Active Transport and Diffusion Barriers Restrict Joubert Syndrome-Associated ARL13B/ARL-13 to an Inv-like Ciliary Membrane Subdomain

PLoS Genetics

Volumn 9, Issue 12, 2013, Pages

  Cevik, Sebiha ^a   Sanders, Anna A W M ^a   Van Wijk, Erwin ^b,c,d   Boldt, Karsten ^e   Clarke, Lara ^a   van Reeuwijk, Jeroen ^b,c   Hori, Yuji ^f   Horn, Nicola ^e   Hetterschijt, Lisette ^b   Wdowicz, Anita ^a   Mullins, Andrea ^a   Kida, Katarzyna ^a   Kaplan, Oktay I ^a,g   van Beersum, Sylvia E C ^b,c   Man Wu, Ka ^b,c   Letteboer, Stef J F ^b,c   Mans, Dorus A ^b,c   Katada, Toshiaki ^f   Kontani, Kenji ^f   Ueffing, Marius ^e,h   Roepman, Ronald ^b,c   Kremer, Hannie ^b,c,d   Blacque, Oliver E ^a   more..

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY   (Netherlands)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f UNIVERSITY OF TOKYO   (Japan)

^g MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADP RIBOSYLATION FACTOR LIKE 13B PROTEIN; GUANOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

ACTIVE TRANSPORT; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE; GENE FUNCTION; GENETIC CONSERVATION; IFT GENE; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MEMBRANE PERMEABILITY; MKS GENE; MOLECULAR IMAGING; MOUSE; NONHUMAN; NPHP GENE; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS;

ADP-RIBOSYLATION FACTORS; ANIMALS; BARDET-BIEDL SYNDROME; BIOLOGICAL TRANSPORT, ACTIVE; CAENORHABDITIS ELEGANS; CEREBELLAR DISEASES; CILIA; CILIARY MOTILITY DISORDERS; CYTOSKELETAL PROTEINS; ENCEPHALOCELE; EYE ABNORMALITIES; HUMANS; KIDNEY DISEASES, CYSTIC; MEMBRANES; POLYCYSTIC KIDNEY DISEASES; RETINA; TRANSCRIPTION FACTORS;

EID: 84892754718     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003977     Document Type: Article

References (68)

