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Metabolomic Study of Hibernating Syrian Hamster Brains: In Search of Neuroprotective Agents

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Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Proteome Res. 2019, 18, 3, 1175-1190
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    Metabolomic Study of Hibernating Syrian Hamster Brains: In Search of Neuroprotective Agents
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    • Carolina Gonzalez-Riano
      Carolina Gonzalez-Riano
      CEMBIO (Centre for Metabolomics and Bioanalysis), Facultad de Farmacia, Universidad CEU San Pablo, Campus Monteprincipe, Boadilla del Monte, 28668 Madrid, Spain
      More by Carolina Gonzalez-Riano
      Orcidhttp://orcid.org/0000-0001-7026-8684
    • Gonzalo León-Espinosa
      Gonzalo León-Espinosa
      Laboratorio Cajal de Circuitos Corticales (CTB), Universidad Politécnica de Madrid, Campus Montegancedo, 28223 Pozuelo de Alarcón, Madrid, Spain
      Instituto Cajal (CSIC), Avenida Doctor Arce 37, 28002 Madrid, Spain
      Facultad de Farmacia, Universidad CEU San Pablo, Campus Monteprincipe, Boadilla del Monte, 28668 Madrid, Spain
      More by Gonzalo León-Espinosa
      Orcidhttp://orcid.org/0000-0002-9921-2614
    • Mamen Regalado-Reyes
      Mamen Regalado-Reyes
      Laboratorio Cajal de Circuitos Corticales (CTB), Universidad Politécnica de Madrid, Campus Montegancedo, 28223 Pozuelo de Alarcón, Madrid, Spain
      More by Mamen Regalado-Reyes
    • Antonia García
      Antonia García
      CEMBIO (Centre for Metabolomics and Bioanalysis), Facultad de Farmacia, Universidad CEU San Pablo, Campus Monteprincipe, Boadilla del Monte, 28668 Madrid, Spain
      More by Antonia García
    • Javier DeFelipe
      Javier DeFelipe
      Laboratorio Cajal de Circuitos Corticales (CTB), Universidad Politécnica de Madrid, Campus Montegancedo, 28223 Pozuelo de Alarcón, Madrid, Spain
      Instituto Cajal (CSIC), Avenida Doctor Arce 37, 28002 Madrid, Spain
      CIBERNED, Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas, Calle de Valderrebollo, 5, 28031 Madrid, Spain
      More by Javier DeFelipe
    • Coral Barbas*
      Coral Barbas
      CEMBIO (Centre for Metabolomics and Bioanalysis), Facultad de Farmacia, Universidad CEU San Pablo, Campus Monteprincipe, Boadilla del Monte, 28668 Madrid, Spain
      *E-mail: [email protected]; phone: +34-91-3724753; fax: +34-91-3724712.
      More by Coral Barbas
      Orcidhttp://orcid.org/0000-0003-4722-491X
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    Journal of Proteome Research

    Cite this: J. Proteome Res. 2019, 18, 3, 1175–1190
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    https://doi.org/10.1021/acs.jproteome.8b00816
    Published January 9, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Syrian hamsters undergo a reversible hyperphosphorylation of protein τ during hibernation, providing a unique natural model that may unveil the physiological mechanisms behind this critical process involved in the development of Alzheimer’s disease and other tauopathies. The hibernation cycle of these animals fluctuates between a pair of stages: 3–4 days of torpor bouts interspersed with periods of euthermia called arousals that last several hours. In this study, we investigated for the first time the metabolic changes in brain tissue during hibernation. A total of 337 metabolites showed statistically significant differences during hibernation. Based on these metabolites, several pathways were found to be significantly regulated and, therefore, play a key role in the regulation of hibernation processes. The increase in the levels of ceramides containing more than 20 C atoms was found in torpor animals, reflecting a higher activity of CerS2 during hibernation, linked to neurofibrillary tangle generation and structural changes in the Golgi apparatus. Our results open up the debate about the possible significance of some metabolites during hibernation, which may possibly be related to τ phosphorylation and dephosphorylation events. In general, this study may provide insights into novel neuroprotective agents because the alterations described throughout the hibernation process are reversible.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jproteome.8b00816.

    • Additional details including a description of the reagents, analytical conditions for the brain tissue fingerprinting by LC–MS, GC–MS, and CE–MS and multiplatform data treatment; figures showing a PCA-X and PLS-DA score plot and OPLS-DA models for the three comparisons obtained after GC–MS, LC–MS, and CE–MS; and a table showing metabolites found to be statistically significant for any of the comparisons performed at different hibernation stages in hamster brain tissue (PDF)

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    Cited By

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    This article is cited by 21 publications.

