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Gbx-2, and Writ-3 in the Embryonic Day 12.5 Mouse Forebrain Defines Potential Transverse and Longitudinal Segmental Boundaries

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Gbx-2, and Writ-3 in the Embryonic Day 12.5 Mouse Forebrain Defines Potential Transverse and Longitudinal Segmental Boundaries The Journal of Neuroscience, July 1993, 13(7): 31553172 Spatially Restricted Expression of D/x- 1, D/x-Z (Tes- I), Gbx-2, and Writ-3 in the Embryonic Day 12.5 Mouse Forebrain Defines Potential Transverse and Longitudinal Segmental Boundaries Alessandro Bulfone,1~2~4~5Luis Puelles,6 Matthew H. Porteus, 1*2*4*5 Michael A. Frohman,’ Gail R. Martin,3*5 and John L. R. Rubensteini,2*4.5 ‘Neurogenetics Laboratory, Departments of *Psychiatry and 3Anatomy, and Programs in 4Neuroscience and 5Developmental Biology, University of California, San Francisco, California 94143-0984, 6Department of Anatomy, Faculty of Medicine, University of Murcia, Murcia, Spain 30100, and ‘Department of Pharmacology, SUNY, Stonybrook, New York 11794-8651 The expression patterns of four genes that are potential cells differentiate and give rise to different neural structures. For regulators of development were examined in the CNS of the instance, along the A-P axis the neural tube subdivides to form embryonic day 12.5 mouse embryo. Three of the genes, Dlx- the spinal cord, the myelencephalon, the metencephalon, the 1, D/x-Z (Tes- I), and Gbx-2, encode homeodomain-contain- mesencephalon, the diencephalon, and the telencephalon. With- ing proteins, and one gene, Wnf-3, encodes a putative se- in each of these regions, subsequent differentiation of different creted differentiation factor. These genes are expressed in neuroepithelial domains results in neural structures of distinct spatially restricted transverse and longitudinal domains in histologies. For example, as viewed from a cross section of the the embryonic neural tube, and are also differentially ex- embryonic telencephalon, the neocortex derives from the dor- pressed within the wall of the neural tube. Dlx-1 and Dlx-2 solateral wall of the cerebral vesicle, the basal ganglia from the are expressed in two separate regions of the forebrain in an ventral wall, and the hippocampus and chorioid plexus from identical pattern. The Gbx-2 gene is expressed in four do- the medial wall. mains, two of which share sharp boundaries with the do- The forebrain has remained relatively difficult to study be- mains of the D/x genes. One boundary is in the basal tel- cause of its complex anatomy and because of the paucity of encephalon between deep and superficial strata of the medial information regarding the mechanisms of its development. ganglionic eminence; the other boundary is in the dienceph- However, several studies over the last century have attempted alon at the zona limitans intrathalamica. The Wnf-3 gene is to describe the early stages of forebrain development in terms expressed in a dorsal longitudinal zone extending from the of a neuromeric theory (von Kupffer, 1906; Rendahl, 1924; von hindbrain into the diencephalon, where its expression ter- Haller, 1929; Bergquist, 1932; Bergquist and Kallen, 1954, 1955; minates at the zona limitans intrathalamica. Reciprocal pat- Coggeshall, 1964; Kallen, 1965; Vaage, 1969; Keyser, 1972; terns of expression are found within the dorsal thalamus for Gribnau and Geijsberts, 1985; Altman and Bayer, 1986, 1988; the Gbx-2 and Wnt-3 genes. These findings are consistent Puelles et al., 1987, 199 1, 1992). Neuromeric theory postulates with neuromeric theories of forebrain development, and the existence of genetic fate determinants that subdivide the based upon them we suggest a model for forebrain seg- neural tube wall into transverse and longitudinal domains that mentation develop along distinct pathways. The initial formulations of the [Key words: forebrain, diencephalon, telencephalon, de- theory were based on studies that principally used morpholog- velopment, segmentation, homeobox, Wnt, Dlx, Gbx] ical data to determine the intersegmental and intrasegmental relationships between regions of the diencephalon and the tel- The embryonic nervous tube is initially composed of an undif- encephalon. Confirmation of the theory will require molecular ferentiated pseudostratified neuroepithelium along its entire evidence from the discovery of the genetic determinants of re- length. Depending upon the position along the anterior-poste- gional fate. rior (A-P), dorsal-ventral (D-V), and medial-lateral (M-L) axes, Hints regarding the genetic mechanisms that control the spec- ification of different regions of the vertebrate body plan have Received Jan. 12, 1993; revised Jan. 30, 1993; accepted Feb. 8, 1993. come from the study of invertebrates. In Drosophila melano- We thank Teresa McGuinness and Danwen Xu for providing the Dlx- 1 cDNA gaster the longitudinal axis of the embryo is subdivided into a clones, Roe1 Nusse for generously providing us with the Writ-S clone, Pat G’Farrell series of segments by the sequential expression of the gap, pair and Thomas Kombere for heloful discussions. and Melanie Bedolli for technical