The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery

Nature Genetics

Volumn 48, Issue 6, 2016, Pages 648-656

  Toriyama, Michinori ^a   Lee, Chanjae ^a   Taylor, S Paige ^b   Duran, Ivan ^b   Cohn, Daniel H ^c   Bruel, Ange Line ^d   Tabler, Jacqueline M ^a   Drew, Kevin ^a   Kelly, Marcus R ^e   Kim, Sukyoung ^a   Park, Tae Joo ^a,p   Braun, Daniella ^f   Pierquin, Ghislaine ^g   Biver, Armand ^h   Wagner, Kerstin ^h   Malfroot, Anne ⁱ   Panigrahi, Inusha ^j   Franco, Brunella ^k,l   Al lami, Hadeel Adel ^m   Yeung, Yvonne ^m   Choi, Yeon Ja ⁿ   Duffourd, Yannis ^d   Faivre, Laurence ^d,o   Rivière, Jean Baptiste ^d,o   Chen, Jiang ⁿ   Liu, Karen J ^m   Marcotte, Edward M ^a   Hildebrandt, Friedhelm ^f   Thauvin Robinet, Christel ^d,o   Krakow, Deborah ^c   Jackson, Peter K ^e   Wallingford, John B ^a   more..

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITÉ DE BOURGOGNE   (France)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f BOSTON CHILDREN S HOSPITAL   (United States)

^g UNIVERSITY OF LIÈGE   (Belgium)

^h Hospital Center   (Luxembourg)

ⁱ UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^j PIGMER   (India)

^k UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^l TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^m KING'S COLLEGE LONDON   (United Kingdom)

ⁿ STONY BROOK UNIVERSITY   (United States)

^o DIJON UNIVERSITY HOSPITAL   (France)

^p Ulsan National Institute of Science and Technology   (South Korea)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; CILIOGENESIS AND PLANAR POLARITY EFFECTOR PROTEIN; CLATHRIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; PROTEIN; PROTEIN BINDING;

ANIMAL TISSUE; ARTICLE; AXONEME; BLINDNESS; CELL POLARITY; CHONDRODYSPLASIA; CILIOPATHY; CRANIOFACIAL MALFORMATION; EUKARYOTIC FLAGELLUM; FRAMESHIFT MUTATION; GENETIC ANALYSIS; KIDNEY POLYCYSTIC DISEASE; KINETOSOME; MISSENSE MUTATION; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEOMICS; SKELETON MALFORMATION; XENOPUS; ANIMAL; FLAGELLUM; GENETICS; HUMAN; METABOLISM; MOUSE; MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; CILIOPATHIES; FLAGELLA; HUMANS; MICE; MUTATION; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEINS;

EID: 84966600215     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3558     Document Type: Article

References (76)

