PUBLICATION

Rhombomere boundaries are Wnt signaling centers that regulate metameric patterning in the zebrafish hindbrain

Authors

Riley, B.B., Chiang, M.Y., Storch, E.M., Heck, R., Buckles, G.R., and Lekven, A.C.

ID

ZDB-PUB-040916-2

Date

2004

Source

Developmental Dynamics : an official publication of the American Association of Anatomists 231(2): 278-291 (Journal)

Registered Authors

Heck, Rebecca, Lekven, Arne, Riley, Bruce

Keywords

boundary-formation, Wnt, tcf/lef, Delta-Notch, erm, ephA4, pou2, radial glia, reticulospinal, commissural neuron

MeSH Terms

Body Patterning*
Mutation
Transcription Factors/genetics
Transcription Factors/metabolism
Membrane Proteins/genetics
Membrane Proteins/metabolism
Morphogenesis*
Intracellular Signaling Peptides and Proteins
Receptors, Notch
Zebrafish
Zebrafish Proteins/genetics
Zebrafish Proteins/metabolism
Signal Transduction/physiology*
Intercellular Signaling Peptides and Proteins/genetics
Intercellular Signaling Peptides and Proteins/metabolism*
Nuclear Proteins/genetics
Nuclear Proteins/metabolism
Hepatocyte Nuclear Factor 3-beta
DNA-Binding Proteins/genetics
DNA-Binding Proteins/metabolism
Animals
Rhombencephalon/anatomy & histology
Rhombencephalon/embryology*
Rhombencephalon/physiology
In Situ Hybridization
Wnt Proteins
Embryonic Structures/anatomy & histology
Embryonic Structures/physiology*
Wnt1 Protein

(all 29)

PubMed

15366005 Full text @ Dev. Dyn.

Abstract

The vertebrate hindbrain develops from a series of segments (rhombomeres) distributed along the anteroposterior axis. We are studying the roles of Wnt and Delta-Notch signaling in maintaining rhombomere boundaries as organizing centers in the zebrafish hindbrain. Several wnt genes (wnt1, wnt3a, wnt8b, and wnt10b) show elevated expression at rhombomere boundaries, whereas several delta genes (dlA, dlB, and dlD) are expressed in transverse stripes flanking rhombomere boundaries. Partial disruption of Wnt signaling by knockdown of multiple wnt genes, or the Wnt mediator tcf3b, ablates boundaries and associated cell types. Expression of dlA is chaotic, and cell types associated with rhombomere centers are disorganized. Similar patterning defects are observed in segmentation mutants spiel-ohne-grenzen (spg) and valentino (val), which fail to form rhombomere boundaries due to faulty interactions between adjacent rhombomeres. Stripes of wnt expression are variably disrupted, with corresponding disturbances in metameric patterning. Mutations in dlA or mind bomb (mib) disrupt Delta-Notch signaling and cause a wide range of patterning defects in the hindbrain. Stripes of wnt1 are initially normal but subsequently dissipate, and metameric patterning becomes increasingly disorganized. Driving wnt1 expression using a heat-shock construct partially rescues metameric patterning in mib mutants. Thus, rhombomere boundaries act as Wnt signaling centers required for precise metameric patterning, and Delta signals from flanking cells provide feedback to maintain wnt expression at boundaries. Similar feedback mechanisms operate in the Drosophila wing disc and vertebrate limb bud, suggesting coaptation of a conserved signaling module that spatially organizes cells in complex organ systems. Developmental Dynamics 231:278-291, 2004. Copyright 2004 Wiley-Liss, Inc.

Genes / Markers

Figures

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Expression

Gene	Fish	Conditions	Stage	Anatomy	Assay	Figure
ascl1a	AB	standard conditions	Prim-5	rhombomere	ISH	text only
ascl1b	AB	standard conditions	Prim-5	rhombomere	ISH	text only
dla	AB	standard conditions	Prim-5	hindbrain	ISH	Fig. 6
dla	AB	standard conditions	Prim-15	rhombomere	ISH	Fig. 1
dla	AB	standard conditions	Prim-5	rhombomere	ISH	Fig. 1
dla	AB + MO1-tcf7l1b	standard conditions	Prim-15	hindbrain	ISH	Fig. 3
dla	AB + MO2-wnt3a + MO2-wnt8b	standard conditions	Prim-15	hindbrain	ISH	Fig. 2
dla	Df(Chr23:acvr1ba,sp5l,wnt1,wnt10b)w5/w5	standard conditions	Prim-15	hindbrain	ISH	Fig. 2
dla	Df(Chr23:acvr1ba,sp5l,wnt1,wnt10b)w5/w5 + MO2-wnt3a	standard conditions	Prim-15	hindbrain	ISH	Fig. 2
dla	Df(Chr23:acvr1ba,sp5l,wnt1,wnt10b)w5/w5 + MO2-wnt3a + MO2-wnt8b	standard conditions	Prim-15	hindbrain	ISH	Fig. 2

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Phenotype

Fish	Conditions	Stage	Phenotype	Figure
AB + MO1-tcf7l1b	standard conditions	Prim-5	axon guidance disrupted, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-5	embryonic pattern specification disrupted, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-5	hindbrain constricted, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-5	hindbrain morphology, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-5	rhombomere primary neuron crowded, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-5	rhombomere primary neuron disorganized, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-15	axon guidance disrupted, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-15	embryonic pattern specification disrupted, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-15	hindbrain commissure neuron absent, abnormal	Fig. 3
AB + MO1-tcf7l1b	standard conditions	Prim-15	hindbrain constricted, abnormal	Fig. 3

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Mutations / Transgenics

Allele	Construct	Type	Affected Genomic Region
b337		Point Mutation	mafba
dx2		Point Mutation	dla
hi349Tg	Tg(F5)	Transgenic Insertion	pou5f3
ta52b		Point Mutation	mib1
w5		Deficiency	acvr1ba sp5l wnt1 wnt10b

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Human Disease / Model

Sequence Targeting Reagents

Target	Reagent	Reagent Type
tcf7l1b	MO1-tcf7l1b	MRPHLNO
wnt3a	MO2-wnt3a	MRPHLNO
wnt8b	MO2-wnt8b	MRPHLNO

Fish

Fish
AB
AB + MO1-tcf7l1b
AB + MO2-wnt3a + MO2-wnt8b
Df(Chr23:acvr1ba,sp5l,wnt1,wnt10b)w5/w5
Df(Chr23:acvr1ba,sp5l,wnt1,wnt10b)w5/w5 + MO2-wnt3a
Df(Chr23:acvr1ba,sp5l,wnt1,wnt10b)w5/w5 + MO2-wnt3a + MO2-wnt8b
dla^dx2/dx2
mafba^b337/b337 (AB)
mib1^ta52b/ta52b
pou5f3^{hi349Tg/hi349Tg}

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Antibodies

Orthology

Engineered Foreign Genes

Mapping

Riley et al., 2004 ZDB-PUB-040916-2 PMID:15366005

Rhombomere boundaries are Wnt signaling centers that regulate metameric patterning in the zebrafish hindbrain

Riley et al., 2004

ZDB-PUB-040916-2
PMID:15366005