cryo-electron tomography of motile cilia and flagella. Cilia 4: 3.
33. Ishikawa R, Shingyoji C. 2007. Induction of beating by imposed bending or mechanical pulse in demembranated, motionless sea urchin sperm flagella at very low ATP concentrations. Cell Struct Funct 32: 17-27.
34. Johnson KA. 1985. Pathway of the microtubule-dynein ATPase and the structure of dynein: A comparison with actomyosin. Annu Rev Biophys Biophys Chem 14: 161-188.
35. Kagami O, Kamiya R. 1992. Translocation and rotation of microtubules caused by multiple species of Chlamydomonas inner-arm dynein. J Cell Sci 103: 653-664.
36. Kamiya R. 2002. Functional diversity of axonemal dyneins as studied in Chlamydomonas mutants. Int Rev Cytol 219: 115-155.
37. Kamiya R, Okamoto M. 1985. A mutant of Chlamydomonas reinhardtii that lacks the flagellar outer dynein arm but can swim. J Cell Sci 74: 181-191.
38. Kamiya R, Yagi T. 2014. Functional diversity of axonemal dyneins as assessed by in vitro and in vivo motility assays of Chlamydomonas mutants. Zoolog Sci 31: 633-644.
39. King SM. 2016. Axonemal dynein arms. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a028100.
40. Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, Bortfeld M, Erat MC, Flückiger I, Gönczy P, et al. 2011. Structural basis of the 9-fold symmetry of centrioles. Cell 144: 364-375.
41. Kon T, Sutoh K, Kurisu G. 2011. X-ray structure of a functional full-length dynein motor domain. Nat Struct Mol Biol 18: 638-642.
42. Kon T, Oyama T, Shimo-Kon R, Imamula K, Shima T, Sutoh K, Kurisu G. 2012. The 2.8 Å crystal structure of the dynein motor domain. Nature 484: 345-350.
43. Lin J, Okada K, Raytchev M, Smith MC, Nicastro D. 2014. Structural mechanism of the dynein power stroke. Nat Cell Biol 16: 479-485.
44. Linck R, Fu X, Lin J, Ouch C, Schefter A, Steffen W, Warren P, Nicastro D. 2014. Insights into the structure and function of ciliary and flagellar doublet microtubules: Tektins, Ca2þ-binding proteins and stable protofilaments. J Biol Chem 89: 17427-17444.
45. Liu Q, Tan G, Levenkova N, Li T, Pugh EN, Rux JJ, Speicher DW, Pierce EA. 2007. The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteomics 6: 1299-1317.
46. Lupetti P, Lanzavecchia S, Mercati D, Cantele F, Dallai R, Mencarelli C. 2005. Three-dimensional reconstruction of axonemal outer dynein arms in situ by electron tomography. Cell Motil Cytoskeleton 62: 69-83.
47. Maheshwari A, Ishikawa T. 2012. Heterogeneity of dynein structure implies coordinated suppression of dynein motor activity in the axoneme. J Struct Biol 179: 235-241.
48. Maheshwari A, Obbineni JM, Bui KH, Shibata K, Toyoshima YY, Ishikawa T. 2015. α-and β-tubulin lattice of the axonemal microtubule doublet and binding proteins revealed by single particle cryo-electron microscopy and tomography. Structure 23: 1584-1595.
49. Mastronarde DN, O’Toole ET, McDonald KL, McIntosh JR, Porter ME. 1992. Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas. J Cell Biol 118: 1145-1162.
50. Mayer U, Küller A, Daiber PC, Neudorf I, Warnken U, Schnölzer M, Frings S, Möhrlen F. 2009. The proteome of rat olfactory sensory cilia. Proteomics 9: 322-334.
51. Mencarelli C, Lupetti P, Rosetto M, Dallai R. 2000.Morphogenesis of the giant sperm axoneme in Asphondylia ruebsaameni Kertesz (Diptera, Cecidomyiidae). Tissue Cell 32: 188-197.
52. Minamino T, Imada K, Namba K. 2008. Molecular motors of the bacterial flagella. Curr Opin Struct Biol 18: 693-701.
53. Mitchell DR. 2016. Evolution of cilia. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a028290.
54. Mitchell DR, Nakatsugawa M. 2004. Bend propagation drives central pair rotation in Chlamydomonas reinhardtii flagella. J Cell Biol 166: 709-715.
