Acute activation of adipocyte lipolysis reveals dynamic lipid remodeling of the hepatic lipidome

Adipose tissue is the site of long-term energy storage. During the fasting state, exercise, and cold exposure, the white adipose tissue mobilizes energy for peripheral tissues through lipolysis. The mobilization of lipids from white adipose tissue to the liver can lead to excess triglyceride accumul...

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Published inJournal of lipid research Vol. 65; no. 2; p. 100434
Main Authors Zhang, Sicheng, Williams, Kevin J., Verlande-Ferrero, Amandine, Chan, Alvin P., Su, Gino B., Kershaw, Erin E., Cox, James E., Maschek, John Alan, Shapira, Suzanne N., Christofk, Heather R., de Aguiar Vallim, Thomas Q., Masri, Selma, Villanueva, Claudio J.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.02.2024
American Society for Biochemistry and Molecular Biology
Elsevier
Subjects
Adipocytes
Adipose tissue triglyceride lipase
Ceramides
Fasting
Lipase
Lipid droplets
Lipidomics
Lipids
Liver
Triglycerides
EE
CE
NAFLD
Fasting
Lipid droplets
Liver
ATGL
Lipids
Lipidomics
Triglycerides
Adipocytes
DAG
WAT
Lipase
iWAT
AR
CER
BAT
VLCFA
Ceramides
Adipose tissue triglyceride lipase
TAG
RER
Online AccessGet full text

