title: Gene regulatory network for neurogenesis in a sea star embryo connects broad neural specification and localized patterning.
abstract: A great challenge in development biology is to understand how interacting networks of regulatory genes can direct the often highly complex patterning of cells in a 3D embryo. Here, we detail the gene regulatory network that describes the distribution of ciliary band-associated neurons in the bipinnaria larva of the sea star. This larva, typically for the ancestral deuterostome dipleurula larval type that it represents, forms two loops of ciliary bands that extend across much of the anterior-posterior and dorsal-ventral ectoderm. We show that the sea star first likely uses maternally inherited factors and the Wnt and Delta pathways to distinguish neurogenic ectoderm from endomesoderm. The broad neurogenic potential of the ectoderm persists throughout much of gastrulation. Nodal, bone morphogenetic protein 2/4 (Bmp2/4), and Six3-dependent pathways then sculpt a complex ciliary band territory that is defined by the expression of the forkhead transcription factor, foxg. Foxg is needed to define two molecularly distinct ectodermal domains, and for the formation of differentiated neurons along the edge of these two territories. Thus, significantly, Bmp2/4 signaling in sea stars does not distinguish differentiated neurons from nonneuronal ectoderm as it does in many other animals, but instead contributes to the patterning of an ectodermal territory, which then, in turn, provides cues to permit the final steps of neuronal differentiation. The modularity between specification and patterning likely reflects the evolutionary history of this gene regulatory network, in which an ancient module for specification of a broad neurogenic potential ectoderm was subsequently overlaid with a module for patterning.
authors: Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213, USA.
authors: Kristen A
authors: KA
authors: Yankura
authors: Claire S
authors: CS
authors: Koechlein
authors: Abigail F
authors: AF
authors: Cryan
authors: Alys
authors: A
authors: Cheatle
authors: Veronica F
authors: VF
authors: Hinman
mesh_terms: D000818:Animals; D001483:Base Sequence; D019521:Body Patterning / Q000502:physiology*; D055396:Bone Morphogenetic Protein 2 / Q000378:metabolism; D055415:Bone Morphogenetic Protein 4 / Q000378:metabolism; D004475:Ectoderm / Q000166:cytology / Q000196:embryology; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000196:embryology*; D004707:Endoderm / Q000166:cytology / Q000196:embryology; D054262:Gastrulation / Q000502:physiology; D018507:Gene Expression Regulation, Developmental / Q000502:physiology; D047908:Intracellular Signaling Peptides and Proteins / Q000378:metabolism; D008565:Membrane Proteins / Q000378:metabolism; D008969:Molecular Sequence Data; D055495:Neurogenesis / Q000502:physiology*; D013215:Starfish / Q000166:cytology / Q000196:embryology*; D051153:Wnt Proteins / Q000378:metabolism; D060449:Wnt Signaling Pathway / Q000502:physiology*
chemical_list: D055396:Bone Morphogenetic Protein 2; D055415:Bone Morphogenetic Protein 4; D047908:Intracellular Signaling Peptides and Proteins; D008565:Membrane Proteins; D051153:Wnt Proteins; C064045:delta protein
keywords: echinoderm; evolution; neural patterning
references: Mech Dev. 2003 Oct;120(10):1165-76
references: 14568105
references: Dev Biol. 2009 Apr 15;328(2):221-33
references: 19389361
references: Development. 1999 Jun;126(11):2309-25
references: 10225991
references: Gene Expr Patterns. 2005 Feb;5(3):381-6
references: 15661644
references: PLoS Genet. 2010 Dec 23;6(12):e1001259
references: 21203442
references: Dev Biol. 2006 Dec 1;300(1):49-62
references: 17081512
references: BMC Biol. 2010 Nov 30;8:143
references: 21118544
references: Nat Rev Genet. 2008 Sep;9(9):663-77
references: 18679435
references: Curr Opin Neurobiol. 1996 Feb;6(1):3-10
references: 8794055
references: Gene Expr Patterns. 2010 Jun;10(4-5):177-84
references: 20398801
references: Development. 2006 Jun;133(12):2337-46
references: 16687447
references: Curr Biol. 1996 Dec 1;6(12):1634-41
references: 8994828
references: Development. 2009 Apr;136(7):1179-89
references: 19270175
references: Dev Cell. 2004 Mar;6(3):397-410
references: 15030762
references: Development. 2011 Sep;138(17):3613-23
references: 21828090
references: Development. 1999 Jan;126(2):345-57
references: 9847248
references: Nature. 1996 Mar 7;380(6569):37-40
references: 8598900
references: Cell. 2003 Jun 27;113(7):853-65
references: 12837244
references: Integr Comp Biol. 2006 Jun;46(3):312-22
references: 21672744
references: PLoS Biol. 2013;11(1):e1001467
references: 23335859
references: Dev Genes Evol. 1999 Mar;209(3):198-205
references: 10079363
references: J Comp Neurol. 2006 May 10;496(2):244-51
references: 16538680
references: Nat Rev Mol Cell Biol. 2005 Jun;6(6):462-75
references: 15928710
references: Development. 2008 Feb;135(3):441-50
references: 18094027
references: Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19404-9
references: 18042699
references: Nature. 2003 Jan 9;421(6919):158-60
references: 12520300
references: Genes Dev. 2003 Feb 1;17(3):368-79
references: 12569128
references: Mol Biol Evol. 2005 Nov;22(11):2275-84
references: 16049193
references: Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13356-61
references: 14595011
references: PLoS Biol. 2009 Nov;7(11):e1000248
references: 19956794
references: Evol Dev. 2004 Mar-Apr;6(2):95-104
references: 15009122
references: Cell Mol Life Sci. 2008 Jan;65(1):128-40
references: 17928954
references: Evol Dev. 2009 Sep-Oct;11(5):513-24
references: 19754708
references: Genes Dev. 2011 Dec 1;25(23):2453-64
references: 22085726
references: Biol Bull. 1999 Oct;197(2):123-131
references: 28281819
references: PLoS Genet. 2012;8(12):e1003164
references: 23300467
references: Brain Behav Evol. 2009;74(3):177-90
references: 20029182
references: Dev Biol. 2010 Nov 1;347(1):71-81
references: 20709054