Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism

Matthew D. Lynes; Farnaz Shamsi; Elahu Gosney Sustarsic; Luiz O. Leiria; Chih Hao Wang; Sheng Chiang Su; Tian Lian Huang; Fei Gao; Niven R. Narain; Emily Y. Chen; Aaron M. Cypess; Tim J. Schulz; Zachary Gerhart-Hines; Michael A. Kiebish; Yu Hua Tseng

doi:10.1016/j.celrep.2018.06.073

Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism

Matthew D. Lynes, Farnaz Shamsi, Elahu Gosney Sustarsic, Luiz O. Leiria, Chih Hao Wang, Sheng Chiang Su, Tian Lian Huang, Fei Gao, Niven R. Narain, Emily Y. Chen, Aaron M. Cypess, Tim J. Schulz, Zachary Gerhart-Hines, Michael A. Kiebish, Yu Hua Tseng

Molecular Pathobiology

Research output: Contribution to journal › Article › peer-review

Abstract

Thermogenic fat expends energy during cold for temperature homeostasis, and its activity regulates nutrient metabolism and insulin sensitivity. We measured cold-activated lipid landscapes in circulation and in adipose tissue by MS/MS^ALL shotgun lipidomics. We created an interactive online viewer to visualize the changes of specific lipid species in response to cold. In adipose tissue, among the approximately 1,600 lipid species profiled, we identified the biosynthetic pathway of the mitochondrial phospholipid cardiolipin as coordinately activated in brown and beige fat by cold in wild-type and transgenic mice with enhanced browning of white fat. Together, these data provide a comprehensive lipid bio-signature of thermogenic fat activation in circulation and tissue and suggest pathways regulated by cold exposure. In this resource, Lynes et al. use a sensitive MS/MS^ALL technique to profile over 1,000 lipid species in the blood and adipose tissue of humans and mice exposed to cold. Using the online viewer they created to view these data, pathways activated by cold exposure can be identified.

Original language	English (US)
Pages (from-to)	781-790
Number of pages	10
Journal	Cell Reports
Volume	24
Issue number	3
DOIs	https://doi.org/10.1016/j.celrep.2018.06.073
State	Published - Jul 17 2018

Keywords

brown adipose tissue
cardiolipin
lipidomics
thermogenesis
white adipose tissue
Metabolomics
Cold Temperature
Humans
Phosphatidylglycerols/metabolism
Adipose Tissue, White/metabolism
Animals
Thermogenesis
Adipose Tissue, Brown/metabolism
Biomarkers/blood
Models, Animal
Cardiolipins/metabolism
Mice
Lipids/blood

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2018.06.073

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Lynes, M. D., Shamsi, F., Sustarsic, E. G., Leiria, L. O., Wang, C. H., Su, S. C., Huang, T. L., Gao, F., Narain, N. R., Chen, E. Y., Cypess, A. M., Schulz, T. J., Gerhart-Hines, Z., Kiebish, M. A., & Tseng, Y. H. (2018). Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism. Cell Reports, 24(3), 781-790. https://doi.org/10.1016/j.celrep.2018.06.073

Lynes, MD, Shamsi, F, Sustarsic, EG, Leiria, LO, Wang, CH, Su, SC, Huang, TL, Gao, F, Narain, NR, Chen, EY, Cypess, AM, Schulz, TJ, Gerhart-Hines, Z, Kiebish, MA & Tseng, YH 2018, 'Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism', Cell Reports, vol. 24, no. 3, pp. 781-790. https://doi.org/10.1016/j.celrep.2018.06.073

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title = "Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism",

abstract = "Thermogenic fat expends energy during cold for temperature homeostasis, and its activity regulates nutrient metabolism and insulin sensitivity. We measured cold-activated lipid landscapes in circulation and in adipose tissue by MS/MSALL shotgun lipidomics. We created an interactive online viewer to visualize the changes of specific lipid species in response to cold. In adipose tissue, among the approximately 1,600 lipid species profiled, we identified the biosynthetic pathway of the mitochondrial phospholipid cardiolipin as coordinately activated in brown and beige fat by cold in wild-type and transgenic mice with enhanced browning of white fat. Together, these data provide a comprehensive lipid bio-signature of thermogenic fat activation in circulation and tissue and suggest pathways regulated by cold exposure. In this resource, Lynes et al. use a sensitive MS/MSALL technique to profile over 1,000 lipid species in the blood and adipose tissue of humans and mice exposed to cold. Using the online viewer they created to view these data, pathways activated by cold exposure can be identified.",

keywords = "brown adipose tissue, cardiolipin, lipidomics, thermogenesis, white adipose tissue, Metabolomics, Cold Temperature, Humans, Phosphatidylglycerols/metabolism, Adipose Tissue, White/metabolism, Animals, Thermogenesis, Adipose Tissue, Brown/metabolism, Biomarkers/blood, Models, Animal, Cardiolipins/metabolism, Mice, Lipids/blood",