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Abstract Adipose tissue is the site of long-term energy storage. During the fasting state, exercise, and cold exposure, the white adipose tissue mobilizes energy for peripheral tissues through lipolysis. The mobilization of lipids from white adipose tissue to the liver can lead to excess triglyceride accumulation and fatty liver disease. Although the white adipose tissue is known to release free fatty acids, a comprehensive analysis of lipids mobilized from white adipocytes in vivo has not been completed. In these studies, we provide a comprehensive quantitative analysis of the adipocyte-secreted lipidome and show that there is interorgan crosstalk with liver. Our analysis identifies multiple lipid classes released by adipocytes in response to activation of lipolysis. Time-dependent analysis of the serum lipidome showed that free fatty acids increase within 30 min of β3-adrenergic receptor activation and subsequently decrease, followed by a rise in serum triglycerides, liver triglycerides, and several ceramide species. The triglyceride composition of liver is enriched for linoleic acid despite higher concentrations of palmitate in the blood. To further validate that these findings were a specific consequence of lipolysis, we generated mice with conditional deletion of adipose tissue triglyceride lipase exclusively in adipocytes. This loss of in vivo adipocyte lipolysis prevented the rise in serum free fatty acids and hepatic triglycerides. Furthermore, conditioned media from adipocytes promotes lipid remodeling in hepatocytes with concomitant changes in genes/pathways mediating lipid utilization. Together, these data highlight critical role of adipocyte lipolysis in interorgan crosstalk between adipocytes and liver.
AbstractList Adipose tissue is the site of long-term energy storage. During the fasting state, exercise, and cold exposure, the white adipose tissue mobilizes energy for peripheral tissues through lipolysis. The mobilization of lipids from white adipose tissue to the liver can lead to excess triglyceride accumulation and fatty liver disease. Although the white adipose tissue is known to release free fatty acids, a comprehensive analysis of lipids mobilized from white adipocytes in vivo has not been completed. In these studies, we provide a comprehensive quantitative analysis of the adipocyte-secreted lipidome and show that there is interorgan crosstalk with liver. Our analysis identifies multiple lipid classes released by adipocytes in response to activation of lipolysis. Time-dependent analysis of the serum lipidome showed that free fatty acids increase within 30 min of β3-adrenergic receptor activation and subsequently decrease, followed by a rise in serum triglycerides, liver triglycerides, and several ceramide species. The triglyceride composition of liver is enriched for linoleic acid despite higher concentrations of palmitate in the blood. To further validate that these findings were a specific consequence of lipolysis, we generated mice with conditional deletion of adipose tissue triglyceride lipase exclusively in adipocytes. This loss of in vivo adipocyte lipolysis prevented the rise in serum free fatty acids and hepatic triglycerides. Furthermore, conditioned media from adipocytes promotes lipid remodeling in hepatocytes with concomitant changes in genes/pathways mediating lipid utilization. Together, these data highlight critical role of adipocyte lipolysis in interorgan crosstalk between adipocytes and liver.
Adipose tissue is the site of long-term energy storage. During the fasting state, exercise, and cold exposure, the white adipose tissue mobilizes energy for peripheral tissues through lipolysis. The mobilization of lipids from white adipose tissue to the liver can lead to excess triglyceride accumulation and fatty liver disease. Although the white adipose tissue is known to release free fatty acids, a comprehensive analysis of lipids mobilized from white adipocytes in vivo has not been completed. In these studies, we provide a comprehensive quantitative analysis of the adipocyte-secreted lipidome and show that there is interorgan crosstalk with liver. Our analysis identifies multiple lipid classes released by adipocytes in response to activation of lipolysis. Time-dependent analysis of the serum lipidome showed that free fatty acids increase within 30 min of β3-adrenergic receptor activation and subsequently decrease, followed by a rise in serum triglycerides, liver triglycerides, and several ceramide species. The triglyceride composition of liver is enriched for linoleic acid despite higher concentrations of palmitate in the blood. To further validate that these findings were a specific consequence of lipolysis, we generated mice with conditional deletion of adipose tissue triglyceride lipase exclusively in adipocytes. This loss of in vivo adipocyte lipolysis prevented the rise in serum free fatty acids and hepatic triglycerides. Furthermore, conditioned media from adipocytes promotes lipid remodeling in hepatocytes with concomitant changes in genes/pathways mediating lipid utilization. Together, these data highlight critical role of adipocyte lipolysis in interorgan crosstalk between adipocytes and liver.Adipose tissue is the site of long-term energy storage. During the fasting state, exercise, and cold exposure, the white adipose tissue mobilizes energy for peripheral tissues through lipolysis. The mobilization of lipids from white adipose tissue to the liver can lead to excess triglyceride accumulation and fatty liver disease. Although the white adipose tissue is known to release free fatty acids, a comprehensive analysis of lipids mobilized from white adipocytes in vivo has not been completed. In these studies, we provide a comprehensive quantitative analysis of the adipocyte-secreted lipidome and show that there is interorgan crosstalk with liver. Our analysis identifies multiple lipid classes released by adipocytes in response to activation of lipolysis. Time-dependent analysis of the serum lipidome showed that free fatty acids increase within 30 min of β3-adrenergic receptor activation and subsequently decrease, followed by a rise in serum triglycerides, liver triglycerides, and several ceramide species. The triglyceride composition of liver is enriched for linoleic acid despite higher concentrations of palmitate in the blood. To further validate that these findings were a specific consequence of lipolysis, we generated mice with conditional deletion of adipose tissue triglyceride lipase exclusively in adipocytes. This loss of in vivo adipocyte lipolysis prevented the rise in serum free fatty acids and hepatic triglycerides. Furthermore, conditioned media from adipocytes promotes lipid remodeling in hepatocytes with concomitant changes in genes/pathways mediating lipid utilization. Together, these data highlight critical role of adipocyte lipolysis in interorgan crosstalk between adipocytes and liver.
ArticleNumber 100434
Author Shapira, Suzanne N.
Verlande-Ferrero, Amandine
Christofk, Heather R.
Williams, Kevin J.
Cox, James E.
Zhang, Sicheng
Masri, Selma
Su, Gino B.
Villanueva, Claudio J.
de Aguiar Vallim, Thomas Q.
Kershaw, Erin E.
Maschek, John Alan
Chan, Alvin P.
Author_xml – sequence: 1
  givenname: Sicheng
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  surname: Zhang
  fullname: Zhang, Sicheng
  organization: Department of Integrative Biology and Physiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA
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  givenname: Kevin J.
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  surname: Williams
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  organization: UCLA Lipidomics Lab, Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA
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  givenname: Amandine
  surname: Verlande-Ferrero
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  surname: Su
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  organization: UCLA Lipidomics Lab, Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA
– sequence: 6
  givenname: Erin E.
  surname: Kershaw
  fullname: Kershaw, Erin E.
  organization: Division of Endocrinology and Metabolism, Department of Medicine, University of Pittsburgh, PA, USA
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  givenname: James E.
  orcidid: 0000-0002-5977-2350
  surname: Cox
  fullname: Cox, James E.
  organization: Department of Biochemistry, University of Utah School of Medicine, Salt Lake City, UT, USA
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  givenname: John Alan
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– sequence: 10
  givenname: Heather R.
  surname: Christofk
  fullname: Christofk, Heather R.
  organization: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles (UCLA), Los Angeles, CA, USA
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  givenname: Thomas Q.
  orcidid: 0000-0001-7642-5046
  surname: de Aguiar Vallim
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  givenname: Selma
  surname: Masri
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  organization: Department of Biological Chemistry, Center for Epigenetics and Metabolism, Chao Family Comprehensive Cancer Center, University of California, Irvine (UCI), Irvine, CA, USA
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  givenname: Claudio J.
  orcidid: 0000-0002-9731-7463
  surname: Villanueva
  fullname: Villanueva, Claudio J.
  email: cvillanueva@ucla.edu
  organization: Department of Integrative Biology and Physiology, University of California, Los Angeles (UCLA), Los Angeles, CA, USA
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Issue 2
Keywords EE
CE
NAFLD
Fasting
Lipid droplets
Liver
ATGL
Lipids
Lipidomics
Triglycerides
Adipocytes
DAG
WAT
Lipase
iWAT
AR
CER
BAT
VLCFA
Ceramides
Adipose tissue triglyceride lipase
TAG
RER
Language English
License This is an open access article under the CC BY license.
Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
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Snippet Adipose tissue is the site of long-term energy storage. During the fasting state, exercise, and cold exposure, the white adipose tissue mobilizes energy for...
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StartPage 100434
SubjectTerms Adipocytes
Adipose tissue triglyceride lipase
Ceramides
Fasting
Lipase
Lipid droplets
Lipidomics
Lipids
Liver
Triglycerides
Title Acute activation of adipocyte lipolysis reveals dynamic lipid remodeling of the hepatic lipidome
URI https://dx.doi.org/10.1016/j.jlr.2023.100434
https://www.ncbi.nlm.nih.gov/pubmed/37640283
https://www.proquest.com/docview/2858989408
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