Zebrafish colgate/hdac1 functions in the non-canonical Wnt pathway during axial extension and in Wnt-independent branchiomotor neuron migration.
Vertebrate gastrulation involves the coordinated movements of populations of cells. These movements include cellular rearrangements in which cells polarize along their medio-lateral axes leading to cell intercalations that result in elongation of the body axis. Molecular analysis of this process has implicated the non-canonical Wnt/Frizzled signaling pathway that is similar to the planar cell polarity pathway (PCP) in Drosophila. Here we describe a zebrafish mutant, colgate (col), which displays defects in the extension of the body axis and the migration of branchiomotor neurons. Activation of the non-canonical Wnt/PCP pathway in these mutant embryos by overexpressing DeltaNdishevelled, rho kinase2 and van gogh-like protein 2 (vangl2) rescues the extension defects suggesting that col acts as a positive regulator of the non-canonical Wnt/PCP pathway. Further, we show that col normally regulates the caudal migration of nVII facial hindbrain branchiomotor neurons and that the mutant phenotype can be rescued by misexpression of vangl2 independent of the Wnt/PCP pathway. We cloned the col locus and found that it encodes histone deacetylase1 (hdac1). Our previous results and studies by others have implicated hdac1 in repressing the canonical Wnt pathway. Here, we demonstrate novel roles for zebrafish hdac1 in activating non-canonical Wnt/PCP signaling underlying axial extension and in promoting Wnt-independent caudal migration of a subset of hindbrain branchiomotor neurons.
Nambiar
Roopa M
RM
Center for Molecular Neurobiology, Molecular, Cell and Developmental Biology Program, Department of Neuroscience, Ohio State University, 105 Rightmire Hall, 1060 Carmack Road, Columbus, OH 43210, USA.
Ignatius
Myron S
MS
Henion
Paul D
PD
D000818:Animals; D001369:Axons / Q000201:enzymology / Q000502:physiology*; D019521:Body Patterning / Q000235:genetics / Q000502:physiology*; D002465:Cell Movement / Q000235:genetics / Q000502:physiology*; D016764:Cell Polarity / Q000235:genetics / Q000502:physiology; D056284:Histone Deacetylase 1; D006655:Histone Deacetylases / Q000235:genetics / Q000502:physiology*; D009046:Motor Neurons / Q000502:physiology*; D009154:Mutation; D012249:Rhombencephalon / Q000166:cytology / Q000196:embryology / Q000201:enzymology; D015398:Signal Transduction / Q000235:genetics / Q000502:physiology*; D051153:Wnt Proteins / Q000235:genetics / Q000502:physiology*; D015027:Zebrafish / Q000196:embryology* / Q000235:genetics; D029961:Zebrafish Proteins / Q000235:genetics / Q000502:physiology*
D051153:Wnt Proteins; D029961:Zebrafish Proteins; C488363:HDAC1 protein, zebrafish; D056284:Histone Deacetylase 1; D006655:Histone Deacetylases
J Neurosci. 2000 Jan 1;20(1):206-18
10627598
Neurosci Lett. 1996 Sep 27;216(2):109-12
8904795
Development. 2000 May;127(10):2227-38
10769246
Nature. 2000 May 4;405(6782):76-81
10811221
Mol Cell Biol. 2000 Sep;20(18):6882-90
10958684
Genesis. 2000 Aug;27(4):159-73
10992326
Nucleic Acids Res. 2001 Apr 1;29(7):1410-9
11266540
Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):3802-7
11274398
Nat Genet. 2001 Jul;28(3):251-5
11431695
Dev Biol. 2001 Jul 15;235(2):388-96
11437445
Science. 2001 Aug 10;293(5532):1074-80
11498575
Curr Opin Cell Biol. 2001 Oct;13(5):635-40
11544034
Dev Cell. 2001 Aug;1(2):251-64
11702784
Nature. 2001 Nov 15;414(6861):258-61
11713509
Nat Cell Biol. 2002 Jan;4(1):20-5
11780127
Dev Biol. 2002 Feb 15;242(2):149-60
11820812
Curr Biol. 2002 Jun 4;12(11):876-84
12062050
Dev Cell. 2002 Jun;2(6):695-706
12062082
Nat Cell Biol. 2002 Aug;4(8):610-5
12105418
Trends Genet. 2002 Sep;18(9):447-55
12175805
Genes Dev. 2002 Aug 15;16(16):2073-84
12183362
Biochem J. 2003 Mar 15;370(Pt 3):737-49
12429021
Mech Dev. 2003 Apr;120(4):467-76
12676324
Curr Biol. 2003 Apr 15;13(8):680-5
12699626
Development. 2003 Sep;130(17):4037-46
12874125
Curr Opin Pharmacol. 2003 Aug;3(4):344-51
12901942
Dev Biol. 2004 Mar 1;267(1):165-80
14975724
Development. 2004 Jun;131(12):2983-95
15169759
Dev Biol. 2004 Oct 1;274(1):110-24
15355792
Proc Can Cancer Conf. 1966;6:313-35
5934780
Nature. 1989 Feb 2;337(6206):461-4
2915691
Neuron. 1990 May;4(5):669-79
2344406
Development. 1992 Dec;116(4):1021-32
1295726
Development. 1993 Jun;118(2):417-25
8223269
J Neurosci. 1994 Jun;14(6):3475-86
7911517
Bioessays. 1995 May;17(5):423-30
7786288
Development. 1995 Jun;121(6):1787-99
7600994
Bioessays. 1995 Nov;17(11):931-9
8526887
Development. 1996 Jan;122(1):271-80
8565839
Dev Genet. 1996;18(1):11-7
8742830
Development. 1996 Dec;123:67-80
9007230
Development. 1996 Dec;123:143-51
9007236
Development. 1996 Dec;123:451-60
9007262
Development. 1996 Dec;122(12):3981-90
9012518
EMBO J. 1997 Jun 2;16(11):3089-96
9214626
Development. 1997 Jul;124(13):2633-44
9217005
Development. 1998 Feb;125(3):393-406
9425135
Cold Spring Harb Symp Quant Biol. 1997;62:227-34
9598355
Dev Genes Evol. 1998 Jul;208(5):245-58
9683740
Trends Genet. 1998 Nov;14(11):452-8
9825673
Genes Dev. 1999 Sep 1;13(17):2218-30
10485845
Mech Dev. 1999 May;83(1-2):27-37
10507837
Nat Genet. 2005 May;37(5):537-43
15852005
Mol Cell. 2005 May 13;18(4):483-90
15893731
Development. 2005 Jul;132(13):3027-43
15944187
Dev Dyn. 2005 Jul;233(3):883-9
15895391
Dev Dyn. 2005 Oct;234(2):279-92
16127722
Nature. 2000 Jan 6;403(6765):41-5
10638745