1. Fisch C, Dupuis-Williams P, (2011) Ultrastructure of cilia and flagella- back to the future!. Biol Cell 103: 249-319.
2. Marshall WF, (2008) Basal bodies platforms for building cilia. Curr Top Dev Biol 85: 1-22.
3. Reiter JF, Blacque OE, Leroux MR, (2012) The base of the cilium: roles for transition fibres and the transition zone in ciliary formation, maintenance and compartmentalization. EMBO Rep 13: 608-18.
4. Shiba D, Yamaoka Y, Hagiwara H, Takamatsu T, Hamada H, et al. (2009) Localization of Inv in a distinctive intraciliary compartment requires the C-terminal ninein-homolog-containing region. J Cell Sci 122: 44-54.
5. Warburton-Pitt S, Jauregui A, Li C, Wang J, Leroux M, et al. (2012) Ciliogenesis in Caenorhabditis elegans requires genetic interactions between ciliary middle segment localized NPHP-2 (inversin) and transition zone-associated proteins. J Cell Sci 125: 2592-3195.
6. Blacque OE, Cevik S, Kaplan OI, (2008) Intraflagellar transport: from molecular characterisation to mechanism. Front Biosci 13: 2633-2652.
7. Ishikawa H, Marshall W, (2011) Ciliogenesis: building the cell's antenna. Nature reviews Molecular cell biology 12: 222-256.
8. Qin H, Burnette DT, Bae YK, Forscher P, Barr MM, et al. (2005) Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr Biol 15: 1695-1699.
9. Huang K, Diener D, Mitchell A, Pazour G, Witman G, et al. (2007) Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J Cell Biol 179: 501-514.
10. Hao L, Thein M, Brust-Mascher I, Civelekoglu-Scholey G, Lu Y, et al. (2011) Intraflagellar transport delivers tubulin isotypes to sensory cilium middle and distal segments. Nat Cell Biol 13: 790-798.
11. Blacque OE, Reardon MJ, Li C, McCarthy J, Mahjoub MR, et al. (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.
12. Ou G, Blacque OE, Snow JJ, Leroux MR, Scholey JM, (2005) Functional coordination of intraflagellar transport motors. Nature 436: 583-587.
13. Lechtreck K-F, Johnson E, Sakai T, Cochran D, Ballif B, et al. (2009) The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol 187: 1117-1149.
14. Wei Q, Zhang Y, Li Y, Zhang Q, Ling K, et al. (2012) The BBSome controls IFT assembly and turnaround in cilia. Nat Cell Biol 14: 950-957.
15. Nachury MV, Seeley ES, Jin H, (2010) Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 26: 59-87.
16. Craige B, Tsao CC, Diener DR, Hou Y, Lechtreck KF, et al. (2010) CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 190: 927-940.
17. Chih B, Liu P, Chinn Y, Chalouni C, Komuves LG, et al. (2011) A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat Cell Biol 14: 61-72.
18. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, et al. (2011) A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43: 776-784.
19. Williams CL, Li C, Kida K, Inglis PN, Mohan S, et al. (2011) MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 192: 1023-1041.
20. Huang L, Szymanska K, Jensen VL, Janecke AR, Innes AM, et al. (2011) TMEM237 Is Mutated in Individuals with a Joubert Syndrome Related Disorder and Expands the Role of the TMEM Family at the Ciliary Transition Zone. Am J Hum Genet 89: 713-730.
21. Hu Q, Milenkovic L, Jin H, Scott MP, Nachury MV, et al. (2010) A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329: 436-439.
22. Kim S, Shindo A, Park T, Oh E, Ghosh S, et al. (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science (New York, NY) 329: 1337-1377.
23. Fan S, Fogg V, Wang Q, Chen XW, Liu CJ, et al. (2007) A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J Cell Biol 178: 387-398.
24. Dishinger JF, Kee HL, Jenkins PM, Fan S, Hurd TW, et al. (2010) Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-beta2 and RanGTP. Nat Cell Biol 12: 703-710.
25. Fan S, Whiteman EL, Hurd TW, McIntyre JC, Dishinger JE, et al. (2011) Induction of Ran GTP Drives Ciliogenesis. Mol Biol Cell pp. 4539-48.
26. Hurd TW, Fan S, Margolis BL, (2011) Localization of retinitis pigmentosa 2 to cilia is regulated by Importin beta2. J Cell Sci 124: 718-726.
27. Kee HL, Dishinger JF, Blasius TL, Liu CJ, Margolis B, et al. (2012) A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 14: 431-437.
28. Inglis PN, Ou G, Leroux MR, Scholey JM (2007) The sensory cilia of C. elegans. WormBook, ed The C elegans Research Community: WormBook. doi/101895/wormbook11231.
29. Pazour G, San Agustin J, Follit J, Rosenbaum J, Witman G, (2002) Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Current biology: CB 12: 80.
30. Bae YK, Qin H, Knobel KM, Hu J, Rosenbaum JL, et al. (2006) General and cell-type specific mechanisms target TRPP2/PKD-2 to cilia. Development 133: 3859-3870.
31. Cantagrel V, Silhavy JL, Bielas SL, Swistun D, Marsh SE, et al. (2008) Mutations in the cilia gene ARL13B lead to the classical form of Joubert syndrome. Am J Hum Genet 83: 170-179.
32. Caspary T, Larkins CE, Anderson KV, (2007) The graded response to Sonic Hedgehog depends on cilia architecture. Dev Cell 12: 767-778.
33. Hori Y, Kobayashi T, Kikko Y, Kontani K, Katada T, (2008) Domain architecture of the atypical Arf-family GTPase Arl13b involved in cilia formation. Biochem Biophys Res Commun 373: 119-124.
34. Duldulao NA, Lee S, Sun Z, (2009) Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/Scorpion. Development 136: 4033-4042.
