Abstract
ABSTRACT The mechanisms that regulate patterning and growth of the developing cerebral cortex remain unclear. Suggesting a role for Wnt signaling in these processes, multiple Wnt genes are expressed in selective patterns in the embryonic cortex. We have examined the role of Wnt-3a signaling at the caudomedial margin of the developing cerebral cortex, the site of hippocampal development. We show that Wnt-3a acts locally to regulate the expansion of the caudomedial cortex, from which the hippocampus develops. In mice lacking Wnt-3a, caudomedial cortical progenitor cells appear to be specified normally, but then underproliferate. By mid-gestation, the hippocampus is missing or represented by tiny populations of residual hippocampal cells. Thus, Wnt-3a signaling is crucial for the normal growth of the hippocampus. We suggest that the coordination of growth with patterning may be a general role for Wnts during vertebrate development.
References
63
Referenced
509
{'key': '2023100913235516000_DEVELOP_127_3_457C1', 'first-page': '443', 'article-title': 'Hippocampal Formation', 'volume-title': 'In The Rat Nervous System', 'author': 'Amaral', 'year': '1995', 'edition': '2nd'}
/ In The Rat Nervous System / Hippocampal Formation by Amaral (1995){'key': '2023100913235516000_DEVELOP_127_3_457C2', 'first-page': '1', 'article-title': 'Time of neuron origin in the hippocampal region', 'volume': '2', 'author': 'Angevine', 'year': '1965', 'journal-title': 'Exp. Neurol. Supplement'}
/ Exp. Neurol. Supplement / Time of neuron origin in the hippocampal region by Angevine (1965)10.1073/pnas.89.19.8879
/ Proc. Natl. Acad. Sci. USA / Early regional specification for a molecular neuronal phenotype in the rat neocortex by Arimatsu (1992)10.1242/dev.124.1.1
/ Development / BMP-7 influences pattern and growth of the developing hindbrain of mouse embryos by Arkell (1997)10.1523/JNEUROSCI.14-09-05525.1994
/ J. Neurosci / Kainate receptor gene expression in the developing rat brain by Bahn (1994)10.1523/JNEUROSCI.11-02-00519.1991
/ J. Neurosci / The early commitment of fetal neurons to the limbic cortex by Barbe (1991)10.1093/cercor/4.3.271
/ Cerebral Cortex / tHomotopic, but not heterotopic, fetal cortical transplants can result in functional sparing following neonatal damage to the frontal cortex by Barth (1994)10.1002/cne.901900108
/ J. Comp. Neurol / Development of the hippocampal region in the rat. II. Morphongenesis during embryonic and early postnatal life by Bayer (1980)10.1002/cne.901900107
/ J. Comp. Neurol / Development of the hippocampal region in the rat. I. Neurogenesis examined with 3H-thymidine autoradiography by Bayer (1980)10.1242/dev.121.8.2407
/ Development / Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta by Bettenhausen (1995)10.1016/0896-6273(95)90065-9
/ Neuron / T-Brain-1: a homolog of brachyury whose expression defines molecularly distinct domains within the cerebral cortex by Bulfone (1995)10.1002/j.1460-2075.1988.tb03074.x
/ EMBO J / Differential distribution of beta-tubulin isotypes in cerebrllum by Burgoyne (1988)10.1101/gad.11.24.3286
/ Genes Dev / Wnt signaling: a common theme in animal development by Cadigan (1997)10.1038/368460a0
/ Nature / Early determination of a mouse somatosensory cortex marker by Cohen-Tannoudji (1994)10.1242/dev.121.7.2177
/ Development / Xwnt-8b: a maternally expressed Xenopus Wnt gene with a potential role in establishing the dorsoventral axis by Cui (1995)10.1242/dev.121.7.2099
/ Development / Dorsalization of the neural tube by the non-neural ectoderm by Dickinson (1995)10.1242/dev.120.6.1453
/ Development / Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system by Dickinson (1994)10.1038/24620
