Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration

Spinal cord injury (SCI) results in severe disruption of communication between the brain and body, causing motor, sensory, and autonomic dysfunctions. While SCI in mammals leads to permanent impairment due to limited regenerative capacity, certain non-mammalian species, such as Xenopus laevis larval...

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Main Authors: Paula G. Slater, Miguel E. Domínguez-Romero, Guillermo Campos, Vania Aravena, Javier Cavieres-Lepe, Verónica Eisner
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Cell and Developmental Biology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2025.1529093/full
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author Paula G. Slater
Paula G. Slater
Miguel E. Domínguez-Romero
Guillermo Campos
Guillermo Campos
Vania Aravena
Vania Aravena
Javier Cavieres-Lepe
Verónica Eisner
author_facet Paula G. Slater
Paula G. Slater
Miguel E. Domínguez-Romero
Guillermo Campos
Guillermo Campos
Vania Aravena
Vania Aravena
Javier Cavieres-Lepe
Verónica Eisner
author_sort Paula G. Slater
collection DOAJ
description Spinal cord injury (SCI) results in severe disruption of communication between the brain and body, causing motor, sensory, and autonomic dysfunctions. While SCI in mammals leads to permanent impairment due to limited regenerative capacity, certain non-mammalian species, such as Xenopus laevis larval stages, exhibit remarkable regenerative abilities. During Xenopus laevis spinal cord regeneration, neural stem precursor cells (NSPCs) surrounding the central canal rapidly proliferate in response to SCI, compensating for cellular loss, restoring canal continuity, and generating new neurons to reestablish lost connections. It has been described that mitochondria and cellular metabolism play essential roles in stem cell proliferation, self-renewal, and differentiation. However, the mitochondrial and cellular metabolic response during spinal cord regeneration remains unexplored. This study uses electron and confocal microscopy to investigate the NSPCs mitochondrial response in Xenopus laevis following SCI. We observed that mitochondria exhibit a rapid and transient response after SCI, characterized by a disruption of the mitochondrial localization, a decrease in mitochondrial number per cell section, and an increase in mitochondrial area and circularity. Furthermore, mitochondria adopted a swollen phenotype, which did not impair mitochondrial function or cellular energy balance. This morphological shift was accompanied by a transient decrease in the mitochondrial membrane potential and a metabolic switch favoring glycolysis. Therefore, these findings demonstrate that a transient metabolic shift toward glycolysis occurs during spinal cord regeneration.
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spelling doaj-art-83a53f605b184b93bbd638833800227d2025-01-29T06:46:14ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-01-011310.3389/fcell.2025.15290931529093Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regenerationPaula G. Slater0Paula G. Slater1Miguel E. Domínguez-Romero2Guillermo Campos3Guillermo Campos4Vania Aravena5Vania Aravena6Javier Cavieres-Lepe7Verónica Eisner8Laboratory of Neuro-Regeneration and Metabolism, Fundación Ciencia & Vida, Huechuraba, Santiago, ChileDepartamento de Ciencias Biológicas y Químicas, Facultad de Medicina y Ciencias, Universidad San Sebastián, Santiago, ChileFacultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileDepartamento de Ciencias Biológicas y Químicas, Facultad de Medicina y Ciencias, Universidad San Sebastián, Santiago, ChileFacultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileDepartamento de Ciencias Biológicas y Químicas, Facultad de Medicina y Ciencias, Universidad San Sebastián, Santiago, ChileFacultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileFacultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileFacultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, ChileSpinal cord injury (SCI) results in severe disruption of communication between the brain and body, causing motor, sensory, and autonomic dysfunctions. While SCI in mammals leads to permanent impairment due to limited regenerative capacity, certain non-mammalian species, such as Xenopus laevis larval stages, exhibit remarkable regenerative abilities. During Xenopus laevis spinal cord regeneration, neural stem precursor cells (NSPCs) surrounding the central canal rapidly proliferate in response to SCI, compensating for cellular loss, restoring canal continuity, and generating new neurons to reestablish lost connections. It has been described that mitochondria and cellular metabolism play essential roles in stem cell proliferation, self-renewal, and differentiation. However, the mitochondrial and cellular metabolic response during spinal cord regeneration remains unexplored. This study uses electron and confocal microscopy to investigate the NSPCs mitochondrial response in Xenopus laevis following SCI. We observed that mitochondria exhibit a rapid and transient response after SCI, characterized by a disruption of the mitochondrial localization, a decrease in mitochondrial number per cell section, and an increase in mitochondrial area and circularity. Furthermore, mitochondria adopted a swollen phenotype, which did not impair mitochondrial function or cellular energy balance. This morphological shift was accompanied by a transient decrease in the mitochondrial membrane potential and a metabolic switch favoring glycolysis. Therefore, these findings demonstrate that a transient metabolic shift toward glycolysis occurs during spinal cord regeneration.https://www.frontiersin.org/articles/10.3389/fcell.2025.1529093/fullmitochondriaglycolitic shiftregenerationneural stem progenitor cells (NSPCs)metabolic regulationXenopus laevis
spellingShingle Paula G. Slater
Paula G. Slater
Miguel E. Domínguez-Romero
Guillermo Campos
Guillermo Campos
Vania Aravena
Vania Aravena
Javier Cavieres-Lepe
Verónica Eisner
Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
Frontiers in Cell and Developmental Biology
mitochondria
glycolitic shift
regeneration
neural stem progenitor cells (NSPCs)
metabolic regulation
Xenopus laevis
title Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
title_full Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
title_fullStr Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
title_full_unstemmed Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
title_short Xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
title_sort xenopus laevis neural stem progenitor cells exhibit a transient metabolic shift toward glycolysis during spinal cord regeneration
topic mitochondria
glycolitic shift
regeneration
neural stem progenitor cells (NSPCs)
metabolic regulation
Xenopus laevis
url https://www.frontiersin.org/articles/10.3389/fcell.2025.1529093/full
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