Intraflagellar transport protein 172 is essential for primary cilia formation and plays a vital role in patterning the mammalian brain

Developmental Biology

Volumn 325, Issue 1, 2009, Pages 24-32

  Gorivodsky, Marat ^a   Mukhopadhyay, Mahua ^a   Wilsch Braeuninger, Michaela ^b   Phillips, Matthew ^a   Teufel, Andreas ^c   Kim, Changmee ^a   Malik, Nasir ^a   Huttner, Wieland ^b   Westphal, Heiner ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Cilia; IFT172; MHB boundary; Nodal; Node; Slb

Indexed keywords

LIM PROTEIN; MESSENGER RNA; PROTEIN IFT172; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AXONEME; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; DISEASE SEVERITY; EMBRYO DEVELOPMENT; EPITHELIUM CELL; EUKARYOTIC FLAGELLUM; GASTRULATION; GENE FUNCTION; GENE MUTATION; GENE TARGETING; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

MAMMALIA;

EID: 57849164934     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.09.019     Document Type: Article

References (62)

1. Ang S.L., and Rossant J. Anterior mesendoderm induces mouse Engrailed genes in explant cultures. Development 118 (1993) 139-149
2. Belo J.A., Leyns L., Yamada G., and De Robertis E.M. The prechordal midline of the chondrocranium is defective in Goosecoid-1 mouse mutants. Mech. Dev. 72 (1998) 15-25
3. Bisgrove B.W., and Yost H.J. The roles of cilia in developmental disorders and disease. Development 133 (2006) 4131-4143
4. Blaess S., Corrales J.D., and Joyner A.L. Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 133 (2006) 1799-1809
5. Brennan J., Lu C.C., Norris D.P., Rodriguez T.A., Beddington R.S., and Robertson E.J. Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411 (2001) 965-969
6. Broccoli V., Boncinelli E., and Wurst W. The caudal limit of Otx2 expression positions the isthmic organizer. Nature 401 (1999) 164-168
7. Camus A., Davidson B.P., Billiards S., Khoo P., Rivera-Perez J.A., Wakamiya M., Behringer R.R., and Tam P.P. The morphogenetic role of midline mesendoderm and ectoderm in the development of the forebrain and the midbrain of the mouse embryo. Development 127 (2000) 1799-1813
8. Chi C.L., Martinez S., Wurst W., and Martin G.R. The isthmic organizer signal FGF8 is required for cell survival in the prospective midbrain and cerebellum. Development 130 (2003) 2633-2644
9. Chiang C., Litingtung Y., Lee E., Young K.E., Corden J.L., Westphal H., and Beachy P.A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383 (1996) 407-413
10. Conlon F.L., Lyons K.M., Takaesu N., Barth K.S., Kispert A., Herrmann B., and Robertson E.J. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120 (1994) 1919-1928
11. 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
12. Cordes S.P., and Barsh G.S. The mouse segmentation gene kr encodes a novel basic domain-leucine zipper transcription factor. Cell 79 (1994) 1025-1034
13. Crossley P.H., and Martin G.R. The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121 (1995) 439-451
14. Davenne M., Maconochie M.K., Neun R., Pattyn A., Chambon P., Krumlauf R., and Rijli F.M. Hoxa2 and Hoxb2 control dorsoventral patterns of neuronal development in the rostral hindbrain. Neuron 22 (1999) 677-691
15. de la Cruz J.M., Bamford R.N., Burdine R.D., Roessler E., Barkovich A.J., Donnai D., Schier A.F., and Muenke M. A loss-of-function mutation in the CFC domain of TDGF1 is associated with human forebrain defects. Hum. Genet. 110 (2002) 422-428
16. Filosa S., Rivera-Perez J.A., Gomez A.P., Gansmuller A., Sasaki H., Behringer R.R., and Ang S.L. Goosecoid and HNF-3beta genetically interact to regulate neural tube patterning during mouse embryogenesis. Development 124 (1997) 2843-2854
17. Gavalas A., Davenne M., Lumsden A., Chambon P., and Rijli F.M. Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124 (1997) 3693-3702
18. Gorivodsky M., and Lonai P. Novel roles of Fgfr2 in AER differentiation and positioning of the dorsoventral limb interface. Development 130 (2003) 5471-5479
19. Gripp K.W., Wotton D., Edwards M.C., Roessler E., Ades L., Meinecke P., Richieri-Costa A., Zackai E.H., Massague J., Muenke M., and Elledge S.J. Mutations in TGIF cause holoprosencephaly and link NODAL signalling to human neural axis determination. Nat. Genet. 25 (2000) 205-208
20. Hagiwara H., Ohwada N., Aoki T., and Takata K. Ciliogenesis and ciliary abnormalities. Med. Electron Microsc. 33 (2000) 109-114
21. 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
22. Howard P.W., and Maurer R.A. Identification of a conserved protein that interacts with specific LIM homeodomain transcription factors. J. Biol. Chem. 275 (2000) 13336-13342
23. Huangfu D., and Anderson K.V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11325-11330
24. 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
25. 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
26. 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 regulation. Nat. Genet. 40 (2008) 69-77
27. 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