1. Hildebrandt, F., Benzing, T., & Katsanis, N. Ciliopathies. N. Engl. J. Med. 364, 1533-1543 (2011
2. Oh, E.C., & Katsanis, N. Cilia in vertebrate development and disease. Development 139, 443-448 (2012
3. Nachury, M.V., et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213 (2007
4. Sang, L., et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 145, 513-528 (2011
5. Garcia-Gonzalo, F.R., et al. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat. Genet. 43, 776-784 (2011
6. Kobayashi, D., & Takeda, H. Ciliary motility: the components and cytoplasmic preassembly mechanisms of the axonemal dyneins. Differentiation 83, S23-S29 (2012
7. Cole, D.G., et al. 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
8. Kozminski, K.G., Johnson, K.A., Forscher, P., & Rosenbaum, J.L. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA 90, 5519-5523 (1993
9. Pazour, G.J., Wilkerson, C.G., & Witman, G.B. A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J. Cell Biol. 141, 979-992 (1998
10. Piperno, G., et al. Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects. J. Cell Biol. 143, 1591-1601 (1998
11. Iomini, C., Babaev-Khaimov, V., Sassaroli, M., & Piperno, G. Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases. J. Cell Biol. 153, 13-24 (2001
12. Pedersen, L.B., Geimer, S., & Rosenbaum, J.L. Dissecting the molecular mechanisms of intraflagellar transport in chlamydomonas. Curr. Biol. 16, 450-459 (2006
13. Rompolas, P., Pedersen, L.B., Patel-King, R.S., & King, S.M. Chlamydomonas FAP133 is a dynein intermediate chain associated with the retrograde intraflagellar transport motor. J. Cell Sci. 120, 3653-3665 (2007
14. Ou, G., Blacque, O.E., Snow, J.J., Leroux, M.R., & Scholey, J.M. Functional coordination of intraflagellar transport motors. Nature 436, 583-587 (2005
15. Mukhopadhyay, S., et al. TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev. 24, 2180-2193 (2010
16. Liem, K.F. Jr., et al. The IFT-A complex regulates Shh signaling through cilia structure and membrane protein trafficking. J. Cell Biol. 197, 789-800 (2012
17. Behal, R.H., et al. Subunit interactions and organization of the Chlamydomonas reinhardtii intraflagellar transport complex A proteins. J. Biol. Chem. 287, 11689-11703 (2012
18. Lucker, B.F., et al. Characterization of the intraflagellar transport complex B core: direct interaction of the IFT81 and IFT74/72 subunits. J. Biol. Chem. 280, 27688-27696 (2005
19. Taschner, M., Bhogaraju, S., & Lorentzen, E. Architecture and function of IFT complex proteins in ciliogenesis. Differentiation 83, S12-S22 (2012
20. Craft, J.M., Harris, J.A., Hyman, S., Kner, P., & Lechtreck, K.F. Tubulin transport by IFT is upregulated during ciliary growth by a cilium-autonomous mechanism. J. Cell Biol. 208, 223-237 (2015
21. Bhogaraju, S., et al. Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science 341, 1009-1012 (2013
22. Tarkar, A., et al. DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nat. Genet. 45, 995-1003 (2013
23. Omran, H., et al. Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins. Nature 456, 611-616 (2008
24. Mitchison, H.M., et al. Mutations in axonemal dynein assembly factor DNAAF3 cause primary ciliary dyskinesia. Nat. Genet. 44, 381-389, S1-S2 (2012
25. Horani, A., et al. Whole-exome capture and sequencing identifies HEATR2 mutation as a cause of primary ciliary dyskinesia. Am. J. Hum. Genet. 91, 685-693 (2012
26. Diggle, C.P., et al. HEATR2 plays a conserved role in assembly of the ciliary motile apparatus. PLoS Genet. 10, e1004577 (2014
27. Seo, S., et al. BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly. Proc. Natl. Acad. Sci. USA 107, 1488-1493 (2010
28. Zhang, Q., Yu, D., Seo, S., Stone, E.M., & Sheffield, V.C. Intrinsic protein-protein interaction-mediated and chaperonin-assisted sequential assembly of stable Bardet-Biedl syndrome protein complex, the BBSome. J. Biol. Chem. 287, 20625-20635 (2012
