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R-Cadherin Expression During Nucleus Formation in Chicken Forebrain Neuromeres

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R-Cadherin Expression During Nucleus Formation in Chicken Forebrain Neuromeres The Journal of Neuroscience, June 1995, 15(6): 4157-4172 R-Cadherin Expression during Nucleus Formation in Chicken Forebrain Neuromeres Susanne I. I. GBnzler and Christoph Redies Department of Biochemistry, Max Planck Institute for Developmental Biology, D-72072 Tiibingen, Germany The primordial neuroepithelium of the vertebrate forebrait dahl, 1924; Vaage, 1969; Kuhlenbeck, 1973; Puelleset al., 1987; consists of transverse and longitudinal morphogenetic Puelles and Rubenstein, 1993) that represent independentmor- compartments (“neuromeres”). During development, neu- phogenetic fields (Bergquist and KallCn, 1953a,b, 1954; Keyser, rons born in the ventricular zone of each neuromere mi- 1972; Puelleset al., 1987). The boundariesbetween neuromeres grate outward to the mantle zone. Here, neuroblasts grad- often coincide with primordial fiber tracts and restrict cell lin- ually accumulate and aggregate either into sheets (“lami- eage and migration. Generally, they coincide with the borders nae”) or into roundish structures (“nuclei”). As brain ar- of expressionof generegulatory proteins (reviewed in Lumsden, chitecture matures, sets of nuclei and laminae derived from 1990, 1993; Figdor and Stern, 1993; Krumlauf et al., 1993; Puel- several neuromeres become connected by fiber tracts to les and Rubenstein, 1993; Wilson et al., 1993). form functional circuits. We show by immunostaining and During development, a percentageof cells born in the prolif- in situ hybridization techniques that, in the E3-E5 chicken erative (ventricular) zone of each neuromerebecome postmitotic embryo, the cell adhesion molecule R-cadherin is ex- and migrate as neuroblastsoutward into the mantle zone (Sauer, pressed in several stripes and patches in the forebrain neu- 1935; Fujita, 1964; Morest, 1970) in two or three sustained roepithelium. This expression pattern reflects, at least in waves of migration (Bergquist, 1957). In the mantle zone, neu- part, the neuromeric organization of the forebrain. For ex- roblasts either accumulate in sheets(“laminae”), for example, ample, in both the ventral and dorsal thalamus, R-cadherin in the cerebellar and cerebral cortices, or they aggregate into expression has a sharp border at the respective caudal roundish structures(“nuclei”), for example, in the diencephalon neuromere boundary. Moreover, focusing on the mid-hy- (Palmgren, 1921; Rendahl, 1924; Kuhlenbeck, 1937; Rose, pothalamic region, we demonstrate that a subset of post- 1942; Keyser, 1972; Altman and Bayer, 1978). Particular nuclei mitotic neuroblasts in the ventricular zone express R-cad- and laminaederived from several neuromeresbecome selective- herin during their migration to the mantle zone, where they ly connected to each other by fiber tracts, sometimesover con- aggregate into particular nuclei. In the mantle zone, R-cad- siderabledistances, to form functional systemsand circuits. herin-expressing neuroblasts accumulate in parallel with While the molecular and developmental processesleading to neuroblasts expressing another cadherin, N-cadherin. The the development of laminated gray matter structures and fiber two types of cells segregate from each other to form ad- tracts have been under intense investigation (for reviews, see jacent nuclei. Some of the R- and the N-cadherin-positive Rakic, 1972; Hatten, 1990, 1993; Goodman and Shatz, 1993; nuclei form parts of particular functional circuits in the ma- Rakic et al., 1994), little is known about the mechanismsand ture brain. In conclusion, our results suggest that cadhe- moleculesregulating the formation of nuclei in the vertebrate rins play a role in the formation of brain nuclei and in the CNS. developmental transformation from neuromeric to func- We have recently demonstratedthat two cell-cell adhesion tional organization in the vertebrate forebrain. molecules,N- and R-cadherin (Hatta et al., 1988; Inuzuka et al., [Key words: pattern formation, segmentation, brain nu- 1991), are expressedby particular di- and mesencephalicnuclei cleus, calcium-dependent cell-cell adhesion, neuroblast and fiber tracts in the developing chicken brain (Redies et al., migration, neural differentiation] 1993). Cadherins are cell surface moleculesthat regulate mor- The primordial epithelium of the vertebrate neural tube is tran- phogenesisin a Caz+-dependentmanner in a variety of tissues siently partitioned into numeroustransverse and longitudinal do- (reviewed in Takeichi, 1988; Ranscht, 1991; Geiger and Ayalon, mains (“neuromeres”) (von Baer, 1828; Palmgren, 1921; Ren- 1992; Pouliot, 1992; Grunwald, 1993). Numerous in vitro ex- perimentsand in viva observationsshow that cadherinscan me- Received Dec. 8, 