The Vertebrate Primary Cilium in Development, Homeostasis, and Disease

Cell

Volumn 137, Issue 1, 2009, Pages 32-45

  Gerdes, Jantje M ^a   Davis, Erica E ^a   Katsanis, Nicholas ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN 2; POLYPEPTIDE; SONIC HEDGEHOG PROTEIN; VESICULAR TRANSPORT PROTEIN; WNT PROTEIN;

AXONEME; CELL ORGANELLE; CELL POLARITY; CELL STRUCTURE; CELL TRANSPORT; CELL TYPE; CONFOCAL MICROSCOPY; EUKARYOTIC FLAGELLUM; FLAGELLUM; GENETIC DISORDER; HOMEOSTASIS; KINETOSOME; MICROTUBULE; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PLEIOTROPY; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VERTEBRATE;

INVERTEBRATA; VERTEBRATA;

EID: 63049116544     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2009.03.023     Document Type: Review

References (118)

1. Abdelkhalek H.B., Beckers A., Schuster-Gossler K., Pavlova M.N., Burkhardt H., Lickert H., Rossant J., Reinhardt R., Schalkwyk L.C., Müller I., et al. The mouse homeobox gene Not is required for caudal notochord development and affected by the truncate mutation. Genes Dev. 18 (2004) 1725-1736
2. Adler P.N., Zhu C., and Stone D. Inturned localizes to the proximal side of wing cells under the instruction of upstream planar polarity proteins. Curr. Biol. 14 (2004) 2046-2051
3. Afzelius B.A. A human syndrome caused by immotile cilia. Science 193 (1976) 317-319
4. Arts H.H., Doherty D., van Beersum S.E., Parisi M.A., Letteboer S.J., Gorden N.T., Peters T.A., Marker T., Voesenek K., Kartono A., et al. Mutations in the gene encoding the basal body protein RPGRIP1L, a nephrocystin-4 interactor, cause Joubert syndrome. Nat. Genet. 39 (2007) 882-888
5. Axelrod J.D., Miller J.R., Shulman J.M., Moon R.T., and Perrimon N. Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12 (1998) 2610-2622
6. Baala L., Audollent S., Martinovic J., Ozilou C., Babron M.C., Sivanandamoorthy S., Saunier S., Salomon R., Gonzales M., Rattenberry E., et al. Pleiotropic effects of CEP290 (NPHP6) mutations extend to Meckel syndrome. Am. J. Hum. Genet. 81 (2007) 170-179
7. Baala L., Romano S., Khaddour R., Saunier S., Smith U.M., Audollent S., Ozilou C., Faivre L., Laurent N., Foliguet B., et al. The Meckel-Gruber syndrome gene, MKS3, is mutated in Joubert syndrome. Am. J. Hum. Genet. 80 (2007) 186-194
8. 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
9. Beales P.L., Bland E., Tobin J.L., Bacchelli C., Tuysuz B., Hill J., Rix S., Pearson C.G., Kai M., Hartley J., et al. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat. Genet. 39 (2007) 727-729
10. Beckers A., Alten L., Viebahn C., Andre P., and Gossler A. The mouse homeobox gene Noto regulates node morphogenesis, notochordal ciliogenesis, and left-right patterning. Proc. Natl. Acad. Sci. USA 104 (2007) 15675-15770
11. Berbari N.F., Lewis J.S., Bishop G.A., Askwith C.C., and Mykytyn K. Bardet-Biedl Syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc. Natl. Acad. Sci. USA 105 (2008) 4242-4246
12. Bergmann C., Fliegauf M., Bruchle N.O., Frank V., Olbrich H., Kirschner J., Schermer B., Schmedding I., Kispert A., Kranzlin B., et al. Loss of nephrocystin-3 function can cause embryonic lethality, Meckel-Gruber-like syndrome, situs inversus, and renal-hepatic-pancreatic dysplasia. Am. J. Hum. Genet. 82 (2008) 959-970
13. Bonnafe E., Touka M., Aitloungis A., Baas D., Barras E., Ucla C., Moreau A., Flamant F., Dubruille R., Couble P., et al. The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol. Biol. Cell 24 (2004) 4417-4427
