Special Issue Reviews–A Peer Reviewed Forum
You have full text access to this OnlineOpen article
Assembly of primary cilia
Article first published online: 4 APR 2008
DOI: 10.1002/dvdy.21521
Copyright © 2008 Wiley-Liss, Inc.
Issue

Developmental Dynamics
Special Issue: Special Focus on the Primary Cilium
Volume 237, Issue 8, pages 1993–2006, August 2008
Additional Information
How to Cite
Pedersen, L. B., Veland, I. R., Schrøder, J. M. and Christensen, S. T. (2008), Assembly of primary cilia. Dev. Dyn., 237: 1993–2006. doi: 10.1002/dvdy.21521
Publication History
- Issue published online: 23 JUL 2008
- Article first published online: 4 APR 2008
- Manuscript Accepted: 21 FEB 2008
Funded by
- Danish Natural Science Research Council. Grant Number: 272-05-0411
- Novo Nordisk Foundation
- Lundbeck Foundation
REFERENCES
- , , , , , . 2003. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426: 570–574.
- , . 1971. Cilia in cell-cultured fibroblasts. II. Incidence in mitotic and post-mitotic BHK 21-C13 fibroblasts. J Anat 109: 277–292.
- , , , , , , . 2004. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117: 527–539.
- , , , . 2004. Cloning and characterization of Kin5, a novel Tetrahymena ciliary kinesin II. Cell Motil Cytoskel 58: 1–9.
- , , , . 2006. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 7: 125–148.
- , , , , , , , , . 2005. Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 132: 5329–5339.
- , , , . 2007. Functional genomics in Trypanosoma brucei identifies evolutionarily conserved components of motile flagella. J Cell Sci 120: 478–491.
- , , , , , , , , , , , , , , , . 2007. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat Genet 39: 727–729.
- , , , . 2005. LmxMPK9, a mitogen-activated protein kinase homologue affects flagellar length in Leishmania mexicana. Mol Microbiol 55: 1606–1615.
- , , , . 2003. A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr Biol 13: 1145–1149.
- , . 2007. Centrosome biogenesis and function: centrosomics brings new understanding. Nat Rev Mol Cell Biol 8: 451–463.
- , . 2006. Bardet-Biedl syndrome: an emerging pathomechanism of intracellular transport. Cell Mol Life Sci 63: 2145–2161.
- , , , , , , , , , , , , , , , , , . 2004. Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev 18: 1630–1642.
- , , . 2008. Intraflagellar transport: from molecular characterisation to mechanism. Front Biosci 13: 2633–2652.
- , , , . 2001. The bld1 mutation identifies the Chlamydomonas osm-6 homolog as a gene required for flagellar assembly. Curr Biol 11: 1591–1594.
- , , , , , . 2007. Mutation of the MAP kinase DYF-5 affects docking and undocking of kinesin-2 motors and reduces their speed in the cilia of Caenorhabditis elegans. Proc Natl Acad Sci USA 104: 7157–7162.
- , , , . 2004. Orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization. Development 131: 3457–3467.
- , , , , , , , . 2007. Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool. J Neurosci 27: 9780–9789.
- , , , . 2007. Sensory cilia and integration of signal transduction in human health and disease. Traffic 8: 97–109.
- . 2003. The intraflagellar transport machinery of Chlamydomonas reinhardtii. Traffic 4: 1–8.
- . 2005. Intraflagellar transport: keeping the motors coordinated. Curr Biol 15: R1–R3.
- , , , , , . 1992. Isolation of a sea urchin egg kinesin-related protein using peptide antibodies. J Cell Sci 101: 291–301.
- , , , , , . 1993. Novel heterotrimeric kinesin-related protein purified from sea urchin eggs. Nature 366: 268–270.
- , , , , , . 1998. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 141: 993–1008.
- , , , , . 1998. Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in C. elegans. Genetics 148: 187–200.
- , . 1966. Cilia of a distinctive structure (9+0) in endocrine and other tissues. Postgrad Med J 42: 403–408.
- , , . 2007a. Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J Cell Sci 120: 7–15.
- , , , , , , , , , , , , , , . 2007b. The Meckel-Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum Mol Genet 16: 173–186.
- , , , , . 2001. Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr Biol 11: 1586–1590.
- , , , , , , , . 2005. Analysis of xbx genes in C. elegans. Development 132: 1923–1934.
- , . 2003. Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421: 753–756.
- , , , , , , . 2006. Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. J Cell Biol 172: 663–669.
- , , , , , , , . 2004. Polarity proteins control ciliogenesis via kinesin motor interactions. Curr Biol 14: 1451–1461.
