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Radial and Tangential Dispersion Patterns in the Mouse Retina Are Cell Proc. Natl. Acad. Sci. USA Vol. 92, pp. 2494-2498, March 1995 Neurobiology Radial and tangential dispersion patterns in the mouse retina are cell-class specific (cell migration/cell lineage/retinal development/transgenic mice/X chromosome inactivation) B. E. REESE*, A. R. HARvEyt, AND S.-S. TANt§ *Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara, CA 93106; tDepartment of Anatomy and Human Biology, University of Western Australia, Nedlands, WA 6009 Australia; and tDepartment of Anatomy and Cell Biology, University of Melbourne, Parkville, Victoria 3052, Australia Communicated by Pasko Rakic, Yale University School ofMedicine, New Haven, CT, December 16, 1994 ABSTRACT The retina is derived from a pseudostratified retinal cells remain clonally segregated, they should appear as germinal zone in which the relative position of a progenitor distinct groups of blue versus white cells. We have used this cell is believed to determine the position ofthe progeny aligned approach to address the issue of whether radially aligned cells in the radial axis. Such a developmental mechanism would in the mature retina reflect such a clonal derivation. ensure that radial arrays of cells which comprise functional units in the mature central nervous system are also clonally MATERIALS AND METHODS related. The present study has tested this hypothesis by using Retinas from adult transgenic mice, derived from founder line X chromosome-inactivation transgenic mosaic mice. We re- H253, which carries a lacZ transgene under control of the port that the retina shows a conspicuous distinction for hydroxymethylglutaryl-CoA reductase gene promoter inserted clonally related neuroblasts of different laminar and func- into the X chromosome (9), were fixed with 4% paraformalde- tional fates: the rod photoreceptor, Muller, and bipolar cells hyde plus 0.2% glutaraldehyde for 15-30 min, rinsed for at least are aligned in the radial axis, whereas the cone photoreceptor, 2 hr, and then histochemically processed either as whole retinas horizontal, amacrine, and ganglion cells are tangentially or after frozen sectioning at 100 ,um. Details of the strain of displaced with respect to them. These results indicate that the mouse, the transgene insertion in the X chromosome, the tar- dispersion of cell classes across the retinal surface is differ- getted expression ofthe transgene product to the nucleus, and the entially constrained. Some classes of retinal neuroblast ex- histochemical reaction to reveal P-galactosidase are provided hibit a significant tangential, as well as radial, component in elsewhere (10). Some whole reacted retinas were then dehy- their dispersion from the germinal zone, whereas others drated and embedded flat in resin, and 5-gm-thick sections were disperse only in the radial dimension. Consequently, the cut in either the radial or the tangential planes, mounted on majority of radial columns within the mature retina must be gelatinized slides, and stained with either nuclear fast red or derived from multiple progenitors. Because the cone photo- neutral red. Others were prepared intact as whole mounts, or receptor, horizontal, amacrine, and ganglion cells establish were immunostained with mouse monoclonal antibodies directed nonrandom matrices in their cellular distributions within the against glial fibrillary acidic protein (GFAP) or calbindin, orwere respective retinal layers, tangential dispersion may be the retrogradely labeled with horseradish peroxidase (HRP) follow- means by which these matrices are constructed. ing injections into the lateral geniculate nucleus. Details of those procedures are provided elsewhere (12). Nerve cells of the retina are derived from a germinal neuro- epithelium in which individual progenitor cells can give nse to RESULTS all classes of retinal neuron, as well as to Muller glial cells Sections of retina cut perpendicular to the retinal surface reveal (1-5). A variety of lineage-tracing studies report that such radially oriented blue and white columns of varying thickness clones of cells are aligned in the radial axis, but it is not clear (Fig. 1 a and b). Sectioned columns can be as thin as a single cell to what extent cells from adjacent clones can intermingle. One diameter, while others maybe several cells thick. The columns are study using chimeric mice reports that the descendants of defined by the photoreceptor cells in the outer nuclear layer and retinal progenitors are aligned in the radial axis (6), suggesting the smaller cells of the inner nuclear layer, the Muller and bipolar that the mature retina is composed of functional columnar cells. Essentially no mixing occurs between blue and white cells units of cells that are clonally derived (7, 8). According to this ofthese types (but see below); furthermore, those oflike color are view, clonal boundaries are rarely transgressed. The present in register