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Wnt Signaling in Hippocampal Development 459 Development 127, 457-467 (2000) 457 Printed in Great Britain © The Company of Biologists Limited 2000 DEV9689 A local Wnt-3a signal is required for development of the mammalian hippocampus Scott M. K. Lee1,*, Shubha Tole2,‡, Elizabeth Grove2 and Andrew P. McMahon1,§ 1Department of Molecular and Cellular Biology, The Biolabs, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA 2Department of Neurobiology, Pharmacology and Physiology, Committees on Developmental Biology and Neurobiology, and Pritzker School of Medicine, University of Chicago, Chicago, IL 60637, USA *Current address: Nina Ireland Laboratory of Developmental Neurobiology, Center for Neurobiology and Psychiatry, Department of Psychiatry and Programs in Neuroscience, Developmental Biology and Biomedical Sciences, 401 Parnassus Avenue, University of California at San Francisco, CA 94143-0984, USA ‡Current address: Department of Biological Sciences, Tata Institute of Fundamental Research, Mumbai-400,005, India §Author for correspondence (e-mail: [email protected]) Accepted 27 October 1999; published on WWW 12 January 2000 SUMMARY The mechanisms that regulate patterning and growth of the appear to be specified normally, but then underproliferate. developing cerebral cortex remain unclear. Suggesting a By mid-gestation, the hippocampus is missing or role for Wnt signaling in these processes, multiple Wnt represented by tiny populations of residual hippocampal genes are expressed in selective patterns in the embryonic cells. Thus, Wnt-3a signaling is crucial for the normal cortex. We have examined the role of Wnt-3a signaling at growth of the hippocampus. We suggest that the the caudomedial margin of the developing cerebral cortex, coordination of growth with patterning may be a general the site of hippocampal development. We show that Wnt- role for Wnts during vertebrate development. 3a acts locally to regulate the expansion of the caudomedial cortex, from which the hippocampus develops. In mice Key words: Wnt, Hippocampus, Pattern formation, Proliferation, lacking Wnt-3a, caudomedial cortical progenitor cells Cortical patterning INTRODUCTION cerebral cortex is divided into allocortex and neocortex, a number of studies are beginning to provide clues about how The embryonic dorsal telencephalon of vertebrates contains the specific areas are specified within the neocortex. A number of cerebral cortex, which is the seat of higher cognitive functions lines of evidence reveal an instructive role for thalamic inputs in mammals. The cerebral cortex is subdivided into many in specifying the functional properties of neocortical areas histologically and functionally distinct regions. The broadest (reviewed in O’Leary et al., 1994). For example, if fetal visual subdivisions are between the six-layered isocortex (neocortex) cortex is transplanted into neonatal somatosensory cortex, the and the non-six-layered allocortices, which include the transplanted tissue gives rise to a somatosensory cortex with archicortex and the paleocortex, as well as transitional cortices many of its normal properties (Schlaggar and O’Leary, 1991). (Zilles and Wree, 1995). The neocortex and the allocortex are A corollary of these studies is that positional information must further subdivided into unique areas based on cytoarchitectural be present in the cortical primordia prior to the ingrowth of and connectional specialization. thalamic axons in order to guide them to their appropriate The hippocampus is an archicortical structure located at the target areas. The existence of pathways regulating the caudomedial edge of the neocortex (Amaral and Witter, 1995). establishment of such positional information can be inferred In the adult, the longitudinal axis of the hippocampus forms a directly from a number of studies examining the mechanisms ‘C’-shape. From its rostral pole, located just dorsal and that specify the differential expression of genes in different posterior to the septal nuclei, the hippocampus curves over and cortical areas (Barbe and Levitt, 1991; Arimatsu et al., 1992; behind the diencephalon to the incipient temporal lobe, its Ferri and Levitt, 1993; Barth and Stanfield, 1994; Cohen- caudal pole. The transverse axis of the hippocampus is divided Tannoudji et al., 1994; Bulfone et al., 1995; Ebrahimi-Gaillard into distinct fields. From proximal to distal they are the dentate and Roger, 1996; Levitt et al., 1997). While these studies all gyrus (DG) and the CA3 and CA1 fields of Ammon’s horn (the point to the existence of positional information within the early CA fields are often referred to as the hippocampus proper). cortical primordia, the molecular mechanisms responsible for Lateral to the hippocampus is the subiculum and the establishing this information remain obscure. pre/parasubiculum, transitional cortices that lie between the Developmentally the hippocampus arises at the caudomedial hippocampus and the adjacent neocortex. edge of the continuous dorsal telencephalic neuroepithelium While little is known about the mechanisms by which the