Broad-Minded Links Cell Cycle-Related Kinase to Cilia Assembly and Hedgehog Signal Transduction

Developmental Cell

Volumn 18, Issue 2, 2010, Pages 237-247

  Ko, Hyuk Wan ^a,b   Norman, Ryan X ^a   Tran, John ^a   Fuller, Kimberly P ^a   Fukuda, Mitsunori ^c   Eggenschwiler, Jonathan T ^a  

^a PRINCETON UNIVERSITY   (United States)

^b Kyung Hee University   (South Korea)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

CELLBIO; DEVBIO; SIGNALING

Indexed keywords

BROAD MINDED PROTEIN; CELL CYCLE RELATED KINASE; CELL PROTEIN; PHOSPHOTRANSFERASE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AXONEME; CELL STRUCTURE; CHLAMYDOMONAS; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME STABILITY; EUKARYOTIC FLAGELLUM; GENE INTERACTION; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; BODY PATTERNING; CARRIER PROTEINS; CILIA; CLONING, MOLECULAR; CYCLIN-DEPENDENT KINASES; DNA; ENZYME STABILITY; EPISTASIS, GENETIC; FEMALE; HEDGEHOG PROTEINS; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MUTATION; NEURAL TUBE; PREGNANCY; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

CHLAMYDOMONAS; DANIO RERIO; ERINACEIDAE; MAMMALIA;

EID: 76249112276     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.12.014     Document Type: Article

References (69)