advice. This work was supported by grants to J.L.R.R. from the Pfizer Scholars, rule, and segment polarity genes (Levine and Harding, 1989). John Merck Scholars, NARSAD Young Investigator and Basil O’Connor-March The final identity of segments is defined by the expression of of Dimes programs, and the NIMH (ROI MH49428-01); the Italian Association the homeotic genes (McGinnis and Krumlauf, 1992). Most of for Cancer Research (AIRC) to A.B.; and the Merck Corporation to M.H.P., who is a member of the MST program at Stanford. the identified products of these genes are transcriptional regu- Corresnondence should be addressed to John L. R. Rubenstein. Neuroaenetics lators containing the homeodomain motif (Gehring, 1987) al- Laboratory, Department of Psychiatry and Programs in Neuroscience r&d De- velopmental Biology, 401 Pamassus Avenue, USCF, San Francisco, CA 94143- though positional information is also mediated by secreted pro- 0984. teins, such as the product of the wingless (wg) gene (Baker, 1987; Copyright 0 1993 Society for Neuroscience 0270-6474/93/133155-18$05.00/O Rijsewijk et al., 1987). For instance, specification of the identity 3156 Bulfone et al. * Segmental Organization of the Embryonic Mouse Forebrain of the anterior and posterior half of each segment requires the domains within the forebrain. The patterns of expression are interaction of wg with several other genes, including the en- consistent with neuromeric models of the forebrain, thus sup- gruifed (en) homeobox gene (DiNardo et al., 1988; Heemskerk porting the concept that, like the hindbrain, the embryonic fore- et al., 199 1). brain is segmented. Regional differentiation of the vertebrate nervous system ap- pears to employ some of the same mechanisms that mediate Materials and Methods Drosophila development. Homologs of many Drosophila de- Mouse embryos. Timed-pregnant BALBX mice were obtained from velopmental control genes have been identified in vertebrates. Simonsen Laboratories, Gilrov. CA. The dav on which a conulatorv For instance, the Hox genes, homologs of genes within the An- plug was found was considered E0.5. The mothers were killed by-cervical dislocation; the embryos were isolated and immediately frozen in tennapedia-Bithorax complex (Acampora et al., 1989; Duboule 2-methylbutane cooled to the temperature of dry ice. The embryos were and Doll& 1989; Graham et al., 1989; Kappen et al., 1989), are stored at -80°C until they were used for cryostat sectioning. expressed in overlapping, but nonidentical, domains along the cDNA probes. Two clones of the D/x-l gene (Price et al., 199 1) were A-P axis in vertebrate embryos (for a review of Hox gene struc- independently isolated. A 2.8 kilobase (kb) clone was purified from an ture and expression, see McGinnis and Krumlauf, 1992). El 5 mouse telencephalon cDNA library (Porteus et al., 1992) by screen- ing the library with a probe containing the Drosophila E86’hdmeobox The Hox genes appear to have an important role in controlling (sift of W. McGinnis. Yale Universitv). The identitv of this clone was the development of the hindbrain. Within the hindbrain, the &firmed by DNA sequencing(A. B&one, D. Xu, &rd J. L. R. Ruben- anterior boundaries of expression of individual Hox genes are stein, unpublished observations). This cDNA is in the vector named found at the boundaries between structures called rhombomeres E61 (Rubenstein et al., 1990). The 2.8 kb clone was used to make a (Hunt et al., 1991) which are thought to represent neuronal digoxigenin probe used to label the sagittal sectionsshown in Figure 1. A 243 base pair (bp) Dlx-I clone was also obtained using PCR from segments (neuromeres). The evidence that differentiation of the the El5 cDNA library (W. McGuinness and J. L. R. Rubenstein, un- hindbrain is controlled by the Hox genes comes from studies published observations). The primers were designed based upon the of mutations that inactivate Hox-I.5 and Hox-1.6 (Chisaka and nucleotide sequence that Price et al. (199 1) submitted to GenBank. This Capecchi, 1991; L&kin et al., 199 1; Chisaka et al., 1992). Dis- fragment, which corresponds to the 243 bp immediately 3’ to the Dlx- I homeobox and overlaps with the 2.8 kb fragment, was subcloned into ruption of these genes results in abnormal differentiation of a a derivative of PBS KS- named PBS KDD- (Dan Denney, Stanford subset of the neural tube-derived cells from the anteriormost University). The 243 bp fragment has no significant homology to the region where these genes are expressed. In sum, available in- Dlx-2 gene,and was used to make a Z5S-labeled probe, which was hy- formation suggeststhat the Hoxgenes have a role in determining bridized to the transverse sections shown in Figure 2, as well as to the regional identities of cells along the A-P axis. This is anal- sagittal and coronal sections (data not shown). This fragment was also used to make digoxigenin probes used to label coronal sections (data ogous to the role that Horn genes play in defining the segmental not shown). Identical results were obtained with both the 2.8 and 0.243 identities in Drosophila (McGinnis and Krumlauf, 1992).
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