Failure of centrosome migration causes a loss of motile cilia in talpid3 mutants

Developmental Dynamics

Volumn 242, Issue 8, 2013, Pages 923-931

  Stephen, Louise A ^a   Davis, Gemma M ^a   Mcteir, Katie E ^a   James, John ^b   Mcteir, Lynn ^a   Kierans, Martin ^b   Bain, Andrew ^a   Davey, Megan G ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Basal body; Centriologenesis; Choroid plexus; Ciliogenesis; Diencephalon; Distal appendage; FOXJ1; Prosencephalon; TALPID3; Telencephalon; Transition fibre

Indexed keywords

ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; AXONEME; CELL FATE; CENTROSOME; CHICKEN; CHOROID PLEXUS; CILIARY MOTILITY; CONTROLLED STUDY; DEVELOPMENTAL GENE; ELECTRON MICROSCOPY; EMBRYO; EMBRYO DEVELOPMENT; EPENDYMA CELL; FOREBRAIN; FOXJ1 GENE; GENE; GENE EXPRESSION; LOSS OF FUNCTION MUTATION; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; RHOMBENCEPHALON; TALPID3 GENE;

BASAL BODY; CENTRIOLOGENESIS; CHOROID PLEXUS; CILIOGENESIS; DIENCEPHALON; DISTAL APPENDAGE; FOXJ1; PROSENCEPHALON; TALPID3; TELENCEPHALON; TRANSITION FIBRE;

ANIMALS; BASAL BODIES; CENTROSOME; CHICK EMBRYO; CHICKENS; CILIA; DIENCEPHALON; FORKHEAD TRANSCRIPTION FACTORS; IN SITU HYBRIDIZATION; PROSENCEPHALON; TELENCEPHALON;

ANIMALIA; ERINACEIDAE;

EID: 84880576588     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23980     Document Type: Article

References (47)