14. Brailov I., Bancila M., Brisogueil M., Miquel M., Hamon M., and Verge D. Localization of 5-HT6 receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res. 872 (2000) 271-275
15. Brody S.L., Yan X.H., Wuerffel M.K., Song S.K., and Shapiro S.D. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 23 (2000) 45-51
16. Buck L., and Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65 (1991) 175-187
17. Caspary T., Larkins C.E., and Anderson K.V. The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell 12 (2007) 767-778
18. Chang B., Khanna H., Hawes N., Jimeno D., He S., Lillo C., Parapuram S.K., Cheng H., Scott A., Hurd R.E., et al. In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum. Mol. Genet. 15 (2006) 1847-1857
19. Chen J., Knowles H., Hebert J., and Hackett B. Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J. Clin. Invest. 102 (1998) 1066-1072
20. Chizhikov V.V., Davenport J., Zhang Q., Shih E.K., Cabello O.A., Fuchs J.L., Yoder B.K., and Millen K.J. Cilia proteins control cerebellar morphogenesis by promoting expansion of the granule progenitor pool. J. Neurosci. 27 (2007) 9780-9789
21. Corbit K.C., Aanstad P., Singla V., Norman A.R., Stainier D.Y.R., and Reiter J.F. Vertebrate Smoothened functions at the primary cilium. Nature 437 (2005) 1018-1021
22. Corbit K.C., Shyer A.E., Dowdle W.E., Gaulden J., Singla V., Chen M.H., Chuang P.T., and Reiter J. Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol. 10 (2008) 70-76
23. Delous M., Baala L., Salomon R., Laclef C., Vierkotten J., Tory K., Golzio C., Lacoste T., Besse L., Ozilou C., et al. The ciliary gene RPGRIP1L is mutated in cerebello-oculo-renal syndrome (Joubert syndrome type B) and Meckel syndrome. Nat. Genet. 39 (2007) 875-881
24. den Hollander A.I., Koenekoop R.K., Yzer S., Lopez I., Arends M.L., Voesenek K.E., Zonneveld M.N., Strom T.M., Meitinger T., Brunner H.G., et al. Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis. Am. J. Hum. Genet. 79 (2006) 556-561
25. Dutcher S.K. Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet. 11 (1995) 398-404
26. 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
27. 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
28. Fan S., Hurd T., Liu C., Straight S., Weimbs T., Hurd E., Domino S., and Margolis B. Polarity proteins control ciliogenesis via kinesin motor interactions. Curr. Biol. 14 (2004) 1451-1461
29. Feistel K., and Blum M. Three types of cilia including a novel 9+4 axoneme on the notochordal plate of the rabbit embryo. Dev. Dyn. 235 (2006) 3348-3358
30. Fliegauf M., Benzing T., and Omran H. When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8 (2007) 880-893
31. Follit J.A., Tuft R.A., Fogarty K.E., and Pazour G.J. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17 (2006) 3781-3792
32. Fromherz S., Giddings Jr. T.H., Gomez-Ospina N., and Dutcher S.K. J. Cell Sci. 117 (2004) 303-314
33. Gerdes J.M., Liu Y., Zaghloul N.A., Leitch C.C., Lawson S., Kato M., Beachy P., Beales P., DeMartino G., Fisher S., et al. Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet. 39 (2007) 1350-1360
34. Gervais F.G., Singaraja R., Xanthoudakis S., Gutekunst C.A., Leavitt B.R., Metzler M., Hackam A.S., Tam J., Vaillancourt J.P., Houtzager V., et al. Recruitment and activation of caspase-8 by the Huntingtin-interacting protein Hip-1 and a novel partner Hippi. Nat. Cell Biol. 4 (2002) 95-105
