The roles of evolutionarily conserved functional modules in cilia-related trafficking

Cilia are present across most eukaryotic phyla and have diverse sensory and motility roles in animal physiology, cell signalling and development. Their biogenesis and maintenance depend on vesicular and intraciliary (intraflagellar) trafficking pathways that share conserved structural and functional modules. The functional units of the interconnected pathways, which include proteins involved in membrane coating as well as small GTPases and their accessory factors, were first experimentally associated with canonical vesicular trafficking. These components are, however, ancient, having been co-opted by the ancestral eukaryote to establish the ciliary organelle, and their study can inform us about ciliary biology in higher organisms.

[1]  J. Lupski,et al.  Impaired photoreceptor protein transport and synaptic transmission in a mouse model of Bardet–Biedl syndrome , 2007, Vision Research.

[2]  R. Parton,et al.  Rab23, a Negative Regulator of Hedgehog Signaling, Localizes to the Plasma Membrane and the Endocytic Pathway , 2003, Traffic.

[3]  V. Sheffield,et al.  BBS proteins interact genetically with the IFT pathway to influence SHH-related phenotypes , 2012, Human molecular genetics.

[4]  J. Asara,et al.  Centriole distal appendages promote membrane docking, leading to cilia initiation. , 2013, Genes & development.

[5]  M. Fukuda,et al.  NDR2‐mediated Rabin8 phosphorylation is crucial for ciliogenesis by switching binding specificity from phosphatidylserine to Sec15 , 2013, The EMBO journal.

[6]  C. Sung,et al.  Cytoplasmic Dynein Regulation by Subunit Heterogeneity and Its Role in Apical Transport , 2001, The Journal of cell biology.

[7]  J. Peränen.  Rab8 GTPase as a regulator of cell shape , 2011, Cytoskeleton.

[8]  Gáspár Jékely,et al.  Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[9]  Wei Guo,et al.  The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. , 2009, Molecular biology of the cell.

[10]  E. Souied,et al.  Exome sequencing identifies mutations in LZTFL1, a BBSome and smoothened trafficking regulator, in a family with Bardet–Biedl syndrome with situs inversus and insertional polydactyly , 2012, Journal of Medical Genetics.

[11]  Sudipto Roy.  The motile cilium in development and disease: emerging new insights , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[12]  G. Pazour,et al.  The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. , 2006, Molecular biology of the cell.

[13]  B. Engel,et al.  Structural Studies of Ciliary Components , 2012, Journal of molecular biology.

[14]  Sir William Dunn.  A “ Holistic ” Kinesin Phylogeny Reveals New Kinesin Families and Predicts Protein Functions , 2006 .

[15]  V. Sheffield,et al.  Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome , 2011, Proceedings of the National Academy of Sciences.

[16]  O. Blacque,et al.  Bardet-Biedl syndrome: an emerging pathomechanism of intracellular transport , 2006, Cellular and Molecular Life Sciences CMLS.

[17]  J. Malicki.  Who drives the ciliary highway? , 2012, Bioarchitecture.

[18]  Nansheng Chen,et al.  MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis , 2011, The Journal of cell biology.

[19]  Yoan Diekmann,et al.  Thousands of Rab GTPases for the Cell Biologist , 2011, PLoS Comput. Biol..

[20]  V. Sheffield,et al.  BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly , 2010, Proceedings of the National Academy of Sciences.

[21]  Jinghua Hu,et al.  The small GTPases ARL-13 and ARL-3 coordinate intraflagellar transport and ciliogenesis , 2010, The Journal of cell biology.

[22]  J. Scholey,et al.  The Retrograde IFT Machinery of C. elegans Cilia: Two IFT Dynein Complexes? , 2011, PloS one.

[23]  André Hoelz,et al.  The structure of the nuclear pore complex. , 2011, Annual review of biochemistry.

[24]  K. Anderson,et al.  The Spinocerebellar Ataxia-Associated Gene Tau Tubulin Kinase 2 Controls the Initiation of Ciliogenesis , 2012, Cell.

[25]  Andrew D. Johnson,et al.  Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins , 2011, Cellular and Molecular Life Sciences.

[26]  S. R. Wicks,et al.  Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. , 2004, Genes & development.

[27]  G. Pazour,et al.  The cytoplasmic tail of fibrocystin contains a ciliary targeting sequence , 2010, The Journal of cell biology.

[28]  Helen Hoffmeister,et al.  Polycystin-2 takes different routes to the somatic and ciliary plasma membrane , 2011, The Journal of cell biology.

