Sulfide catabolism ameliorates hypoxic brain injury.

Animals Brain / metabolism Brain Injuries / genetics Cells, Cultured Female Hydrogen Sulfide / metabolism Hypoxia Male Membrane Potential, Mitochondrial Mice, Inbred C57BL Mice, Inbred DBA Mice, Knockout Mitochondria / metabolism NAD / metabolism Quinone Reductases / genetics RNA Interference Rats, Sprague-Dawley

Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
25 05 2021
Historique:
received: 11 06 2020
accepted: 27 04 2021
entrez: 26 5 2021
pubmed: 27 5 2021
medline: 16 6 2021
Statut: epublish

Résumé

The mammalian brain is highly vulnerable to oxygen deprivation, yet the mechanism underlying the brain's sensitivity to hypoxia is incompletely understood. Hypoxia induces accumulation of hydrogen sulfide, a gas that inhibits mitochondrial respiration. Here, we show that, in mice, rats, and naturally hypoxia-tolerant ground squirrels, the sensitivity of the brain to hypoxia is inversely related to the levels of sulfide:quinone oxidoreductase (SQOR) and the capacity to catabolize sulfide. Silencing SQOR increased the sensitivity of the brain to hypoxia, whereas neuron-specific SQOR expression prevented hypoxia-induced sulfide accumulation, bioenergetic failure, and ischemic brain injury. Excluding SQOR from mitochondria increased sensitivity to hypoxia not only in the brain but also in heart and liver. Pharmacological scavenging of sulfide maintained mitochondrial respiration in hypoxic neurons and made mice resistant to hypoxia. These results illuminate the critical role of sulfide catabolism in energy homeostasis during hypoxia and identify a therapeutic target for ischemic brain injury.

Identifiants

DOI: 10.1038/s41467-021-23363-x PMID: 34035265 PMC: PMC8149856
pubmed: 34035265
doi: 10.1038/s41467-021-23363-x
pii: 10.1038/s41467-021-23363-x
pmc: PMC8149856
doi:

Substances chimiques

NAD 0U46U6E8UK
Quinone Reductases EC 1.6.99.-
sulfide quinone reductase EC 1.8.5.-
Hydrogen Sulfide YY9FVM7NSN

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

3108

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL101930
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS096237
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL113303
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL149264
Pays : United States
Organisme : NINDS NIH HHS
ID : R21 NS116671
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM121307
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS112373
Pays : United States

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Auteurs

Eizo Marutani (E)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Masanobu Morita (M)

Department of Environmental Medicine and Molecular Toxicology, Tohoku University Graduate School of Medicine, Sendai, Japan.

Shuichi Hirai (S)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Shinichi Kai (S)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.
ORCID: 0000-0002-1804-3071

Robert M H Grange (RMH)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Yusuke Miyazaki (Y)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Fumiaki Nagashima (F)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Lisa Traeger (L)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Aurora Magliocca (A)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Tomoaki Ida (T)

Department of Environmental Medicine and Molecular Toxicology, Tohoku University Graduate School of Medicine, Sendai, Japan.

Tetsuro Matsunaga (T)

Department of Environmental Medicine and Molecular Toxicology, Tohoku University Graduate School of Medicine, Sendai, Japan.

Daniel R Flicker (DR)

Department of Systems Biology, Harvard Medical School, Boston, MA, USA.
Howard Hughes Medical Institute and Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.

Benjamin Corman (B)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Division of Rheumatology, Allergy and Immunology, Department of Medicine, Massachusetts General Hospital, Boston, MA, USA.

Naohiro Mori (N)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Yumiko Yamazaki (Y)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.

Annabelle Batten (A)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.

Rebecca Li (R)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
ORCID: 0000-0002-1567-9541

Tomohiro Tanaka (T)

Division of Cardiocirculatory Signaling, National Institute for Physiological Sciences & Exploratory Research Center on Life and Living Systems & Center for Novel Science Initiatives, National Institutes of Natural Sciences, Okazaki, Japan.
ORCID: 0000-0001-7442-4912

Takamitsu Ikeda (T)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.
ORCID: 0000-0002-1245-2958

Akito Nakagawa (A)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.

