Proteomic analysis of isolated ciliary transition zones reveals the presence of ESCRT proteins

Current Biology

Volumn 25, Issue 3, 2015, Pages 379-384

  Diener, Dennis R ^a   Lupetti, Pietro ^b   Rosenbaum, Joel L ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS; CHLAMYDOMONAS; VERTEBRATA;

ESCRT PROTEIN; NUCLEOPORIN; PROTEOME;

CHLAMYDOMONAS; ELECTRON MICROSCOPY; EUKARYOTIC FLAGELLUM; GENETICS; METABOLISM; PROCEDURES; PROTEOMICS; ULTRASTRUCTURE;

CHLAMYDOMONAS; CILIA; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; MICROSCOPY, ELECTRON; NUCLEAR PORE COMPLEX PROTEINS; PROTEOME; PROTEOMICS;

EID: 84922899440     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.11.066     Document Type: Article

References (49)

1. N.B. Gilula, and P. Satir The ciliary necklace. A ciliary membrane specialization J. Cell Biol. 53 1972 494 509
2. B. Craige, C.C. Tsao, D.R. Diener, Y. Hou, K.F. Lechtreck, J.L. Rosenbaum, and G.B. Witman CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content J. Cell Biol. 190 2010 927 940
3. C.L. Williams, C. Li, K. Kida, P.N. Inglis, S. Mohan, L. Semenec, N.J. Bialas, R.M. Stupay, N. Chen, and O.E. Blacque et al. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis J. Cell Biol. 192 2011 1023 1041
4. F.R. Garcia-Gonzalo, K.C. Corbit, M.S. Sirerol-Piquer, G. Ramaswami, E.A. Otto, T.R. Noriega, A.D. Seol, J.F. Robinson, C.L. Bennett, and D.J. Josifova et al. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition Nat. Genet. 43 2011 776 784
5. Q. Hu, and W.J. Nelson Ciliary diffusion barrier: the gatekeeper for the primary cilium compartment Cytoskeleton (Hoboken) 68 2011 313 324
6. J.F. Reiter, O.E. Blacque, and M.R. Leroux The base of the cilium: roles for transition fibres and the transition zone in ciliary formation, maintenance and compartmentalization EMBO Rep. 13 2012 608 618
7. J.L. Tobin, and P.L. Beales The nonmotile ciliopathies Genet. Med. 11 2009 386 402
8. K. Szymanska, and C.A. Johnson The transition zone: an essential functional compartment of cilia Cilia 1 2012 10
9. K. Madhivanan, and R.C. Aguilar Ciliopathies: the trafficking connection Traffic 15 2014 1031 1056
10. L. Sang, J.J. Miller, K.C. Corbit, R.H. Giles, M.J. Brauer, E.A. Otto, L.M. Baye, X. Wen, S.J. Scales, and M. Kwong et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways Cell 145 2011 513 528
11. B. Chih, P. Liu, Y. Chinn, C. Chalouni, L.G. Komuves, P.E. Hass, W. Sandoval, and A.S. Peterson A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain Nat. Cell Biol. 14 2012 61 72
12. D.L. Ringo Flagellar motion and fine structure of the flagellar apparatus in Chlamydomonas J. Cell Biol. 33 1967 543 571
13. S. Geimer, and M. Melkonian The ultrastructure of the Chlamydomonas reinhardtii basal apparatus: identification of an early marker of radial asymmetry inherent in the basal body J. Cell Sci. 117 2004 2663 2674
14. R.G.W. Anderson, and C.E. Hein Distribution of anionic sites on the oviduct ciliary membrane J. Cell Biol. 72 1977 482 492
15. T. Cavalier-Smith Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii J. Cell Sci. 16 1974 529 556
16. K.P. Gaffal The basal body-root complex of Chlamydomonas reinhardtii during mitosis Protoplasma 143 1988 118 129
17. J.D. Parker, L.K. Hilton, D.R. Diener, M.Q. Rasi, M.R. Mahjoub, J.L. Rosenbaum, and L.M. Quarmby Centrioles are freed from cilia by severing prior to mitosis Cytoskeleton (Hoboken) 67 2010 425 430
18. W.J. Snell Characterization of the Chlamydomonas flagellar collar Cell Motil. Cytoskeleton 3 1983 273 280
19. M.A. Sanders, and J.L. Salisbury Centrin-mediated microtubule severing during flagellar excision in Chlamydomonas reinhardtii J. Cell Biol. 108 1989 1751 1760
20. G.J. Pazour, N. Agrin, J. Leszyk, and G.B. Witman Proteomic analysis of a eukaryotic cilium J. Cell Biol. 170 2005 103 113
21. K.F. Lechtreck, E.C. Johnson, T. Sakai, D. Cochran, B.A. Ballif, J. Rush, G.J. Pazour, M. Ikebe, and G.B. Witman The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella J. Cell Biol. 187 2009 1117 1132
22. P.G. Czarnecki, and J.V. Shah The ciliary transition zone: from morphology and molecules to medicine Trends Cell Biol. 22 2012 201 210
23. A.R. Barker, K.S. Renzaglia, K. Fry, and H.R. Dawe Bioinformatic analysis of ciliary transition zone proteins reveals insights into the evolution of ciliopathy networks BMC Genomics 15 2014 531