1. Asleson C.M., and Lefebvre P.A. Genetic analysis of flagellar length control in Chlamydomonas reinhardtii: a new long-flagella locus and extragenic suppressor mutations. Genetics 148 (1998) 693-702
2. Bai C.B., Stephen D., and Joyner A.L. All mouse ventral spinal cord patterning by hedgehog is Gli dependent and involves an activator function of Gli3. Dev. Cell 6 (2004) 103-115
3. Barsel S.E., Wexler D.E., and Lefebvre P.A. Genetic analysis of long-flagella mutants of Chlamydomonas reinhardtii. Genetics 118 (1988) 637-648
4. Bengs F., Scholz A., Kuhn D., and Wiese M. LmxMPK9, a mitogen-activated protein kinase homologue affects flagellar length in Leishmania mexicana. Mol. Microbiol. 55 (2005) 1606-1615
5. Berman S.A., Wilson N.F., Haas N.A., and Lefebvre P.A. A novel MAP kinase regulates flagellar length in Chlamydomonas. Curr. Biol. 13 (2003) 1145-1149
6. Bulgakov O.V., Eggenschwiler J.T., Hong D.H., Anderson K.V., and Li T. FKBP8 is a negative regulator of mouse sonic hedgehog signaling in neural tissues. Development 131 (2004) 2149-2159
7. Burghoorn J., Dekkers M.P., Rademakers S., de Jong T., Willemsen R., and Jansen G. Mutation of the MAP kinase DYF-5 affects docking and undocking of kinesin-2 motors and reduces their speed in the cilia of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104 (2007) 7157-7162
8. 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
9. Chailley B., and Boisvieux-Ulrich E. Detection of plasma membrane cholesterol by filipin during microvillogenesis and ciliogenesis in quail oviduct. J. Histochem. Cytochem. 33 (1985) 1-10
10. Chen M.H., Wilson C.W., Li Y.J., Law K.K., Lu C.S., Gacayan R., Zhang X., Hui C.C., and Chuang P.T. Cilium-independent regulation of Gli protein function by Sufu in Hedgehog signaling is evolutionarily conserved. Genes Dev. 23 (2009) 1910-1928
11. Cho A., Ko H.W., and Eggenschwiler J.T. FKBP8 cell-autonomously controls neural tube patterning through a Gli2- and Kif3a-dependent mechanism. Dev. Biol. 321 (2008) 27-39
12. 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
13. Davidge J.A., Chambers E., Dickinson H.A., Towers K., Ginger M.L., McKean P.G., and Gull K. Trypanosome IFT mutants provide insight into the motor location for mobility of the flagella connector and flagellar membrane formation. J. Cell Sci. 119 (2006) 3935-3943
14. Dessaud E., McMahon A.P., and Briscoe J. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135 (2008) 2489-2503
15. Dolle P., Izpisua-Belmonte J.C., Falkenstein H., Renucci A., and Duboule D. Coordinate expression of the murine Hox-5 complex homoeobox-containing genes during limb pattern formation. Nature 342 (1989) 767-772
16. Eggenschwiler J.T., and Anderson K.V. Dorsal and lateral fates in the mouse neural tube require the cell-autonomous activity of the open brain gene. Dev. Biol. 227 (2000) 648-660
17. Eggenschwiler J.T., and Anderson K.V. Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 23 (2007) 345-373
18. Eggenschwiler J.T., Espinoza E., and Anderson K.V. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 412 (2001) 194-198
19. Eggenschwiler J.T., Bulgakov O.V., Qin J., Li T., and Anderson K.V. Mouse Rab23 regulates hedgehog signaling from smoothened to Gli proteins. Dev. Biol. 290 (2006) 1-12
20. Endoh-Yamagami S., Evangelista M., Wilson D., Wen X., Theunissen J.W., Phamluong K., Davis M., Scales S.J., Solloway M.J., de Sauvage F.J., and Peterson A.S. The mammalian Cos2 homolog Kif7 plays an essential role in modulating Hh signal transduction during development. Curr. Biol. 19 (2009) 1320-1326
21. Ericson J., Rashbass P., Schedl A., Brenner-Morton S., Kawakami A., van Heyningen V., Jessell T.M., and Briscoe J. Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90 (1997) 169-180
22. 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
23. Fu Z., Larson K.A., Chitta R.K., Parker S.A., Turk B.E., Lawrence M.W., Kaldis P., Galaktionov K., Cohn S.M., Shabanowitz J., et al. Identification of yin-yang regulators and a phosphorylation consensus for male germ cell-associated kinase (MAK)-related kinase. Mol. Cell. Biol. 26 (2006) 8639-8654
24. Goodrich L.V., Milenkovic L., Higgins K.M., and Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277 (1997) 1109-1113
25. Grosshans B.L., Ortiz D., and Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103 (2006) 11821-11827
26. 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
27. Hoover A.N., Wynkoop A., Zeng H., Jia J., Niswander L.A., and Liu A. C2cd3 is required for cilia formation and Hedgehog signaling in mouse. Development 135 (2008) 4049-4058
28. Hou Y., Pazour G.J., and Witman G.B. A dynein light intermediate chain, D1bLIC, is required for retrograde intraflagellar transport. Mol. Biol. Cell 15 (2004) 4382-4394
29. Huangfu D., and Anderson K.V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102 (2005) 11325-11330
30. 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
31. Hui C.C., and Joyner A.L. A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3 (1993) 241-246
32. Hui C.C., Slusarski D., Platt K.A., Holmgren R., and Joyner A.L. Expression of three mouse homologs of the Drosophila segment polarity gene Cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev. Biol. 162 (1994) 402-413
33. Ingham P.W. Hedgehog signalling. Curr. Biol. 18 (2008) R238-R241
34. Itoh T., Satoh M., Kanno E., and Fukuda M. Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes Cells 11 (2006) 1023-1037
35. Jia J., and Jiang J. Decoding the Hedgehog signal in animal development. Cell. Mol. Life Sci. 63 (2006) 1249-1265