Dmitriy N Atochin (DN)

Harvard Medical School, Boston, MA, USA.
Cardiovascular Research Center, Division of Cardiology, Department of Medicine, Harvard Medical School, Massachusetts General Hospital, Charlestown, MA, USA.

Hideshi Ihara (H)

Department of Biological Science, Graduate School of Science, Osaka Prefecture University, Osaka, Japan.
ORCID: 0000-0002-8971-5138

Benjamin A Olenchock (BA)

Harvard Medical School, Boston, MA, USA.
Division of Cardiovascular Medicine, Department of Medicine, The Brigham and Women's Hospital, Boston, MA, USA.

Xinggui Shen (X)

Department of Pathology and Translational Pathobiology, Louisiana State University Health Sciences Center-Shreveport, Shreveport, LA, USA.

Motohiro Nishida (M)

Division of Cardiocirculatory Signaling, National Institute for Physiological Sciences & Exploratory Research Center on Life and Living Systems & Center for Novel Science Initiatives, National Institutes of Natural Sciences, Okazaki, Japan.
Department of Physiology, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan.
ORCID: 0000-0002-2587-5458

Kenjiro Hanaoka (K)

Graduate School of Pharmaceutical Sciences, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.
ORCID: 0000-0003-0797-4038

Christopher G Kevil (CG)

Department of Pathology and Translational Pathobiology, Louisiana State University Health Sciences Center-Shreveport, Shreveport, LA, USA.
ORCID: 0000-0003-0863-7260

Ming Xian (M)

Department of Chemistry, Brown University, Providence, RI, USA.

Donald B Bloch (DB)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.
Division of Rheumatology, Allergy and Immunology, Department of Medicine, Massachusetts General Hospital, Boston, MA, USA.

Takaaki Akaike (T)

Department of Environmental Medicine and Molecular Toxicology, Tohoku University Graduate School of Medicine, Sendai, Japan.

Allyson G Hindle (AG)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA.
Harvard Medical School, Boston, MA, USA.
School of Life Sciences, University of Nevada Las Vegas, Las Vegas, NV, USA.
ORCID: 0000-0002-1983-9573

Hozumi Motohashi (H)

Department of Gene Expression Regulation, Institute of Development, Aging and Cancer, Tohoku University, Sendai, Japan. hozumim@med.tohoku.ac.jp.
ORCID: 0000-0002-7261-1033

Fumito Ichinose (F)

Anesthesia Center for Critical Care Research of the Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA, USA. fichinose@mgh.harvard.edu.
Harvard Medical School, Boston, MA, USA. fichinose@mgh.harvard.edu.
ORCID: 0000-0003-4535-1632

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Plaies et blessures › Traumatismes du système nerveux › Traumatismes cranioencéphaliques › Lésions encéphaliques › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Cellules › Cellules cultivées › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Produits chimiques inorganiques › Sulfure d'hydrogène › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › États, signes et symptômes pathologiques › Signes et symptômes › Signes et symptômes respiratoires › Hypoxie › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Phénomènes physiologiques › Phénomènes électrophysiologiques › Potentiel de membrane mitochondriale › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lignées consanguines de souris › Souris de lignée C57BL › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Lignées consanguines de souris › Souris de lignée DBA › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › Souris transgéniques › Souris knockout › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Cellules › Structures cellulaires › Fractions subcellulaires › Mitochondries › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Nucléotides › Ribonucléotides › Nucléotides adényliques › NAD › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Oxidoreductases › NADH, NADPH oxidoreductases › Quinone reductases › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Épigenèse génétique › Extinction de l'expression des gènes › Interférence par ARN › Sulfide catabolism ameliorates hypoxic brain injury.
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Rats › Rat Sprague-Dawley › Sulfide catabolism ameliorates hypoxic brain injury.