between the two nuclear layers. study has addressed this question of clonal restriction by using Some neurons of the retina do not respect this columnar X chromosome-inactivation transgenic mosaics. organization (e.g., four cells indicated in Fig. la). When We have examined sections and whole mounts of retinas examined at higher magnification, most of these cells are from mature transgenic mice in which the lacZ gene, encoding larger neurons of the retina, the ganglion cells, the amacrine the enzyme ,B-galactosidase, had been integrated on one X cells, and the horizontal cells (e.g., Fig. lb). For example, chromosome (9, 10). Because of X inactivation in hemizygous regions of the ganglion cell layer overlying a blue column may females, the transgene is randomly switched off in -50% of all fail to contain any blue cells. Likewise, blue cells in the proliferating cells of the optic vesicle by embryonic day 9.5 ganglion cell layer are occasionally found overlying white (10), prior to the onset of retinal neurogenesis (11), conse- columns (arrows in Fig. 1 a and b). Although slightly oblique quently generating mosaicism within the population of pre- sections may create the appearance of blue cells in white cursors from which all mature retinal neurons will descend. columns (the section passing sequentially through a blue and Subsequent histochemistry can reveal the nuclei of all trans- then a white radial column), or radial sections may just graze gene-active cells as staining blue, and to the extent that mature a single blue cell on the edge of a blue column, an examination The publication costs of this article were defrayed in part by page charge Abbreviations: GFAP, glial fibrillary acidic protein; HRP, horse- payment. This article must therefore be hereby marked "advertisement" in radish peroxidase. accordance with 18 U.S.C. §1734 solely to indicate this fact. §To whom reprint requests should be addressed. 2494 Downloaded by guest on September 28, 2021 Neurobiology: Reese et aL Proc. Natl. Acad ScL USA 92 (1995) 2495 of such retinas in whole-mount preparations discounts this entire retina (Fig. lc). Some of the blue columns are small and explanation for the many ganglion, amacrine, and horizontal round, likely to correspond to single clones of cells, whereas cells that are clearly out of register with like-color columns. others are large and irregular in shape, undoubtedly polyclonal Retinal whole mounts prepared from such transgenic mice in nature, given the likelihood of neighboring clones being of reveal the distribution of blue and white territories across the the same color. At higher power, the whole-mount preparation b a i. a- A s. gc6r. FIG. 1. Distribution of B3-galactosidase-positive cells in retinas of transgenic mice. (a and b) Sections of retina reveal radial blue and white columns of variable widths. Both 100-Mum-thick sections (a) as well as thinner, 5-,um counterstained sections (b) reveal the columns to be defined by the segregation of blue and white photoreceptors in the outer nuclear layer (onl) and by the segregation of blue and white bipolar and Muller cells of the inner nuclear layer (inl). These cells of like color are aligned in the radial axis. By contrast, the blue cells in the retinal ganglion cell layer (gcl; arrows), as well as the larger blue cells in the inner nuclear layer-the amacrine (e.g., double arrowheads) and horizontal cells (e.g., arrowheads)-are occasionally out of register with the columns of blue cells that course through the outer and inner nuclear layers. (c) Whole mounts of the retina reveal the entire distribution of blue and white columns, viewed end-on. Columns vary not only in size, but also in shape. The smallest columns are likely to be individual clones of retinal cells. (d-g) At higher magnification, the cells of the individual layers can be focused sequentially through such whole-mounted retinas, starting in the outer nuclear layer (d), to the outer margin of the inner nuclear layer (e), to the inner margin of the inner nuclear layer (f), to the ganglion cell layer (g). The small (bipolar and Muller) cells of the inner nuclear layer are grouped together in columns (vertical white arrows in e andf) that are in register with the columns of cells of the outer nuclear layer (vertical white arrows in d). Blue neurons in the ganglion cell layer (e.g., arrows in g) as well as blue amacrine and horizontal cells of the inner nuclear layer (e.g., double arrowheads in f and arrowheads in e, respectively) are out of register with the other blue cells of the inner nuclear layer as well as with those of the outer nuclear layer (d). (h) When such whole mounts are focused at the outer margin ofthe outer nuclear layer, occasional blue cells are observed in white columns, presumed to be cones (diagonal arrows). (Bar in g = 125 Am for a, 30 ,um for b, 500 Lm for c, and 12.5 ,um for d-h.) Downloaded by guest on September 28, 2021 2496 Neurobiology: Reese et al.
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