Induction of ATF3 Gene Network by Triglyceride-Rich Lipoprotein Lipolysis Products Increases Vascular Apoptosis and Inflammation
Open accessAbstract
Objective—: Elevation of triglyceride-rich lipoproteins (TGRLs) contributes to the risk of atherosclerotic cardiovascular disease. Our work has shown that TGRL lipolysis products in high physiological to pathophysiological concentrations cause endothelial cell injury; however, the mechanisms remain to be delineated. Approach and Results—: We analyzed the transcriptional signaling networks in arterial endothelial cells exposed to TGRL lipolysis products. When human aortic endothelial cells in culture were exposed to TGRL lipolysis products, activating transcription factor 3 (ATF3) was identified as a principal response gene. Induction of ATF3 mRNA and protein was confirmed by quantitative reverse-transcription polymerase chain reaction and Western blot respectively. Immunofluorescence analysis showed that ATF3 accumulated in the nuclei of cells treated with lipolysis products. Nuclear expression of phosphorylated c-Jun N-terminal kinase (JNK), previously shown to be an initiator of the ATF3 signaling cascade, also was demonstrated. Small interfering RNA (siRNA)–mediated inhibition of ATF3 blocked lipolysis products–induced transcription of E-selectin and interleukin-8, but not interleukin-6 or nuclear factor-κB. c-Jun, a downstream protein in the JNK pathway, was phosphorylated, whereas expression of nuclear factor-κB–dependent JunB was downregulated. Additionally, JNK siRNA suppressed ATF3 and p-c-Jun protein expression, suggesting that JNK is upstream of the ATF3 signaling pathway. In vivo studies demonstrated that infusion of TGRL lipolysis products into wild-type mice induced nuclear ATF3 accumulation in carotid artery endothelium. ATF3 −/− mice were resistant to vascular apoptosis precipitated by treatment with TGRL lipolysis products. Also peripheral blood monocytes isolated from postprandial humans had increased ATF3 expression as compared with fasting monocytes. Conclusions—: This study demonstrates that TGRL lipolysis products activate ATF3-JNK transcription factor networks and induce endothelial cells inflammatory response.
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Sustained production of these cytokines perpetuates vascular inflammation and influences systemic immune responses, linking metabolic dyslipidemia to chronic inflammatory states that exacerbate atherogenesis.
“Moreover, the sustained production of these cytokines not only perpetuates vascular inflammation but also influences systemic immune responses, linking metabolic dyslipidemia to chronic inflammatory states that exacerbate atherogenesis [19–21].”
From Targeting triglycerides for cardiovascular risk reduction (2026) · cites this paper as [19]
The Discussion (page unavailable) reports cytokine induction by triglyceride-rich lipoprotein lipolysis products and concludes that these products can cause vascular inflammation, potentially increasing susceptibility to atherosclerosis. The Results report increased inflammatory gene expression in postprandial blood mononuclear cells. The paper does not establish sustained cytokine production, effects on systemic immune responses, or chronic inflammatory states. (LLM, conf=0.87)
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- Authors
- Aung, H. H., Lame, M. W., Gohil, K., An, C.-I., Wilson, D. W., & Rutledge, J. C.
- Affiliations
- University of California, Davis (US)
- From the Division of Cardiovascular Medicine, Department of Internal Medicine (H.H.A., C.-I.A., J.C.R.), and Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine (K.G.), School of Medicine, University of California, Davis; and Department of Molecular Biosciences (M.W.L.), and Department of Pathology, Microbiology, and Immunology (D.W.W.), School of Veterinary Medicine, University of California, Davis.
- Venue
- Arteriosclerosis, Thrombosis, and Vascular Biology
- Published
- 2013-09
- Volume
- 33
- Issue
- 9
- Pages
- 2088-2096
- ISSN
- 1079-5642 (ISSN-L)
- 1524-4636
- PMC
- PMC3921073
- OpenAlex
- W1972882874
- Cited by
- 86
- References
- 43
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 7 · 2023: 4 · 2022: 8 · 2021: 5 · 2020: 4 · 2019: 7 · 2018: 8 · 2017: 8 · 2016: 10 · 2015: 2 · 2014: 9 · 2013: 1
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Arteriosclerosis Thrombosis and Vascular Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Ohio State University
- National Institute on Aging (NIH-NIA AG039094, R01AG039094, R01AG045541)
- National Heart, Lung, and Blood Institute (R01HL055667, NIH-HL55667)
- National Institute of Diabetes and Digestive and Kidney Diseases (U24DK092993)
- National Institute of Environmental Health Sciences (NIH-ES 011985-02)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- triglyceride-rich lipoproteins, ATF3, JNK signaling, c-Jun phosphorylation, endothelial injury, vascular inflammation, E-selectin, interleukin-8, atherosclerosis
- MeSH terms
- Animals, Cells, Cultured, Enzyme Activation, Fluorescent Antibody Technique, Gene Expression Regulation, Humans, Inflammation, Leukocytes, Mononuclear, Lipolysis, Lipoprotein Lipase, Lipoproteins, Mice, Inbred C57BL, Phosphorylation, RNA, Messenger, Transfection, Triglycerides, Blotting, Western, Interleukin-8, Apoptosis, Mice, Knockout, Inflammation Mediators, E-Selectin, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, RNA Interference, Endothelial Cells, JNK Mitogen-Activated Protein Kinases, Mice, Activating Transcription Factor 3
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