Unraveling the 2,3-diketo-L-gulonic acid-dependent and -independent impacts of L-ascorbic acid on somatic cell reprogramming.

Asc DKG MET Metabolite TCA cycle

Journal

Cell & bioscience
ISSN: 2045-3701
Titre abrégé: Cell Biosci
Pays: England
ID NLM: 101561195

Informations de publication

Date de publication:
30 Nov 2023
Historique:
received: 13 08 2023
accepted: 31 10 2023
medline: 1 12 2023
pubmed: 1 12 2023
entrez: 1 12 2023
Statut: epublish

Résumé

L-ascorbic acid (Asc) plays a pivotal role in regulating various biological processes, including somatic cell reprogramming, through multiple pathways. However, it remains unclear whether Asc regulates reprogramming directly or functions through its metabolites. Asc exhibited dual capabilities in promoting reprogramming through both 2,3-diketo-L-gulonic acid (DKG), a key metabolite during Asc degradation, dependent and independent routes. On the one hand, Asc facilitated reprogramming by promoting cell proliferation and inducing the conversion from pre-induced pluripotent stem cells (pre-iPSCs) to iPSCs through DKG-independent pathways. Additionally, Asc triggered mesenchymal-epithelial transition (MET) and activated glycolysis via DKG-dependent mechanisms. Notably, DKG alone activated a non-canonical tricarboxylic acid cycle characterized by increased succinate, fumarate, and malate. Consequently, this shift redirected oxidative phosphorylation toward glycolysis and induced MET. Moreover, owing to its antioxidant capabilities, Asc directly inhibited glycolysis, thereby preventing positive feedback between glycolysis and epithelial-mesenchymal transition, ultimately resulting in a higher level of MET. These findings unveil the intricate functions of Asc in the context of reprogramming. This study sheds light on the DKG-dependent and -independent activities of Asc during reprogramming, offering novel insights that may extend the application of Asc to other biological processes.

Sections du résumé

BACKGROUND BACKGROUND
L-ascorbic acid (Asc) plays a pivotal role in regulating various biological processes, including somatic cell reprogramming, through multiple pathways. However, it remains unclear whether Asc regulates reprogramming directly or functions through its metabolites.
RESULTS RESULTS
Asc exhibited dual capabilities in promoting reprogramming through both 2,3-diketo-L-gulonic acid (DKG), a key metabolite during Asc degradation, dependent and independent routes. On the one hand, Asc facilitated reprogramming by promoting cell proliferation and inducing the conversion from pre-induced pluripotent stem cells (pre-iPSCs) to iPSCs through DKG-independent pathways. Additionally, Asc triggered mesenchymal-epithelial transition (MET) and activated glycolysis via DKG-dependent mechanisms. Notably, DKG alone activated a non-canonical tricarboxylic acid cycle characterized by increased succinate, fumarate, and malate. Consequently, this shift redirected oxidative phosphorylation toward glycolysis and induced MET. Moreover, owing to its antioxidant capabilities, Asc directly inhibited glycolysis, thereby preventing positive feedback between glycolysis and epithelial-mesenchymal transition, ultimately resulting in a higher level of MET.
CONCLUSION CONCLUSIONS
These findings unveil the intricate functions of Asc in the context of reprogramming. This study sheds light on the DKG-dependent and -independent activities of Asc during reprogramming, offering novel insights that may extend the application of Asc to other biological processes.

Identifiants

pubmed: 38037169
doi: 10.1186/s13578-023-01160-x
pii: 10.1186/s13578-023-01160-x
pmc: PMC10688016
doi:

Types de publication

Journal Article

Langues

eng

Pagination

218

Subventions

Organisme : National Key R&D Program of China
ID : 2021YFA1100401
Organisme : KNational Key R&D Program of China
ID : 2021YFA1101304
Organisme : National Natural Science Foundation of China
ID : U21A20203
Organisme : National Natural Science Foundation of China
ID : 32070717
Organisme : National Natural Science Foundation of China
ID : 32170741
Organisme : National Natural Science Foundation of China
ID : 32100472
Organisme : Science and Technology Program of Guangzhou
ID : 202102020044
Organisme : Science and Technology Program of Guangzhou
ID : 202102020183
Organisme : Science and Technology Program of Guangzhou
ID : 202201011654
Organisme : Science and Technology Planning Project of Guangdong Province
ID : 2020B1212060052

Informations de copyright

© 2023. The Author(s).

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Auteurs

Lining Liang (L)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
Centre for Regenerative Medicine and Health, Hong Kong Institute of Science & Innovation, Chinese Academy of Sciences, Hong Kong SAR, China.

Meiai He (M)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Yixin Zhang (Y)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Chenchen Wang (C)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.

Zhaohui Qin (Z)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Qian Li (Q)

Guangzhou Laboratory, Guangzhou, China.

Tingting Yang (T)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
Centre for Regenerative Medicine and Health, Hong Kong Institute of Science & Innovation, Chinese Academy of Sciences, Hong Kong SAR, China.

Fei Meng (F)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
Centre for Regenerative Medicine and Health, Hong Kong Institute of Science & Innovation, Chinese Academy of Sciences, Hong Kong SAR, China.

Yusheng Zhou (Y)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
Centre for Regenerative Medicine and Health, Hong Kong Institute of Science & Innovation, Chinese Academy of Sciences, Hong Kong SAR, China.

Haofei Ge (H)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
Joint School of Life Sciences, Guangzhou Medical University, Guangzhou, China.

Weining Song (W)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Shiyu Chen (S)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Linna Dong (L)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Qiwen Ren (Q)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.
University of Chinese Academy of Sciences, Beijing, China.

Changpeng Li (C)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.

Lin Guo (L)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.

Hao Sun (H)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China.

Wei Zhang (W)

Guangzhou Laboratory, Guangzhou, China.

Duanqing Pei (D)

Centre for Regenerative Medicine and Health, Hong Kong Institute of Science & Innovation, Chinese Academy of Sciences, Hong Kong SAR, China. peiduanqing@westlake.edu.cn.
Laboratory of Cell Fate Control, School of Life Sciences, Westlake University, Hangzhou, China. peiduanqing@westlake.edu.cn.

Hui Zheng (H)

Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, GIBH-CUHK Joint Research Laboratory on Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, #190 Kaiyuan Ave. Science City, Guangzhou, 510530, China. zheng_hui@gibh.ac.cn.
Centre for Regenerative Medicine and Health, Hong Kong Institute of Science & Innovation, Chinese Academy of Sciences, Hong Kong SAR, China. zheng_hui@gibh.ac.cn.
University of Chinese Academy of Sciences, Beijing, China. zheng_hui@gibh.ac.cn.
Joint School of Life Sciences, Guangzhou Medical University, Guangzhou, China. zheng_hui@gibh.ac.cn.

Classifications MeSH