35. Cevik S, Hori Y, Kaplan OI, Kida K, Toivenon T, et al. (2010) Joubert syndrome Arl13b functions at ciliary membranes and stabilizes protein transport in Caenorhabditis elegans. J Cell Biol 188: 953-969.
36. Li Y, Wei Q, Zhang Y, Ling K, Hu J, (2010) The small GTPases ARL-13 and ARL-3 coordinate intraflagellar transport and ciliogenesis. J Cell Biol 189: 1039-1051.
37. Larkins C, Aviles G, East M, Kahn R, Caspary T, (2011) Arl13b regulates ciliogenesis and the dynamic localization of Shh signaling proteins. Mol Biol Cell 22: 4694-5397.
38. Higginbotham H, Eom TY, Mariani LE, Bachleda A, Hirt J, et al. (2012) Arl13b in primary cilia regulates the migration and placement of interneurons in the developing cerebral cortex. Dev Cell 23: 925-938.
39. Humbert MC, Weihbrecht K, Searby CC, Li Y, Pope RM, et al. (2012) ARL13B, PDE6D, and CEP164 form a functional network for INPP5E ciliary targeting. Proc Natl Acad Sci U S A 109: 19691-6.
40. Li Y, Zhang Q, Wei Q, Zhang Y, Ling K, et al. (2012) SUMOylation of the small GTPase ARL-13 promotes ciliary targeting of sensory receptors. J Cell Biol 199: 589-598.
41. Snow JJ, Ou G, Gunnarson AL, Walker MR, Zhou HM, et al. (2004) Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat Cell Biol 6: 1109-1113.
42. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, et al. (2009) Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. Embo J 28: 183-192.
43. Chun DK, McEwen JM, Burbea M, Kaplan JM, (2008) UNC-108/Rab2 regulates postendocytic trafficking in Caenorhabditis elegans. Mol Biol Cell 19: 2682-2695.
44. Hsiao Y-C, Tuz K, Ferland R, (2012) Trafficking in and to the primary cilium. Cilia 1: 4.
45. Ou G, Koga M, Blacque OE, Murayama T, Ohshima Y, et al. (2007) Sensory Ciliogenesis in Caenorhabditis elegans: Assignment of IFT components into Distinct Modules Based on Transport and Phenotypic Profiles. Mol Biol Cell 18: 1554-69.
46. Mukhopadhyay S, Wen X, Chih B, Nelson C, Lane W, et al. (2010) 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.
47. Lechtreck K, Brown J, Sampaio J, Craft J, Shevchenko A, et al. (2013) Cycling of the signaling protein phospholipase D through cilia requires the BBSome only for the export phase. J Cell Biol 201: 249-261.
48. Pan F, Malmberg R, Momany M, (2007) Analysis of septins across kingdoms reveals orthology and new motifs. BMC evolutionary biology 7: 103.
49. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG, (1986) Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol 117: 456-487.
50. Gloeckner CJ, Boldt K, Schumacher A, Roepman R, Ueffing M, (2007) A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 7: 4228-4234.
51. Lucker BF, Behal RH, Qin H, Siron LC, Taggart WD, et al. (2005) Characterization of the intraflagellar transport complex B core: direct interaction of the IFT81 and IFT74/72 subunits. J Biol Chem 280: 27688-27696.
52. Lucker BF, Miller MS, Dziedzic SA, Blackmarr PT, Cole DG, (2010) Direct interactions of intraflagellar transport complex B proteins IFT88, IFT52, and IFT46. J Biol Chem 285: 21508-21518.
53. Sang L, Miller JJ, Corbit KC, Giles RH, Brauer MJ, et al. (2011) Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 145: 513-528.
54. Boldt K, Mans DA, Won J, van Reeuwijk J, Vogt A, et al. (2011) Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice. J Clin Invest 121: 2169-2180.
55. Shiba D, Manning D, Koga H, Beier D, Yokoyama T, (2010) Inv acts as a molecular anchor for Nphp3 and Nek8 in the proximal segment of primary cilia. Cytoskeleton (Hoboken, NJ) 67: 112-119.
56. Follit J, Xu F, Keady B, Pazour G, (2009) Characterization of mouse IFT complex B. Cell Motil Cytoskeleton 66: 457-468.
57. Franklin J, Ullu E, (2010) Biochemical analysis of PIFTC3, the Trypanosoma brucei orthologue of nematode DYF-13, reveals interactions with established and putative intraflagellar transport components. Mol Microbiol 78: 173-186.
58. Blacque OE, Perens EA, Boroevich KA, Inglis PN, Li C, et al. (2005) Functional genomics of the cilium, a sensory organelle. Curr Biol 15: 935-941.
59. Zhang Q, Liu Q, Austin C, Drummond I, Pierce E, (2012) Knockdown of ttc26 disrupts ciliogenesis of the photoreceptor cells and the pronephros in zebrafish. Mol Biol Cell 23: 3069-3078.
60. Nakada C, Ritchie K, Oba Y, Nakamura M, Hotta Y, et al. (2003) Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nat Cell Biol 5: 626-632.
61. Sarikas A, Hartmann T, Pan Z-Q, (2011) The cullin protein family. Genome Biol 12: 220.
62. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
63. Hobert O, (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32: 728-730.
64. Gloeckner CJ, Boldt K, Ueffing M, (2009) Strep/FLAG tandem affinity purification (SF-TAP) to study protein interactions. Curr Protoc Protein Sci Chapter 19: Unit19 20.
65. Bendall SC, Hughes C, Stewart MH, Doble B, Bhatia M, et al. (2008) Prevention of amino acid conversion in SILAC experiments with embryonic stem cells. Mol Cell Proteomics 7: 1587-1597.
66. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, et al. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 4: 2010-2021.
67. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372.
68. Letteboer SJ, Roepman R, (2008) Versatile screening for binary protein-protein interactions by yeast two-hybrid mating. Methods Mol Biol 484: 145-159.