Cited by 339Atherosclerosis and Cardiovascular DiseasesCholesterol and Lipid MetabolismCell death mechanisms and regulation

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Altered Activation of Endothelial Anti- and Proapoptotic Pathways by High-Density Lipoprotein from Patients with Coronary Artery Disease: Role of High-Density Lipoprotein–Proteome Remodeling

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Riwanto, Meliana, Rohrer, Lucia, Roschitzki, Bernd, Besler, Christian, Mocharla, Pavani, Mueller, Maja, Perisa, Damir, Heinrich, Kathrin, Altwegg, Lukas, von Eckardstein, Arnold, Lüscher, Thomas F., Landmesser, Ulf·2013·Circulation

DOI 10.1161/circulationaha.112.108753

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Abstract

Background—: Endothelial dysfunction and injury are thought to play an important role in the progression of coronary artery disease (CAD). High-density lipoprotein from healthy subjects (HDL Healthy ) has been proposed to exert endothelial antiapoptotic effects that may represent an important antiatherogenic property of the lipoprotein. The present study therefore aimed to compare effects of HDL CAD and HDL Healthy on the activation of endothelial anti- and proapoptotic pathways and to determine which changes of the lipoprotein are relevant for these processes. Methods and Results—: HDL was isolated from patients with stable CAD (HDL sCAD ), an acute coronary syndrome (HDL ACS ), and healthy subjects. HDL Healthy induced expression of the endothelial antiapoptotic Bcl-2 protein Bcl-xL and reduced endothelial cell apoptosis in vitro and in apolipoprotein E–deficient mice in vivo. In contrast, HDL sCAD and HDL ACS did not inhibit endothelial apoptosis, failed to activate endothelial Bcl-xL, and stimulated endothelial proapoptotic pathways, in particular, p38-mitogen-activated protein kinase–mediated activation of the proapoptotic Bcl-2 protein tBid. Endothelial antiapoptotic effects of HDL Healthy were observed after inhibition of endothelial nitric oxide synthase and after delipidation, but not completely mimicked by apolipoprotein A-I or reconstituted HDL, suggesting an important role of the HDL proteome. HDL proteomics analyses and subsequent validations and functional characterizations suggested a reduced clusterin and increased apolipoprotein C-III content of HDL sCAD and HDL ACS as mechanisms leading to altered effects on endothelial apoptosis. Conclusions—: The present study demonstrates for the first time that HDL CAD does not activate endothelial antiapoptotic pathways, but rather stimulates potential endothelial proapoptotic pathways. HDL-proteome remodeling plays an important role for these altered functional properties of HDL. These findings provide novel insights into mechanisms leading to altered vascular effects of HDL in coronary disease.

