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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
Open accessAbstract
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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“Unlike HDL from healthy subjects, HDL from patients with CHD, kidney disease or diabetes mellitus have no protective vascular effects or may even cause paradoxical harmful effects [55, 56, 61, 70, 71, 75, 76].”
From HDL cholesterol: reappraisal of its clinical relevance (2017) · cites this paper as [75]
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“…et al. 2009), systemic lupus erythematosus and rheumatoid arthritis (McMahon et al. 2006), scleroderma (Weihrauch et al. 2007), metabolic syndrome (de Souza et al. 2008), diabetes (Persegol et al. 2006; Sorrentino et al. 2010), and CAD (Ansell et al. 2003; Besler et al. 2011; Riwanto et al. 2013).”
BackgroundMethodResultInfluentialSelf-citationRached, F. H., Lhomme, M., Camont, L., Gomes, F. L. T., Dauteuille, C., Robillard, P., Santos, R. D., Lesnik, P., Junior, C. V. S., Chapman, M. J., et al. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2015.05.007 · Cited by 61
High-Density Lipoprotein Mediated Cellular Cholesterol Efflux in Acute Coronary Syndromes
Hafiane, A., Jabor, B., Ruel, I. L., Ling, J., & Genest, J. J. (2013) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2013.09.006 · Cited by 59
Gordon, S. M., Chung, J. H. N., Playford, M. P., Dey, A. K., Sviridov, D. O., Seifuddin, F., Chen, Y., Pirooznia, M., Chen, M. Y., Mehta, N. N., et al. (2018) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2018.09.032 · Cited by 59
Deepening our understanding of HDL proteome
Ronsein, G. E., & Vaisar, T. (2019) · Expert Review of Proteomics · doi:10.1080/14789450.2019.1650645 · Cited by 57
Role of HDL in Those with Diabetes
Santos‐Gallego, C. G., & Rosenson, R. S. (2014) · Current Cardiology Reports · doi:10.1007/s11886-014-0512-5 · Cited by 59
Detrimental Effect of Hypercholesterolemia on High-Density Lipoprotein Particle Remodeling in Pigs
Padró, T., Cubedo, J., Camino-López, S., Béjar, M. T., Ben‐Aicha, S., Mendieta, G., Escolá‐Gil, J. C., Escate, R., Gutiérrez, M., Casaní, L., et al. (2017) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.05.018 · Cited by 57
“As such at a proteomic level, HDL from CAD patients has failed to inhibit endothelial apoptosis likely because of a reduction in clusterin and an increase in apolipoprotein (apo) C-III content (25).”
BackgroundSignal Transduction by HDL: Agonists, Receptors, and Signaling Cascades
Nofer, J. (2014) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-09665-0_6 · Cited by 55
“For instance, the relatively high content of apolipoprotein J (apoJ) in HDL particles obtained from healthy subjects endowed them with important antiatherogenic property to promote endothelial survival by stimulation of the expression of antiapoptotic protein Bcl-XL (Riwanto et al. 2013).”
BackgroundResultHDL Cholesterol, Apolipoproteins, and Cardiovascular Risk in Hemodialysis Patients
Silbernagel, G., Genser, B., Drechsler, C., Scharnagl, H., Grammer, T. B., Stojaković, T., Krane, V., Ritz, E., Wanner, C., & März, W. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013080816 · Cited by 58
High-Density Lipoprotein Carries Markers That Track With Recovery From Stroke
Plubell, D. L., Fenton, A. M., Rosário, S., Bergstrom, P., Wilmarth, P. A., Clark, W. M., Zakai, N. A., Quinn, J. F., Minnier, J., Alkayed, N. J., et al. (2020) · Circulation Research · doi:10.1161/circresaha.120.316526 · Cited by 56
Rocha, N. A., East, C., Zhang, J., & McCullough, P. A. (2017) · Current Atherosclerosis Reports · doi:10.1007/s11883-017-0697-3 · Cited by 54
Tsukamoto, K., Mani, D. R., Shi, J., Zhang, S., Haagensen, D. E., Otsuka, F., Guan, J., Smith, J. D., Weng, W., Liao, R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315986110 · Cited by 55
Protein modification and maintenance systems as biomarkers of ageing
Vanhooren, V., Santos, A. N., Voutetakis, K., Petropoulos, I., Libert, C., Simm, A., Gonos, E. S., & Friguet, B. (2015) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2015.03.009 · Cited by 60
“Recently, Riwanto et al. (2013) reported a higher prevalence f sCLU, a component of HDL, in healthy subjects compared to atients with coronary artery disease suggesting a protective role f sCLU in vascular disease progression (Riwanto et al., 2013).”