- , , , , , . 2007. A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J Cell Biol 178: 387–398.
- , , , , , , , . 2006. Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Nat Genet 38: 112–117.
- , , . 2006. Clustering of cyclic-nucleotide-gated channels in olfactory cilia. Biophys J 91: 179–188.
- , , , . 2006. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol Biol Cell 17: 3781–3792.
- , , . 1999. A novel WD40 protein, CHE-2, acts cell-autonomously in the formation of C. elegans sensory cilia. Development 126: 4839–4848.
- , . 1972. The ciliary necklace. A ciliary membrane specialization. J Cell Biol 53: 494–509.
- , , , , , , . 2007. Knockdown of the intraflagellar transport protein IFT46 stimulates selective gene expression in mouse chondrocytes and affects early development in zebrafish. J Biol Chem 282: 30960–30973.
- , , , , , , . 2007. Cep164, a novel centriole appendage protein required for primary cilium formation. J Cell Biol 179: 321–330.
- , , . 2002. Identification of a novel light intermediate chain (D2LIC) for mammalian cytoplasmic dynein 2. Mol Biol Cell 13: 817–829.
- , , , , . 2003. Identification of CHE-13, a novel intraflagellar transport protein required for cilia formation. Exp Cell Res 284: 251–263.
- , , , , . 2001. The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128: 1493–1505.
- , , . 2004. A dynein light intermediate chain, D1bLIC, is required for retrograde intraflagellar transport. Mol Biol Cell 15: 4382–4394.
- , , , , , . 2007. Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. J Cell Biol 176: 653–665.
- , , , , , , , , , , . 2006. Hippi is essential for node cilia assembly and Sonic hedgehog signaling. Dev Biol 300: 523–533.
- , , , . 1977. Temperature-sensitive mutations affecting flagellar assembly and function in Chlamydomonas reinhardtii. J Cell Biol 72: 67–85.
- , , , , , . 2003. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426: 83–87.
- , , . 2003. To beat or not to beat: roles of cilia in development and disease. Hum Mol Genet 12: R27–35.
- , , . 2005. Odf2-deficient mother centrioles lack distal/subdistal appendages and the ability to generate primary cilia. Nat Cell Biol 7: 517–524.
- , . 2006. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28: 191–198.
- , , , , , , , . 2006. Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr Biol 16: 1211–1216.
- , , , , , , , . 2004. Pericentrin forms a complex with intraflagellar transport proteins and polycystin-2 and is required for primary cilia assembly. J Cell Biol 166: 637–643.
- , , , , , , , , , , , , . 2004. The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat Genet 36: 462–470.
- , , , , , . 1996. Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain. J Biol Chem 271: 19358–19366.
- , , , . 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc Natl Acad Sci USA 90: 5519–5523.
- , , . 1995. The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J Cell Biol 131: 1517–1527.
- , , , , , , , , , . 2004. Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat Genet 36: 994–998.
- , , , , , , , . 2006. MKS1, encoding a component of the flagellar apparatus basal body proteome, is mutated in Meckel syndrome. Nat Genet 38: 155–157.
- , , , , , , , , , . 2001. Targeted disruption of the zetaPKC gene results in the impairment of the NF-kappaB pathway. Mol Cell 8: 771–780.
- , , , , , , , , . 2007. A role for Alstrom syndrome protein, alms1, in kidney ciliogenesis and cellular quiescence. PLoS Genet 3: e8.
- , , , , , , , , , , , , , , , , , , , , . 2004. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117: 541–552.
- , , , . 2003. The microtubule plus-end proteins EB1 and dynactin have differential effects on microtubule polymerization. Mol Biol Cell 14: 1405–1417.
- , , , , , , . 2003. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc Natl Acad Sci USA 100: 5286–5291.
- , , , , , , . 2007. The von Hippel-Lindau tumour suppressor interacts with microtubules through kinesin-2. FEBS Lett 581: 4571–4576.
- , , , , . 2007. Spatial distribution of intraflagellar transport proteins in vertebrate photoreceptors. Vision Res 48: 413–423.
- , , , , . 1999. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 96: 5043–5048.
- , , , , . 2000. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102: 175–187.
- , , , . 2002. Kinesin-II is not essential for mitosis and cell growth in Chlamydomonas. 52: 195–201.
- , , , , , , , , . 2005. Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli Dev Biol 287: 378–389.
- , , , , , , , . 2002. Molecular structure of cytoplasmic dynein 2 and its distribution in neuronal and ciliated cells. J Cell Sci 115: 4801–4808.
