Cilia and developmental signaling

Annual Review of Cell and Developmental Biology

Volumn 23, Issue , 2007, Pages 345-373

  Eggenschwiler, Jonathan T ^a   Anderson, Kathryn V ^b  

^a PRINCETON UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Hedgehog; Intraflagellar transport; PDGFR ; Wnt

Indexed keywords

CARRIER PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

DEVELOPMENT; EUKARYOTIC FLAGELLUM; FIBROBLAST; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE; ANIMAL; GENETIC DISORDER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MORPHOGENESIS; MOUSE; NEURAL TUBE; PHYSIOLOGY; PROTEIN TRANSPORT;

ERINACEIDAE; INVERTEBRATA; MAMMALIA; VERTEBRATA;

ANIMALS; BODY PATTERNING; CILIA; GENETIC DISEASES, INBORN; HEDGEHOG PROTEINS; HUMANS; MICE; NEURAL TUBE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 36849036264     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.23.090506.123249     Document Type: Review

References (141)

1. Adler PN. 2002. Planar signaling and morphogenesis in Drosophila. Dev. Cell 2(5):525-35
2. Afzelius BA. 1976. A human syndrome caused by immotile cilia. Science 193(4250):317-19
3. Afzelius BA. 2004. Cilia-related diseases. J. Pathol. 204(4):470-77
4. Albrecht-Buehler G. 1977. Phagokinetic tracks of 3T3 cells: parallels between the orientation of track segments and of cellular structures which contain actin or tubulin. Cell 12(2):333-39
5. Ansley SJ, Badano JL, Blacque OE, Hill J, Hoskins BE, et al. 2003. Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425(6958):628-33
6. Avidor-Reiss T, Maer AM, Koundakjian E, Polyanovsky A, Keil T, et al. 2004. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117(4):527-39
7. Baala L, Romano S, Khaddour R, Saunier S, Smith UM, et al. 2007. The Meckel-Gruber syndrome gene, MKS3, is mutated in Joubert syndrome. Am. J. Hum. Genet. 80(1):186-94
8. Badano JL, Mitsuma N, Beales PL, Katsanis N. 2006. The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7:125-48
9. Barnfield PC, Zhang X, Thanabalasingham V, Yoshida M, Hui CC. 2005. Negative regulation of Gli1 and Gli2 activator function by Suppressor of fused through multiple mechanisms. Differentiation 73(8):397-405
10. Blacque OE, Li C, Inglis PN, Esmail MA, Ou G, et al. 2006. The WD repeat-containing protein IFTA-1 is required for retrograde intraflagellar transport. Mol. Biol. Cell 17(12):5053-62
11. Bonnafe E, Touka M, Ait-Lounis A, Baas D, Barras E, et al. 2004. The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol. Cell Biol. 24(10):4417-27
12. Bostrom H, Willetts K, Pekny M, Leveen P, Lindahl P, et al. 1996. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85(6):863-73
13. Brailov I, Bancila M, Brisorgueil MJ, Miquel MC, Hamon M, Verge D. 2000. Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res. 872(1-2):271-75
14. Brazelton WJ, Amundsen CD, Silflow CD, Lefebvre PA. 2001. bld1 mutation identifies the Chlamydomonas osm-6 homolog as a gene required for flagellar assembly. Curr. Biol. 11(20):1591-94
15. Brito JM, Teillet MA, Le Douarin NM. 2006. An early role for sonic hedgehog from foregut endoderm in jaw development: ensuring neural crest cell survival. Proc. Natl. Acad. Sci. USA 103(31):11607-12
16. Bulgakov OV, Eggenschwiler JT, Hong DH, Anderson KV, Li T. 2004. FKBP8 is a negative regulator of mouse sonic hedgehog signaling in neural tissues. Development 131(9):2149-59
17. Buttitta L, Mo R, Hui CC, Fan CM. 2003. Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 130(25):6233-43
18. Camner P, Mossberg B, Afzelius BA. 1975. Evidence of congenitally nonfunctioning cilia in the tracheobronchial tract in two subjects. Am. Rev. Respir. Dis. 112(6):807-9
