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PMID: 21186369 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin.

Nature medicine ·Vol. 17 ·No. 1 ·2011-01-00 ·Pages 55-63

Holland WL, Miller RA, Wang ZV, Sun K, Barth BM, Bui HH, Davis KE, Bikman BT, Halberg N, Rutkowski JM, Wade MR, Tenorio VM, Kuo MS, Brozinick JT, Zhang BB, Birnbaum MJ, Summers SA, Scherer PE

Abstract

The adipocyte-derived secretory factor adiponectin promotes insulin sensitivity, decreases inflammation and promotes cell survival. No unifying mechanism has yet explained how adiponectin can exert such a variety of beneficial systemic effects. Here, we show that adiponectin potently stimulates a ceramidase activity associated with its two receptors, AdipoR1 and AdipoR2, and enhances ceramide catabolism and formation of its antiapoptotic metabolite--sphingosine-1-phosphate (S1P)--independently of AMP-dependent kinase (AMPK). Using models of inducible apoptosis in pancreatic beta cells and cardiomyocytes, we show that transgenic overproduction of adiponectin decreases caspase-8-mediated death, whereas genetic ablation of adiponectin enhances apoptosis in vivo through a sphingolipid-mediated pathway. Ceramidase activity is impaired in cells lacking both adiponectin receptor isoforms, leading to elevated ceramide levels and enhanced susceptibility to palmitate-induced cell death. Combined, our observations suggest a unifying mechanism of action for the beneficial systemic effects exerted by adiponectin, with sphingolipid metabolism as its core upstream signaling component.

MeSH Terms
Adenylate Kinase/metabolism Adiponectin/deficiency,genetics,physiology,therapeutic use Animals Apoptosis/physiology Calcium-Calmodulin-Dependent Protein Kinase Kinase/metabolism Ceramidases/drug effects,metabolism Ceramides/metabolism Enzyme Activation Gene Expression Regulation Humans Insulin/physiology Kinetics Leptin/deficiency Mice Mice, Obese Myocardial Infarction/drug therapy Myocytes, Cardiac/physiology Receptors, Adiponectin/physiology
Chemicals
Adiponectin Ceramides Insulin Leptin Receptors, Adiponectin Calcium-Calmodulin-Dependent Protein Kinase Kinase Adenylate Kinase Ceramidases
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Holland William L
Touchstone Diabetes Center, The University of Texas Southwestern Medical Center, Dallas, Texas, USA.
Miller Russell A
Wang Zhao V
Sun Kai
Barth Brian M
Bui Hai H
Davis Kathryn E
Bikman Benjamin T
Halberg Nils
Rutkowski Joseph M
Wade Mark R
Tenorio Vincent M
Kuo Ming-Shang
Brozinick Joseph T
Zhang Bei B
Birnbaum Morris J
Summers Scott A
Scherer Philipp E
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Article Info
Journal
Nature medicine
Abbr.
Nat Med
ISSN
1546-170X
Published
2011-01-00
Epub
2010-00-26
Pages
55-63
Language
English
Region
United States
NLM ID
9502015
PMCID
PMC3134999
Subset
IM
Grants
NIDDK NIH HHS · F32 DK081279 · United States
NIDDK NIH HHS · P01 DK049210-15 · United States
NIDDK NIH HHS · F32 DK085935-01A1 · United States
NHLBI NIH HHS · T32 HL007360 · United States
NIDDK NIH HHS · F32 DK081279-01A1 · United States
NIDDK NIH HHS · R21 DK073181-01A1 · United States
NCI NIH HHS · R01 CA112023 · United States
NIDDK NIH HHS · TL1 DK081181 · United States
NIDDK NIH HHS · R01 DK055758-11 · United States
NIDDK NIH HHS · F32 DK083866 · United States
NIDDK NIH HHS · P01 DK088761 · United States
NIDDK NIH HHS · F32-DK083866 · United States
NIDDK NIH HHS · P01 DK088761-01 · United States
NIDDK NIH HHS · RC1 DK086629 · United States
NHLBI NIH HHS · T32-HL007360 · United States
NIDDK NIH HHS · R01 DK056886-12 · United States
NIDDK NIH HHS · F32 DK085935 · United States
NIDDK NIH HHS · R01 DK081456 · United States
NIDDK NIH HHS · R01-DK55758 · United States
NIDDK NIH HHS · TL1 DK081181-01 · United States
NIDDK NIH HHS · RC1-DK086629 · United States
NIDDK NIH HHS · P01-DK088761 · United States
NHLBI NIH HHS · T32 HL007360-33 · United States
NIDDK NIH HHS · F32-DK085935 · United States
NIDDK NIH HHS · R01 DK056886 · United States
NIDDK NIH HHS · F32-DK081279 · United States
NIDDK NIH HHS · R21-DK073181 · United States
NIDDK NIH HHS · R21 DK073181 · United States
NCI NIH HHS · R01 CA112023-05 · United States
NIDDK NIH HHS · R01-DK56886 · United States
NCI NIH HHS · R01-CA112023 · United States
NIDDK NIH HHS · F32 DK083866-01 · United States
NIDDK NIH HHS · P01-DK49210 · United States
NIDDK NIH HHS · TL1-DK081181 · United States
NIDDK NIH HHS · P01 DK049210 · United States
NIDDK NIH HHS · RC1 DK086629-02 · United States
NIDDK NIH HHS · R01 DK055758 · United States
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