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RhoE deficiency alters postnatal subventricular zone development and the number of calbindin-expressing neurons in the olfactory bulb of mouse

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Abstract

The subventricular zone represents an important reservoir of progenitor cells in the adult brain. Cells from the subventricular zone migrate along the rostral migratory stream and reach the olfactory bulb, where they originate different types of interneurons. In this work, we have analyzed the role of the small GTPase RhoE/Rnd3 in subventricular zone cell development using mice-lacking RhoE expression. Our results show that RhoE null mice display a remarkable postnatal broadening of the subventricular zone and caudal rostral migratory stream. This broadening was caused by an increase in progenitor proliferation, observed in the second postnatal week but not before, and by an altered migration of the cells, which appeared in disorganized cell arrangements that impaired the appropriate contact between cells in the rostral migratory stream. In addition, the thickness of the granule cell layer in the olfactory bulb was reduced, although the density of granule cells did not differ between wild-type and RhoE null mice. Finally, the lack of RhoE expression affected the olfactory glomeruli inducing a severe reduction of calbindin-expressing interneurons in the periglomerular layer. This was already evident in the newborns and even more pronounced 15 days later when RhoE null mice displayed 89 % less cells than control mice. Our results indicate that RhoE has pleiotropic functions on subventricular cells because of its role in proliferation and tangential migration, affecting mainly the development of calbindin-expressing cells in the olfactory bulb.

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Acknowledgments

This work was supported by the Universidad CEU Cardenal Herrera (PRUCH and Santander-Copernicus), Consellería de Educación de la Generalitat Valenciana (GVPROMETEO-2009/011), Red RETICS (RD06/0010/0022) and Instituto de Salud Carlos III (PI10/01686, FEDER co-funding), DURSI (09 2009SGR1313) and MINECO SAF2010-16427 and SAF2013-49176-C2-1-R. The work was also supported by fellowships from the Generalitat Valenciana to BBL and from the Universidad CEU Cardenal Herrera to EM.

Conflict of interest

The authors declare that they have no conflict of interest.

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  1. Enric Mocholí

    Present address: Department of Pathology, Albert Einstein College of Medicine, Bronx, New York, NY, 10461, USA

Authors and Affiliations

  1. Departamento de Ciencias Biomédicas, Facultad de Ciencias de la Salud, Universidad CEU Cardenal Herrera, Moncada, Valencia, Spain

    Begoña Ballester-Lurbe, Enric Mocholí, Enric Poch & Ignacio Pérez-Roger

  2. Instituto de Ciencias Biomédicas, Universidad CEU Cardenal Herrera, Moncada, Valencia, Spain

    Begoña Ballester-Lurbe, Enric Poch, María García-Manzanares, Ignacio Pérez-Roger & José Terrado

  3. Laboratorio de Neurobiologia Comparada, Instituto Cavanilles de Biodiversidad y Biologia Evolutiva, Universidad de Valencia and CIBER de Enfermedades Neurodegenerativas (CIBERNED), Valencia, Spain

    Susana González-Granero & José M. García-Verdugo

  4. Departamento de Medicina y Cirugía Animal, Facultad de Veterinaria, Universidad CEU Cardenal Herrera, Avda Seminario s.n., 46113, Moncada, Valencia, Spain

    María García-Manzanares & José Terrado

  5. Systems Biology Program, Center for Genomic Regulation (CRG), Barcelona, Spain

    Mara Dierssen

  6. University Pompeu Fabra, Barcelona, Spain

    Mara Dierssen

  7. CIBER de Enfermedades Raras (CIBERER), Barcelona, Spain

    Mara Dierssen

  8. Laboratorio de Señalización de Proteínas Rho en Neuropatologías, Centro de Investigación Príncipe Felipe, Valencia, Spain

    Rosa M. Guasch

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  1. Begoña Ballester-Lurbe
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  2. Susana González-Granero
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Correspondence to José Terrado.

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Ballester-Lurbe, B., González-Granero, S., Mocholí, E. et al. RhoE deficiency alters postnatal subventricular zone development and the number of calbindin-expressing neurons in the olfactory bulb of mouse. Brain Struct Funct 220, 3113–3130 (2015). https://doi.org/10.1007/s00429-014-0846-1

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