The Emerging Complexity of the Vertebrate Cilium: New Functional Roles for an Ancient Organelle

Developmental Cell

Volumn 11, Issue 1, 2006, Pages 9-19

  Davis, Erica E ^a   Brueckner, Martina ^b   Katsanis, Nicholas ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; PROTEOME; WNT PROTEIN;

CELL COMPOSITION; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL ORGANELLE; CELL STRUCTURE; CELL SURFACE; CELL TYPE; COMPLEX FORMATION; EUKARYOTIC FLAGELLUM; HUMAN; KINETOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE;

ANIMALS; CHEMORECEPTORS; CILIA; EVOLUTION; HEDGEHOG PROTEINS; HUMANS; MECHANORECEPTORS; MODELS, BIOLOGICAL; MORPHOGENESIS; MOVEMENT; PROTEOME; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; VERTEBRATES; WNT PROTEINS;

VERTEBRATA;

EID: 33745496759     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2006.06.009     Document Type: Review

References (97)

1. Aebersold R., and Mann M. Mass spectrometry-based proteomics. Nature 422 (2003) 198-207
2. Amack J.D., and Yost H.J. The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr. Biol. 14 (2004) 685-690
3. Andersen J.S., Wilkinson C.J., Mayor T., Mortensen P., Nigg E.A., and Mann M. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426 (2003) 570-574
4. Avidor-Reiss T., Maer A.M., Koundakjian E., Polyanovsky A., Keil T., Subramaniam S., and Zuker C.S. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117 (2004) 527-539
5. Badano J.L., Leitch C.C., Ansley S.J., May-Simera H., Lawson S., Lewis R.A., Beales P.L., Dietz H.C., Fisher S., and Katsanis N. Dissection of epistasis in oligogenic Bardet-Biedl syndrome. Nature 439 (2006) 326-330
6. Badano J.L., Mitsuma N., Beales P.L., and Katsanis N. The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7 (2006) 125-148
7. Bellomo D., Lander A., Harragan I., and Brown N.A. Cell proliferation in mammalian gastrulation: the ventral node and notochord are relatively quiescent. Dev. Dyn. 205 (1996) 471-485
8. Bisgrove B.W., Snarr B.S., Emrazian A., and Yost H.J. Polaris and Polycystin-2 in dorsal forerunner cells and Kupffer's vesicle are required for specification of the zebrafish left-right axis. Dev. Biol. 287 (2005) 274-288
9. Blacque O.E., Perens E.A., Boroevich K.A., Inglis P.N., Li C., Warner A., Khattra J., Holt R.A., Ou G., Mah A.K., et al. Functional genomics of the cilium, a sensory organelle. Curr. Biol. 15 (2005) 935-941
10. Brailov I., Bancila M., Brisorgueil M.J., Miquel M.C., Hamon M., and Verge D. Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res. 872 (2000) 271-275
11. Broadhead R., Dawe H.R., Farr H., Griffiths S., Hart S.R., Portman N., Shaw M.K., Ginger M.L., Gaskell S.J., McKean P.G., and Gull K. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440 (2006) 224-227
12. Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52 (2002) 297-354
13. Chauvet V., Tian X., Husson H., Grimm D.H., Wang T., Hiesberger T., Igarashi P., Bennett A.M., Ibraghimov-Beskrovnaya O., Somlo S., and Caplan M.J. Mechanical stimuli induce cleavage and nuclear translocation of the polycystin-1 C terminus. J. Clin. Invest. 114 (2004) 1433-1443
14. Christensen S.T., Guerra C.F., Awan A., Wheatley D.N., and Satir P. Insulin receptor-like proteins in Tetrahymena thermophila ciliary membranes. Curr. Biol. 13 (2003) R50-R52
15. Corbit K.C., Aanstad P., Singla V., Norman A.R., Stainier D.Y., and Reiter J.F. Vertebrate Smoothened functions at the primary cilium. Nature 437 (2005) 1018-1021
16. Delmas P. Polycystins: from mechanosensation to gene regulation. Cell 118 (2004) 145-148
17. Dutcher S.K. Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet. 11 (1995) 398-404
18. Dutcher S.K. Purification of basal bodies and basal body complexes from Chlamydomonas reinhardtii. Methods Cell Biol. 47 (1995) 323-334
19. Dutcher S.K. Elucidation of basal body and centriole functions in Chlamydomonas reinhardtii. Traffic 4 (2003) 443-451
20. Dwyer N.D., Troemel E.R., Sengupta P., and Bargmann C.I. Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell 93 (1998) 455-466