author = "Lynes, {Matthew D.} and Farnaz Shamsi and Sustarsic, {Elahu Gosney} and Leiria, {Luiz O.} and Wang, {Chih Hao} and Su, {Sheng Chiang} and Huang, {Tian Lian} and Fei Gao and Narain, {Niven R.} and Chen, {Emily Y.} and Cypess, {Aaron M.} and Schulz, {Tim J.} and Zachary Gerhart-Hines and Kiebish, {Michael A.} and Tseng, {Yu Hua}",

note = "Funding Information: This work was supported in part by U.S. NIH grants R01DK077097 and R01DK102898 (to Y.-H.T.) and by grant P30DK036836 (to Joslin Diabetes Center{\textquoteright}s Diabetes Research Center; DRC) from the National Institute of Diabetes and Digestive and Kidney Diseases . M.D.L. was supported by NIH grants T32DK007260 , F32DK102320 , and K01DK111714 . We thank H. Pan in the Joslin Bioinformatics Core. This manuscript is dedicated to the memory of Sean Peters. Publisher Copyright: {\textcopyright} 2018 The Authors",

year = "2018",

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doi = "10.1016/j.celrep.2018.06.073",

language = "English (US)",

volume = "24",

pages = "781--790",

journal = "Cell Reports",

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T1 - Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism

AU - Lynes, Matthew D.

AU - Shamsi, Farnaz

AU - Sustarsic, Elahu Gosney

AU - Leiria, Luiz O.

AU - Wang, Chih Hao

AU - Su, Sheng Chiang

AU - Huang, Tian Lian

AU - Gao, Fei

AU - Narain, Niven R.

AU - Chen, Emily Y.

AU - Cypess, Aaron M.

AU - Schulz, Tim J.

AU - Gerhart-Hines, Zachary

AU - Kiebish, Michael A.

AU - Tseng, Yu Hua

N1 - Funding Information: This work was supported in part by U.S. NIH grants R01DK077097 and R01DK102898 (to Y.-H.T.) and by grant P30DK036836 (to Joslin Diabetes Center’s Diabetes Research Center; DRC) from the National Institute of Diabetes and Digestive and Kidney Diseases . M.D.L. was supported by NIH grants T32DK007260 , F32DK102320 , and K01DK111714 . We thank H. Pan in the Joslin Bioinformatics Core. This manuscript is dedicated to the memory of Sean Peters. Publisher Copyright: © 2018 The Authors

PY - 2018/7/17

Y1 - 2018/7/17

N2 - Thermogenic fat expends energy during cold for temperature homeostasis, and its activity regulates nutrient metabolism and insulin sensitivity. We measured cold-activated lipid landscapes in circulation and in adipose tissue by MS/MSALL shotgun lipidomics. We created an interactive online viewer to visualize the changes of specific lipid species in response to cold. In adipose tissue, among the approximately 1,600 lipid species profiled, we identified the biosynthetic pathway of the mitochondrial phospholipid cardiolipin as coordinately activated in brown and beige fat by cold in wild-type and transgenic mice with enhanced browning of white fat. Together, these data provide a comprehensive lipid bio-signature of thermogenic fat activation in circulation and tissue and suggest pathways regulated by cold exposure. In this resource, Lynes et al. use a sensitive MS/MSALL technique to profile over 1,000 lipid species in the blood and adipose tissue of humans and mice exposed to cold. Using the online viewer they created to view these data, pathways activated by cold exposure can be identified.

AB - Thermogenic fat expends energy during cold for temperature homeostasis, and its activity regulates nutrient metabolism and insulin sensitivity. We measured cold-activated lipid landscapes in circulation and in adipose tissue by MS/MSALL shotgun lipidomics. We created an interactive online viewer to visualize the changes of specific lipid species in response to cold. In adipose tissue, among the approximately 1,600 lipid species profiled, we identified the biosynthetic pathway of the mitochondrial phospholipid cardiolipin as coordinately activated in brown and beige fat by cold in wild-type and transgenic mice with enhanced browning of white fat. Together, these data provide a comprehensive lipid bio-signature of thermogenic fat activation in circulation and tissue and suggest pathways regulated by cold exposure. In this resource, Lynes et al. use a sensitive MS/MSALL technique to profile over 1,000 lipid species in the blood and adipose tissue of humans and mice exposed to cold. Using the online viewer they created to view these data, pathways activated by cold exposure can be identified.

KW - brown adipose tissue

KW - cardiolipin

KW - lipidomics

KW - thermogenesis

KW - white adipose tissue

KW - Metabolomics

KW - Cold Temperature

KW - Humans

KW - Phosphatidylglycerols/metabolism

KW - Adipose Tissue, White/metabolism

KW - Animals

KW - Thermogenesis

KW - Adipose Tissue, Brown/metabolism

KW - Biomarkers/blood

KW - Models, Animal

KW - Cardiolipins/metabolism

KW - Mice

KW - Lipids/blood

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DO - 10.1016/j.celrep.2018.06.073

M3 - Article

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AN - SCOPUS:85049754305

SN - 2211-1247

VL - 24

SP - 781

EP - 790

JO - Cell Reports

JF - Cell Reports

IS - 3

ER -

Cold-Activated Lipid Dynamics in Adipose Tissue Highlights a Role for Cardiolipin in Thermogenic Metabolism

Abstract

Keywords

ASJC Scopus subject areas

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