- , , , , , . 2007. Loss of centrosome integrity induces p38–p53-p21-dependent G1-S arrest. Nat Cell Biol 9: 160–170.
- , , , , , . 2005. Mutant kinesin-2 motor subunits increase chromosome loss. Mol Biol Cell 16: 3810–3820.
- , , , , . 2002. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 21: 281–293.
- , , , , . 2005. The FLA3 KAP subunit is required for localization of kinesin-2 to the site of flagellar assembly and processive anterograde intraflagellar transport. Mol Biol Cell 16: 1341–1354.
- , , , , , . 2007. Distinct IFT mechanisms contribute to the generation of ciliary structural diversity in C. elegans. EMBO J 26: 2966–2980.
- , , , , , . 2000. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127: 2347–2355.
- , , , , , , , , , . 2004. Bardet-Biedl syndrome type 4 (BBS4)-null mice implicate Bbs4 in flagella formation but not global cilia assembly. Proc Natl Acad Sci USA 101: 8664–8669.
- , , , , , , , , , , . 2007. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129: 1201–1213.
- , , , , , , , , , , , , . 2004a. Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin. Proc Natl Acad Sci USA 101: 16588–16593.
- , , , , , . 2004b. Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat Cell Biol 6: 328–334.
- , , , , , , , . 1998. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95: 829–837.
- , , , , , , , , , , . 1999. Direct interaction of the beta-domain of VHL tumor suppressor protein with the regulatory domain of atypical PKC isotypes. Biochem Biophys Res Commun 263: 491–497.
- , . 2006. oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr Biol 16: 945–957.
- , , , , , . 1999. Movement of motor and cargo along cilia. Nature 398: 674.
- , , , , . 2005. Functional coordination of intraflagellar transport motors. Nature 436: 583–587.
- , . 2007. The primary cilium: keeper of the key to cell division. Cell 129: 1255–1257.
- , , . 2005. Cilium-generated signaling and cilia-related disorders. Lab Invest 85: 452–463.
- , , , , , , , , , . 2006. Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. J Cell Biol 174: 1035–1045.
- , , , , . 2007. The Zebrafish fleer gene encodes an essential regulator of cilia tubulin polyglutamylation. Mol Biol Cell 18: 4353–4364.
- , . 2002. Intraflagellar transport and cilia-dependent diseases. Trends Cell Biol 12: 551–555.
- , , . 1998. A dynein light chain is essential for retrograde particle movement in intraflagellar transport (IFT). J Cell Biol 141: 979–992.
- , , . 1999. The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J Cell Biol 144: 473–481.
- , , , , , , . 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151: 709–718.
- , , , , , , , . 2002. The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance. J Cell Biol 157: 103–113.
- , , , . 2003. The microtubule plus end-tracking protein EB1 is localized to the flagellar tip and basal bodies in Chlamydomonas reinhardtii. Curr Biol 13: 1969–1974.
- , , , , , . 2005. Chlamydomonas IFT172 is encoded by FLA11, interacts with CrEB1, and regulates IFT at the flagellar tip. Curr Biol 15: 262–266.
- , , . 2006. Dissecting the molecular mechanisms of intraflagellar transport in Chlamydomonas. Curr Biol 16: 450–459.
- , , , . 1986. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456–487.
- , , , , , . 2003. A novel dynein light intermediate chain colocalizes with the retrograde motor for intraflagellar transport at sites of axoneme assembly in Chlamydomonas and mammalian cells. Mol Biol Cell 14: 2041–2056.
- * , , , , , , , , , , , . 2005. Cytoplasmic dynein nomenclature. J Cell Biol 171: 411–413.
- , , , , , , , . 2006. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet 2: e1.
- , . 1997. Transport of a novel complex in the cytoplasmic matrix of Chlamydomonas flagella. Proc Natl Acad Sci USA 94: 4457–4462.
- , , , , , . 1997. Confocal analysis of primary cilia structure and colocalization with the Golgi apparatus in chondrocytes and aortic smooth muscle cells. Cell Biol Int 21: 483–494.
- , , , , . 1999. Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol Biol Cell 10: 693–712.
- , , . 2001. An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr Biol 11: 457–461.
- , , , , . 2004. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J Cell Biol 164: 255–266.
- , , , . 2007. Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr Biol 17: 193–202.
- , . 2005. Cilia and the cell cycle? J Cell Biol 169: 707–710.
- , , , , , , . 2004. Targeted deletion of the novel cytoplasmic dynein mD2LIC disrupts the embryonic organiser, formation of the body axes and specification of ventral cell fates. Development 131: 4999–5007.
- . 1965. Olfactory cilia in the frog. J Cell Biol 25: 209–230.