19. Cano DA, Murcia NS, Pazour GJ, Hebrok M. 2004. Orpk mouse model of polycystic kidney disease reveals essential role of primary cilia in pancreatic tissue organization. Development 131(14):3457-67
20. Caspary T, Larkins CE, Anderson KV. 2007. The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell 12:767-78
21. Chazaud C, Rossant J. 2006. Disruption of early proximodistal patterning and AVE formation in Apc mutants. Development 133(17):3379-87
22. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, et al. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383(6599):407-13
23. Ciruna B, Weidinger G, Knaut H, Thisse B, Thisse C, et al. 2002. Production of maternal-zygotic mutant zebrafish by germ-line replacement. Proc. Natl. Acad. Sci. USA 99(23):14919-24
24. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL. 1998. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141(4):993-1008
25. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DY, Reiter JF. 2005. Vertebrate Smoothened functions at the primary cilium. Nature 437(7061):1018-21
26. DasGupta R, Fuchs E. 1999. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126(20):4557-68
27. Davey MG, Paton IR, Yin Y, Schmidt M, Bangs FK, et al. 2006. The chicken talpid3 gene encodes a novel protein essential for Hedgehog signaling. Genes. Dev. 15;20(10):1365-77
28. Dawe HR, Smith UM, Cullinane AR, Gerrelli D, Cox P, et al. 2007. The Meckel-Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum. Mol. Genet. 16(2):173-86
29. Dutcher SK. 1995. Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet. 11(10):398-404
30. Eggenschwiler JT, Espinoza E, Anderson KV. 2001. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signaling pathway. Nature 412(6843):194-98
31. Fan S, Hurd TW, Liu CJ, Straight SW, Weimbs T, et al. 2004. Polarity proteins control ciliogenesis via kinesin motor interactions. Curr. Biol. 14(16):1451-61
32. Ferrante MI, Zullo A, Barra A, Bimonte S, Messaddeq N, et al. 2006. Oral-facial-digital type I protein is required for primary cilia formation and left-right axis specification. Nat. Genet. 38(1):112-17
33. Fischer JA, Eun SH, Doolan BT. 2006. Endocytosis, endosome trafficking, and the regulation of Drosophila development. Annu. Rev. Cell Dev. Biol. 22:181-206
34. Follit JA, Tuft RA, Fogarty KE, Pazour GJ. 2006. The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17(9):3781-92
35. Forsberg-Nilsson K, Behar TN, Afrakhte M, Barker JL, McKay RD. 1998. Platelet-derived growth factor induces chemotaxis of neuroepithelial stem cells. J. Neurosci. Res. 53(5):521-30
36. - mice. Genes Dev. 13(6):709-17
37. Greenberg ME, Ziff EB. 1984. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature 311(5985):433-38
38. Guo N, Hawkins C, Nathans J. 2004. Frizzled6 controls hair patterning in mice. Proc. Natl. Acad. Sci. USA 101(25):9277-81
39. Hagstrom SA, North MA, Nishina PL, Berson EL, Dryja TP. 1998. Recessive mutations in the gene encoding the tubby-like protein TULP1 in patients with retinitis pigmentosa. Nat. Genet. 18(2):174-76
40. Hagstrom SA, Adamian M, Scimeca M, Pawlyk BS, Yue G, Li T. 2001. A role for the Tubby-like protein 1 in rhodopsin transport. Invest. Ophthalmol. Vis. Sci. 42(9):1955-62
41. Han YG, Kwok BH, Kernan MJ. 2003. Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr. Biol. 13(19):1679-86
42. Haycraft CJ, Banizs B, Aydin-Son Y, Zhang Q, Michaud EJ, Yoder BK. 2005. Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 1(4):e53
43. Haycraft CJ, Zhang Q, Song B, Jackson WS, Detloff PJ, et al. 2007. Intraflagellar transport is essential for endochondral bone formation. Development 134(2):307-16
