Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population - PubMed (original) (raw)
Comparative Study
Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population
Silvia De Marchis et al. J Neurosci. 2007.
Abstract
The subventricular zone (SVZ) of the lateral ventricle develops from residual progenitors of the embryonic lateral ganglionic eminence (LGE) and maintains neurogenic activity throughout life. Precursors from LGE/SVZ migrate to the olfactory bulb (OB) where they differentiate into local interneurons, principally in the granule layer and glomerular layer (GL). By in situ dye labeling, we show that neonatal and adult SVZ progenitors differentially contribute to neurochemically distinct types of periglomerular interneurons in the GL. Namely, calbindin-positive periglomerular cells are preferentially generated during early life, whereas calretinin- and tyrosine hydroxylase-expressing neurons are mainly produced at later ages. Furthermore, homochronic/heterochronic transplantation demonstrates that progenitor cells isolated from the LGE or SVZ at different stages (embryonic day 15 and postnatal days 2 and 30) engraft into the SVZ of neonatal or adult mice, migrate to the OB, and differentiate into local interneurons, including granule and periglomerular cells as well as other types of interneurons. The total number of integrated cells and the relative proportion of granule or periglomerular neurons change, according to the donor age, whereas they are weakly influenced by the recipient age. Analysis of the neurochemical phenotypes acquired by transplanted cells in the GL shows that donor cells of different ages also differentiate according to their origin, regardless of the host age. This suggests that progenitor cells at different ontogenetic stages are intrinsically directed toward specific lineages. Neurogenic processes occurring during development and in adult OB are not equivalent and produce different types of periglomerular interneurons as a consequence of intrinsic properties of the SVZ progenitors.
Figures
Figure 1.
Neurochemical diversity of SVZ-derived cells (FG positive; green) generated at different ages. Double labeling shows as yellow in the overlay. A, Schematic drawings illustrating the FG injection site in newborn and adult mice. B, Quantification of FG-positive GL cells double-labeled for CB, CR, NC, or TH, among the total number of FG-positive cells counted in the GL at 30 d survival in newborn and adult injected animals. Error bars indicate SEM. *p < 0.05; **p < 0.01. C, Olfactory bulb GL stained in red for TH; the arrows indicate single-labeled cells, whereas the arrowhead shows a FG-positive neuron expressing TH. D–G, Confocal analysis of FG-positive cells in sections labeled for CB, CR, NC, and TH. Scale bars: C, 30 μm; (in G) D–G, 10 μm.
Figure 2.
Homochronic and heterochronic transplantation to the neonatal and adult SVZ. A, Schematic drawings illustrating the transplantation experiments: donors cells derived from the LGE/SVZ of embryonic, neonatal, and adult mice were transplanted into the SVZ of neonatal and adult recipients. Analysis of the engrafted cells integrated into the OB was performed at 1 and 2 months of survival. B, Integration rate of EGFP-positive cells into the GL in the different donor–recipient combinations. MANOVA analysis shows a significant effect of donor and host with interaction between them and no effect of survival time. Host effect was observed only in the case of embryo donors (p < 0.05). Donor effect was observed both in adult (embryo vs newborn, _p_ > 0.01; embryo vs adult, p > 0.001) and newborn (embryo vs adult, p > 0.01) recipients. Error bars indicate SEM. **p < 0.01; ***p < 0.001.
Figure 3.
Morphological characterization of EGFP-positive cells in the OB. A, EGFP-positive cells (green) derived from neonatal donors integrated in the OB of an adult mouse 1 month after transplant in a tissue section double stained for CB (red). EGFP-positive cells are predominantly localized in the GCL. The arrowhead shows an EGFP-positive cell integrated in the GL. B, D, EGFP-positive GCs derived from LGE embryonic progenitors, integrated in the OB GCL. E, EGFP-positive nongranule cells derived from LGE embryonic progenitors, integrated in the OB GCL. F, EGFP-positive cells derived from neonatal SVZ progenitors, integrated in the OB EPL, in a section double stained for TH. Scale bars: A, 100 μm; B, F, 50 μm; C–E, 20 μm.
Figure 4.
Neurochemical phenotype of EGFP-positive cells integrated in the OB GL in the different donor–recipient combinations. A–C, Quantification of percentage of EGFP-positive cells integrated in the GL double stained for CB (A), CR (B), and TH (C). Comparison of the results obtained transplanting embryonic and neonatal progenitors into newborn and adult mice. D–N, Representative images of EGFP-positive cells double stained for CB (D, G, L), CR (E, H, M), and TH (F, I, N). Error bars indicate SEM. **p < 0.01. Scale bars: (in D) D, E, G, H, L, M, 20 μm; (in F) F, I, N, 20 μm.
References
- Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron. 2004;41:683–686. - PubMed
- Bailey MS, Puche AC, Shipley MT. Development of the olfactory bulb: evidence for glia-neuron interactions in glomerular formation. J Comp Neurol. 1999;415:423–448. - PubMed
- Bayer SA. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res. 1983;50:329–340. - PubMed
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