[29]  U. Lopes,et al.  The GTPase TcRjl of the human pathogen Trypanosoma cruzi is involved in the cell growth and differentiation. , 2012, Biochemical and biophysical research communications.

[30]  J. Rosenbaum,et al.  Chapter Two Intraflagellar Transport (IFT) , 2008 .

[31]  G. Pazour,et al.  Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella , 2007, The Journal of cell biology.

[32]  Andrej Sali,et al.  On a bender—BARs, ESCRTs, COPs, and finally getting your coat , 2011, The Journal of cell biology.

[33]  Jinghua Hu,et al.  The BBSome controls IFT assembly and turnaround in cilia , 2012, Nature Cell Biology.

[34]  B. Tang,et al.  Rabs and other small GTPases in ciliary transport , 2011, Biology of the cell.

[35]  B. Yoder,et al.  IFTA-2 is a conserved cilia protein involved in pathways regulating longevity and dauer formation in Caenorhabditis elegans , 2006, Journal of Cell Science.

[36]  S. Somlo,et al.  Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif , 2006, Journal of Cell Science.

[37]  M. Neil,et al.  Remodelling of Cortical Actin Where Lytic Granules Dock at Natural Killer Cell Immune Synapses Revealed by Super-Resolution Microscopy , 2011, PLoS biology.

[38]  Mark C. Field,et al.  RAB-Like 2 Has an Essential Role in Male Fertility, Sperm Intra-Flagellar Transport, and Tail Assembly , 2012, PLoS genetics.

[39]  Yehuda Ben-Shahar,et al.  Motile Cilia of Human Airway Epithelia Are Chemosensory , 2009, Science.

[40]  Norman E. Davey,et al.  A Proteome-wide Screen for Mammalian SxIP Motif-Containing Microtubule Plus-End Tracking Proteins , 2012, Current Biology.

[41]  J. Rosenbaum,et al.  Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles , 2001, Current Biology.

[42]  Mark C. Field,et al.  Rab23 is a flagellar protein in Trypanosoma brucei , 2011, BMC Research Notes.

[43]  H. Zentgraf,et al.  Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis , 2012, The Journal of cell biology.

[44]  J. Rosenbaum,et al.  Polarity of flagellar assembly in Chlamydomonas , 1992, The Journal of cell biology.

[45]  M. Leroux,et al.  Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. , 2009, Trends in cell biology.

[46]  Tanya M. Teslovich,et al.  Comparative Genomics Identifies a Flagellar and Basal Body Proteome that Includes the BBS5 Human Disease Gene , 2004, Cell.

[47]  K. Anderson,et al.  Mouse Rab23 regulates hedgehog signaling from smoothened to Gli proteins. , 2006, Developmental biology.

[48]  P. Sengupta,et al.  elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8 , 2008, Nature Cell Biology.

[49]  J. Scholey,et al.  Sensory ciliogenesis in Caenorhabditis elegans: assignment of IFT components into distinct modules based on transport and phenotypic profiles. , 2007, Molecular biology of the cell.

[50]  V. Sheffield,et al.  An ARL3-UNC119-RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium. , 2011, Genes & development.

[51]  V. Sheffield,et al.  A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. , 2008, Developmental cell.

[52]  J. Bonifacino,et al.  Signals for sorting of transmembrane proteins to endosomes and lysosomes. , 2003, Annual review of biochemistry.

[53]  S. Geimer,et al.  Intraflagellar transport (IFT) cargo , 2004, The Journal of cell biology.

[54]  David S. Williams,et al.  Live-Cell Imaging Evidence for the Ciliary Transport of Rod Photoreceptor Opsin by Heterotrimeric Kinesin-2 , 2012, The Journal of Neuroscience.

[55]  D. Deretic,et al.  The Arf GAP ASAP1 provides a platform to regulate Arf4‐ and Rab11–Rab8‐mediated ciliary receptor targeting , 2012, The EMBO journal.

[56]  K. Mostov,et al.  Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes , 1994, The Journal of cell biology.

[57]  J. Scholey,et al.  Functional coordination of intraflagellar transport motors , 2005, Nature.

[58]  P. Dupuis‐Williams,et al.  Ultrastructure of cilia and flagella – back to the future! , 2011, Biology of the cell.

[59]  C. Basquin,et al.  Crystal structure of the intraflagellar transport complex 25/27 , 2011, The EMBO journal.

