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Clonal Architecture of the Mouse Hippocampus

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Clonal Architecture of the Mouse Hippocampus The Journal of Neuroscience, May 1, 2002, 22(9):3520–3530 Clonal Architecture of the Mouse Hippocampus Loren A. Martin,1 Seong-Seng Tan,2 and Dan Goldowitz1 1Department of Anatomy and Neurobiology, University of Tennessee Health Science Center, Memphis, Tennessee 38163, and 2Howard Florey Institute, University of Melbourne, Parkville VIC 3010, Australia Experimental mouse chimeras have proven useful in analyzing layer in a symmetrical manner. Clonally related populations of the cell lineages of various tissues. Here we use experimental GABAergic interneurons are dispersed throughout the hip- mouse chimeras to study cell lineage of the hippocampus. We pocampus and originate from progenitors that are separate examined clonal architecture and lineage relationships of the hip- from either pyramidal or granule cells. Granule and pyramidal pocampal pyramidal cells, dentate granule cells, and GABAergic cells, however, are closely linked in their lineages. Our quanti- interneurons. We quantitatively analyzed like-genotype cohorts of tative analyses yielded estimates of the size of the progenitor these neuronal populations in the hippocampus of the most pools that establish the pyramidal, granule, and GABAergic highly skewed chimeras to provide estimates of the size of the interneuronal populations as consisting of 7000, 400, and 40 progenitor pool that gives rise to these neuronal groups. We progenitors, respectively, for each side of the hippocampus. also compared the percentage chimerism across various brain Last, we found that the hippocampal pyramidal and granule structures to gain insights into the origins of the hippocampus cells share a lineage with cortical and diencephalic cells, point- relative to other neighboring regions of the brain. Our qualitative ing toward a common lineage that crosses the di-telencephalic analyses demonstrate that like-genotype cohorts of pyramidal boundaries. cells are aligned in radial arrays across the pyramidal cell layer, whereas like-genotype cohorts in the C-shaped dentate gyrus Key words: dentate gyrus; cell lineage; granule cell; pyramidal colonize either the outer shell or inner core of the granule cell cell; GABAergic interneuron; chimera At the junction where the dorsal telencephalon meets the dien- 1995, 1997; Morita et al., 1995; Pellegrini et al., 1996; Acampora et cephalon, the hippocampal rudiments form, eventually develop- al., 1997; Furuta et al., 1997; Porter et al., 1997; Suda et al., 1997; ing into the dentate gyrus and hippocampus proper (collectively Yoshida et al., 1997; Grove et al., 1998; Galceran et al., 1999, 2000; termed the hippocampus in this paper). The hippocampus has Grove and Tole, 1999; Theil et al., 1999; Zhao et al., 1999; Lee et been at the forefront of research in the neurosciences, with al., 2000; Liu et al., 2000; Tole et al., 2000a,b)]. This evolving numerous studies examining its development and how its simple molecular picture therefore suggests a unique set of genes defining structure subserves the complex functions of learning and mem- hippocampal development. ory. However, to our knowledge, the early origins of the hip- To elucidate the patterned development and lineal origins of pocampus have never been analyzed thoroughly. Cell lineage the hippocampus, and to complement the emerging molecular analysis is the principal means to explore the cellular dynamics organization, we used aggregation and blastocyst-injection chi- involved in the formation of a tissue. To date, lineage-based meras to retrospectively analyze like-genotype cohorts of the dissection of hippocampal development has been limited to one three major cell types in the adult mammalian hippocampus. We retroviral study showing that clonally related neurons can cross examined the underlying clonal architecture and lineage relation- cytoarchitectonic regions within the hippocampus proper (Grove ships of the pyramidal cells, granule cells, and GABAergic inter- et al., 1992). neurons of the hippocampus. We found that the hippocampus In recent years, molecular approaches to understanding mam- proper follows a radial clonal architecture, whereas the dentate malian forebrain development have begun to demonstrate dis- gyrus follows an outside-in neurogenetic gradient in its clonal tinct organizational patterns of gene expression and function organization. Furthermore, the two sides of the hippocampus throughout embryogenesis (for review, see Rubenstein et al., arise from distinct progenitor populations. We also demonstrate 1998). For the hippocampus, this has led to a growing number of that the GABAergic interneuronal population arises separately genes linked to hippocampal development [Gli3, BETA2/NeuroD, Tlx, and