PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals

Developmental Biology

Volumn 339, Issue 2, 2010, Pages 418-428

  Zeng, Huiqing ^a   Hoover, Amber N ^a   Liu, Aimin ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Cilia; Gli3; Hedgehog; Inturned; Mouse; Planar cell polarity

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; INTURNED PROTEIN; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI; TRANSCRIPTION FACTOR GLI1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR POSTERIOR AXIS; ARTICLE; CELL POLARITY; CELL STRAIN 3T3; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STEM CELL; EUKARYOTIC FLAGELLUM; FEMALE; GENE TARGETING; INDUCED MUTATION; MALE; NERVOUS SYSTEM DEVELOPMENT; NEURAL TUBE DEFECT; NONHUMAN; POLYDACTYLY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ERINACEIDAE; MAMMALIA;

EID: 77149146791     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.01.003     Document Type: Article

References (46)

1. Adler P.N., Charlton J., and Park W.J. The Drosophila tissue polarity gene inturned functions prior to wing hair morphogenesis in the regulation of hair polarity and number. Genetics 137 (1994) 829-836
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. Carreira-Barbosa F., Concha M.L., Takeuchi M., Ueno N., Wilson S.W., and Tada M. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 130 (2003) 4037-4046
4. 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
5. 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
6. 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
7. 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
8. Gerdes J.M., Davis E.E., and Katsanis N. The vertebrate primary cilium in development, homeostasis, and disease. Cell 137 (2009) 32-45
9. 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
10. Gray R.S., Abitua P.B., Wlodarczyk B.J., Szabo-Rogers H.L., Blanchard O., Lee I., Weiss G.S., Liu K.J., Marcotte E.M., Wallingford J.B., and Finnell R.H. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nat. Cell Biol. 11 (2009) 1225-1232
11. 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. e53 (2005) 1
12. Heydeck W., Zeng H., and Liu A. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev. Dyn. 238 (2009) 3035-3042
13. 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
14. Huangfu D., and Anderson K.V. Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11325-11330
15. 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
16. Inglis P.N., Boroevich K.A., and Leroux M.R. Piecing together a ciliome. Trends Genet. 22 (2006) 491-500
17. Jia J., Kolterud A., Zeng H., Hoover A., Teglund S., Toftgard R., and Liu A. Suppressor of Fused inhibits mammalian Hedgehog signaling in the absence of cilia. Dev. Biol. 330 (2009) 452-460
18. Jiang J., and Hui C.C. Hedgehog signaling in development and cancer. Dev. Cell 15 (2008) 801-812
19. 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
20. Kibar Z., Vogan K.J., Groulx N., Justice M.J., Underhill D.A., and Gros P. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat. Genet. 28 (2001) 251-255
21. Levin M. The embryonic origins of left-right asymmetry. Crit. Rev. Oral Biol. Med. 15 (2004) 197-206
22. 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
23. Lu P., Minowada G., and Martin G.R. Increasing Fgf4 expression in the mouse limb bud causes polysyndactyly and rescues the skeletal defects that result from loss of Fgf8 function. Development 133 (2006) 33-42
24. Montcouquiol M., Rachel R.A., Lanford P.J., Copeland N.G., Jenkins N.A., and Kelley M.W. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423 (2003) 173-177
25. Murdoch J.N., Doudney K., Paternotte C., Copp A.J., and Stanier P. Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. Hum. Mol. Genet. 10 (2001) 2593-2601
26. 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
27. Ocbina P.J., and Anderson K.V. Intraflagellar transport, cilia, and mammalian Hedgehog signaling: analysis in mouse embryonic fibroblasts. Dev. Dyn. 237 (2008) 2030-2038
28. 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
29. Park W.J., Liu J., Sharp E.J., and Adler P.N. The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development 122 (1996) 961-969
30. Rohatgi R., Milenkovic L., and Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 317 (2007) 372-376
31. Rohatgi R., Milenkovic L., Corcoran R.B., and Scott M.P. Hedgehog signal transduction by Smoothened: pharmacologic evidence for a 2-step activation process. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 3196-3201
32. Rosenbaum J.L., and Witman G.B. Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3 (2002) 813-825
33. 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
34. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Kronig C., Schermer B., Benzing T., Cabello O.A., Jenny A., Mlodzik M., Polok B., Driever W., Obara T., and Walz G. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37 (2005) 537-543
35. Stecca B., and Ruiz i Altaba A. A GLI1-p53 inhibitory loop controls neural stem cell and tumour cell numbers. Embo J. 28 (2009) 663-676
36. Takeuchi M., Nakabayashi J., Sakaguchi T., Yamamoto T.S., Takahashi H., Takeda H., and Ueno N. The prickle-related gene in vertebrates is essential for gastrulation cell movements. Curr. Biol. 13 (2003) 674-679
37. 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
38. Veeman M.T., Slusarski D.C., Kaykas A., Louie S.H., and Moon R.T. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13 (2003) 680-685
39. 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
40. Wang Y., Zhou Z., Walsh C.T., and McMahon A.P. Selective translocation of intracellular Smoothened to the primary cilium in response to Hedgehog pathway modulation. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 2623-2628
41. Watanabe D., Saijoh Y., Nonaka S., Sasaki G., Ikawa Y., Yokoyama T., and Hamada H. The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 130 (2003) 1725-1734
42. 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
43. Winklbauer R., Medina A., Swain R.K., and Steinbeisser H. Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413 (2001) 856-860
44. Ybot-Gonzalez P., Savery D., Gerrelli D., Signore M., Mitchell C.E., Faux C.H., Greene N.D., and Copp A.J. Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134 (2007) 789-799
45. Yun U.J., Kim S.Y., Liu J., Adler P.N., Bae E., Kim J., and Park W.J. The inturned protein of Drosophila melanogaster is a cytoplasmic protein located at the cell periphery in wing cells. Dev. Genet. 25 (1999) 297-305
46. Zallen J.A. Planar polarity and tissue morphogenesis. Cell 129 (2007) 1051-1063