35. Gherman A., Davis E.E., and Katsanis N. The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat. Genet. 38 (2006) 961-962
36. Graser S., Stierhof Y.D., Lavoie S.B., Gassner O.S., Lamla S., Le Clech M., and Nigg E.A. Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol. 179 (2007) 321-330
37. Han Y.G., Spassky N., Romaguera-Ros M., Garcia-Verdugo J.M., Aguilar A., Schneider-Maunoury S., and Alvarez-Buylla A. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci. 11 (2008) 277-284
38. 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
39. Haraguchi K., Hayashi T., Jimbo T., Yamamoto T., and Akiyama T. Role of the kinesin-2 family protein, KIF3, during mitosis. J. Biol. Chem. 281 (2006) 4094-4099
40. 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) 480-488
41. Haycraft C.J., Zhang Q., Song B., Jackson W.S., Detloff P.J., Serra R., and Yoder B.K. Intraflagellar transport is essential for endochondral bone formation. Development 134 (2007) 307-316
42. Hill P., Wang B., and Ruther U. The molecular basis of Pallister Hall associated polydactyly. Hum. Mol. Genet. 16 (2007) 2089-2096
43. Hirokawa N., Tanaka Y., Okada Y., and Takeda S. Nodal flow and the generation of left-right asymmetry. Cell 125 (2006) 33-45
44. Houde C., Dickinson R., Houtzager V., Cullum R., Montpetit R., Metzler M., Simpson E., Roy S., Hayden M., Hoodless P., and Nicholson D. Hippi is essential for node cilia assembly and Sonic hedgehog signaling. Dev. Biol. 300 (2006) 523-533
45. Huangfu D., and Anderson K.V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102 (2005) 11325-11330
46. 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
47. Itoh K., Brott B.K., Bae G.-U., Ratcliffe M.J., and Sokol S.Y. Nuclear localization is required for Dishevelled function in Wnt/beta-catenin signaling. J. Biol. 4 (2005) 3
48. Jekely G., and Arendt D. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28 (2006) 191-198
49. Jones C., Roper V.C., Foucher I., Qian D., Banizs B., Petit C., Yoder B.K., and Chen P. Ciliary proteins link basal body polarization to planar cell polarity. Nat. Genet. 40 (2008) 69-77
50. Karmous-Benailly H., Martinovic J., Gubler M.C., Sirot Y., Clech L., Ozilou C., Auge J., Brahimi N., Etchevers H., Detrait E., et al. Antenatal presentation of Bardet-Biedl syndrome may mimic Meckel syndrome. Am. J. Hum. Genet. 76 (2005) 493-504
51. Keller L.C., Geimer S., Romijn E., Yates III J., Zamora I., and Marshall W.F. Molecular architecture of the centriole proteome: the conserved WD40 domain protein POC1 is required for centriole duplication and length control. Mol. Biol. Cell 20 (2008) 1150-1166
52. Kovacs J.J., Whalen E.J., Liu R., Xiao K., Kim J., Chen M., Wang J., Chen W., and Lefkowitz R.J. Beta-arrestin-mediated localization of smoothened to the primary cilium. Science 320 (2008) 1777-1781
53. Koyama E., Young B., Nagayama M., Shibukawa Y., Enomoto-Iwamoto M., Iwamoto M., Maeda Y., Lanske B., Song B., Serra R., and Pacifici M. Conditional Kif3a ablation causes abnormal hedgehog siganling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 134 (2007) 2159-2169
54. 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
55. Kulaga H.M., Leitch C.C., Eichers E.R., Badano J.L., Lesemann A., Hoskins B.E., Lupski J.R., Beales P.L., Reed R.R., and Katsanis N. Loss of BBS proteins causes anosmia in humans and defects in olfactory cilia structure and function in the mouse. Nat. Genet. 36 (2004) 994-998