/ Nature / Control of neural crest cell fate by the Wnt signalling pathway by Dorskey (1998)10.1002/(SICI)1096-9861(19960129)365:1<129::AID-CNE10>3.0.CO;2-L
/ J. Comp. Neurol / Development of spinal cord projections from neocortical transplants heterotypically placed in the neocortex of newborn hosts in highly dependent on the embryonc locus of origin of the graft by Ebrahimi-Gaillard (1996)10.1093/cercor/3.3.187
/ Cerebral Cortex / Cerebral cortical progenitors are fated to produce region-specific neuronal populations by Ferri (1993)10.1523/JNEUROSCI.11-06-01577.1991
/ J. Neurosci / Transient and persistent expression of NT-3/HDNF mRNA in the rat brain during postnatal development by Freidman (1991)10.1242/dev.124.11.2203
/ Development / Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development by Furuta (1997)10.1083/jcb.119.3.493
/ J. Cell Biol / Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation by Gavrieli (1992)10.1016/0896-6273(92)90289-P
/ Neuron / Neuronal precursor cells in the rat hippocampal formation contribute to more than one cytoarchitectonic area by Grove (1992)10.1242/dev.125.12.2315
/ Development / The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice by Grove (1998)10.1016/0925-4773(95)00385-E
/ Mech. Dev / Wnt expression patterns in chick embryo nervous system by Hollyday (1995)10.1038/40146
/ Nature / Wnt signalling required for expansion of neural crest and CNS progenitors by Ikeya (1997)10.1242/dev.121.6.1787
/ Development / Zebrafish wnt8 and wnt8b share a common activity but are involved in distinct developmental pathways by Kelly (1995)10.1242/dev.121.6.1927
/ Development / Dorsal-ventral patterning and differentiation of noggin-induced neural tissue in the absence of mesoderm by Knecht (1995)10.1093/hmg/7.5.813
/ Human Molecular Genetics / A novel mammalian wnt gene, WNT8B, shows brain-restricted expression in early development, with sharply delimited expression boundaries in the developing forebrain by Lako (1998)10.1101/gad.12.21.3394
/ Genes Dev / Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord by Lee (1998)10.1146/annurev.neuro.20.1.1
/ Annu. Rev. Neurosci / Patterning and specification of the cerebral cortex by Levitt (1997)10.1016/S0092-8674(01)80015-5
/ Cell / A role for the roof plate and its resident TGFB-related proteins in neuronal patterning in the dorsal spinal cord by Liem (1997)10.1016/0092-8674(95)90276-7
/ Cell / Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm by Liem (1995)10.1126/science.274.5290.1109
/ Science / Patterning the vertebrate neuraxis by Lumsden (1996)10.1016/0006-8993(88)90055-8
/ Brain Research / Use of bromodeoxyuridine immunohistochemistry to examine the proliferation, migration, and time of origin of cells in the central nervous system by Miller (1988)10.1016/S0168-9525(97)01093-7
/ Trends in Genetics / WNTs modulate cell fate and behavior during vertebrate development by Moon (1997)10.1242/dev.113.4.1207
/ Development / Contiguous patterns of c-kit and steel expression: analysis of muations at the W and Sl loci by Motro (1991)10.1242/dev.122.6.1781
/ Development / Distinct mitogenic and cell fate specification functions of wingless in different regions of the wing by Neumann (1996)10.1242/dev.124.4.871
/ Development / Long-range action of wingless organizes the dorsal-ventral axis of the drosophila wing by Neumann (1997)10.1146/annurev.ne.17.030194.002223
/ Annu. Rev. Neurosci / Specification of neocortical areas and thalamocortical connections by O’Leary (1994)10.1242/dev.119.1.247
/ Development / Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds by Parr (1993)10.1016/0166-2236(93)90080-6
/ Trends in Neurosci / Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization by Puelles (1993)10.1101/gad.5.3.381
