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Adiponectin Inhibits Tumor Necrosis Factor-α–Induced Vascular Inflammatory Response via Caveolin-Mediated Ceramidase Recruitment and Activation
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Rationale: Anti-inflammatory and vascular protective actions of adiponectin are well recognized. However, many fundamental questions remain unanswered. Objective: The current study attempted to identify the adiponectin receptor subtype responsible for adiponectin’s vascular protective action and investigate the role of ceramidase activation in adiponectin anti-inflammatory signaling. Methods and Results: Adiponectin significantly reduced tumor necrosis factor (TNF)α–induced intercellular adhesion molecule-1 expression and attenuated TNFα-induced oxidative/nitrative stress in human umbilical vein endothelial cells. These anti-inflammatory actions were virtually abolished by adiponectin receptor 1 (AdipoR1-), but not AdipoR2-, knockdown (KD). Treatment with adiponectin significantly increased neutral ceramidase (nCDase) activity (3.7-fold; P <0.01). AdipoR1-KD markedly reduced globular adiponectin–induced nCDase activation, whereas AdipoR2-KD only slightly reduced. More importantly, small interfering RNA-mediated nCDase-KD markedly blocked the effect of adiponectin on TNFα-induced intercellular adhesion molecule-1 expression. AMP-activated protein kinase-KD failed to block adiponectin-induced nCDase activation and modestly inhibited adiponectin anti-inflammatory effect. In contrast, in caveolin-1 KD (Cav1-KD) cells, >87% of adiponectin-induced nCDase activation was lost. Whereas adiponectin treatment failed to inhibit TNFα-induced intercellular adhesion molecule-1 expression, treatment with sphingosine-1-phosphate or SEW (sphingosine-1-phosphate receptor agonist) remained effective in Cav1-KD cells. AdipoR1 and Cav1 colocalized and coprecipitated in human umbilical vein endothelial cells. Adiponectin treatment did not affect this interaction. There is weak basal Cav1/nCDase interaction, which significantly increased after adiponectin treatment. Knockout of AdipoR1 or Cav1 abolished the inhibitory effect of adiponectin on leukocyte rolling and adhesion in vivo. Conclusions: These results demonstrate for the first time that adiponectin inhibits TNFα-induced inflammatory response via Cav1-mediated ceramidase recruitment and activation in an AdipoR1-dependent fashion.
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“Elevated TNF directly inhibits adiponectin63, arresting muscle protein synthesis and mitochondrial processes64.”
From Sarcopenic obesity in older adults: aetiology, epidemiology and treatment strategies (2018) · cites this paper as [63]
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Metadata
- Authors
- Wang, Y., Wang, X., Lau, W. B., Yuan, Y., Booth, D., Li, J.-J., Scalia, R., Preston, K., Gao, E., Koch, W., & Ma, X.-L.
- Affiliations
- Thomas Jefferson University (US)
- From the Department of Emergency Medicine (Y.W., X.W., W.B.L., Y.Y., J.-J.L., X.-L.M.) and Department of Pathology (D.B.), Thomas Jefferson University, Philadelphia, PA; and Department of Physiology, Cardiovascular Research Center (R.S., K.P.) and Center for Translational Medicine (E.G., W.K.), Temple University, Philadelphia, PA.
- Venue
- Circulation Research
- Published
- 2014-02-28
- Volume
- 114
- Issue
- 5
- Pages
- 792-805
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC3961763
- OpenAlex
- W2081966889
- Cited by
- 104
- References
- 51
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 8 · 2023: 9 · 2022: 9 · 2021: 11 · 2020: 12 · 2019: 7 · 2018: 9 · 2017: 12 · 2016: 11 · 2015: 4 · 2014: 4
- FWCI
- 7.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- The Medicine Forum (submittedVersion)
- Funders
- National Institutes of Health (1s10od010408-01)
- National Heart, Lung, and Blood Institute (T32HL091804, HL 63828, R01HL063828, R01HL096686, P01HL108806, HL-096686)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK096521, R01DK064344)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
- Keywords
- adiponectin, TNF-α, caveolin-1, neutral ceramidase, AdipoR1, AdipoR2, endothelial inflammation, ICAM-1, sphingosine-1-phosphate, AMPK, leukocyte adhesion, vascular inflammation, anti-inflammatory signaling, human umbilical vein endothelial cells
- MeSH terms
- Enzyme Activation, Humans, Tumor Necrosis Factor-alpha, Vasculitis, Signal Transduction, Reactive Oxygen Species, Reactive Nitrogen Species, RNA, Small Interfering, Leukocyte Rolling, Endothelial Cells, Caveolin 1, Adiponectin, Receptors, Adiponectin, Ceramidases, Gene Knockdown Techniques, Human Umbilical Vein Endothelial Cells
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