56. Le Bot N., Antony C., White J., Karsenti E., and Vernos I. Role of Xklp3, a Subunit of the Xenopus Kinesin II Heterotrimeric Complex, in Membrane Transport betwewen the Endoplasmic Reticulum and the Golgi Apparatus. J. Cell Biol. 143 (1998) 1559-1573
57. Lefkowitz R.J., Rajagopal K., and Whalen E.J. New roles for beta-arrestins in cell signaling: not just for seven-transmembrane receptors. Mol. Cell 24 (2006) 643-652
58. Leitch C.C., Zaghloul N.A., Davis E.E., Stoetzel C., Diaz-Font A., Rix S., Al-Fadhel M., Lewis R.A., Eyaid W., Banin E., et al. Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome. Nat. Genet. 40 (2008) 443-448
59. Levin M., Thorlin T., Robinson K.R., Nogi T., and Mercola M. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111 (2002) 77-89
60. 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 genomic identification of conserved flagellar and basal body proteins that includes a novel gene for Bardet-Biedl syndrome. Cell 117 (2004) 541-552
61. Lin F., Hiesberger T., Cordes K., Sinclair A., Goldstein L., Somlo S., and Igarashi P. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc. Natl. Acad. Sci. USA 100 (2003) 5286-5291
62. Liu A., Wang B., and Niswander L. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 132 (2005) 3103-3111
63. Liu Q., Tan G., Levenkova N., Li T., Pugh Jr. E.N., Rux J.J., Speicher D.W., and Pierce E.A. The proteome of the mouse photoreceptor sensory cilium complex. Mol. Cell. Proteomics 6 (2007) 1299-1317
64. Liu S., Lu W., Obara T., Kuida S., Lehoczky J., Dewar K., Drummond I., and Beier D. A defect in a novel Nek-family kinase causes cystic kidney disease in the mouse and in zebrafish. Development 129 (2002) 5839-5846
65. Liu Y., Pathak N., Kramer-Zucker A., and Drummond I.A. Notch signaling controls the ifferentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134 (2007) 1111-1122
66. Lum L., and Beachy P. The Hedgehog response network: sensors, switches, and routers. Science 304 (2004) 1755-1759
67. Ma M., and Jiang Y.J. Jagged2a-notch signaling mediates cell fate choice in the zebrafish pronephric duct. PLoS Genet. 3 (2007) e18
68. Mahjoub M.R., Trapp M.L., and Quarmby L.M. NIMA-related kinases defective in murine models of polycystic kidney diseases localize to primary cilia and centrosomes. J. Am. Soc. Nephrol. 16 (2005) 3485-3489
69. Marshall W.F., and Kintner C. Cilia orientation and the fluid mechanics of development. Curr. Opin. Cell Biol. 20 (2008) 48-52
70. Marszalek J.R., Ruiz-Lozano P., Roberts E., Chien K.R., and Goldstein L.S. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl. Acad. Sci. USA 96 (1999) 5043-5048
71. May S.R., Ashique A.M., Karlen M., Wang B., Shen Y., Zarbalis K., Reiter J., Ericson J., and Peterson A.S. Loss of 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
72. McEwen D.P., Koenekoop R.K., Khanna H., Jenkins P.M., Lopez I., Swaroop A., and Martens J.R. Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons. Proc. Natl. Acad. Sci. USA 104 (2007) 15917-15922
73. 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
74. Moritz O.L., Tam B.M., Hurd L.L., Peranen J., Deretic D., and Papermaster D.S. Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell 12 (2001) 2341-2351
75. Nachury M.V., Loktev A.V., Zhang Q., Westlake C.J., Peränen J., Merdes A., Slusarski D.C., Scheller R.H., Bazan J.F., Sheffield V.C., and Jackson P.K. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129 (2007) 1201-1203
76. 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