/ Genes Dev / Expression of two members of the Wnt family during mouse development – resrticted temporal and spatial patterns in the developing neural tube by Roelink (1991)10.1126/science.7939711
/ Science / The embryonic vertebrate forebrain: the prosomeric model by Rubenstein (1994)10.1146/annurev.neuro.21.1.445
/ Annu. Rev. Neurosci / Regionalization of the prosencepalic neural plate by Rubenstein (1998)10.1126/science.2047863
/ Science / Potential of visual cortex to develop an array of functional units unique to somatosensory cortex by Schlaggar (1991)10.1242/dev.121.12.3923
/ Development / Longitudinal organization of the anterior neural plate and neural tube by Shimamura (1995)10.1242/dev.116.3.745
/ Development / The wingless product is required for cell proliferation in Malpighian tube anlage of Drosophila melanogaster by Skaer (1992)10.1002/cne.901850303
/ J. Comp. Neurol / The development of the hippocampus and dentate gyrus in normal and reeler mice by Stanfield (1979)10.1002/cne.901850302
/ J. Comp. Neurol / The morphology of the hippocampus and dentate gyrus in normal and reeler mice by Stanfield (1979)10.1007/978-1-4615-6619-9_4
/ Cerebral Cortex / The development of the hippocampal region by Stanfield (1988)10.1101/gad.8.2.174
/ Genes Dev / Wnt-3a regulates somite and tailbud formation in the mouse embryo by Takada (1994)10.1126/science.274.5290.1115
/ Science / Diversity and pattern in the developing spinal cord by Tanabe (1996)10.1242/dev.124.24.4959
/ Development / Early specification and autonomous development of cortical fields in the mouse hippocampus by Tole (1997)10.1016/0092-8674(94)90139-2
/ Cell / Drosophila wingless sustains engrailed expression only in adjoining cells: evidence from mosaic embryos by Vincent (1994)10.1126/science.1734520
/ Science / Widespread dispersion of neuronal clones across functional regions of the cerebral cortex by Walsh (1992)10.1016/0092-8674(87)90664-7
/ Cell / Expression of the proto-oncogene int-1 is restricted to specific neural cells in the developing mouse embryo by Wilkinson (1987)10.1523/JNEUROSCI.13-08-03582.1993
/ J. Neurosci / A complex mosaic of high-affinity dainate receptors in rat brain by Wisden (1993)10.1016/0896-6273(94)90357-3
/ Neuron / BIG-1: a new TAG-1/F3-related member of the immunoglobulin superfamily with neurite outgrowth-promoting activity by Yoshihari (1994)10.1006/dbio.1997.8502
/ Dev. Biol / Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse by Yoshikawa (1997)10.1016/S0092-8674(00)81991-1
/ Cell / Direct and long-range action of a wingless morphogen gradient by Zecca (1996){'key': '2023100913235516000_DEVELOP_127_3_457C63', 'first-page': '649', 'article-title': 'Cortex: Areal and Laminar Structure', 'volume-title': 'In The Rat Nervous System, 2nd ed', 'author': 'Zilles', 'year': '1995'}
/ In The Rat Nervous System, 2nd ed / Cortex: Areal and Laminar Structure by Zilles (1995)
Dates
Type | When |
---|---|
Created | 4 years, 4 months ago (April 26, 2021, 12:23 a.m.) |
Deposited | 1 year, 10 months ago (Oct. 9, 2023, 9:24 a.m.) |
Indexed | 2 days, 12 hours ago (Sept. 3, 2025, 6:04 a.m.) |
Issued | 25 years, 7 months ago (Feb. 1, 2000) |
Published | 25 years, 7 months ago (Feb. 1, 2000) |
Published Online | 25 years, 7 months ago (Feb. 1, 2000) |
Published Print | 25 years, 7 months ago (Feb. 1, 2000) |
@article{Lee_2000, title={A local Wnt-3a signal is required for development of the mammalian hippocampus}, volume={127}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.127.3.457}, DOI={10.1242/dev.127.3.457}, number={3}, journal={Development}, publisher={The Company of Biologists}, author={Lee, Scott M. K. and Tole, Shubha and Grove, Elizabeth A. and McMahon, Andrew P.}, year={2000}, month=feb, pages={457–467} }