members of the gene families: BMP, LIM, EMX, OTX, from the principal hippocampal neurons, and their progenitors WNT, and LEF1/TCF (Boncinelli et al., 1993; Monaghan et al., contribute to the dentate gyrus and hippocampus proper alike. Quantitative analyses of like-genotype cells in the hippocampus provide upper estimates for the size of the progenitor pools of Received July 31, 2001; revised Jan. 18, 2002; accepted Jan. 28, 2002. each of the three major hippocampal cell types. Finally, observa- This research was supported by a University of Tennessee Health Science Center, tions of like-genotype cells across brain regions in several chime- Center for Neuroscience Predoctoral Fellowship (L.A.M.) and by a grant from Cure Autism Now. We thank Dr. Dave Airey for statistical advice, Richard Cushing for ras indicate that the hippocampus shares lineage with telence- technical support, and the anonymous reviewers for key comments and suggestions. phalic and diencephalic structures. These new insights into the Correspondence should be addressed to Dan Goldowitz, Department of Anatomy clonal architecture of the hippocampus form a developmental and Neurobiology, University of Tennessee Health Science Center, 855 Monroe Avenue, Memphis, TN 38163. E-mail: [email protected]. foundation for the emerging molecular events that are critical for Copyright © 2002 Society for Neuroscience 0270-6474/02/223520-11$15.00/0 understanding hippocampal development and function. Martin et al. • Cell Lineage Analysis of the Hippocampus J. Neurosci., May 1, 2002, 22(9):3520–3530 3521 MATERIALS AND METHODS Direct counts of all ␤-gal-positive neurons were made for the pyrami- dal, granule, and GABAergic neurons in serial sections. To determine Aggregation chimeras. Aggregation chimeras were made by a standard the percentage of labeled cells for the pyramidal and granule cell pop- method of fusing two four- to eight-cell embryos (Goldowitz et al., 1992). ulations, we calculated the total pyramidal and granule cell number for The original stocks of mice were obtained from the Jackson Laboratory each section by multiplying the area of each individual layer by its (Bar Harbor, ME) and maintained in our colony at the University of packing density (ϳ4 cells/1000 ␮m 2 for the pyramidal cell layer and 16 Tennessee Animal Care Facility. We used the B6;129S-Gtrosa26 cells/1000 ␮m 2 for the granule cell layer). Numerical estimates of hip- (ROSA26) transgenic mouse line to mark cells in chimeras, because this pocampal interneurons were obtained by direct counts of all GABAergic line has a constitutive expression of ␤-galactosidase (␤-gal) in CNS cells across a sampling of the hippocampus. The total number of hip- neurons that permits the analysis of cell lineage (Friedrich and Soriano, pocampal interneurons was estimated by multiplying the average number 1991; Goldowitz et al., 2000). The other component of chimeras came of GABAergic perikarya per section by the total number of sections from either hybrid 129/B6 or ICR mice. The use of two genetically through each hippocampus (ϳ200). This total number was then corrected distinct embryos in combination with the ROSA26 embryo to produce for perikarya that may have been counted twice using the Abercrombie chimeras provided added validity to our findings derived from the chi- correction factor (Abercrombie, 1946). meric combinations. Embryos were harvested from the oviducts of the Analysis of lineage relationships. To identify lineage relationships that donor mothers2dafter the appearance of a vaginal plug. The embryos may exist between the cell populations of the hippocampus and those of were then subjected to a light pronase treatment to remove the zonae other brain regions, the percentages of X-gal-labeled cells for the pyra- pellucidae and aggregated and cultured overnight (37°C, 5% CO )in 2 midal, granule, and GABAergic cells were compared with each other and drops of medium (Mullen and Whitten, 1971) covered with paraffin oil. to rough visual estimates of the percentage chimerism of the following The following afternoon, successfully fused embryos were transplanted brain regions: motor cortex; somatosensory cortex; piriform cortex; au- into the uterine horns of pseudopregnant ICR females. Avertin was ditory cortex; visual cortex; entorhinal, ectorhinal, and perirhinal corti- administered intraperitoneally as the general anesthetic for the ICR host ces; basal ganglia; globus pallidus; substantia nigra; subthalamic nucleus; females before transplantation. All surgical procedures and animal care amygdala; reticular nucleus; zona incerta; nucleus reunions; medial dor- were in accordance with National Institutes of Health guidelines for sal thalamus; lateral dorsal thalamus; ventral thalamus; habenula; lateral animal welfare and The Society for Neuroscience policy on the use of
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