1994; accepted Jan. 24, 1995. diate the aggregation and sorting of cells (Nose and Takeichi, We are grateful to V. Kastner for expert technical assistance, to M. Takeichi, 1986; Hatta et al., 1987; Nagafuchi et al., 1987; Nose et al., E. de la Rosa, U. DrBger, and H. Fujisawa for their kind gifts of antibodies 1988; Miyatani et al., 1989; Inuzuka et al., 1991). Based on and cDNAs, to P G. Layer and B. Weiss for help with the AChE staining technique, to J. Berger for assistance with the scanning electron microscopy, these findings, we postulatedthat N- and R-cadherin might also to K. Arndt and T. Voizt for anatomical suggestions. to J. Jung for assistance YY regulate the formation and segregationof developing nuclei in with image processing, to V. Kastner and R. Bishop for impro&g the syntax, and to U. Schwarr for comments and generous support of this study. This work the embryonic brain (Redies et al., 1993). The present study was supported by the Max Planck Society. provides support for this hypothesis. By focusing on the ex- Correspondence should be addressed to Dr. C. Redies, Department of Bio- pressionof R-cadherin in the forebrain of the chicken embryo, chemistr;, Max Planck Institute for Developmental Biology, Postfach 2109, D- 7201 I Tiibingen, Germany. we demonstratethat, at early stagesof development (E3-E5), Copyright 0 1995 Society for Neuroscience 0270.6474/95/154157-16$05.00/O R-cadherin is expressedin several forebrain neuromeresin a 4158 GBnzler and Redies l R-Cadherin Expression during Brain Nucleus Formation Figure 1. Transverse sections through the hypothalamus of a chicken embryo of 5 d incubation (E5). A, Section stained with nuclear dye Hoechst 33258. The ventricular zone is characterized by a high density of cellular nuclei. In the mantle zone, cellular nuclei are spaced farther apart. B, Section immunostained for R-cadherin. C, Nomarski optical image of a section hybridized in situ with digoxigenin-labeled antisense RNA probe The Journal of Neuroscience, June 1995, 15(6) 4159 stripe-like or patchy fashion. Most of these regions later give were described previously (Redies et al., 1992, 1993). Briefly, heads rise to R-cadherin-positive nuclei and fiber tracts (Redies et al., from E2-E8 embryos were fixed in 4% formaldehyde dissolved in Hanks’ balanced salt solution supplemented with 1 mM Ca2+ and 1 mM 1993; Arndt and Redies, unpublished observations). In one par- Mg2+ (HBSS) for I-2 hr, incubated in a graded series of sucrose solu- ticular forebrain region, the mid-hypothalamic region (Kuenzel tions 112% (w/v). 15%. 18% sucrose in HBSSl for 30-60 min each. and van Tienhoven, 1982) we studied R-cadherin-expressing embedded in Tissue Tek (Miles), and frozen in liquid nitrogen. Cryostat neuroblasts during their migration and aggregation into partic- sections of 8 km thickness were mounted and dried on coated glass slides. After postfixation in 4% formaldehyde/HBSS and washing in ular nuclei in detail. Tris-buffered saline (pH 7.6) supplemented with 1 mM Ca’+ (TBS/CaZ+), This work has been published in preliminary form (Redies membranes were permeabilized in methanol at ~20°C and washed and Ganzler, 1994). again in TBWCa”. Unspecific binding sites for antibody were blocked by 5% skim milk in TBS/Ca2+ with 0.3% Triton X-100 (blocking so- Materials and Methods lution) for 20 min. The sections were incubated with the first antibodies appropriately diluted in blocking solution for 1 hr. After washing in Animals und antibodies. Fertilized Hisex chicken eggs (Gallus domes- TBS/Ca*+, secondary antibodies were applied to the sections for 30 min. ticus) were incubated at 37°C and 65% humidity in a forced-draft in- For double-label immunohistochemistry with the antibodies RCD-2 cubator. Embryos were staged according to Hamburger and Hamilton and R5, sections were first immunostained with the antibody RCD-2 as (1951). Embryos of 2-8 d incubation (E2-E8) were used. The stages described above but without methanol treatment. After postfixation in were E2 (HHl9), E3.5 (HH21), E4 (HH24), E4.5 (HH26), E5 (HH27), 2% formaldehyde/0.025% glutaraldehyde in PBS at 4°C for 5 min, sec- E6 (HH29), E7 (HH31), and E8 (HH34). tions were sequentially incubated with antibody R5, biotinylated sec- For immunohistochemistry, the following antibodies were used: mouse ondary antibodies, and FITC-labeled streptavidin. monoclonal antibody RCD-2 against chicken R-cadherin (Redies et al., 1992); mouse monoclonal antibody 29B8 against the 160 kDa subunit of Sections were counterstained in Hoechst 33258 (Sigma) for 5 min to chicken neurofilament (Hatta et al., 1987) (generous gift of H. Fujisawa); visualize nuclei, washed in TBS, and embedded in a solution of 90% mouse monoclonal antibody R5, which is directed against a vimentin- glycerol and 10% TBS/CaZ+ supplemented by phenylenediamine to pre- vent photobleaching. Fluorescence was visualized
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