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BackgroundSelf-citation
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Background
Sports and HDL-Quality Reflected By Serum Amyloid A and Surfactant Protein B
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Method
Apolipoprotein Profiles in Very Preterm and Term‐Born Preschool Children
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“In another study, HDL particles with high apolipoprotein C-III content stimulated endothelial pro-apoptotic pathways.(46) Finally, apolipoprotein C-III exerts several proatherogenic properties independent of lipid metabolism.”
Background
Apolipoproteins in circulation: At the interface of thrombosis and stroke initiation
Etuzé, T., Vivien, D., & Dubois, F. (2025) · Progress in Lipid Research · doi:10.1016/j.plipres.2025.101343 · Cited by 6
High-density lipoproteins negatively regulate innate immunity and facilitate red-spotted grouper nervous necrosis virus entry via scavenger receptor B type 1
Han, H., Wang, Y., Xu, S., Han, C., Qin, Q., & Wei, S. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.06.126 · Cited by 5
Modern Concepts of the Role of Fine Particles (PM 2.5) in the Genesis of Atherosclerosis and Myocardial Damage: Clinical and Epidemiological Data, the Main Pathophysiological Mechanisms
Chaulin, A. M., & Сергеев, А. К. (2022) · Current Cardiology Reviews · doi:10.2174/1573403x18666220817103105 · Cited by 5
“Specific antiatherogenic effects of HDLs that are impaired by the effect of PM 2.5 include restricting the transport of excess cholesterol to the subendothelial space and macrophages, increasing the breakdown of oxidized phospholipids and ox-LDLs, and inhibiting LDLs oxidation [77, 78].”
BackgroundInfluential
The Complexity of High-Density Lipoproteins
Asztalos, B. F., Tani, M., & Ishida, B. Y. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-407867-3.00003-2 · Cited by 5
Changes in circulating ApoJ-Glyc levels in patients with suspected acute coronary syndrome: The EDICA trial
Kaski, J. C., Lluch, N., López-Sendón, J. L., Gorog, D. A., Antorrena, I., y, P. A., Herrero, P., Sionís, A., González‐Juanatey, J. R., Íñiguez, A., et al. (2023) · International Journal of Cardiology · doi:10.1016/j.ijcard.2023.131291 · Cited by 5
HDL and Endothelium
Maranhão, R. C., Filho, A. C. M., Sigal, G. A., Chagas, A. C. P., & da Luz, P. L. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812348-5.00022-2 · Cited by 5
The role of LDL-bound apoJ in the development of atherosclerosis
Rull, A., Ordóñez‐Llanos, J., & Sánchez‐Quesada, J. L. (2015) · Clinical Lipidology · doi:10.2217/clp.15.21 · Cited by 5
Hyperlipidaemia and cardiovascular disease
Nofer, J. (2013) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e3283638c5e · Cited by 5
HDL Are Host Defense Lipoproteins
von Eckardstein, A., & Robert, J. (2026) · Circulation Research · doi:10.1161/circresaha.126.327426 · Cited by 5
Embryotoxicity of statins and other prescribed drugs with reported off-target effects on cholesterol biosynthesis
Hartley, T., Abdelmagid, H., Abdulsalam, Z., Mansion, A., Howe, E., Ramirez, D., White, K., & Tadjuidje, E. (2024) · Reproductive Toxicology · doi:10.1016/j.reprotox.2024.108820 · Cited by 4
Lipoprotein dysfunction in patients with chronic kidney disease (CKD). Pathogenesis and treatment of CKD dyslipidemia (literature review)
Ермоленко, В. М. (2024) · Nephrology (Saint-Petersburg) · doi:10.36485/1561-6274-2024-28-1-13-29 · Cited by 6
Pleiotropic functions and clinical importance of circulating HDL-PON1 complex
Mahrooz, A. (2024) · Advances in clinical chemistry · doi:10.1016/bs.acc.2024.04.003 · Cited by 4
Uncovering the role of apolipoprotein C-III in insulin resistance
Aguilar-Recarte, D., Palomer, X., & Vázquez‐Carrera, M. (2021) · Clínica e Investigación en Arteriosclerosis (English Edition) · doi:10.1016/j.artere.2021.04.002 · Cited by 4
Adverse effects on macrophage lipid transport and survival by high density lipoprotein from patients with coronary heart disease
Sini, S., Damayanthi, D., Harikrishnan, S., & Jayakumari, N. (2018) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22192 · Cited by 4
Tackling Residual Atherosclerotic Risk in Statin-Treated Adults: Focus on Emerging Drugs
Takata, K., & Nicholls, S. J. (2018) · American Journal of Cardiovascular Drugs · doi:10.1007/s40256-018-0312-1 · Cited by 4
High-density lipoproteins
Sparks, C. E., Corsetti, J. P., & Sparks, J. D. (2014) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000079 · Cited by 4
The Application of Proteomic Techniques in the Study of HDL Particle Characterization and Biomarker Discovery
Burillo, E., Jorge, I., Martínez-López, D., Camafeita, E., Vázquez, J., & Martı́n-Ventura, J. L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-812513-7.00011-2 · Cited by 3
Novel Associations between Related Proteins and Cellular Effects of High-Density Lipoprotein
Choi, S., Park, Y. E., Cheon, E. J., Kim, K. Y., Kim, M., Ann, S.-J., Noh, H.-M., Lee, J., Lee, C. J., Lee, S., et al. (2019) · Korean Circulation Journal · doi:10.4070/kcj.2019.0195 · Cited by 3
High-density lipoproteins at the interface between central nervous system and plasma lipoprotein metabolism
Robert, J., Cheng, W. H., Hayat, A., Ward-Able, T., & Wellington, C. L. (2015) · Clinical Lipidology · doi:10.2217/clp.14.64 · Cited by 3
Atheromarkers of high-density lipoproteins. Part II. Impairments in the composition, structure, and functions of high-density lipoproteins as both the cause of their atherogenic properties and their atheromarkers: a review of literature
Nv, P. (2017) · Russian Journal of Preventive Medicine · doi:10.17116/profmed201720437-44 · Cited by 3
“Однако было показано, что обогащение апоС-III ЛВП, но сопровождающееся сниженным содержанием кластеров этого апопротеина при КБС, связано со сниженной антиапоптотической активностью в отношении эндотелия [16].”
Investigation of dysfunctional HDL using myeloperoxidase / paraoxonase ratio in lymphoma
Neşeli̇oğlu, S., Pekcan, G., Gök, G., Yurt, E. F., & Erel, Ö. (2019) · Harran Üniversitesi Tıp Fakültesi Dergisi · doi:10.35440/hutfd.579011 · Cited by 3
“anti-oxidative activity and cholesterol efflux capacity (28-35).”