29. Goetz, S.C., Liem, K.F. Jr., & Anderson, K.V. The spinocerebellar ataxia-associated gene Tau tubulin kinase 2 controls the initiation of ciliogenesis. Cell 151, 847-858 (2012
30. Ye, X., Zeng, H., Ning, G., Reiter, J.F., & Liu, A. C2cd3 is critical for centriolar distal appendage assembly and ciliary vesicle docking in mammals. Proc. Natl. Acad. Sci. USA 111, 2164-2169 (2014
31. Singla, V., Romaguera-Ros, M., Garcia-Verdugo, J.M., & Reiter, J.F. Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev. Cell 18, 410-424 (2010
32. Joo, K., et al. CCDC41 is required for ciliary vesicle docking to the mother centriole. Proc. Natl. Acad. Sci. USA 110, 5987-5992 (2013
33. Adler, P.N., Charlton, J., & Park, W.J. The Drosophila tissue polarity gene inturned functions prior to wing hair morphogenesis in the regulation of hair polarity and number. Genetics 137, 829-836 (1994
34. Collier, S., & Gubb, D. Drosophila tissue polarity requires the cell-autonomous activity of the fuzzy gene, which encodes a novel transmembrane protein. Development 124, 4029-4037 (1997
35. Collier, S., Lee, H., Burgess, R., & Adler, P. The WD40 repeat protein fritz links cytoskeletal planar polarity to frizzled subcellular localization in the Drosophila epidermis. Genetics 169, 2035-2045 (2005
36. Kim, S.K., et al. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329, 1337-1340 (2010
37. Park, T.J., Haigo, S.L., & Wallingford, J.B. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 38, 303-311 (2006
38. Huttlin, E.L., et al. The BioPlex network: a systematic exploration of the human interactome. Cell 162, 425-440 (2015
39. Rual, J.F., et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 437, 1173-1178 (2005
40. Wang, Y., Yan, J., Lee, H., Lu, Q., & Adler, P.N. The proteins encoded by the Drosophila planar polarity effector genes inturned, fuzzy and fritz interact physically and can re-pattern the accumulation of upstream planar cell polarity proteins. Dev. Biol. 394, 156-169 (2014
41. Gray, R.S., et al. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nat. Cell Biol. 11, 1225-1232 (2009
42. Alazami, A.M., et al. Molecular characterization of Joubert syndrome in Saudi Arabia. Hum. Mutat. 33, 1423-1428 (2012
43. Lopez, E., et al. C5orf42 is the major gene responsible for OFD syndrome type VI. Hum. Genet. 133, 367-377 (2014
44. Shaheen, R., et al. Genomic analysis of Meckel-Gruber syndrome in Arabs reveals marked genetic heterogeneity and novel candidate genes. Eur. J. Hum. Genet. 21, 762-768 (2013
45. Srour, M., et al. Mutations in C5orf42 cause Joubert syndrome in the French Canadian population. Am. J. Hum. Genet. 90, 693-700 (2012
46. Damerla, R.R., et al. Novel Jbts17 mutant mouse model of Joubert syndrome with cilia transition zone defects and cerebellar and other ciliopathy related anomalies. Hum. Mol. Genet. 24, 3994-4005 (2015
47. Brooks, E.R., & Wallingford, J.B. Control of vertebrate intraflagellar transport by the planar cell polarity effector Fuz. J. Cell Biol. 198, 37-45 (2012
48. Brooks, E.R., & Wallingford, J.B. The small GTPase Rsg1 is important for the cytoplasmic localization and axonemal dynamics of intraflagellar transport proteins. Cilia 2, 13 (2013
49. Gurrieri, F., Franco, B., Toriello, H., & Neri, G. Oral-facial-digital syndromes: review and diagnostic guidelines. Am. J. Med. Genet. A. 143A, 3314-3323 (2007
50. Tabler, J.M., et al. Fuz mutant mice reveal shared mechanisms between ciliopathies and FGF-related syndromes. Dev. Cell 25, 623-635 (2013
51. Merrill, A.E., et al. Ciliary abnormalities due to defects in the retrograde transport protein DYNC2H1 in short-rib polydactyly syndrome. Am. J. Hum. Genet. 84, 542-549 (2009