44. Hearn T, Spalluto C, Phillips VJ, Renforth GL, Copin N, et al. 2005. Subcellular localization of ALMS1 supports involvement of centrosome and basal body dysfunction in the pathogenesis of obesity, insulin resistance, and type 2 diabetes. Diabetes 54(5):1581-87
45. Heldin CH, Westermark B. 1999. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79(4):1283-316
46. Hoeller D, Volarevic S, Dikic I. 2005. Compartmentalization of growth factor receptor signaling. Curr. Opin. Cell Biol. 17(2):107-11
47. Hooper JE, Scott MP. 2005. Communicating with Hedgehogs. Nat. Rev. Mol. Cell Biol. 6(4):306-17
48. Houde C, Dickinson RJ, Houtzager VM, Cullum R, Montpetit R, et al. 2006. Hippi is essential for node cilia assembly and Sonic hedgehog signaling. Dev. Biol. 300(2):523-33
49. Hu MC, Mo R, Bhella S, Wilson CW, Chuang PT, et al. 2006. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 133(3):569-78
50. Huangfu D, Anderson KV. 2005. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102(32):11325-30
51. Huangfu D, Anderson KV. 2006. Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133(1):3-14
52. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV. 2003. Hedgehog signaling in the mouse requires intraflagellar transport proteins. Nature 426(6962):83-87
53. Hui CC, Joyner AL. 1993. A mouse model of Greig cephalopolysyndactyly syndrome: The extra-toes J mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3(3):241-46
54. Ingham PW, McMahon AP. 2001. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15(23):3059-87
55. Izraeli S, Lowe LA, Bertness VL, Campaner S, Hahn H, et al. 2001. Genetic evidence that Sil is required for the Sonic Hedgehog response pathway. Genesis 31(2):72-77
56. Karcher C, Fischer A, Schweickert A, Bitzer E, Horie S, et al. 2005. Lack of a laterality phenotype in Pkd1 knock-out embryos correlates with absence of polycystin-1 in nodal cilia. Differentiation 73(8):425-32
57. Kartagener M. 1933. Zur Pathogenese der Bronchiektasien: Bronchiektasien bei Situs viscerum inversus. Beiträge Klin. Tuberk. 83:489-501
58. Kim JC, Badano JL, Sibold S, Esmail MA, Hill J, et al. 2004. The Bardet-Biedl protein BBS4 targets cargo to the pericentriolar region and is required for microtubule anchoring and cell cycle progression. Nat. Genet. 36(5):462-70
59. Kim JC, Ou YY, Badano JL, Esmail MA, Leitch CC, et al. 2005. MKKS/BBS6, a divergent chaperonin-like protein linked to the obesity disorder Bardet-Biedl syndrome, is a novel centrosomal component required for cytokinesis. J. Cell Sci. 118(Pt. 5):1007-20
60. Kimelman D, Xu W. 2006. β-catenin destruction complex: insights and questions from a structural perspective. Oncogene 25(57):7482-91
61. Klinghoffer RA, Hamilton TG, Hoch R, Soriano P. 2002. An allelic series at the PDGFαR locus indicates unequal contributions of distinct signaling pathways during development. Dev. Cell 2(1):103-13
62. Kogerman P, Grimm T, Kogerman L, Krause D, Unden AB, et al. 1999. Mammalian suppressor-of-fused modulates nuclear-cytoplasmic shuttling of Gli-1. Nat. Cell Biol. 1(5):312-19
63. Kozminski KG, Johnson KA, Forscher P, Rosenbaum JL. 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA 90(12):5519-23
64. Kozminski KG, Beech PL, Rosenbaum JL. 1995. The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131 (6, Pt. 1):1517-27
65. Lei Q, Jeong Y, Misra K, Li S, Zelman AK, et al. 2006. Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev. Cell 11(3):325-37
66. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, et al. 2004. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117(4):541-52
67. Lin F, Hiesberger T, Cordes K, Sinclair AM, Goldstein LS, et al. 2003. Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease. Proc. Natl. Acad. Sci. USA 100(9):5286-91