36. Kim J., Kato M., and Beachy P.A. Gli2 trafficking links Hedgehog-dependent activation of Smoothened in the primary cilium to transcriptional activation in the nucleus. Proc. Natl. Acad. Sci. U.S.A. 106 (2009) 21666-71
37. Liem Jr. K.F., He M., Ocbina P.J., and Anderson K.V. Mouse Kif7/Costal2 is a cilia-associated protein that regulates Sonic hedgehog signaling. Proc. Natl. Acad. Sci. USA 106 (2009) 13377-13382
38. Liu Y., Wu C., and Galaktionov K. p42, a novel cyclin-dependent kinase-activating kinase in mammalian cells. J. Biol. Chem. 279 (2004) 4507-4514
39. Lum L., Zhang C., Oh S., Mann R.K., von Kessler D.P., Taipale J., Weis-Garcia F., Gong R., Wang B., and Beachy P.A. Hedgehog signal transduction via Smoothened association with a cytoplasmic complex scaffolded by the atypical kinesin, Costal-2. Mol. Cell 12 (2003) 1261-1274
40. Matise M.P., Epstein D.J., Park H.L., Platt K.A., and Joyner A.L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125 (1998) 2759-2770
41. Methot N., and Basler K. Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of Cubitus interruptus. Cell 96 (1999) 819-831
42. Methot N., and Basler K. Suppressor of fused opposes hedgehog signal transduction by impeding nuclear accumulation of the activator form of Cubitus interruptus. Development 127 (2000) 4001-4010
43. Morgan G.W., Denny P.W., Vaughan S., Goulding D., Jeffries T.R., Smith D.F., Gull K., and Field M.C. An evolutionarily conserved coiled-coil protein implicated in polycystic kidney disease is involved in basal body duplication and flagellar biogenesis in Trypanosoma brucei. Mol. Cell. Biol. 25 (2005) 3774-3783
44. Nachury M.V., Loktev A.V., Zhang Q., Westlake C.J., Peranen 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) 1201-1213
45. Nagy A., Gertenstein M., Vintersten K., and Behringer R. Manipulating the Mouse Embryo: A Laboratory Manual. Third Edition (2003), Cold Spring Harbor Press, Cold Spring Harbor, New York
46. Pan X., Eathiraj S., Munson M., and Lambright D.G. TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature 442 (2006) 303-306
47. Pazour G.J., and Bloodgood R.A. Targeting proteins to the ciliary membrane. Curr. Top. Dev. Biol. 85 (2008) 115-149
48. Pedersen L.B., and Rosenbaum J.L. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 85 (2008) 23-61
49. 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
50. Persson M., Stamataki D., te Welscher P., Andersson E., Bose J., Ruther U., Ericson J., and Briscoe J. Dorsal-ventral patterning of the spinal cord requires Gli3 transcriptional repressor activity. Genes Dev. 16 (2002) 2865-2878
51. Qin H., Rosenbaum J.L., and Barr M.M. An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr. Biol. 11 (2001) 457-461
52. Quinlan R.J., Tobin J.L., and Beales P.L. Modeling ciliopathies: primary cilia in development and disease. Curr. Top. Dev. Biol. 84 (2008) 249-310
53. Rohatgi R., Milenkovic L., and Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 317 (2007) 372-376
54. Rosenbaum J.L., Moulder J.E., and Ringo D.L. Flagellar elongation and shortening in Chlamydomonas. The use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J. Cell Biol. 41 (1969) 600-619
55. Ruel L., Rodriguez R., Gallet A., Lavenant-Staccini L., and Therond P.P. Stability and association of Smoothened, Costal2 and Fused with Cubitus interruptus are regulated by Hedgehog. Nat. Cell Biol. 5 (2003) 907-913
56. Schottenfeld J., Sullivan-Brown J., and Burdine R.D. Zebrafish curly up encodes a Pkd2 ortholog that restricts left-side-specific expression of southpaw. Development 134 (2007) 1605-1615
57. Svard J., Heby-Henricson K., Persson-Lek M., Rozell B., Lauth M., Bergstrom A., Ericson J., Toftgard R., and Teglund S. Genetic elimination of Suppressor of fused reveals an essential repressor function in the mammalian Hedgehog signaling pathway. Dev. Cell 10 (2006) 187-197
58. Tam L.W., Dentler W.L., and Lefebvre P.A. Defective flagellar assembly and length regulation in LF3 null mutants in Chlamydomonas. J. Cell Biol. 163 (2003) 597-607
59. Tam L.W., Wilson N.F., and Lefebvre P.A. A CDK-related kinase regulates the length and assembly of flagella in Chlamydomonas. J. Cell Biol. 176 (2007) 819-829
60. 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
61. Varjosalo M., and Taipale J. Hedgehog: functions and mechanisms. Genes Dev. 22 (2008) 2454-2472
62. Varjosalo M., Li S.P., and Taipale J. Divergence of hedgehog signal transduction mechanism between Drosophila and mammals. Dev. Cell 10 (2006) 177-186
63. Vierkotten J., Dildrop R., Peters T., Wang B., and Ruther U. Ftm is a novel basal body protein of cilia involved in Shh signalling. Development 134 (2007) 2569-2577
64. Wang B., Fallon J.F., and Beachy P.A. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100 (2000) 423-434
65. Wilson N.F., Iyer J.K., Buchheim J.A., and Meek W. Regulation of flagellar length in Chlamydomonas. Semin. Cell Dev. Biol. 19 (2008) 494-501
66. Wilson C.W., Nguyen C.T., Chen M.H., Yang J.H., Gacayan R., Huang J., Chen J.N., and Chuang P.T. Fused has evolved divergent roles in vertebrate Hedgehog signalling and motile ciliogenesis. Nature 459 (2009) 98-102
67. Wohlbold L., Larochelle S., Liao J.C., Livshits G., Singer J., Shokat K.M., and Fisher R.P. The cyclin-dependent kinase (CDK) family member PNQALRE/CCRK supports cell proliferation but has no intrinsic CDK-activating kinase (CAK) activity. Cell Cycle 5 (2006) 546-554
68. 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
69. Zohn I.E., Anderson K.V., and Niswander L. Using genomewide mutagenesis screens to identify the genes required for neural tube closure in the mouse. Birth Defects Res. A Clin. Mol. Teratol. 73 (2005) 583-590