1. Alfaro-Cervello C, Soriano-Navarro M, Mirzadeh Z, Alvarez-Buylla A, Garcia-Verdugo JM. 2012. Biciliated ependymal cell proliferation contributes to spinal cord growth. J Comp Neurol 520:3528-3552.
2. Bangs F, Welten M, Davey MG, Fisher M, Yin Y, Downie H, Paton B, Baldock R, Burt DW, Tickle C. 2010. Identification of genes downstream of the Shh signalling in the developing chick wing and syn-expressed with Hoxd13 using microarray and 3D computational analysis. Mech Dev 127:428-441.
3. Bangs F, Antonio N, Thongnuek P, Welten M, Davey MG, Briscoe J, Tickle C. 2011. Generation of mice with functional inactivation of talpid3, a gene first identified in chicken. Development 138:3261-3272.
4. Banizs B, Pike MM, Millican CL, Ferguson WB, Komlosi P, Sheetz J, Bell PD, Schwiebert EM, Yoder BK. 2005. Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 132:5329-5339.
5. Ben J, Elworthy S, Ng a. SM, Van Eeden F, Ingham PW. 2011. Targeted mutation of the talpid3 gene in zebrafish reveals its conserved requirement for ciliogenesis and Hedgehog signalling across the vertebrates. Development 138:4969-4978.
6. Besse L, Neti M, Anselme I, Gerhardt C, Rüther U, Laclef C, Schneider-Maunoury S. 2011. Primary cilia control telencephalic patterning and morphogenesis via Gli3 proteolytic processing. Development 138:2079-2088.
7. Broom ER, Gilthorpe JD, Butts T, Campo-Paysaa F, Wingate RJT. 2012. The roof plate boundary is a bi-directional organiser of dorsal neural tube and choroid plexus development. Development 139:4261-4270.
8. Buxton P, Davey MG, Paton IR, Morrice DR, Francis-West PH, Burt DW, Tickle C. 2004. Craniofacial development in the talpid3 chicken mutant. Differentiation 72:348-362.
9. Cohen H, Davies S. 1937. The development of the cerebrospinal fluid spaces and choroid plexuses in the chick. J Anat 72:23-53.
10. Cruz C, Ribes V, Kutejova E, Cayuso J, Lawson V, Norris D, Stevens J, Davey M, Blight K, Bangs F, Mynett A, Hirst E, Chung R, Balaskas N, Brody SL, Marti E, Briscoe J. 2010. Foxj1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling. Development 137:4271-4282.
11. Davey MG, Paton IR, Yin Y, Schmidt M, Bangs FK, Morrice DR, Smith TG, Buxton P, Stamataki D, Tanaka M, Münsterberg AE, Briscoe J, Tickle C, Burt DW. 2006. The chicken talpid3 gene encodes a novel protein essential for Hedgehog signaling. Genes Dev 20:1365-1377.
12. Davey MG, James J, Paton IR, Burt DW, Tickle C. 2007. Analysis of talpid3 and wild-type chicken embryos reveals roles for Hedgehog signalling in development of the limb bud vasculature. Dev Biol 301:155-165.
13. Dawe HR, Farr H, Gull K. 2007. Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J Cell Sci 120:7-15.
14. Delous M, Baala L, Salomon R, Laclef C, Vierkotten J, Tory K, Golzio C, Lacoste T, Besse L, Ozilou C, Moutkine I, Hellman NE, Anselme I, Silbermann F, Vesque C, Gerhardt C, Rattenberry E, Wolf MTF, Gubler MC, Martinovic J, Encha-Razavi F, Boddaert N, Gonzales M, Macher MA, Nivet H, Champion G, Berthélémé JP, Niaudet P, McDonald F, Hildebrandt F, Johnson C A, Vekemans M, Antignac C, Rüther U, Schneider-Maunoury S, Attié-Bitach T, Saunier S. 2007. The ciliary gene RPGRIP1L is mutated in cerebello-oculo-renal syndrome (Joubert syndrome type B) and Meckel syndrome. Nature Genet 39:875-881.
15. Doolin PF, Birge Wesley J. 1966. Ultrastructural cilia and basal bodies of the epithelium of the choroid plexus in the chick embryo. J Cell Biol 29:333-345.
16. Dziegielewska KM, Ek J, Habgood MD, Saunders NR. 2001. Development of the choroid plexus. Microsc Res Tech 20:5-20.
17. Ede DA, Kelly WA. 1964. Developmental abnormalities in the head region of the talpid mutant of the fowl. J Embryol Exp Morphol 12:161-182.
18. Eggenschwiler JT, Anderson KV. 2007. Cilia and developmental signaling. Annu Rev Cell Dev Biol 23:345-373.
19. el-Gammal S. 1981. The development of the diencephalic choroid plexus in the chick. A scanning electron-microscopic study. Cell Tissue Res 219:297-311.
20. el-Gammal S. 1983. Regional surface changes during the development of the telencephalic choroid plexus in the chick. Cell Tissue Res 231:251-263.
21. Essner JJ, Vogan KJ, Wagner MK, Tabin CJ, Yost HJ, Brueckner M. 2002. Conserved function for embryonic nodal cilia. Nature 418:37-38.
22. Gros J, Feistel K, Viebahn C, Blum M, Tabin CJ. 2009. Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 324:941-944.
23. Grove Ea, Tole S, Limon J, Yip L, Ragsdale CW. 1998. The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125:2315-2325.
24. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
25. Hébert JM, Fishell G. 2008. The genetics of early telencephalon patterning: some assembly required. Nature Rev Neurosci 9:678-685.
26. Hildebrandt F, Benzing T, Katsanis N, Ph D. 2011. Ciliopathies. N Engl J Med 364:1533-1543.
27. Huangfu D, Anderson K V. 2005. Cilia and Hedgehog responsiveness in the mouse. Proc Natl Acad Sci USA 102:11325-11330.
28. Ishikawa H, Marshall WF. 2011. Ciliogenesis: building the cell's antenna. Nature Rev Mol Cell Biol 12:222-234.
29. Kuschel S, Rüther U, Theil T. 2003. A disrupted balance between Bmp/Wnt and Fgf signaling underlies the ventralization of the Gli3 mutant telencephalon. Dev Biol 260:484-495.
30. Lim L, Zhou H, Costa RH. 1997. The winged helix transcription factor HFH-4 is expressed during choroid plexus epithelial development in the mouse embryo. Proc Natl Acad Sci USA 94:3094-3099.
31. Masyuk AI, Masyuk TV, LaRusso NF. 2008. Cholangiocyte primary cilia in liver health and disease. Dev Dyn 237:2007-2012.
32. McGrath J, Somlo S, Makova S, Tian X, Brueckner M. 2003. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114:61-73.
33. Nieto MA, Ketan P, G. WD. 1996. In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 219-235.
34. Noreikat K, Wolff M, Kummer W, Kölle S. 2012. Ciliary activity in the oviduct of cycling, pregnant, and muscarinic receptor knockout mice. Biol Reprod 86:120.
35. Paintrand M, Delacroix H, Bornens M, Moudjou M. 1992. Centrosome organization their sensitivity and centriole architecture: to divalent cations. J Struct Biol 128:107-128.
36. Piasecki BP, Silflow CD. 2009. The UNI1 and UNI2 genes function in the transition of triplet to doublet microtubules between the centriole and cilium in chlamydomonas. Mol Biol Cell 20:368-378.
37. Satir P, Christensen ST. 2007. Overview of structure and function of mammalian cilia. Annu Rev Physiol 69:377-400.
38. Stubbs JL, Vladar EK, Axelrod JD, Kintner C. 2012. Multicilin promotes centriole assembly and ciliogenesis during multiciliate cell differentiation. Nature Cell Biol 14:140-147.
39. Sturrock RR. 1979. A morphological study of the development of the mouse choroid plexus. J Anat 129:777-793.
40. Subramanian L, Tole S. 2009. Mechanisms underlying the specification, positional regulation, and function of the cortical hem. Cerebral Cortex 19 Suppl 1:i90-i95.
41. Tanos BE, Yang H-J, Soni R, Wang W-J, Macaluso FP, Asara JM, Tsou M-FB. 2013. Centriole distal appendages promote membrane docking, leading to cilia initiation. Genes Dev 27:163-168.
42. Theil T, Alvarez-Bolado G, Walter a, Rüther U. 1999. Gli3 is required for Emx gene expression during dorsal telencephalon development. Development 126:3561-3571.
43. Vierkotten J, Dildrop R, Peters T, Wang B, Rüther U. 2007. Ftm is a novel basal body protein of cilia involved in Shh signalling. Development 134:2569-2577.
44. Vladar EK, Stearns T. 2007. Molecular characterization of centriole assembly in ciliated epithelial cells. J Cell Biol 178:31-42.
45. Von Frowein J, Wizenmann A, Götz M. 2006. The transcription factors Emx1 and Emx2 suppress choroid plexus development and promote neuroepithelial cell fate. Dev Biol 296:239-252.
46. Yin Y, Bangs F, Paton IR, Prescott A, James J, Davey MG, Whitley P, Genikhovich G, Technau U, Burt DW, Tickle C. 2009. The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation. Development 136:655-664.
47. Yu X, Ng CP, Habacher H, Roy S. 2008. Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nature Genet 40:1445-1453.