[60]  J. B. Rattner,et al.  Primary ciliogenesis defects are associated with human astrocytoma/glioblastoma cells , 2009, BMC Cancer.

[61]  Andrew D. Johnson,et al.  Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. , 2008, Molecular biology of the cell.

[62]  C. Sung,et al.  The cell biology of vision , 2010, The Journal of cell biology.

[63]  S. Pfeffer.  Transport-vesicle targeting: tethers before SNAREs , 1999, Nature Cell Biology.

[64]  G. Bishop,et al.  Bardet–Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia , 2008, Proceedings of the National Academy of Sciences.

[65]  Keith Gull,et al.  Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells , 2006, Journal of Cell Science.

[66]  Josef D. Franke,et al.  The Compartmentalized Bacteria of the Planctomycetes-Verrucomicrobia-Chlamydiae Superphylum Have Membrane Coat-Like Proteins , 2010, PLoS biology.

[67]  G. Kreitzer,et al.  Organization of vesicular trafficking in epithelia , 2005, Nature Reviews Molecular Cell Biology.

[68]  W. Snell,et al.  Intraflagellar Transport Particles Participate Directly in Cilium-Generated Signaling in Chlamydomonas , 2006, Cell.

[69]  R. E. Stephens.  Tubulin and tektin in sea urchin embryonic cilia: pathways of protein incorporation during turnover and regeneration. , 1994, Journal of cell science.

[70]  R. Nitschke,et al.  Differential role of Rab proteins in ciliary trafficking: Rab23 regulates Smoothened levels , 2010, Journal of Cell Science.

[71]  J. Nathans,et al.  Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[72]  M. Eliáš,et al.  The RJL family of small GTPases is an ancient eukaryotic invention probably functionally associated with the flagellar apparatus. , 2009, Gene.

[73]  R. Lewis,et al.  Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome , 2008, Nature Genetics.

[74]  Deborah A. Cochran,et al.  The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella , 2009, The Journal of cell biology.

[75]  B. Wickstead,et al.  More than one way to build a flagellum: comparative genomics of parasitic protozoa , 2004, Current Biology.

[76]  T. Cavalier-smith,et al.  Predation and eukaryote cell origins: a coevolutionary perspective. , 2009, The international journal of biochemistry & cell biology.

[77]  G. Pazour,et al.  IFT20 is required for opsin trafficking and photoreceptor outer segment development , 2011, Molecular biology of the cell.

[78]  S. Sorokin,et al.  CENTRIOLES AND THE FORMATION OF RUDIMENTARY CILIA BY FIBROBLASTS AND SMOOTH MUSCLE CELLS , 1962, The Journal of cell biology.

[79]  J. Reiter,et al.  The primary cilium at the crossroads of mammalian hedgehog signaling. , 2008, Current topics in developmental biology.

[80]  T. Ideker,et al.  Functional genomic screen for modulators of ciliogenesis and cilium length , 2010, Nature.

[81]  U. Wolfrum,et al.  Rhodopsin’s Carboxy-Terminal Cytoplasmic Tail Acts as a Membrane Receptor for Cytoplasmic Dynein by Binding to the Dynein Light Chain Tctex-1 , 1999, Cell.

[82]  C. Sung,et al.  The Cytoplasmic Tail of Rhodopsin Acts as a Novel Apical Sorting Signal in Polarized MDCK Cells , 1998, The Journal of cell biology.

[83]  V. Sheffield,et al.  A Core Complex of BBS Proteins Cooperates with the GTPase Rab8 to Promote Ciliary Membrane Biogenesis , 2007, Cell.

[84]  P. Chavrier,et al.  ARF6 controls post-endocytic recycling through its downstream exocyst complex effector , 2003, The Journal of cell biology.

[85]  B. Yoder,et al.  Primary Cilia and Signaling Pathways in Mammalian Development, Health and Disease , 2009, Nephron Physiology.

[86]  C. L. Jackson,et al.  ARF family G proteins and their regulators: roles in membrane transport, development and disease , 2011, Nature Reviews Molecular Cell Biology.

[87]  J. Reiter,et al.  The primary cilium at the crossroads of mammalian hedgehog signaling. , 2008, Current topics in developmental biology.

[88]  F. Barr,et al.  Functional dissection of Rab GTPases involved in primary cilium formation , 2007, The Journal of cell biology.

[89]  K. Kozminski,et al.  A motility in the eukaryotic flagellum unrelated to flagellar beating. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Colin A. Johnson,et al.  Planar Cell Polarity Acts Through Septins to Control Collective Cell Movement and Ciliogenesis , 2010, Science.