Role of biological markers in stem cell aging and its implications in therapeutic processes
Sittadjody, S., Ali, A., Thangasamy, T., Akila, M., Kumaran, R., & Opara, E. C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820071-1.00010-4 · Cited by 4
Deciphering the association of cholesteryl ester transfer protein (CETP) gene polymorphisms with high-density lipoprotein cholesterol (HDL-c) levels in the Bangladeshi population
Saiedullah, M., Nila, N. N., Mahmud, Z., Tamanna, S., Hassan, M. Z., & Howlader, M. Z. H. (2025) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2025.101992 · Cited by 3
“…to be reverse cholesterol transport (RCT) [15,16]; however, other functions, including nitric oxide promotion and endothelial function enhancement [17] and antioxidative, anti-inflammatory [18], antithrombotic [17] and antiapoptotic [19] effects, have a profound impact on the vascular system.”
HDL remodeling and enrichment with apoCIII and apoE in Indigenous Australians
Kockx, M., Wang, J., Howard, N. J., Suryawanshi, A., Nicholls, S. J., Brown, A., & Kritharides, L. (2025) · Journal of clinical lipidology · doi:10.1016/j.jacl.2025.08.006 · Cited by 2
Apolipoprotein CIII in statin-treated type 2 diabetic patients: Its implications for plaque progression and instability: The pre-specified analysis from the OPTIMAL randomized controlled trial
Kitahara, S., Kataoka, Y., Nicholls, S. J., Funabashi, S., Nakatsuka, K., Nishimura, K., Makino, H., Matsubara, M., Matsuo, M., Omura‐Ohata, Y., et al. (2025) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2025.120470 · Cited by 2
How can cholesterol efflux capacity be used as a risk factor for atherosclerotic cardiovascular disease?
Ogura, M. (2025) · Expert Review of Cardiovascular Therapy · doi:10.1080/14779072.2025.2569403 · Cited by 2
“More broadly, proteomic analyses [26] have identified both FABP5 and ORM1 as molecules that may mechanistically contribute to impaired cholesterol efflux.”
Cardiovascular Benefits of Air Purification in Children: Comprehensive Insights from a Randomized, Double-Blind, Crossover Trial
Xue, X., Fang, J., Li, Q., Zhu, Y., Zhou, L., Lei, J., Ding, R., Liu, Y., Sun, Q., Du, Y., et al. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c06712 · Cited by 3
Insights to HDL dysfunctionality: hypothesis of exhausted HDL
Mahrooz, A. (2026) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2026.113145 · Cited by 2
Associations between neutrophil-to-high-density lipoprotein cholesterol ratio and albuminuria: A cross-sectional study
Pang, P., Wang, J., Wu, J., & Lin, K. (2026) · Journal of International Medical Research · doi:10.1177/03000605261416749 · Cited by 2
“55 HDL-C plays a critical role in protecting vascular endothelial cells.”
HDL, heart disease, and the lung
Frey, K., & von Eckardstein, A. (2022) · Journal of Lipid Research · doi:10.1016/j.jlr.2022.100217 · Cited by 2
Over-expression of Apolipoprotein J Inhibits Cholesterol Crystal-Induced Inflammatory Responses via Suppressing NLRP3 Inflammasome Activation in THP-1 Macrophages
Li, Y. W., Song, Y.-Q., Zhang, Y., Liu, T., & Qin, Q. (2021) · Folia Biologica · doi:10.14712/fb2021067050183 · Cited by 3
“Several studies have found that the concentration of serum ApoJ in patients with coronary heart disease was significantly higher than that in the control group, suggesting that ApoJ, as a component of HDLs, may play a role in protection against the progression of atherosclerotic diseases (Poulakou et al., 2008; Riwant…”
Lipid Profiles Impact on the Oncologic Outcome of Upper Tract Urothelial Carcinoma
Tu, K.-Y., Li, C., Li, W., Yeh, H., Ke, H., Wu, W., Chien, T., Wen, S., Wang, Y., & Lee, H.-Y. (2024) · World Journal of Oncology · doi:10.14740/wjon1800 · Cited by 2
Associations of an HDL apolipoproteomic index with cardiometabolic risk factors before and after exercise training in the HERITAGE Family Study
Maravi, J. S. M., Leszczynski, E. C., Schwartz, C. S., Dev, P. K., Barber, J. L., Reasons, R. J., Pearce, R. W., McPhaul, M. J., Konrad, R. J., Robbins, J., et al. (2024) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2024.117587 · Cited by 2
Revising the high-density lipoprotein targeting strategies – Insights from human and preclinical studies
Nesan, D., & Ng, D. S. (2014) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2014.937523 · Cited by 2
Protection Against Ischemia/Reperfusion Injury by High-Density Lipoprotein and Its Components
Fogelman, A. M., Reddy, S. T., & Navab, M. (2013) · Circulation Research · doi:10.1161/circresaha.113.302943 · Cited by 2
Influence of exercise training on HDL function
Adams, V., & Erbs, S. (2014) · Clinical Lipidology · doi:10.2217/clp.14.34 · Cited by 2
A Novel Biomarker Approach to Exploit HDL for Risk Assessment
von Eckardstein, A. (2019) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2019.02.040 · Cited by 2
Apolipoprotein and sphingolipid measurements: Can be used in the clinical practice of atrial fibrillation diagnosing and evaluating the cryoablation effectiveness?
Bielawiec, P., Harasim‐Symbor, E., Gołaszewska, K., Chabowski, A., Hodun, K., & Sztolsztener, K. (2025) · PLoS ONE · doi:10.1371/journal.pone.0315905 · Cited by 1
Improvements in cholesterol efflux capacity of HDL after bariatric surgery in patients with obesity: a meta-analysis
Jamialahmadi, T., Mirhadi, E., Reiner, Ž., Ahmad, S., Sheeha, B. H. B., Rab, S. O., Almahmeed, W. A., & Sahebkar, A. (2025) · BMC Surgery · doi:10.1186/s12893-025-03233-9 · Cited by 1
“This alteration is significant as similar changes in apoC-III and apoJ have been observed in HDL from patients with coronary artery disease [35].”
Dusty Punch Cards and an Eternal Enigma: High-Density Lipoproteins and Atherosclerosis
Kleber, M. E., Grammer, T. B., Kassner, U., Silbernagel, G., & März, W. (2014) · Drugs · doi:10.1007/s40265-014-0189-5 · Cited by 1
Ersonified diagnostic and correction dyslipidemia approach by profiling of apolipoproteins
Kachkovsky, M. A., Vvedenskaya, I. P., Vvedensky, V. Y., Supilnikov, A. A., Ponomareva, J. V., & Milyakova, M. N. (2020) · Bulletin of the Medical Institute REAVIZ (REHABILITATION DOCTOR AND HEALTH) · doi:10.20340/vmi-rvz.2020.4.11 · Cited by 1