68. Litingtung Y, Dahn RD, Li Y, Fallon JF, Chiang C. 2002. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 418(6901):979-83
69. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22(4):361-65
70. Liu A, Wang B, Niswander LA. 2005. Mouse intraflagellar transport proteins regulate both the activator and repressor functions of Gli transcription factors. Development 132(13):3103-11
71. Lum L, Beachy PA. 2004. The Hedgehog response network: sensors, switches, and routers. Science 304(5678):1755-59
72. Mak HY, Nelson LS, Basson M, Johnson CD, Ruvkun G. 2006. Polygenic control of Caenorhabditis elegans fat storage. Nat. Genet. 38(3):363-68
73. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LS. 1999. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc. Natl. Acad. Sci. USA 96(9):5043-48
74. May SR, Ashique AM, Karlen M, Wang B, Shen Y, et al. 2005. 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(2):378-89
75. McGrath J, Somlo S, Makova S, Tian X, Brueckner M. 2003. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114(1):61-73
76. McMahon AP, Ingham PW, Tabin CJ. 2003. Developmental roles and clinical significance of hedgehog signaling. Curr. Top. Dev. Biol. 53:1-114
77. Meguid MM, Fetissov SO, Varma M, Sato T, Zhang L, et al. 2000. Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition 16(10):843-57
78. Méthot N, Basler K. 2000. Suppressor of Fused opposes Hedgehog signal transduction by impeding nuclear accumulation of the activator form of Cubitus interruptus. Development 127(18):4001-10
79. Mo R, Freer AM, Zinyk DL, Crackower MA, Michaud J, et al. 1997. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124(1):113-23
80. Montcouquiol M, Sans N, Huss D, Kach J, Dickman JD, et al. 2006. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J. Neurosci. 26(19):5265-75
81. Murcia NS, Richards WG, Yoder BK, Mucenski ML, Dunlap JR, Woychik RP. 2000. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127(11):2347-55
82. Nauli SM, Zhou J. 2004. Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26(8):844-56
83. Nishimura DY, Fath M, Mullins RF, Searby C, Andrews M, et al. 2004. Bbs2-null mice have neurosensory deficits, a defect in social dominance, and retinopathy associated with mislocalization of rhodopsin. Proc. Natl. Acad. Sci. USA 101(47):16588-93
84. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, et al. 1998. 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(6):829-37
85. Nonaka S, Yoshiba S, Watanabe D, Ikeuchi S, Goto T, et al. 2005. De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol. 3(8):e268
86. Nusse R. 2003. Wnts and Hedgehogs: lipid-modified proteins and similarities in signaling mechanisms at the cell surface. Development 130(22):5297-305
87. Ohlemiller KK, Hughes RM, Mosinger-Ogilvie J, Speck JD, Grosof DH, Silverman MS. 1995. Cochlear and retinal degeneration in the tubby mouse. Neuroreport 6(6):845-49
88. Omori Y, Malicki J. 2006. oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr. Biol. 16(10):945-57
89. Orentas DM, Hayes JE, Dyer KL, Miller RH. 1999. Sonic hedgehog signaling is required during the appearance of spinal cord oligodendrocyte precursors. Development 126(11):2419-29
90. Orozco JT, Wedaman KP, Signor D, Brown H, Rose L, Scholey JM. 1999. Movement of motor and cargo along cilia. Nature 398(6729):674
91. Ou G, Blacque OE, Snow JJ, Leroux MR, Scholey JM. 2005. Functional coordination of intraflagellar transport motors. Nature 436(7050):583-87
92. Paces-Fessy M, Boucher D, Petit E, Paute-Briand S, Blanchet-Tournier MF. 2004. The negative regulator of Gli, Suppressor of fused (Sufu), interacts with SAP18, Galectin3 and other nuclear proteins. Biochem. J. 378(Pt. 2):353-62
