The I1 dynein-associated tether and tether head complex is a conserved regulator of ciliary motility

We characterized the composition and three-dimensional structure of a conserved, dynein-associated tether/tether-head complex and its interactions with other ciliary structures. The complex is a conserved regulator of I1 dynein and a “missing link” within the signaling pathway that is critical for control of ciliary motility.

[1]  G. Witman,et al.  Chlamydomonas flagellar mutants lacking radial spokes and central tubules. Structure, composition, and function of specific axonemal components , 1978, The Journal of cell biology.

[2]  U. Goodenough,et al.  Outer and inner dynein arms of cilia and flagella , 1985, Cell.

[3]  W. Sale,et al.  Regulation of dynein-driven microtubule sliding by the radial spokes in flagella. , 1992, Science.

[4]  G. Piperno,et al.  Mutations in the "dynein regulatory complex" alter the ATP-insensitive binding sites for inner arm dyneins in Chlamydomonas axonemes , 1994, The Journal of cell biology.

[5]  J R Kremer,et al.  Computer visualization of three-dimensional image data using IMOD. , 1996, Journal of structural biology.

[6]  P. Lefebvre,et al.  The role of central apparatus components in flagellar motility and microtubule assembly. , 1997, Cell motility and the cytoskeleton.

[7]  E. O'Toole,et al.  The Chlamydomonas Dhc1 gene encodes a dynein heavy chain subunit required for assembly of the I1 inner arm complex. , 1997, Molecular biology of the cell.

[8]  S. Dutcher,et al.  Phosphoregulation of an Inner Dynein Arm Complex in Chlamydomonas reinhardtii Is Altered in Phototactic Mutant Strains , 1997, The Journal of cell biology.

[9]  W. Sale,et al.  Regulation of Flagellar Dynein by Phosphorylation of a 138-kD Inner Arm Dynein Intermediate Chain , 1997, The Journal of cell biology.

[10]  E. O'Toole,et al.  Domains in the 1α Dynein Heavy Chain Required for Inner Arm Assembly and Flagellar Motility in Chlamydomonas , 1999, The Journal of cell biology.

[11]  W. Sale,et al.  Casein Kinase I Is Anchored on Axonemal Doublet Microtubules and Regulates Flagellar Dynein Phosphorylation and Activity* , 2000, The Journal of Biological Chemistry.

[12]  W. Sale,et al.  The 9 + 2 Axoneme Anchors Multiple Inner Arm Dyneins and a Network of Kinases and Phosphatases That Control Motility , 2000, The Journal of cell biology.

[13]  Elizabeth F. Smith.  Regulation of flagellar dynein by the axonemal central apparatus. , 2002, Cell motility and the cytoskeleton.

[14]  B. Afzelius.  Cilia‐related diseases , 2004, The Journal of pathology.

[15]  Triscia W. Hendrickson,et al.  IC138 is a WD-repeat dynein intermediate chain required for light chain assembly and regulation of flagellar bending. , 2004, Molecular biology of the cell.

[16]  Conrad C. Huang,et al.  UCSF Chimera—A visualization system for exploratory research and analysis , 2004, J. Comput. Chem..

[17]  David N Mastronarde,et al.  Automated electron microscope tomography using robust prediction of specimen movements. , 2005, Journal of structural biology.

[18]  G. Pazour,et al.  Proteomic analysis of a eukaryotic cilium , 2005, The Journal of cell biology.

[19]  J. McIntosh,et al.  The Molecular Architecture of Axonemes Revealed by Cryoelectron Tomography , 2006, Science.

[20]  G. Murphy,et al.  Electron cryotomography sample preparation using the Vitrobot , 2006, Nature Protocols.

[21]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[22]  Triscia W. Hendrickson,et al.  Keeping an eye on I1: I1 dynein as a model for flagellar dynein assembly and regulation. , 2007, Cell motility and the cytoskeleton.

[23]  E. Dymek,et al.  A conserved CaM- and radial spoke–associated complex mediates regulation of flagellar dynein activity , 2007, The Journal of cell biology.

[24]  M. Gorovsky,et al.  Glutamylation on α-Tubulin Is Not Essential but Affects the Assembly and Functions of a Subset of Microtubules in Tetrahymena thermophila , 2008, Eukaryotic Cell.

[25]  H. Omran,et al.  When cilia go bad: cilia defects and ciliopathies , 2008, Nature Reviews Molecular Cell Biology.

[26]  W. Sale,et al.  IC97 is a novel intermediate chain of I1 dynein that interacts with tubulin and regulates interdoublet sliding. , 2009, Molecular biology of the cell.

[27]  W. Sale,et al.  IC138 defines a subdomain at the base of the I1 dynein that regulates microtubule sliding and flagellar motility. , 2009, Molecular biology of the cell.