adjacent to the telencephalic roof (Stanfield and Cowan, 458 S. M. K. Lee and others 1979a,b, 1988; Bayer, 1980a,b). A strip of cortical progenitor 3a acts at 10.5 dpc to regulate the proliferative expansion of cells along this edge, the cortical hem (or hem), expresses caudomedial cortical progenitor cells. The loss of this many members of the Bone Morphogenetic Protein (BMP) and ‘hippocampal’ progenitor pool leads to a failure of normal Wnt families of inductive signaling factors (Furuta et al., 1997; hippocampal development in Wnt-3a mutants. Grove et al., 1998). A number of studies have revealed roles for BMP and Wnt signaling in the regulation of dorsal patterning at more caudal regions of the vertebrate neuraxis MATERIALS AND METHODS (Dickinson et al., 1994; Liem et al., 1995, 1997; Arkell and Beddington, 1997; Ikeya et al., 1997; Lee et al., 1998;). Thus Embryo collection, histology and RNA in situ analysis the cortical hem is a candidate source of information regulating The Wnt-3a mouse line was maintained on an outbred Swiss Webster the induction and/or patterning of hippocampal development at background and genotyping was performed as described (Takada et the caudomedial margin of the continuous cerebral cortical al., 1994; Yoshikawa et al., 1997). Embryos from heterozygous neuroepithelium. intercrosses were dissected into PBS and fixed in either 4% Wnt-3a expression marks the cortical hem from 9.75 dpc paraformaldehyde (for RNA in situ analysis and TUNEL) or in (Roelink and Nusse, 1991; Parr et al., 1993; Grove et al., 1998) Bouin’s fixative (for histological analysis and bromodeoxyuridine (BrdU) detection). For analysis of tissue sections, embryos were either and is the only Wnt gene expressed exclusively in the cortical sectioned at 5-7 µm on a conventional microtome or 40 µm on a hem at this time, suggesting a role for Wnt-3a signaling in the freezing microtome. Sections for general histology were stained induction and/or patterning of the hippocampus. In Wnt-3a with haematoxylin and eosin. All analyses were performed using mutants, medial hippocampal fields are absent and lateral previously published protocols: whole-mount RNA in situ hippocampal fields are severely reduced. We show that Wnt- hybridization according to Parr et al. (1993) with modifications described in Knecht et al. (1995), section in situ hybridization with 35S-labeled probes according to Wilkinson et al. (1987), section in situ hybridization with digoxigenin (DIG)-labeled probes was performed according to Tole et al. (1997), and TUNEL analysis according to Gavrieli et al. (1992). BrdU detection and cell counting Pregnant females were injected intraperitoneally with 50 µg BrdU/g body weight and killed 30 minutes later. The uterine horns were immediately removed into ice-cold PBS. Embryos were dissected and processed as described above (note that exclusively 5 µm Fig. 1. Expression of Wnt genes during early cerebral cortical development. (A-L) Whole-mount in situ hybridizations using digoxigenin (DIG)-labeled probes. (M-R) In situ hybridizations to tissue sections using 35S-labeled probes. At 8.5 dpc (A-C), prior to cephalic neural tube closure, Wnt-7b and Wnt-8b are expressed in similar domains along the dorsocaudal edge of the telencephalon (B,C) with the expression of Wnt-7b extending further rostrally than Wnt-8b (black arrowheads mark the telencephalon/diencephalon boundary). By 9.5 dpc (D-I), after cephalic neural tube closure, the domain of Wnt-8b expression (E,H) comes to lie at the caudomedial edge of the dorsal telencephalon. The expression of Wnt-7b (F,I) is broader than Wnt-8b, and includes much of the dorsal telencephalon. At both 8.5 dpc (A) and 9.5 dpc (D,G), Wnt-3a is expressed in the dorsal CNS with an anterior limit at the prosomere 2/ prosomere 3 (p2/p3) boundary in the anterior diencephalon. Wnt-3a expression initiates in the dorsal telencephalon at 9.75 dpc and at 10.5 dpc (J-L) Wnt-3a (J) and Wnt-8b (K) are expressed in nested domains at the caudomedial edge of the dorsal telencephalon. Wnt-8b expression extends further rostrocaudally and laterally than the domain of Wnt- 3a expression, which is limited to the presumptive cortical hem. (M- R) At 12.5 dpc, six Wnt genes are expressed in the dorsal cerebral cortex. Wnt-2b, Wnt-3a, Wnt-5a and Wnt-7b are expressed adjacent to the choroid plexus (CP) in the cortical hem (white arrowheads in M-P). Wnt-8b is expressed in a much broader domain along the medial wall of the telencephalic vesicle. A second site of Wnt-8b expression is the eminentia thalami, ventral to the CP. In all cases, Wnt gene expression is extremely low or undetectable in the CP. Wnt-7a is expressed broadly in the cortical neuroepithelium, but is excluded from the cortical hem. Between 10.5 dpc and 12.5 dpc Wnt- 7b expression in the cortical neuroepithelium turns off and a second phase of Wnt-7b expression is initiated in the cortical mantle layer (P). Abbreviations: CP, choroid plexus. Wnt signaling in hippocampal development 459 Fig. 2. Histological analysis of cerebral cortical development in 18.5 dpc Wnt-3a mutants.
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