55. Mollaret I, Justine JL. 1997. Immunocytochemical study of tubulin in the 9þ“1” sperm axoneme of a monogenean (Platyhelminthes), Pseudodactylogyrus sp. Tissue Cell 29: 699-706.
56. Movassagh T, Bui KH, Sakakibara H, Oiwa K, Ishikawa T. 2010. Nucleotide-induced global conformational changes of flagellar dynein arms revealed by in situ analysis. Nat Struct Mol Biol 17: 761-767.
57. Nakazawa Y, Ariyoshi T, Noga A, Kamiya R, Hirono M. 2014. Space-dependent formation of central pair microtubules and their interactions with radial spokes. PLoS ONE 9: e110513.
58. Neuwald AF, Aravind L, Spouge JL, Koonin EV. 1999. Assembly, operation , and disassembly of protein complexes AAA:Aclass of chaperone-like ATPases associatedwith the assembly, operation, and disassembly of protein complexes. Genome Res 9: 27-43.
59. Nicastro D, Fu X, Heuser T, Tso A, Porter ME, Linck RW. 2011. Cryo-electron tomography reveals conserved features of doublet microtubules in flagella. Proc Natl Acad Sci 108: E845-853.
60. Nogales E, Wolf SG, Downing KH. 1998. Structure of the ab tubulin dimer by electron crystallography. Nature 391: 199-203.
61. Oda T, Kikkawa M. 2013. Novel structural labeling method using cryo-electron tomography and biotin-streptavidin system. J Struct Biol 183: 305-311.
62. Oda T, Yanagisawa H, Kamiya R, Kikkawa M. 2014a. Cilia and flagella. A molecular ruler determines the repeat length in eukaryotic cilia and flagella. Science 346: 857-860.
63. Oda T, Yanagisawa H, Kikkawa M. 2014b. Detailed structural and biochemical characterization of the nexin-dynein regulatory complex. Mol Biol Cell 26: 294-304.
64. Oda T, Yanagisawa H, Yagi T, Kikkawa M. 2014c. Mechanosignaling between central apparatus and radial spokes controls axonemal dynein activity. J Cell Biol 204: 807-819.
65. Paschal BM, Mikami A, Pfister KK, Vallee RB. 1992.Homology of the 74-kD cytoplasmic dynein subunit with a flagellar dynein polypeptide suggests an intracellular targeting function. J Cell Biol 118: 1133-1143.
66. Pazour GJ, Agrin N, Leszyk J, Witman GB. 2005. Proteomic analysis of a eukaryotic cilium. J Cell Biol 170: 103-113.
67. Pigino G, Ishikawa T. 2012. Axonemal radial spokes: 3D structure, function and assembly. Bioarchitecture 2: 50-58.
68. Pigino G, Bui KH, Maheshwari A, Lupetti P, Diener D, Ishikawa T. 2011. Cryoelectron tomography of radial spokes in cilia and flagella. J Cell Biol 195: 673-687.
69. Pigino G, Maheshwari A, Bui KH, Shingyoji C, Kamimura S, Ishikawa T. 2012. Comparative structural analysis of eukaryotic flagella and cilia from Chlamydomonas, Tetrahymena, and sea urchins. J Struct Biol 178: 199-206.
70. Prensier G, Vivier E, Goldstein S, Schrével J. 1980. Motile flagellum with a “3 þ 0” ultrastructure. Science 207: 1493-1494.
71. Ray S, Meyhöfer E, Milligan RA, Howard J. 1993. Kinesin follows the microtubule’s protofilament axis. J Cell Biol 121: 1083-1093.
72. Roberts AJ, Numata N, Walker ML, Kato YS, Malkova B, Kon T, Ohkura R, Arisaka F, Knight PJ, Sutoh K, et al. 2009. AAAþ ring and linker swing mechanism in the dynein motor. Cell 136: 485-95.
73. Roberts AJ, Malkova B, Walker ML, Sakakibara H, Numata N, Kon T, Ohkura R, Edwards TA, Knight PJ, Sutoh K, et al. 2012. ATP-driven remodeling of the linker domain in the dynein motor. Struct Lond Engl 20: 1670-1680.
74. Roberts AJ, Kon T, Knight PJ, Sutoh K, Burgess SA. 2013. Functions and mechanics of dynein motor proteins. Nat Rev Mol Cell Biol 14: 713-726.
