Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain

Although scurvy, the severe form of vitamin C deficiency, has been almost eradicated, the prevalence of subclinical vitamin C deficiency is much higher than previously estimated and its impact on human health might not be fully understood. Vitamin C is an essential molecule, especially in the centra...

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Main Authors: Nery Jara, Manuel Cifuentes, Fernando Martínez, Iván González-Chavarría, Katterine Salazar, Lucas Ferrada, Francisco Nualart
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/11/10/2030
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author Nery Jara
Manuel Cifuentes
Fernando Martínez
Iván González-Chavarría
Katterine Salazar
Lucas Ferrada
Francisco Nualart
author_facet Nery Jara
Manuel Cifuentes
Fernando Martínez
Iván González-Chavarría
Katterine Salazar
Lucas Ferrada
Francisco Nualart
author_sort Nery Jara
collection DOAJ
description Although scurvy, the severe form of vitamin C deficiency, has been almost eradicated, the prevalence of subclinical vitamin C deficiency is much higher than previously estimated and its impact on human health might not be fully understood. Vitamin C is an essential molecule, especially in the central nervous system where it performs numerous, varied and critical functions, including modulation of neurogenesis and neuronal differentiation. Although it was originally considered to occur only in the embryonic brain, it is now widely accepted that neurogenesis also takes place in the adult brain. The subventricular zone (SVZ) is the neurogenic niche where the largest number of new neurons are born; however, the effect of vitamin C deficiency on neurogenesis in this key region of the adult brain is unknown. Therefore, through BrdU labeling, immunohistochemistry, confocal microscopy and transmission electron microscopy, we analyzed the proliferation and cellular composition of the SVZ and the lateral ventricle (LVE) of adult guinea pigs exposed to a vitamin-C-deficient diet for 14 and 21 days. We found that neuroblasts in the SVZ and LVE were progressively and significantly decreased as the days under vitamin C deficiency elapsed. The neuroblasts in the SVZ and LVE decreased by about 50% in animals with 21 days of deficiency; this was correlated with a reduction in BrdU positive cells in the SVZ and LVE. In addition, the reduction in neuroblasts was not restricted to a particular rostro–caudal area, but was observed throughout the LVE. We also found that vitamin C deficiency altered cellular morphology at the ultrastructural level, especially the cellular and nuclear morphology of ependymal cells of the LVE. Therefore, vitamin C is essential for the maintenance of the SVZ cell populations required for normal activity of the SVZ neurogenic niche in the adult guinea pig brain. Based on our results from the guinea pig brain, we postulate that vitamin C deficiency could also affect neurogenesis in the human brain.
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spelling doaj.art-e3042f2c75d74f58babc3d9959ea34e82023-11-23T22:39:38ZengMDPI AGAntioxidants2076-39212022-10-011110203010.3390/antiox11102030Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig BrainNery Jara0Manuel Cifuentes1Fernando Martínez2Iván González-Chavarría3Katterine Salazar4Lucas Ferrada5Francisco Nualart6Laboratorio de Neurobiología y Células Madre, NeuroCellT, Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción 4030000, ChileDepartment of Cell Biology, Genetics and Physiology, University of Malaga, 29010 Malaga, SpainLaboratorio de Neurobiología y Células Madre, NeuroCellT, Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción 4030000, ChileLaboratorio de Lipoproteínas y Cáncer, Departamento de Fisiopatología, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción 4030000, ChileLaboratorio de Neurobiología y Células Madre, NeuroCellT, Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción 4030000, ChileLaboratorio de Neurobiología y Células Madre, NeuroCellT, Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción 4030000, ChileLaboratorio de Neurobiología y Células Madre, NeuroCellT, Departamento de Biología Celular, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción 4030000, ChileAlthough scurvy, the severe form of vitamin C deficiency, has been almost eradicated, the prevalence of subclinical vitamin C deficiency is much higher than previously estimated and its impact on human health might not be fully understood. Vitamin C is an essential molecule, especially in the central nervous system where it performs numerous, varied and critical functions, including modulation of neurogenesis and neuronal differentiation. Although it was originally considered to occur only in the embryonic brain, it is now widely accepted that neurogenesis also takes place in the adult brain. The subventricular zone (SVZ) is the neurogenic niche where the largest number of new neurons are born; however, the effect of vitamin C deficiency on neurogenesis in this key region of the adult brain is unknown. Therefore, through BrdU labeling, immunohistochemistry, confocal microscopy and transmission electron microscopy, we analyzed the proliferation and cellular composition of the SVZ and the lateral ventricle (LVE) of adult guinea pigs exposed to a vitamin-C-deficient diet for 14 and 21 days. We found that neuroblasts in the SVZ and LVE were progressively and significantly decreased as the days under vitamin C deficiency elapsed. The neuroblasts in the SVZ and LVE decreased by about 50% in animals with 21 days of deficiency; this was correlated with a reduction in BrdU positive cells in the SVZ and LVE. In addition, the reduction in neuroblasts was not restricted to a particular rostro–caudal area, but was observed throughout the LVE. We also found that vitamin C deficiency altered cellular morphology at the ultrastructural level, especially the cellular and nuclear morphology of ependymal cells of the LVE. Therefore, vitamin C is essential for the maintenance of the SVZ cell populations required for normal activity of the SVZ neurogenic niche in the adult guinea pig brain. Based on our results from the guinea pig brain, we postulate that vitamin C deficiency could also affect neurogenesis in the human brain.https://www.mdpi.com/2076-3921/11/10/2030vitamin Cascorbic acidsubventricular zonelateral ventricle extensionsadult neurogenesis
spellingShingle Nery Jara
Manuel Cifuentes
Fernando Martínez
Iván González-Chavarría
Katterine Salazar
Lucas Ferrada
Francisco Nualart
Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain
Antioxidants
vitamin C
ascorbic acid
subventricular zone
lateral ventricle extensions
adult neurogenesis
title Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain
title_full Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain
title_fullStr Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain
title_full_unstemmed Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain
title_short Vitamin C Deficiency Reduces Neurogenesis and Proliferation in the SVZ and Lateral Ventricle Extensions of the Young Guinea Pig Brain
title_sort vitamin c deficiency reduces neurogenesis and proliferation in the svz and lateral ventricle extensions of the young guinea pig brain
topic vitamin C
ascorbic acid
subventricular zone
lateral ventricle extensions
adult neurogenesis
url https://www.mdpi.com/2076-3921/11/10/2030
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