[28]  W. Sale,et al.  Regulation of dynein-driven microtubule sliding by the axonemal protein kinase CK1 in Chlamydomonas flagella , 2009, The Journal of cell biology.

[29]  T. Mitchison,et al.  Cell biology: How cilia beat , 2010, Nature.

[30]  Benjamin Thomas,et al.  Comparative evaluation of label‐free SINQ normalized spectral index quantitation in the central proteomics facilities pipeline , 2011, Proteomics.

[31]  D. Nicastro,et al.  The CSC is required for complete radial spoke assembly and wild-type ciliary motility , 2011, Molecular biology of the cell.

[32]  Phillip V. Bayly,et al.  bop5 mutations reveal new roles for the IC138 phosphoprotein in the regulation of flagellar motility and asymmetric waveforms , 2011, Molecular biology of the cell.

[33]  John M Heumann,et al.  Clustering and variance maps for cryo-electron tomography using wedge-masked differences. , 2011, Journal of structural biology.

[34]  R. Kamiya,et al.  An axonemal PP2A B‐subunit is required for PP2A localization and flagellar motility , 2011, Cytoskeleton.

[35]  W. Sale,et al.  Distinct roles of 1α and 1β heavy chains of the inner arm dynein I1 of Chlamydomonas flagella , 2011, Molecular biology of the cell.

[36]  W. Sale,et al.  Regulation of ciliary motility: conserved protein kinases and phosphatases are targeted and anchored in the ciliary axoneme. , 2011, Archives of biochemistry and biophysics.

[37]  D. Nicastro,et al.  The CSC connects three major axonemal complexes involved in dynein regulation , 2012, Molecular biology of the cell.

[38]  D. Nicastro,et al.  One of the Nine Doublet Microtubules of Eukaryotic Flagella Exhibits Unique and Partially Conserved Structures , 2012, PloS one.

[39]  D. Nicastro,et al.  Cryoelectron tomography reveals doublet-specific structures and unique interactions in the I1 dynein , 2012, Proceedings of the National Academy of Sciences.

[40]  M. Kikkawa.  Big steps toward understanding dynein , 2013, The Journal of cell biology.

[41]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[42]  M. Kikkawa,et al.  Novel structural labeling method using cryo-electron tomography and biotin-streptavidin system. , 2013, Journal of structural biology.

[43]  W. Sale,et al.  The MIA complex is a conserved and novel dynein regulator essential for normal ciliary motility , 2013, The Journal of cell biology.

[44]  M. Edamatsu.  Identification of biotin carboxyl carrier protein in Tetrahymena and its application in in vitro motility systems of outer arm dynein. , 2014, Journal of microbiological methods.

[45]  L. Ostrowski,et al.  Cryo-electron tomography reveals ciliary defects underlying human RSPH1 primary ciliary dyskinesia , 2014, Nature Communications.

[46]  M. Jonikas,et al.  High-Throughput Genotyping of Green Algal Mutants Reveals Random Distribution of Mutagenic Insertion Sites and Endonucleolytic Cleavage of Transforming DNA[W][OPEN] , 2014, Plant Cell.

[47]  W. Baumeister,et al.  Volta potential phase plate for in-focus phase contrast transmission electron microscopy , 2014, Proceedings of the National Academy of Sciences.

[48]  R. Kamiya,et al.  Functional Diversity of Axonemal Dyneins as Assessed by in Vitro and in Vivo Motility Assays of Chlamydomonas Mutants , 2014, Zoological Science.

[49]  P. Koprowski,et al.  The CSC proteins FAP61 and FAP251 build the basal substructures of radial spoke 3 in cilia , 2015, Molecular biology of the cell.

[50]  D. Nicastro,et al.  In Situ Localization of N and C Termini of Subunits of the Flagellar Nexin-Dynein Regulatory Complex (N-DRC) Using SNAP Tag and Cryo-electron Tomography* , 2015, The Journal of Biological Chemistry.

[51]  Jacob M. Robertson,et al.  An Indexed, Mapped Mutant Library Enables Reverse Genetics Studies of Biological Processes in Chlamydomonas reinhardtii[OPEN] , 2016, Plant Cell.

[52]  F. Zhang,et al.  Biallelic Mutations in CFAP43 and CFAP44 Cause Male Infertility with Multiple Morphological Abnormalities of the Sperm Flagella. , 2017, American journal of human genetics.

[53]  W. Sale,et al.  Ciliary Motility: Regulation of Axonemal Dynein Motors. , 2017, Cold Spring Harbor perspectives in biology.

[54]  D. Nicastro,et al.  Asymmetric distribution and spatial switching of dynein activity generates ciliary motility , 2018, Science.

[55]  D. Nicastro,et al.  Ciliary proteins Fap43 and Fap44 interact with each other and are essential for proper cilia and flagella beating , 2018, Cellular and Molecular Life Sciences.