21. Efimenko E., Bubb K., Mak H.Y., Holzman T., Leroux M.R., Ruvkun G., Thomas J.H., and Swoboda P. Analysis of xbx genes in C. elegans. Development 132 (2005) 1923-1934
22. Eley L., Turnpenny L., Yates L.M., Craighead A.S., Morgan D., Whistler C., Goodship J.A., and Strachan T. A perspective on inversin. Cell Biol. Int. 28 (2004) 119-124
23. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., and Yost H.J. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132 (2005) 1247-1260
24. Evans J.E., Snow J.J., Gunnarson A.L., Ou G., Stahlberg H., McDonald K.L., and Scholey J.M. Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. J. Cell Biol. 172 (2006) 663-669
25. Fromherz S., Giddings Jr. T.H., Gomez-Ospina N., and Dutcher S.K. Mutations in α-tubulin promote basal body maturation and flagellar assembly in the absence of δ-tubulin. J. Cell Sci. 117 (2004) 303-314
26. Gibbons B.H., Baccetti B., and Gibbons I.R. Live and reactivated motility in the 9+0 flagellum of Anguilla sperm. Cell Motil. 5 (1985) 333-350
27. Guay-Woodford L.M. Murine models of polycystic kidney disease: molecular and therapeutic insights. Am. J. Physiol. Renal Physiol. 285 (2003) F1034-F1049
28. Hanaoka K., Qian F., Boletta A., Bhunia A.K., Piontek K., Tsiokas L., Sukhatme V.P., Guggino W.B., and Germino G.G. Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408 (2000) 990-994
29. Handel M., Schulz S., Stanarius A., Schreff M., Erdtmann-Vourliotis M., Schmidt H., Wolf G., and Hollt V. Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89 (1999) 909-926
30. Haycraft C.J., Banizs B., Aydin-Son Y., Zhang Q., Michaud E.J., and Yoder B.K. Gli2 and gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 1 (2005) e53
31. Huangfu D., and Anderson K.V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102 (2005) 11325-11330
32. Huangfu D., and Anderson K.V. Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133 (2006) 3-14
33. Huangfu D., Liu A., Rakeman A.S., Murcia N.S., Niswander L., and Anderson K.V. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426 (2003) 83-87
34. Ingham P.W., and McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15 (2001) 3059-3087
35. Iomini C., Tejada K., Mo W., Vaananen H., and Piperno G. Primary cilia of human endothelial cells disassemble under laminar shear stress. J. Cell Biol. 164 (2004) 811-817
36. Jenkins P.M., Hurd T.W., Zhang L., McEwen D.P., Brown R.L., Margolis B., Verhey K.J., and Martens J.R. Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr. Biol. 16 (2006) 1211-1216
37. Jensen C.G., Poole C.A., McGlashan S.R., Marko M., Issa Z.I., Vujcich K.V., and Bowser S.S. Ultrastructural, tomographic and confocal imaging of the chondrocyte primary cilium in situ. Cell Biol. Int. 28 (2004) 101-110
38. Karcher C., Fischer A., Schweickert A., Bitzer E., Horie S., Witzgall R., and Blum M. Lack of a laterality phenotype in Pkd1 knock-out embryos correlates with absence of polycystin-1 in nodal cilia. Differentiation 73 (2005) 425-432
39. Katsanis N. Ciliary proteins and exencephaly. Nat. Genet. 38 (2006) 135-136
40. Keller L.C., Romijn E.P., Zamora I., Yates III J.R., and Marshall W.F. Proteomic analysis of isolated chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr. Biol. 15 (2005) 1090-1098
41. Kramer-Zucker A.G., Olale F., Haycraft C.J., Yoder B.K., Schier A.F., and Drummond I.A. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132 (2005) 1907-1921
42. Landfear S.M. Cell biology: when the tail wags the dog. Nature 440 (2006) 153-154
43. Li J.B., Gerdes J.M., Haycraft C.J., Fan Y., Teslovich T.M., May-Simera H., Li H., Blacque O.E., Li L., Leitch C.C., et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117 (2004) 541-552
44. Liu A., Wang B., and Niswander L.A. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 132 (2005) 3103-3111
45. Logan C.Y., and Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 781-810
46. Low S.H., Vasanth S., Larson C.H., Mukherjee S., Sharma N., Kinter M.T., Kane M.E., Obara T., and Weimbs T. Polycystin-1, STAT6, and P100 function in a pathway that transduces ciliary mechanosensation and is activated in polycystic kidney disease. Dev. Cell 10 (2006) 57-69