77. Nishimura T., Kato K., Yamaguchi T., Fukata Y., Ohno S., and Kaibuchi K. Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nat. Cell Biol. 6 (2004) 328-334
78. Nurnberger J., Bacallao R.L., and Phillips C.L. Inversin forms a complex with catenins and N-cadherin in polarized epithelial cells. Mol. Biol. Cell 13 (2002) 3096-3106
79. O'Connell M.J., Krien M.J., and Hunter T. Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol. 13 (2003) 221-228
80. Oishi I., Kawakami Y., Raya A., Callol-Massot C., and Bemonte J.I. Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat. Genet. 38 (2006) 1316-1322
81. Omori Y., Zhao C., Saras A., Mukhopadhyay S., Kim W., Furukawa T., Sengupta P., Veraksa A., and Malicki J. Elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat. Cell Biol. 10 (2008) 437-444
82. Pan J., Wang Q., and Snell W. An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev. Cell 6 (2004) 445-451
83. 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
84. Poole C.A., Jensen C.G., Snyder J.A., Gray C.G., Hermanutz V.L., and Wheatley D.N. Confocal Analysis of primary cilia structures and colocalization with the Golgi Apparatus in chondrocytes and aortic smooth muscle cells. Cell Biol. Int. 21 (1997) 483-494
85. Pugacheva E.N., Jablonski S.A., Hartman T.R., Henske E.P., and Golemis E.A. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 129 (2007) 1351-1363
86. Qian Q., Li M., Cai Y., Ward C.J., Somlo S., Harris P.C., and Torres V.E. Analysis of the polycystins in aortic vascular smooth muscle cells. J. Am. Soc. Nephrol. 14 (2003) 2280-2287
87. Reese T.S. Olfactory cilia in the frog. J. Cell Biol. 25 (1965) 209-230
88. Rohatgi R., Milenkovic L., and Scott M. Patched1 regulates hedgehog signaling at the primary cilium. Science 317 (2007) 372-376
89. 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
90. Rothbacher U., Laurent M.N., Deardorff M.A., Klein P.S., Cho K.W.Y., and Fraser S.E. Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis. EMBO J. 19 (2000) 1010-1022
91. Sayer J.A., Otto E.A., O'Toole J.F., Nurnberg G., Kennedy M.A., Becker C., Hennies H.C., Helou J., Attanasio M., Fausett B.V., et al. The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat. Genet. 38 (2006) 674-681
92. Schneider L., Clement C.A., Teilmann S.C., Pazour G.J., Hoffmann E.K., Satir P., and Christensen S.T. PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15 (2005) 1861-1866
93. Scholey J.M. Intraflagellar transport motors in cilia: moving along the cell's antenna. J. Cell Biol. 180 (2008) 23-29
94. Seto E.S., and Bellen H.J. The ins and outs of Wingless signaling. Trends Cell Biol. 14 (2004) 45-53
95. Shi S.H., Cheng T., Jan L.Y., and Jan Y.N. APC and GSK-3beta are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14 (2004) 2025-2032
96. 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
97. Sorokin S. Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15 (1964) 363-377
98. Spassky N., Han Y., Aguilar A., Strehl L., Besse L., Laclef C., Ros M.R., Garcia-Verdugo J., and Alvarez-Buylla A. Primary cilia are required for cerebrellar development and Shh-dependent expansion of progenitor pool. Dev. Biol. 317 (2008) 246-259
99. Spektor A., Tsang W., Khoo D., and Dynlacht B. Cep97 and CP110 Suppress a Cilia Assembly Program. Cell 130 (2007) 678-690
100. Stubbs J.L., Oishi I., Izpisua Belmonte J.C., and Kintner C. The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat. Genet. 40 (2008) 1454-1460