Authors: Riwanto, M., Rohrer, L., Roschitzki, B., Besler, C., Mocharla, P., Mueller, M., Perisa, D., Heinrich, K., Altwegg, L., von Eckardstein, A., Lüscher, T. F., & Landmesser, U.
Affiliations: University of Zurich (CH)
From Cardiology, Cardiovascular Center, University Hospital Zurich, Switzerland (M.R., C.B., P.M., M.M., K.H., L.A., T.F.L., U.L.); Cardiovascular Research, Institute of Physiology, University of Zurich, Switzerland (M.R., C.B., P.M., K.H., L.A., T.F.L., U.L.); Center for Integrative Human Physiology, University of Zurich, Switzerland (M.R., L.R., C.B., L.A., A.v.E., T.F.L., U.L.); Institute of Clinical Chemistry, University Hospital Zurich, Switzerland (L.R., A.v.E.); and Functional Genomics Center...
ORCID: Rohrer, Lucia
Roschitzki, Bernd
Besler, Christian
Heinrich, Kathrin
Lüscher, Thomas F.
Landmesser, Ulf
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2013-02-26
Volume: 127
Issue: 8
Pages: 891-904
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/circulationaha.112.108753
OpenAlex: W2769328074
Cited by: 337
References: 58
Citations by year: 2026: 8 · 2025: 10 · 2024: 10 · 2023: 11 · 2022: 25 · 2021: 22 · 2020: 19 · 2019: 35 · 2018: 30 · 2017: 29 · 2016: 26 · 2015: 42 · 2014: 41 · 2013: 29
FWCI: 25.46
Type: journal article
Language: en
Open access: green
www.zora.uzh.ch
Licence: other-oa
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
Zurich Open Repository and Archive (University of Zurich)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Keywords: high-density lipoprotein, coronary artery disease, endothelial cell apoptosis, Bcl-xL, tBid, p38 MAPK, clusterin, apolipoprotein C-III, HDL proteome, endothelial dysfunction, acute coronary syndrome, ApoE-deficient mice, nitric oxide synthase, anti-apoptotic pathways
MeSH terms: Animals, Apolipoproteins E, Coronary Artery Disease, Endothelium, Vascular, Female, Flow Cytometry, Humans, Lipoproteins, HDL, Male, Mice, Inbred C57BL, Middle Aged, Signal Transduction, Apoptosis, Mice, Knockout, Proteome, Mice

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Altered Activation of Endothelial Anti- and Proapoptotic Pathways by High-Density Lipoprotein from Patients with Coronary Artery Disease: Role of High-Density Lipoprotein–Proteome Remodeling

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