Facultative protein selenation regulates redox sensitivity, adipose tissue thermogenesis, and obesity.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
19 05 2020
Historique:
pubmed: 3 5 2020
medline: 11 8 2020
entrez: 3 5 2020
Statut: ppublish

Résumé

Oxidation of cysteine thiols by physiological reactive oxygen species (ROS) initiates thermogenesis in brown and beige adipose tissues. Cellular selenocysteines, where sulfur is replaced with selenium, exhibit enhanced reactivity with ROS. Despite their critical roles in physiology, methods for broad and direct detection of proteogenic selenocysteines are limited. Here we developed a mass spectrometric method to interrogate incorporation of selenium into proteins. Unexpectedly, this approach revealed facultative incorporation of selenium as selenocysteine or selenomethionine into proteins that lack canonical encoding for selenocysteine. Selenium was selectively incorporated into regulatory sites on key metabolic proteins, including as selenocysteine-replacing cysteine at position 253 in uncoupling protein 1 (UCP1). This facultative utilization of selenium was initiated by increasing cellular levels of organic, but not inorganic, forms of selenium. Remarkably, dietary selenium supplementation elevated facultative incorporation into UCP1, elevated energy expenditure through thermogenic adipose tissue, and protected against obesity. Together, these findings reveal the existence of facultative protein selenation, which correlates with impacts on thermogenic adipocyte function and presumably other biological processes as well.

Identifiants

pubmed: 32358195
pii: 2001387117
doi: 10.1073/pnas.2001387117
pmc: PMC7245117
doi:

Substances chimiques

Reactive Oxygen Species 0
Ucp1 protein, mouse 0
Uncoupling Protein 1 0
Selenium H6241UJ22B
Cysteine K848JZ4886

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

10789-10796

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK123095
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK117149
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA080946
Pays : United States
Organisme : Medical Research Council
ID : MC_UU_00015/3
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM132129
Pays : United States

Informations de copyright

Copyright © 2020 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no competing interest.

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Auteurs

Mark P Jedrychowski (MP)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115; Mark_Jedrychowski@hms.harvard.edu EdwardT_Chouchani@dfci.harvard.edu Bruce_Spiegelman@dfci.harvard.edu.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Gina Z Lu (GZ)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

John Szpyt (J)

Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Marco Mariotti (M)

Division of Genetics, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA 02115.

Ryan Garrity (R)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Joao A Paulo (JA)

Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Devin K Schweppe (DK)

Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Dina Laznik-Bogoslavski (D)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Lawrence Kazak (L)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Michael P Murphy (MP)

Medical Research Council (MRC) Mitochondrial Biology Unit, University of Cambridge, Cambridge CB20XY, United Kingdom.
Department of Medicine, University of Cambridge, Cambridge CB20XY, United Kingdom.

Vadim N Gladyshev (VN)

Division of Genetics, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA 02115.

Steven P Gygi (SP)

Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Edward T Chouchani (ET)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115; Mark_Jedrychowski@hms.harvard.edu EdwardT_Chouchani@dfci.harvard.edu Bruce_Spiegelman@dfci.harvard.edu.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

Bruce M Spiegelman (BM)

Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115; Mark_Jedrychowski@hms.harvard.edu EdwardT_Chouchani@dfci.harvard.edu Bruce_Spiegelman@dfci.harvard.edu.
Department of Cell Biology, Harvard Medical School, Boston, MA 02115.

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