BackgroundShao, B., & Heinecke, J. W. (2017) · Expert Review of Proteomics · doi:10.1080/14789450.2018.1402680 · Cited by 55
The emerging role of apolipoprotein C-III: beyond effects on triglyceride metabolism
Luo, M., & Peng, D. (2016) · Lipids in Health and Disease · doi:10.1186/s12944-016-0352-y · Cited by 56
“patients according to the results from enzyme-linked immunosorbent assay method [25] (Table 1) and mass spectrometry [26].”
BackgroundResultApoCIII: A multifaceted protein in cardiometabolic disease
D’Erasmo, L., Costanzo, A. D., Gallo, A., Bruckert, É., & Arca, M. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154395 · Cited by 52
Reciprocal Multifaceted Interaction Between HDL (High-Density Lipoprotein) and Myocardial Infarction
Sposito, A. C., Júnior, J. C. D. L., Moura, F. A., Barreto, J., Bonilha, I., Santana, M., Virginio, V. W., Sun, L., de Carvalho, L. S. F., Soares, A., et al. (2019) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.312880 · Cited by 48
Clusterin and Its Role in Insulin Resistance and the Cardiometabolic Syndrome
Wittwer, J. A., & Bradley, D. P. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.612496 · Cited by 51
Maïga, S. F., Kalopissis, A. D., & Chabert, M. (2013) · Biochimie · doi:10.1016/j.biochi.2013.08.027 · Cited by 53
Therapeutic applications of reconstituted HDL: When structure meets function
Darabi, M., Guillas, I., Goff, W. L., Chapman, M. J., & Kontush, A. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.10.010 · Cited by 51
Advances in the Understanding of Plaque Composition and Treatment Options
Tomey, M. I., Narula, J., & Kovacic, J. C. (2014) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2014.01.042 · Cited by 49
“Recent evidence has highlighted the importance rather of HDL particle number (29,30) and the HDL proteome in predicting risk and plaque progression (31), as well as additional candidate mediators such as HDL-associated lipoprotein-associated phospholipase A2 (32).”
BackgroundThe role of high-density lipoproteins in the regulation of angiogenesis
Tan, J. T. M., Ng, M., & Bursill, C. A. (2015) · Cardiovascular Research · doi:10.1093/cvr/cvv104 · Cited by 49
High-density lipoprotein and inflammation in cardiovascular disease
Connelly, M. A., SHALAUROVA, I. Y., & Otvos, J. D. (2016) · Translational research · doi:10.1016/j.trsl.2016.01.006 · Cited by 46
Harbaum, L., Ghataorhe, P., Wharton, J., Jiménez, B., Howard, L., Gibbs, J. S. R., Nicholson, J. K., Rhodes, C. J., & Wilkins, M. R. (2018) · Thorax · doi:10.1136/thoraxjnl-2018-212144 · Cited by 44
Lipoproteins as Biomarkers and Therapeutic Targets in the Setting of Acute Coronary Syndrome
Rosenson, R. S., Brewer, H. B., & Rader, D. J. (2014) · Circulation Research · doi:10.1161/circresaha.114.302805 · Cited by 45
“The ability of HDL from patients with ACS or stable CAD to inhibit apoptosis is impaired as well.(44) In addition, in patients with a recent MI, the HDL proteome is enriched in inflammatory proteins.”
BackgroundDysfunctional HDL as a Therapeutic Target for Atherosclerosis Prevention
Ossoli, A., Pavanello, C., Giorgio, E., Calabresi, L., & Gomaraschi, M. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180316115726 · Cited by 46
Identification of DKK-1 as a novel mediator of statin effects in human endothelial cells
Pontremoli, M., Brioschi, M., Baetta, R., Ghilardi, S., & Banfi, C. (2018) · Scientific Reports · doi:10.1038/s41598-018-35119-7 · Cited by 46
Yalçınkaya, M., Kerksiek, A., Gebert, K., Annema, W., Sibler, R., Radosavljevic, S., Lütjohann, D., Rohrer, L., & von Eckardstein, A. (2020) · Journal of Lipid Research · doi:10.1194/jlr.ra119000509 · Cited by 45
“For functional validation of our candidate lipids, reconstituted HDLs (rHDLs) were produced by the use of the cholate dialysis method (31, 32).”
MethodSelf-citationKrishnan, S., Huang, J., Lee, H., Guerrero, A., Berglund, L., Anuurad, E., Lebrilla, C. B., & Zivkovic, A. M. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00730 · Cited by 44
Metadata
- 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
- Venue
- Circulation
- Published
- 2013-02-26
- Volume
- 127
- Issue
- 8
- Pages
- 891-904
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- 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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