47. Manton I., Kowallik K., and von Stosch H.A. Observations on the fine structure and development of the spindle at mitosis and meiosis in a marine centric diatom (Lithodesmium undulatum). IV. The second meiotic division and conclusion. J. Cell Sci. 7 (1970) 407-443
48. May S.R., Ashique A.M., Karlen M., Wang B., Shen Y., Zarbalis K., Reiter J., Ericson J., and Peterson A.S. 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 (2005) 378-389
49. McGrath J., Somlo S., Makova S., Tian X., and Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114 (2003) 61-73
50. Mitchell D.R. Speculations on the evolution of 9+2 organelles and the role of central pair microtubules. Biol. Cell. 96 (2004) 691-696
51. Mochizuki T., Saijoh Y., Tsuchiya K., Shirayoshi Y., Takai S., Taya C., Yonekawa H., Yamada K., Nihei H., Nakatsuji N., et al. Cloning of inv, a gene that controls left/right asymmetry and kidney development. Nature 395 (1998) 177-181
52. Nauli S.M., Alenghat F.J., Luo Y., Williams E., Vassilev P., Li X., Elia A.E., Lu W., Brown E.M., Quinn S.J., et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33 (2003) 129-137
53. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., and Hirokawa N. 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 (1998) 829-837
54. Nonaka S., Shiratori H., Saijoh Y., and Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418 (2002) 96-99
55. Nonaka S., Yoshiba S., Watanabe D., Ikeuchi S., Goto T., Marshall W.F., and Hamada H. De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol. 3 (2005) e268
56. Okada Y., Nonaka S., Tanaka Y., Saijoh Y., Hamada H., and Hirokawa N. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol. Cell 4 (1999) 459-468
57. Okada Y., Takeda S., Tanaka Y., Belmonte J.C., and Hirokawa N. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121 (2005) 633-644
58. Olbrich H., Haffner K., Kispert A., Volkel A., Volz A., Sasmaz G., Reinhardt R., Hennig S., Lehrach H., Konietzko N., et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat. Genet. 30 (2002) 143-144
59. Ostrowski L.E., Blackburn K., Radde K.M., Moyer M.B., Schlatzer D.M., Moseley A., and Boucher R.C. A proteomic analysis of human cilia: identification of novel components. Mol. Cell. Proteomics 1 (2002) 451-465
60. Otto E.A., Schermer B., Obara T., O'Toole J.F., Hiller K.S., Mueller A.M., Ruf R.G., Hoefele J., Beekmann F., Landau D., et al. Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat. Genet. 34 (2003) 413-420
61. Ou G., Blacque O.E., Snow J.J., Leroux M.R., and Scholey J.M. Functional coordination of intraflagellar transport motors. Nature 436 (2005) 583-587
62. Park T.J., Haigo S.L., and 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 (2006) 303-311
63. Pazour G.J., Dickert B.L., Vucica Y., Seeley E.S., Rosenbaum J.L., Witman G.B., and Cole D.G. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151 (2000) 709-718
64. Pazour G.J., San Agustin J.T., Follit J.A., Rosenbaum J.L., and Witman G.B. Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr. Biol. 12 (2002) R378-R380
65. Pazour G.J., Agrin N., Leszyk J., and Witman G.B. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170 (2005) 103-113
66. Pennekamp P., Karcher C., Fischer A., Schweickert A., Skryabin B., Horst J., Blum M., and Dworniczak B. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 12 (2002) 938-943
67. Perkins L.A., Hedgecock E.M., Thomson J.N., and Culotti J.G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117 (1986) 456-487
68. Poole C.A., Jensen C.G., Snyder J.A., Gray C.G., Hermanutz V.L., and Wheatley D.N. Confocal analysis of primary cilia structure and colocalization with the Golgi apparatus in chondrocytes and aortic smooth muscle cells. Cell Biol. Int. 21 (1997) 483-494
69. Porter M.E., and Sale W.S. The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J. Cell Biol. 151 (2000) F37-F42