101. Tabin C.J. The key to left-right asymmetry. Cell 127 (2006) 27-32
102. Tan P.L., Barr T., Inglis P.N., Mitsuma N., Huang S.M., Garcia-Gonzalez M.A., Bradley B.A., Coforio S., Albrecht P.J., Watnick T., et al. Loss of Bardet Biedl syndrome proteins causes defects in peripheral sensory innervation and function. Proc. Natl. Acad. Sci. USA 104 (2007) 17524-17529
103. Taulman P.D., Haycraft C.J., Balkovetz D.F., and Yoder B.K. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol. Biol. Cell 12 (2001) 589-599
104. Torkko J.M., Manninen A., Schuck S., and Simons K. Depletion of apical transport proteins perturbs epithelial cyst formation and ciliogenesis. J. Cell Sci. 121 (2008) 1193-1203
105. Tran P.V., Haycraft C.J., Besschetnova T.Y., Turbe-Doan A., Stottmann R.W., Herron B.J., Chesebro A.L., Qiu H., Scherz P.J., Shah J.V., et al. THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia. Nat. Genet. 40 (2008) 403-410
106. Tsang W.Y., Bossard C., Khanna H., Peranen J., Swaroop A., Malhotra V., and Dynlacht B.D. CP110 suppresses primary cilia formation through its interaction with CEP290, a protein deficient in human ciliary disease. Dev. Cell 15 (2008) 187-197
107. Tsiokas L., Kim S., and Ong E.C. Cell biology of polycystin-2. Cell. Signal. 19 (2007) 444-453
108. Upadhya P., Birkenmeier E., Birkenmeier C., and Barker J. Mutations in a NIMA-related kinase gene, Nek1, cause pleiotropic effects including a progressive polycystic kidney disease in mice. Proc. Natl. Acad. Sci. USA 97 (2000) 217-221
109. Valente E.M., Silhavy J.L., Brancati F., Barrano G., Krishnaswami S.R., Castori M., Lancaster M.A., Boltshauser E., Boccone L., Al-Gazali L., et al. Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome. Nat. Genet. 38 (2006) 623-625
110. Veeman M.T., Axelrod J.D., and Moon R.T. A second canon: functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5 (2003) 367-377
111. Vieira O.V., Gaus K., Verkade P., Fullekrug J., Vaz W.L., and Simons K. FAPP2, cilium formation, and compartmentalization of the apical membrane in polarized Madin-Darby canine kidney (MDCK) cells. Proc. Natl. Acad. Sci. USA 103 (2006) 18556-18561
112. Vierkotten J., Dildrop R., Peters T., Wang B., and Ruther U. Ftm is a novel basal body protein of cilia invilved in Shh signaling. Development 134 (2007) 2569-2577
113. Wang S., Luo Y., Wilson P.D., Witman G.B., and Zhou J. The autosomal recessive polycystic kidney disease protein is localized to primary cilia, with concentration in the basal body area. J. Am. Soc. Nephrol. 15 (2004) 592-602
114. Wolf M.T., Saunier S., O'Toole J.F., Wanner N., Groshong T., Attanasio M., Salomon R., Stallmach T., Sayer J.A., Waldherr R., et al. Mutational analysis of the RPGRIP1L gene in patients with Joubert syndrome and nephronophthisis. Kidney Int. 72 (2007) 1520-1526
115. Yoder B.K. Role of primary cilia in the pathogenesis of polycystic kidney disease. J. Am. Soc. Nephrol. 18 (2007) 1381-1388
116. Yoshimura S., Egerer J., Fuchs E., Haas A.K., and Barr F.A. Functional dissection of Rab GTPases involved in primary cilium formation. J. Cell Biol. 178 (2007) 363-369
117. Yu X., Ng C.P., Habacher H., and Roy S. Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat. Genet. 40 (2008) 1445-1453
118. Zhang M., Bolfing M., Knowles H., Karnes H., and Hackett B. Foxj1 regulates asymmetric gene expression during left-right axis patterning in mice. Biochem. Biophys. Res. Commun. 324 (2004) 1413-1420