93. Pan X, Ou G, Civelekoglu-Scholey G, Blacque OE, Endres NF, et al. 2006. Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. J. Cell Biol. 174:1035-45
94. Pan Y, Bai CB, Joyner AL, Wang B. 2006. Hedgehog signaling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell Biol. 26(9):3365-77
95. Park TJ, Haigo SL, Wallingford JB. 2006. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 38(3):303-11
96. Pazour GJ, Dickert BL, Vucica Y, Seeley ES, Rosenbaum JL, et al. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151(3):709-18
97. Pedersen LB, Geimer S, Rosenbaum JL. 2006. Dissecting the molecular mechanisms of intraflagellar transport in Chlamydomonas. Curr. Biol. 16(5):450-59
98. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG. 1986. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117(2):456-87
99. Pietras K, Sjoblom T, Rubin K, Heldin CH, Ostman A. 2003. PDGF receptors as cancer drug targets. Cancer Cell 3(5):439-43
100. Piontek KB, Huso DL, Grinberg A, Liu L, Bedja D, et al. 2004. Functional floxed allele of Pkd1 that can be conditionally inactivated in vivo. J. Am. Soc. Nephrol. 15(12):3035-43
101. Piperno G, Siuda E, Henderson S, Segil M, Vaananen H, Sassaroli M. 1998. Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects. J. Cell Biol. 143(6):1591-601
102. Pledger WJ, Hart CA, Locatell KL, Scher CD. 1981. Platelet-derived growth factor-modulated proteins: constitutive synthesis by a transformed cell line. Proc. Natl. Acad. Sci. USA 78(7):4358-62
103. Rana AA, Barbera JP, Rodriguez TA, Lynch D, Hirst E, et al. 2004. Targeted deletion of the novel cytoplasmic dynein mD2LIC disrupts the embryonic organizer, formation of the body axes and specification of ventral cell fates. Development 131(20):4999-5007
104. Romio L, Fry AM, Winyard PJ, Malcolm S, Woolf AS, Feather SA. 2004. OFD1 is a centrosomal/ basal body protein expressed during mesenchymal-epithelial transition in human nephrogenesis. J. Am. Soc. Nephrol. 15(10):2556-68
105. Rosenbaum JL, Witman GB. 2002. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3(11):813-25
106. Ross AJ, May-Simera H, Eichers ER, Kai M, Hill J, et al. 2005. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 37(10):1135-40
107. Rubin LL, de Sauvage FJ. 2006. Targeting the Hedgehog pathway in cancer. Nat. Rev. Drug Discov. 5(12):1026-33
108. Saadi-Kheddouci S, Berrebi D, Romagnolo B, Cluzeaud F, Peuchmaur M, et al. 2001. Early development of polycystic kidney disease in transgenic mice expressing an activated mutant of the beta-catenin gene. Oncogene 20(42):5972-81
109. Santagata S, Boggon TJ, Baird CL, Gomez CA, Zhao J, et al. 2001. G-protein signaling through tubby proteins. Science 292(5524):2041-50
110. Satir P. 1999. The cilium as a biological nanomachine. FASEB J. 13(Suppl. 2): S235-37
111. Schneider L, Clement CA, Teilmann SC, Pazour GJ, Hoffmann EK, et al. 2005. PDGFRαα signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15(20):1861-66
112. Sekimizu K, Nishioka N, Sasaki H, Takeda H, Karlstrom RO, Kawakami A. 2004. The zebrafish iguana locus encodes Dzip1, a novel zinc-finger protein required for proper regulation of Hedgehog signaling. Development 131(11):2521-32
113. Shiratori H, Hamada H. 2006. The left-right axis in the mouse: from origin to morphology. Development 133(11):2095-104
114. Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, et al. 2005. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37(5):537-43
115. Singla V, Reiter JF. 2006. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313(5787):629-33
116. Smith UM, Consugar M, Tee LJ, McKee BM, Maina EN. 2006. The transmembrane protein meckelin (MKS3) is mutated in Meckel-Gruber syndrome and the wpk rat. Nat. Genet. 38(2):191-96