70. Praetorius H.A., and Spring K.R. Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 184 (2001) 71-79
71. Praetorius H.A., and Spring K.R. Removal of the MDCK cell primary cilium abolishes flow sensing. J. Membr. Biol. 191 (2003) 69-76
72. Quarmby L.M. Cellular deflagellation. Int. Rev. Cytol. 233 (2004) 47-91
73. Quarmby L.M., and Parker J.D. Cilia and the cell cycle?. J. Cell Biol. 169 (2005) 707-710
74. Rosenbaum J.L., and Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3 (2002) 813-825
75. Ross A.J., May-Simera H., Eichers E.R., Kai M., Hill J., Jagger D.J., Leitch C.C., Chapple J.P., Munro P.M., Fisher S., et al. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 37 (2005) 1135-1140
76. Sarmah B., Latimer A.J., Appel B., and Wente S.R. Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev. Cell 9 (2005) 133-145
77. Satir P. The cilium as a biological nanomachine. FASEB J. 13 Suppl 2 (1999) S235-S237
78. Sawamoto K., Wichterle H., Gonzalez-Perez O., Cholfin J.A., Yamada M., Spassky N., Murcia N.S., Garcia-Verdugo J.M., Marin O., Rubenstein J.L., et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311 (2006) 629-632
79. Schneider L., Clement C.A., Teilmann S.C., Pazour G.J., Hoffmann E.K., Satir P., and Christensen S.T. PDGFRαα signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15 (2005) 1861-1866
80. Schwartz E.A., Leonard M.L., Bizios R., and Bowser S.S. Analysis and modeling of the primary cilium bending response to fluid shear. Am. J. Physiol. 272 (1997) F132-F138
81. Setou M., Nakagawa T., Seog D.H., and Hirokawa N. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288 (2000) 1796-1802
82. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Kronig C., Schermer B., Benzing T., Cabello O.A., Jenny A., et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37 (2005) 537-543
83. Smith U.M., Consugar M., Tee L.J., McKee B.M., Maina E.N., Whelan S., Morgan N.V., Goranson E., Gissen P., Lilliquist S., et al. The transmembrane protein meckelin (MKS3) is mutated in Meckel-Gruber syndrome and the wpk rat. Nat. Genet. 38 (2006) 191-196
84. Snow J.J., Ou G., Gunnarson A.L., Walker M.R., Zhou H.M., Brust-Mascher I., and Scholey J.M. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6 (2004) 1109-1113
85. Stoetzel C., Laurier V., Davis E.E., Muller J., Rix S., Badano J.L., Leitch C.C., Salem N., Chouery E., Corbani S., et al. BBS10 encodes a vertebrate-specific chaperonin-like protein and is a major BBS locus. Nat. Genet. 38 (2006) 521-524
86. Stolc V., Samanta M.P., Tongprasit W., and Marshall W.F. Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes. Proc. Natl. Acad. Sci. USA 102 (2005) 3703-3707
87. Sulik K., Dehart D.B., Iangaki T., Carson J.L., Vrablic T., Gesteland K., and Schoenwolf G.C. Morphogenesis of the murine node and notochordal plate. Dev. Dyn. 201 (1994) 260-278
88. Supp D.M., Brueckner M., Kuehn M.R., Witte D.P., Lowe L.A., McGrath J., Corrales J., and Potter S.S. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 126 (1999) 5495-5504
89. Tabin C.J., and Vogan K.J. A two-cilia model for vertebrate left-right axis specification. Genes Dev. 17 (2003) 1-6
90. Tallquist M., and Kazlauskas A. PDGF signaling in cells and mice. Cytokine Growth Factor Rev. 15 (2004) 205-213
91. Tanaka Y., Okada Y., and Hirokawa N. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435 (2005) 172-177
92. Torban E., Kor C., and Gros P. Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet. 20 (2004) 570-577
93. Veeman M.T., Axelrod J.D., and Moon R.T. A second canon. Functions and mechanisms of β-catenin-independent Wnt signaling. Dev. Cell 5 (2003) 367-377
94. Webber W.A., and Lee J. Fine structure of mammalian renal cilia. Anat. Rec. 182 (1975) 339-343
95. Wheatley D.N. Landmarks in the first hundred years of primary (9+0) cilium research. Cell Biol. Int. 29 (2005) 333-339
96. Wiederhold M.L. Mechanosensory transduction in "sensory" and "motile" cilia. Annu. Rev. Biophys. Bioeng. 5 (1976) 39-62
97. Zimmerman K.W. Beitrage zur Kenntniss einiger Drusen und epithelien. Arch. Mikrosk. Anat. 52 (1898) 552-706