- , . 2006. Vesicle transport, cilium formation, and membrane specialization: the origins of a sensory organelle. Proc Natl Acad Sci USA 103: 18383–18384.
- , , , . 2007. Chlamydomonas FAP133 is a dynein intermediate chain associated with the retrograde intraflagellar transport motor. J Cell Sci 120: 3653–3665.
- , . 2002. Intraflagellar transport. Nat Rev Mol Cell Biol 3: 813–825.
- , . 2004. Design and regulation of the AAA+ microtubule motor dynein. J Struct Biol 146: 58–71.
- , . 2006. Overview of structure and function of mammalian cilia. Annu Rev Physiol 69: 377–400.
- , , , , . 2003. XBX-1 encodes a dynein light intermediate chain required for retrograde intraflagellar transport and cilia assembly in Caenorhabditis elegans. Mol Biol Cell 14: 2057–2070.
- , , , , , , , , , , , , , . 2006. The von Hippel-Lindau tumor suppressor protein controls ciliogenesis by orienting microtubule growth. J Cell Biol 175: 547–554.
- . 1996. Kinesin-II, a membrane traffic motor in axons, axonemes, and spindles. J Cell Biol 133: 1–4.
- . 2003. Intraflagellar transport. Annu Rev Cell Dev Biol 19: 423–443.
- . 2008. Intraflagellar transport motors in cilia: moving along the cell's antenna. J Cell Biol 180: 23–29.
- , , , . 2007. EB1 is required for primary cilia assembly in fibroblasts. Curr Biol 17: 1134–1139.
- , , , . 2000. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288: 1796–1802.
- , , , , , , , . 2007. Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. J Cell Biol 179: 1133–1140.
- , , , , . 1993. C. elegansosm-3 gene mediating osmotic avoidance behaviour encodes a kinesin-like protein. Neuroreport 4: 891–894.
- , , , , , , . 1999a. Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J Cell Biol 147: 519–530.
- , , , . 1999b. Two heteromeric kinesin complexes in chemosensory neurons and sensory cilia of Caenorhabditis elegans. Mol Biol Cell 10: 345–360.
- . 2002. A healthy understanding of intraflagellar transport. Cell Motil Cytoskeleton 52: 1–8.
- , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , . 2006. The transmembrane protein meckelin (MKS3) is mutated in Meckel-Gruber syndrome and the wpk rat. Nat Genet 38: 191–196.
- , , , , , , . 2004. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat Cell Biol 6: 1109–1113.
- . 1962. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J Cell Biol 15: 363–377.
- . 1968. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J Cell Sci 3: 207–230.
- , , , , , . 2004. A genetic screen identifies cilia genes as a principal cause of cystic kidney. Development 131: 4085–4093.
- , , , , , . 1999. Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A−/− mice analysis. J Cell Biol 145: 825–836.
- , , , , , . 2007. pVHL and GSK3b are components of a primary cilium-maintenance signalling network. Nat Cell Biol 9: 588–595.
- , . 2004. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42: 703–716.
- , , , , , . 2006. FAPP2, cilium formation, and compartmentalization of the apical membrane in polarized Madin-Darby canine kidney (MDCK) cells. Proc Natl Acad Sci USA 103: 18556–18561.
- , , . 2007. Nephrocystin and ciliary defects not only in the kidney? Pediatr Nephrol 22: 765–769.
- , , . 1994. The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein. J Cell Biol 126: 175–188.
- . 1967. Cilia and centrioles of the rat adrenal cortex. J Anat Lond. 101: 23–37.
- . 1969. Cilia in cell-cultured fibroblasts: I. On their occurence and relative frequencies in primary cultures and established cell lines. J Anat 105: 351–362.
- , . 2000. Length control of primary cilia: analysis of monociliate and multiciliate PtK1 cells. Biol Cell 92: 573–582.
- , , . 1996. Expression of primary cilia in mammalian cells. Cell Biol Int 20: 73–81.
- , . 2004. Regulation of flagellar assembly by glycogen synthase kinase 3 in Chlamydomonas reinhardtii. Eukaryot Cell 3: 1307–1319.
- . 2003. Cell motility: deaf Drosophila keep the beat. Curr Biol 13: R796–R798.
- , . 1998. Characterization of the KIF3C neural kinesin-like motor from mouse. Mol Biol Cell 9: 249–261.
- , , . 2001. Functional analysis of mouse kinesin motor Kif3C. Mol Cell Biol 21: 5306–5311.

1097-0177/asset/DVDY_left.gif?v=1&s=b87335326ab8ecd1f573539da0b5fa6abef26532)