24. T.A. Lohret, L. Zhao, and L.M. Quarmby Cloning of Chlamydomonas p60 katanin and localization to the site of outer doublet severing during deflagellation Cell Motil. Cytoskeleton 43 1999 221 231
25. R.J. Finst, P.J. Kim, E.R. Griffis, and L.M. Quarmby Fa1p is a 171 kDa protein essential for axonemal microtubule severing in Chlamydomonas J. Cell Sci. 113 2000 1963 1971
26. E. Morita, L.A. Colf, M.A. Karren, V. Sandrin, C.K. Rodesch, and W.I. Sundquist Human ESCRT-III and VPS4 proteins are required for centrosome and spindle maintenance Proc. Natl. Acad. Sci. USA 107 2010 12889 12894
27. J.L. Rosenbaum, and G.B. Witman Intraflagellar transport Nat. Rev. Mol. Cell Biol. 3 2002 813 825
28. H.L. Kee, and K.J. Verhey Molecular connections between nuclear and ciliary import processes Cilia 2 2013 11
29. H.L. Kee, J.F. Dishinger, T.L. Blasius, C.J. Liu, B. Margolis, and K.J. Verhey A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia Nat. Cell Biol. 14 2012 431 437
30. D.K. Breslow, E.F. Koslover, F. Seydel, A.J. Spakowitz, and M.V. Nachury An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier J. Cell Biol. 203 2013 129 147
31. S. Fan, V. Fogg, Q. Wang, X.W. Chen, C.J. Liu, and B. Margolis A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions J. Cell Biol. 178 2007 387 398
32. S. Fan, and B. Margolis The Ran importin system in cilia trafficking Organogenesis 7 2011 147 153
33. J.S. Andersen, C.J. Wilkinson, T. Mayor, P. Mortensen, E.A. Nigg, and M. Mann Proteomic characterization of the human centrosome by protein correlation profiling Nature 426 2003 570 574
34. Q. Liu, G. Tan, N. Levenkova, T. Li, E.N. Pugh Jr., J.J. Rux, D.W. Speicher, and E.A. Pierce The proteome of the mouse photoreceptor sensory cilium complex Mol. Cell. Proteomics 6 2007 1299 1317
35. D. Takao, J.F. Dishinger, H.L. Kee, J.M. Pinskey, B.L. Allen, and K.J. Verhey An assay for clogging the ciliary pore complex distinguishes mechanisms of cytosolic and membrane protein entry Curr. Biol. 24 2014 2288 2294
36. C. Bissig, and J. Gruenberg ALIX and the multivesicular endosome: ALIX in Wonderland Trends Cell Biol. 24 2014 19 25
37. K. Huang, D.R. Diener, and J.L. Rosenbaum The ubiquitin conjugation system is involved in the disassembly of cilia and flagella J. Cell Biol. 186 2009 601 613
38. A. Caballe, and J. Martin-Serrano ESCRT machinery and cytokinesis: the road to daughter cell separation Traffic 12 2011 1318 1326
39. J.F. Nabhan, R. Hu, R.S. Oh, S.N. Cohen, and Q. Lu Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein Proc. Natl. Acad. Sci. USA 109 2012 4146 4151
40. K. Bergman, U.W. Goodenough, D.A. Goodenough, J. Jawitz, and H. Martin Gametic differentiation in Chlamydomonas reinhardtii. II. Flagellar membranes and the agglutination reaction J. Cell Biol. 67 1975 606 622
41. C.R. Wood, K. Huang, D.R. Diener, and J.L. Rosenbaum The cilium secretes bioactive ectosomes Curr. Biol. 23 2013 906 911
42. O. Arnaiz, A. Malinowska, C. Klotz, L. Sperling, M. Dadlez, F. Koll, and J. Cohen Cildb: a knowledgebase for centrosomes and cilia Database (Oxford) 2009 2009 bap022
43. J. Hu, S.G. Wittekind, and M.M. Barr STAM and Hrs down-regulate ciliary TRP receptors Mol. Biol. Cell 18 2007 3277 3289
44. O.I. Kaplan, D.B. Doroquez, S. Cevik, R.V. Bowie, L. Clarke, A.A. Sanders, K. Kida, J.Z. Rappoport, P. Sengupta, and O.E. Blacque Endocytosis genes facilitate protein and membrane transport in C. elegans sensory cilia Curr. Biol. 22 2012 451 460
45. C.A. Clement, K.D. Ajbro, K. Koefoed, M.L. Vestergaard, I.R. Veland, M.P. Henriques de Jesus, L.B. Pedersen, A. Benmerah, C.Y. Andersen, L.A. Larsen, and S.T. Christensen TGF-β signaling is associated with endocytosis at the pocket region of the primary cilium Cell Rep. 3 2013 1806 1814
46. C.H. Sung, and M.R. Leroux The roles of evolutionarily conserved functional modules in cilia-related trafficking Nat. Cell Biol. 15 2013 1387 1397
47. W. Dentler A role for the membrane in regulating Chlamydomonas flagellar length PLoS ONE 8 2013 e53366
48. C.R. Wood, and J.L. Rosenbaum Proteins of the ciliary axoneme are found on cytoplasmic membrane vesicles during growth of cilia Curr. Biol. 24 2014 1114 1120
49. G.J. Hills, J.M. Phillips, M.R. Gay, and K. Roberts Self-assembly of a plant cell wall in vitro J. Mol. Biol. 96 1975 431 441