28. Liu A., and Joyner A.L. Early anterior/posterior patterning of the midbrain and cerebellum. Annu. Rev. Neurosci. 24 (2001) 869-896
29. Liu A., Losos K., and Joyner A.L. FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development 126 (1999) 4827-4838
30. Lowe L.A., Yamada S., and Kuehn M.R. Genetic dissection of nodal function in patterning the mouse embryo. Development 128 (2001) 1831-1843
31. Manley N.R., and Capecchi M.R. The role of Hoxa-3 in mouse thymus and thyroid development. Development 121 (1995) 1989-2003
32. Martinez S., Crossley P.H., Cobos I., Rubenstein J.L., and Martin G.R. FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development 126 (1999) 1189-1200
33. 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
34. McMahon A.P., and Bradley A. The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62 (1990) 1073-1085
35. McMahon A.P., Joyner A.L., Bradley A., and McMahon J.A. The midbrain-hindbrain phenotype of Wnt-1-/Wnt-1- mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell 69 (1992) 581-595
36. Norris D.P., Brennan J., Bikoff E.K., and Robertson E.J. The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129 (2002) 3455-3468
37. Pan J., Wang Q., and Snell W.J. Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85 (2005) 452-463
38. 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
39. Pedersen L.B., Miller M.S., Geimer S., Leitch J.M., Rosenbaum J.L., and Cole D.G. Chlamydomonas IFT172 is encoded by FLA11, interacts with CrEB1, and regulates IFT at the flagellar tip. Curr. Biol. 15 (2005) 262-266
40. 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
41. Rohatgi R., Milenkovic L., and Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 317 (2007) 372-376
42. Rosenbaum J.L., and Witman G.B. Intraflagellar transport. Nat. Rev., Mol. Cell Biol. 3 (2002) 813-825
43. 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., Tan P.L., Phillips H.M., Leroux M.R., Henderson D.J., Murdoch J.N., Copp A.J., Eliot M.M., Lupski J.R., Kemp D.T., Dollfus H., Tada M., Katsanis N., Forge A., and Beales P.L. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 37 (2005) 1135-1140
44. Rubenstein J.L. Intrinsic and extrinsic control of cortical development. Novartis Found Symp. 228 (2000) 67-75 discussion 75-82, 109-113
45. Schier A.F., and Shen M.M. Nodal signalling in vertebrate development. Nature 403 (2000) 385-389
46. Schneider-Maunoury S., Topilko P., Seitandou T., Levi G., Cohen-Tannoudji M., Pournin S., Babinet C., and Charnay P. Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75 (1993) 1199-1214
47. 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
48. Scholey J.M., and Anderson K.V. Intraflagellar transport and cilium-based signaling. Cell 125 (2006) 439-442
49. Schwarz M., Alvarez-Bolado G., Urbanek P., Busslinger M., and Gruss P. Conserved biological function between Pax-2 and Pax-5 in midbrain and cerebellum development: evidence from targeted mutations. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 14518-14523
50. Shen M.M. Nodal signaling: developmental roles and regulation. Development 134 (2007) 1023-1034
51. Sun Z., Amsterdam A., Pazour G.J., Cole D.G., Miller M.S., and Hopkins N. A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131 (2004) 4085-4093
52. Tam P.P., and Behringer R.R. Mouse gastrulation: the formation of a mammalian body plan. Mech. Dev. 68 (1997) 3-25
53. Tsujikawa M., and Malicki J. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42 (2004) 703-716
54. Vincent S.D., Dunn N.R., Hayashi S., Norris D.P., and Robertson E.J. Cell fate decisions within the mouse organizer are governed by graded Nodal signals. Genes Dev. 17 (2003) 1646-1662
55. Whitman M. Nodal signaling in early vertebrate embryos: themes and variations. Dev. Cell 1 (2001) 605-617
56. Wilkinson D.G., Bhatt S., Chavrier P., Bravo R., and Charnay P. Segment-specific expression of a zinc-finger gene in the developing nervous system of the mouse. Nature 337 (1989) 461-464
57. Wolf C., Thisse C., Stoetzel C., Thisse B., Gerlinger P., and Perrin-Schmitt F. The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev. Biol. 143 (1991) 363-373
58. Yamamoto M., Saijoh Y., Perea-Gomez A., Shawlot W., Behringer R.R., Ang S.L., Hamada H., and Meno C. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428 (2004) 387-392
59. Yamanaka Y., Tamplin O.J., Beckers A., Gossler A., and Rossant J. Live imaging and genetic analysis of mouse notochord formation reveals regional morphogenetic mechanisms. Dev. Cell 13 (2007) 884-896
60. Ye W., Bouchard M., Stone D., Liu X., Vella F., Lee J., Nakamura H., Ang S.L., Busslinger M., and Rosenthal A. Distinct regulators control the expression of the mid-hindbrain organizer signal FGF8. Nat. Neurosci. 4 (2001) 1175-1181
61. Zhang X.M., Ramalho-Santos M., and McMahon A.P. Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R symmetry by the mouse node. Cell 106 (2001) 781-792
62. Zhou X., Sasaki H., Lowe L., Hogan B.L., and Kuehn M.R. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 361 (1993) 543-547