117. Soriano P. 1997. The PDGFα receptor is required for neural crest cell development and for normal patterning of the somites. Development 124(14):2691-700
118. Stiles CD, Capone GT, Scher CD, Antoniades HN, Van Wyk JJ, Pledger WJ. 1979. Dual control of cell growth by somatomedins and platelet-derived growth factor. Proc. Natl. Acad. Sci. USA 76(3):1279-83
119. St-Jacques B, Hammerschmidt M, McMahon AP. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13(16):2072-86
120. Sun Z, Amsterdam A, Pazour GJ, Cole DG, Miller MS, Hopkins N. 2004. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131(16):4085-93
121. Supp DM, Brueckner M, Kuehn MR, Witte DP, Lowe LA, et al. 1999. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 126(23):5495-504
122. Svard J, Heby-Henricson K, Persson-Lek M, Rozell B, Lauth M, et al. 2006. Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev. Cell 10(2):187-97
123. - mice analysis. J. Cell Biol. 145(4):825-36
124. te Welscher P, Zuniga A, Kuijper S, Drenth T, Goedemans HJ, et al. 2002. Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 298(5594):827-30
125. Tempe D, Casas M, Karaz S, Blanchet-Tournier MF, Concordet JP. 2006. Multisite protein kinase A and glycogen synthase kinase 3β phosphorylation leads to Gli3 ubiquitination by SCFβTrCP. Mol. Cell Biol. 26(11):4316-26
126. Tickle C. 2006. Making digit patterns in the vertebrate limb. Nat. Rev. Mol. Cell Biol. 7(1):45-53
127. Tsujikawa M, Malicki J. 2004. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42(5):703-16
128. Tucker RW, Pardee AB, Fujiwara K. 1979a. Centriole ciliation is related to quiescence and DNA synthesis in 3T3 cells. Cell 17(3):527-35
129. Tucker RW, Scher CD, Stiles CD. 1979b. Centriole deciliation associated with the early response of 3T3 cells to growth factors but not to SV40. Cell 18(4):1065-72
130. Uren A, Yu JC, Gholami NS, Pierce JH, Heidaran MA. 1994. The α PDGFR tyrosine kinase mediates locomotion of two different cell types through chemotaxis and chemokinesis. Biochem. Biophys. Res. Commun. 204(2):628-34
131. Vieira AR, Avila JR, Daack-Hirsch S, Dragan E, Felix TM, et al. 2005. Medical sequencing of candidate genes for nonsyndromic cleft lip and palate. PLoS Genet. 1(6):e64
132. Walther Z, Vashishtha M, Hall JL. 1994. The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein. J. Cell Biol. 126(1):175-88
133. Wang B, Fallon JF, Beachy PA. 2000. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100(4):423-34
134. Wang B, Li Y. 2006. Evidence for the direct involvement of βTrCP in Gli3 protein processing. Proc. Natl. Acad. Sci. USA 103(1):33-38
135. Wang Q, Pan J, Snell WJ. 2006. Intraflagellar transport particles participate directly in cilium-generated signaling in Chlamydomonas. Cell 125(3):549-62
136. Wang Y, Nathans J. 2007. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134(4):647-58
137. Watanabe D, Saijoh Y, Nonaka S, Sasaki G, Ikawa Y, et al. 2003. The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 130(9):1725-34
138. Wigley WC, Fabunmi RP, Lee MG, Marino CR, Muallem S, et al. 1999. Dynamic association of proteasomal machinery with the centrosome. J. Cell Biol. 145(3):481-90
139. Wolff C, Roy S, Lewis KE, Schauerte H, Joerg-Rauch G, et al. 2004. Iguana encodes a novel zinc-finger protein with coiled-coil domains essential for Hedgehog signal transduction in the zebrafish embryo. Genes Dev. 18(13):1565-76
140. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ, et al. 1997. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90(1):181-92
141. Franco, B., Ballabio, A., X-inactivation and human disease: X-linked dominant male-lethal disorders, Current Opinion in Genetics and Development, 2006, 16, 3, 254, 259, 10.1016/j.gde.2006.04.012