[91]  E. Nigg,et al.  Molecular Basis of Tubulin Transport Within the Cilium by IFT74 and IFT81 , 2013, Science.

[92]  Paul M. Jenkins,et al.  The AP-1 clathrin adaptor facilitates cilium formation and functions with RAB-8 in C. elegans ciliary membrane transport , 2010, Journal of Cell Science.

[93]  V. Sheffield,et al.  Identification and Functional Analysis of the Vision-Specific BBS3 (ARL6) Long Isoform , 2010, PLoS genetics.

[94]  J. Scholey.  Intraflagellar transport motors in cilia: moving along the cell's antenna , 2008, The Journal of cell biology.

[95]  K. Porter,et al.  FINE STRUCTURE OF CELL DIVISION IN CHLAMYDOMONAS REINHARDI , 1968, The Journal of cell biology.

[96]  J. Rosenbaum,et al.  Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. , 2008, Current topics in developmental biology.

[97]  U. Wolfrum,et al.  Intraflagellar transport proteins in ciliogenesis of photoreceptor cells , 2011, Biology of the cell.

[98]  G. Walz,et al.  Inversin, Wnt signaling and primary cilia. , 2012, Differentiation; research in biological diversity.

[99]  J. Reiter,et al.  Scoring a backstage pass: Mechanisms of ciliogenesis and ciliary access , 2012, The Journal of cell biology.

[100]  Dylan T Burnette,et al.  Intraflagellar Transport Is Required for the Vectorial Movement of TRPV Channels in the Ciliary Membrane , 2005, Current Biology.

[101]  Michel Bornens,et al.  The Centrosome in Cells and Organisms , 2012, Science.

[102]  G. Pazour,et al.  Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella , 2007, The Journal of cell biology.

[103]  Elena F. Koslover,et al.  Single molecule imaging reveals a major role for diffusion in the exploration of ciliary space by signaling receptors , 2013, eLife.

[104]  P. Satir,et al.  Primary cilia and coordination of receptor tyrosine kinase (RTK) signalling , 2012, The Journal of pathology.

[105]  R. Alam,et al.  Uncoordinated 119 Protein Controls Trafficking of Lck via the Rab11 Endosome and Is Critical for Immunological Synapse Formation1 , 2009, The Journal of Immunology.

[106]  E. Bedrick,et al.  A conserved signal and GTPase complex are required for the ciliary transport of polycystin-1 , 2011, Molecular biology of the cell.

[107]  Wei Guo,et al.  Coordination of Rab8 and Rab11 in primary ciliogenesis , 2010, Proceedings of the National Academy of Sciences.

[108]  Bethan E. Hoskins,et al.  The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression , 2004, Nature Genetics.

[109]  R. Wait,et al.  The X-linked retinitis pigmentosa protein RP2 facilitates G protein traffic. , 2012, Human molecular genetics.

[110]  D. Baylor,et al.  A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[111]  Mark C. Field,et al.  Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode , 2007, Journal of Cell Science.

[112]  S. Geimer,et al.  Electron-tomographic analysis of intraflagellar transport particle trains in situ , 2009, The Journal of cell biology.

[113]  Shankar Subramaniam,et al.  Decoding Cilia Function Defining Specialized Genes Required for Compartmentalized Cilia Biogenesis , 2004, Cell.

[114]  Nicholas Katsanis,et al.  Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. , 2009, The Journal of clinical investigation.

[115]  J. Reiter,et al.  The base of the cilium: roles for transition fibres and the transition zone in ciliary formation, maintenance and compartmentalization , 2012, EMBO reports.

[116]  Jinghua Hu,et al.  The emerging role of Arf/Arl small GTPases in cilia and ciliopathies , 2012, Journal of cellular biochemistry.

[117]  V. Sheffield,et al.  A Novel Protein LZTFL1 Regulates Ciliary Trafficking of the BBSome and Smoothened , 2011, PLoS genetics.

[118]  Kate Baker,et al.  Making sense of cilia in disease: The human ciliopathies , 2009, American journal of medical genetics. Part C, Seminars in medical genetics.

[119]  William Arbuthnot Sir Lane,et al.  TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. , 2010, Genes & development.

[120]  M. Scott,et al.  Lateral transport of Smoothened from the plasma membrane to the membrane of the cilium , 2009, The Journal of cell biology.

[121]  S. Gygi,et al.  The Conserved Bardet-Biedl Syndrome Proteins Assemble a Coat that Traffics Membrane Proteins to Cilia , 2010, Cell.