75. Sale WS, Satir P. 1977. Direction of active sliding of microtubules in Tetrahymena cilia. Proc Natl Acad Sci 74: 2045-2049.
76. Satir P, Heuser T, Sale WS. 2014. A structural basis for how motile cilia beat. Bioscience 64: 1073-1083.
77. Schmidt H, Gleave ES, Carter AP. 2012. Insights into dynein motor domain function from a 3.3-A° crystal structure. Nat Struct Mol Biol 19: 492-497.
78. Schmidt H, Zalyte R, Urnavicius L, Carter AP. 2014. Structure of human cytoplasmic dynein-2 primed for its power stroke. Nature 518: 435-438.
79. Schrevel J, Besse C. 1975. A functional flagella with a 6 þ 0 pattern. J Cell Biol 66: 492-507.
80. Segal RA, Huang B, Ramanis Z, Luck DJ. 1984. Mutant strains of Chlamydomonas reinhardtii that move backwards only. J Cell Biol 98: 2026-2034.
81. Shimizu T, Johnson KA. 1983. Presteady state kinetic analysis of vanadate-induced inhibition of the dyneinATPase. J Biol Chem 258: 13833-13840.
82. Shimizu T, Hosoya N, Hisanaga S, Marchese-Ragona SP, Pratt MM. 1992. Activation of ATPase activity of 14S dynein from Tetrahymena cilia by microtubules. Eur J Biochem 206: 911-917.
83. Shimizu Y, Sakakibara H, Kojima H, Oiwa K. 2014. Slow axonemal dynein e facilitates the motility of faster dynein c. Biophys J 106: 2157-2165.
84. Smith JC, Northey JGB, Garg J, Pearlman RE, Siu KWM. 2005. Robust method for proteome analysis by MS/MS using an entire translated genome: Demonstration on the ciliome of Tetrahymena thermophila. J Proteome Res 4: 909-919.
85. Starling D, Randall J. 1971. Flagella of temporary dikaryons of Chlamydomonas reinhardii. Genet Res 18: 107.
86. Sugino K, Naitoh Y. 1982. Simulated cross-bridge patterns corresponding to ciliary beating in paramecium. Nature 295: 609-611.
87. Sui H, Downing KH. 2006. Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature 442: 475-478.
88. Takahashi Y, Edamatsu M, Toyoshima YY. 2004. Multiple ATP-hydrolyzing sites that potentially function in cytoplasmic dynein. Proc Natl Acad Sci 101: 12865-12869.
89. Ueno H, Bui KH, Ishikawa T, Imai Y, Yamaguchi T, Ishikawa T. 2014. Structure of dimeric axonemal dynein in cilia suggests an alternative mechanism of force generation. Cytoskeleton (Hoboken) 71: 412-422.
90. van Breugel M, Hirono M, Andreeva A, Yanagisawa H, Yamaguchi S, Nakazawa Y, Morgner N, Petrovich M, Ebong IO, Robinson CV, et al. 2011. Structures of SAS-6 suggest its organization in centrioles. Science 331: 1196-1199.
91. Warner FD, Satir P. 1974. The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. J Cell Biol 63: 35-63.
92. Woolley DM. 1997. Studies on the eel sperm flagellum. I: The structure of the inner dynein arm complex. J Cell Sci 110: 85-94.
93. Woolley DM. 1998. Studies on the eel sperm flagellum. 2: The kinematics of normal motility. Cell Motil Cytoskeleton 39: 233-245.
94. Yagi T, Uematsu K, Liu Z, Kamiya R. 2009. Identification of dyneins that localize exclusively to the proximal portion of Chlamydomonas flagella. J Cell Sci 122: 1306-1314.
95. Yamamoto R, Song K, Yanagisawa HA, Fox L, Yagi T, Wirschell M, Hirono M, Kamiya R, Nicastro D, Sale WS. 2013. The MIA complex is a conserved and novel dynein regulator essential for normal ciliary motility. J Cell Biol 201: 263-278.
96. Yang P, Yang C, Sale WS. 2004. Flagellar radial spoke protein 2 is a calmodulin binding protein required for motility in Chlamydomonas reinhardtii. Eukaryot Cell 3: 72-81.
97. Yang P, Diener DR, Yang C, Kohno T, Pazour GJ, Dienes JM, Agrin NS, King SM, Sale WS, Kamiya R, et al. 2006. Radial spoke proteins of Chlamydomonas flagella. J Cell Sci 119: 1165-1174.