    1. Carolina González-Riano, Danuta Dudzik, Antonia Garcia, Alberto Gil-de-la-Fuente, Ana Gradillas, Joanna Godzien, Ángeles López-Gonzálvez, Fernanda Rey-Stolle, David Rojo, Francisco J. Ruperez, Jorge Saiz, Coral Barbas. Recent Developments along the Analytical Process for Metabolomics Workflows. Analytical Chemistry 2020, 92 (1) , 203-226. https://doi.org/10.1021/acs.analchem.9b04553
    2. Caiyun Liu, Haixin Yu, Zhengchao Li, Shulian Chen, Xiaoyin Li, Xuyi Chen, Bo Chen. The future of artificial hibernation medicine. Neural Regeneration Research 2024, 19 (1) , 22-28. https://doi.org/10.4103/1673-5374.375305
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    10. Yonggang Niu, Xuejing Zhang, Haiying Zhang, Tisen Xu, Lifeng Zhu, Kenneth B. Storey, Qiang Chen. Metabolic responses of plasma to extreme environments in overwintering Tibetan frogs Nanorana parkeri: a metabolome integrated analysis. Frontiers in Zoology 2021, 18 (1) https://doi.org/10.1186/s12983-021-00428-7
    11. Borja Lanzon, Marina Martin-Taboada, Victor Castro-Alves, Rocio Vila-Bedmar, Ignacio González de Pablos, Daniel Duberg, Pilar Gomez, Elias Rodriguez, Matej Orešič, Tuulia Hyötyläinen, Enrique Morales, Francisco J. Ruperez, Gema Medina-Gomez. Lipidomic and Metabolomic Signature of Progression of Chronic Kidney Disease in Patients with Severe Obesity. Metabolites 2021, 11 (12) , 836. https://doi.org/10.3390/metabo11120836
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    13. , Oleksandr Shylo, Viktoria Lomako, , Oleksandr Semenchenko, . Gel Chromatographic Examination of Serum of Rats and Hamsters Under Artificial and Natural Hibernation. Problems of Cryobiology and Cryomedicine 2021, 31 (3) , 191-202. https://doi.org/10.15407/cryo31.03.191
    14. Carolina Gonzalez-Riano, Silvia Tapia-González, Gertrudis Perea, Candela González-Arias, Javier DeFelipe, Coral Barbas. Metabolic Changes in Brain Slices over Time: a Multiplatform Metabolomics Approach. Molecular Neurobiology 2021, 58 (7) , 3224-3237. https://doi.org/10.1007/s12035-020-02264-y
    15. Lu Dai, Leon Schurgers, Paul G. Shiels, Peter Stenvinkel. A biomimetic natural sciences approach to understanding the mechanisms of ageing in burden of lifestyle diseases. Clinical Science 2021, 135 (10) , 1251-1272. https://doi.org/10.1042/CS20201452
    16. Zhe Shi, Meng Qin, Lu Huang, Tao Xu, Ying Chen, Qin Hu, Sha Peng, Zhuang Peng, Li‐Na Qu, Shan‐Guang Chen, Qin‐Hui Tuo, Duan‐Fang Liao, Xiao‐Ping Wang, Ren‐Rong Wu, Ti‐Fei Yuan, Ying‐Hui Li, Xin‐Min Liu. Human torpor: translating insights from nature into manned deep space expedition. Biological Reviews 2021, 96 (2) , 642-672. https://doi.org/10.1111/brv.12671
    17. Antoine Duquette, Camille Pernègre, Ariane Veilleux Carpentier, Nicole Leclerc. Similarities and Differences in the Pattern of Tau Hyperphosphorylation in Physiological and Pathological Conditions: Impacts on the Elaboration of Therapies to Prevent Tau Pathology. Frontiers in Neurology 2021, 11 https://doi.org/10.3389/fneur.2020.607680
    18. Carolina Gonzalez-Riano, Mª. Fernanda Rey-Stolle, Coral Barbas, Antonia García. GC-MS Nontargeted Metabolomics of Neural Tissue. 2021, 199-219. https://doi.org/10.1007/978-1-0716-0864-7_16
    19. Carolina Gonzalez-Riano, Antonia García, Coral Barbas. Untargeted Metabolomics Determination of Postmortem Changes in Brain Tissue Samples by UHPLC-ESI-QTOF-MS and GC-EI-Q-MS. 2021, 245-265. https://doi.org/10.1007/978-1-0716-0864-7_20
    20. Gonzalo León-Espinosa, Javier DeFelipe, Alberto Muñoz. The Golgi Apparatus of Neocortical Glial Cells During Hibernation in the Syrian Hamster. Frontiers in Neuroanatomy 2019, 13 https://doi.org/10.3389/fnana.2019.00092
    21. Giacomo Gattoni, Graziella Bernocchi. Calcium-Binding Proteins in the Nervous System during Hibernation: Neuroprotective Strategies in Hypometabolic Conditions?. International Journal of Molecular Sciences 2019, 20 (9) , 2364. https://doi.org/10.3390/ijms20092364
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    Journal of Proteome Research

    Cite this: J. Proteome Res. 2019, 18, 3, 1175–1190
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jproteome.8b00816
    Published January 9, 2019
    Copyright © 2019 American Chemical Society
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