[122]  J. García-Verdugo,et al.  A Transition Zone Complex Regulates Mammalian Ciliogenesis and Ciliary Membrane Composition , 2011, Nature Genetics.

[123]  O. Weisz,et al.  Apical trafficking in epithelial cells: signals, clusters and motors , 2009, Journal of Cell Science.

[124]  Keith A. Boroevich,et al.  Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome , 2004, Nature Genetics.

[125]  P. Bastin,et al.  A novel function for the atypical small G protein Rab-like 5 in the assembly of the trypanosome flagellum , 2009, Journal of Cell Science.

[126]  S. Cevik,et al.  Intraflagellar transport: from molecular characterisation to mechanism. , 2008, Frontiers in bioscience : a journal and virtual library.

[127]  G. Pazour,et al.  Intraflagellar transport is required for polarized recycling of the TCR/CD3 complex to the immune synapse , 2009, Nature Cell Biology.

[128]  D. Baird,et al.  Jcb: Article , 2022 .

[129]  M. Leroux,et al.  cAMP and cGMP signaling: sensory systems with prokaryotic roots adopted by eukaryotic cilia. , 2010, Trends in cell biology.

[130]  Hongmin Qin,et al.  Intraflagellar Transport (IFT) Protein IFT25 Is a Phosphoprotein Component of IFT Complex B and Physically Interacts with IFT27 in Chlamydomonas , 2009, PloS one.

[131]  W. Marshall,et al.  Ciliogenesis: building the cell's antenna , 2011, Nature Reviews Molecular Cell Biology.

[132]  N. Katsanis,et al.  Mutations in SDCCAG8/NPHP10 Cause Bardet-Biedl Syndrome and Are Associated with Penetrant Renal Disease and Absent Polydactyly , 2011, Molecular Syndromology.

[133]  E. Lorentzen,et al.  Architecture and function of IFT complex proteins in ciliogenesis. , 2012, Differentiation; research in biological diversity.

[134]  Mark C. Field,et al.  First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. , 2009, Current opinion in cell biology.

[135]  Anirban Datta,et al.  A molecular network for de novo generation of the apical surface and lumen , 2010, Nature Cell Biology.

[136]  J. García-Verdugo,et al.  Ofd1, a human disease gene, regulates the length and distal structure of centrioles. , 2010, Developmental cell.

[137]  Hongmin Qin,et al.  Intraflagellar Transport Protein 27 Is a Small G Protein Involved in Cell-Cycle Control , 2007, Current Biology.

[138]  Yun Lu,et al.  Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments , 2011, Nature Cell Biology.

[139]  D. Deretic,et al.  Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4 , 2009, The EMBO journal.

[140]  U. Wolfrum,et al.  Intraflagellar transport molecules in ciliary and nonciliary cells of the retina , 2010, The Journal of cell biology.

[141]  M. P. Healey,et al.  Mutations in a Guanylate Cyclase GCY-35/GCY-36 Modify Bardet-Biedl Syndrome–Associated Phenotypes in Caenorhabditis elegans , 2011, PLoS genetics.

[142]  B. Wickstead,et al.  Dyneins Across Eukaryotes: A Comparative Genomic Analysis , 2007, Traffic.

[143]  Thomas L Casavant,et al.  Homozygosity mapping with SNP arrays identifies TRIM32, an E3 ubiquitin ligase, as a Bardet-Biedl syndrome gene (BBS11). , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[144]  M. Arkin,et al.  Small molecule inhibitors of Smoothened ciliary localization and ciliogenesis , 2012, Proceedings of the National Academy of Sciences.

[145]  G. Pazour,et al.  IFT25 links the signal-dependent movement of Hedgehog components to intraflagellar transport. , 2012, Developmental cell.

[146]  M. Cheetham,et al.  Arl3 and RP2 mediated assembly and traffic of membrane associated cilia proteins , 2012, Vision Research.

[147]  S. Cevik,et al.  Endocytosis Genes Facilitate Protein and Membrane Transport in C. elegans Sensory Cilia , 2012, Current Biology.

[148]  S. Doxsey,et al.  The Centrosome Regulates the Rab11- Dependent Recycling Endosome Pathway at Appendages of the Mother Centriole , 2012, Current Biology.

[149]  F. Renaud,et al.  THE DEVELOPMENT OF BASAL BODIES AND FLAGELLA IN ALLOMYCES ARBUSCULUS , 1964, The Journal of cell biology.