52. Mill, P., et al. Human and mouse mutations in WDR35 cause short-rib polydactyly syndromes due to abnormal ciliogenesis. Am. J. Hum. Genet. 88, 508-515 (2011
53. Hsieh, Y.C., & Hou, J.W. Oral-facial-digital syndrome with Y-shaped fourth metacarpals and endocardial cushion defect. Am. J. Med. Genet. 86, 278-281 (1999
54. Panigrahi, I., Das, R.R., Kulkarni, K.P., & Marwaha, R.K. Overlapping phenotypes in OFD type II and OFD type VI: report of two cases. Clin. Dysmorphol. 22, 109-114 (2013
55. Saari, J., Lovell, M.A., Yu, H.C., & Bellus, G.A. Compound heterozygosity for a frame shift mutation and a likely pathogenic sequence variant in the planar cell polarity-ciliogenesis gene WDPCP in a girl with polysyndactyly, coarctation of the aorta, and tongue hamartomas. Am. J. Med. Genet. A. 167A, 421-427 (2015
56. Li, Y., et al. Global genetic analysis in mice unveils central role for cilia in congenital heart disease. Nature 521, 520-524 (2015
57. Cui, C., et al. Wdpcp, a PCP protein required for ciliogenesis, regulates directional cell migration and cell polarity by direct modulation of the actin cytoskeleton. PLoS Biol. 11, e1001720 (2013
58. Butler, M.T., & Wallingford, J.B. Control of vertebrate core planar cell polarity protein localization and dynamics by Prickle 2. Development 142, 3429-3439 (2015
59. Zilber, Y., et al. The PCP effector Fuzzy controls cilial assembly and signaling by recruiting Rab8 and Dishevelled to the primary cilium. Mol. Biol. Cell 24, 555-565 (2013
60. van Dam, T.J., et al. Evolution of modular intraflagellar transport from a coatomer-like progenitor. Proc. Natl. Acad. Sci. USA 110, 6943-6948 (2013
61. Pan, X., et al. 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 (2006
62. Snow, J.J., et al. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6, 1109-1113 (2004
63. Harris, J.A., Liu, Y., Yang, P., Kner, P., & Lechtreck, K.F. Single particle imaging reveals IFT-independent transport and accumulation of EB1 in Chlamydomonas flagella. Mol. Biol. Cell 27, 295-307 (2016
64. Seo, J.H., et al. Mutations in the planar cell polarity gene, Fuzzy, are associated with neural tube defects in humans. Hum. Mol. Genet. 20, 4324-4333 (2011
65. Ooi, Y.S., Stiles, K.M., Liu, C.Y., Taylor, G.M., & Kielian, M. Genome-wide RNAi screen identifies novel host proteins required for alphavirus entry. PLoS Pathog. 9, e1003835 (2013
66. Giles, R.H., Ajzenberg, H., & Jackson, P.K. 3D spheroid model of mIMCD3 cells for studying ciliopathies and renal epithelial disorders. Nat. Protoc. 9, 2725-2731 (2014
67. Moody, S.A., & Kline, M.J. Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres. Anat. Embryol. (Berl) 182, 347-362 (1990
68. Zeng, H., Hoover, A.N., & Liu, A. PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals. Dev. Biol. 339, 418-428 (2010
69. Karpinka, J.B., et al. Xenbase, the Xenopus model organism database; new virtualized system, data types and genomes. Nucleic Acids Res. 43, D756-D763 (2015
70. Park, T.J., Mitchell, B.J., Abitua, P.B., Kintner, C., & Wallingford, J.B. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet. 40, 871-879 (2008
71. Nakayama, T., et al. Cas9-based genome editing in Xenopus tropicalis. Methods Enzymol. 546, 355-375 (2014
72. Lee, C., Kieserman, E., Gray, R.S., Park, T.J., & Wallingford, J. Whole-mount fluorescence immunocytochemistry on Xenopus embryos. CSH Protoc. 2008, pdb.prot4957 (2008
73. Sive, H.L., Grainger, R.M., & Harland, R.M. Early Development of Xenopus Laevis: A Laboratory Manual (Cold Spring Harbor Press, 2000
74. Söding, J. Protein homology detection by HMM-HMM comparison. Bioinformatics 21, 951-960 (2005
75. Lobley, A., Sadowski, M.I., & Jones, D.T. pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics 25, 1761-1767 (2009
76. Hasegawa, H., & Holm, L. Advances and pitfalls of protein structural alignment. Curr. Opin. Struct. Biol. 19, 341-348 (2009