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Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL
Open accessAbstract
HDL lowers the risk for atherosclerotic cardiovascular disease by promoting cholesterol efflux from macrophage foam cells. However, other antiatherosclerotic properties of HDL are poorly understood. To test the hypothesis that the lipoprotein carries proteins that might have novel cardioprotective activities, we used shotgun proteomics to investigate the composition of HDL isolated from healthy subjects and subjects with coronary artery disease (CAD). Unexpectedly, our analytical strategy identified multiple complement-regulatory proteins and a diverse array of distinct serpins with serine-type endopeptidase inhibitor activity. Many acute-phase response proteins were also detected, supporting the proposal that HDL is of central importance in inflammation. Mass spectrometry and biochemical analyses demonstrated that HDL3 from subjects with CAD was selectively enriched in apoE, raising the possibility that HDL carries a unique cargo of proteins in humans with clinically significant cardiovascular disease. Collectively, our observations suggest that HDL plays previously unsuspected roles in regulating the complement system and protecting tissue from proteolysis and that the protein cargo of HDL contributes to its antiinflammatory and antiatherogenic properties.
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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 [56]
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Schittmayer, M., & Birner‐Gruenberger, R. (2009) · Journal of Proteomics · doi:10.1016/j.jprot.2009.05.006 · Cited by 23
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The complement system in lipid-mediated pathologies
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“Modulation of HDL cargo has been observed and reported in many diseases, such as Coronary Heart Disease, Acute Coronary Syndrome, End Stage Renal Disease and Liver Disease (Alwaili et al., 2012; Trieb et al., 2016; Vaisar et al., 2007; Weichhart et al., 2012; Yan et al., 2014).”
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“Several approaches have been developed for lipoprotein isolation (94–97) ; deli-pidation (98,99) ; sample preparation (solubilisation and digestion) (100–103) ; and the characterisation of protein component of lipoproteins using MS (104,105) .”
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“However, using shotgun proteomics it has been demonstrated that C3 and C4 are present on HDL in vivo (8).”
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“the particle composition and biologic properties of HDL have reinforced a need for assessment of HDL function [14].”
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“HDL is a complex mixture of lipoproteins associated with many minor proteins and lipids which influence HDL function [29, 30].”
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Vendrame, F., Olops, L., Saad, S. T. O., Costa, F. F., & Fertrin, K. Y. (2018) · Journal of clinical lipidology · doi:10.1016/j.jacl.2018.08.002 · Cited by 20
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“Prior studies by Vaisar and colleagues have documented the presence of many proteins within HDL that play an important role in lipid metabolism, protease inhibition, complement regulation, the acute-phase reaction, and inflammation [ 16 ].”
Self-citationSacks, F. M., Furtado, J. D., & Jensen, M. K. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2022.159182 · Cited by 19
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“Vaisar et al. reported that HDL is enriched in several proteins involved in the complement cascade, suggesting a role in innate immunity [51].”
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Atherothrombosis and Plaque Heterology: Different Location or a Unique Disease?
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“For example, the protein composition of HDL differs in those with cardiovascular disease compared to those without cardiovascular disease [23].”
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“The majority of these proteins have been previously identified as HDL proteins via other isolation methods [49,50].”
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“This new result from our studies that also points to activation of the complement is consistent with reports on the interaction of C3 with HDL in plasma samples [26].”
BackgroundResultHigh Density Lipoprotein – Should we Raise it?
Landmesser, U. (2012) · Current Vascular Pharmacology · doi:10.2174/157016112803520710 · Cited by 17
“Moreover, HDL is a highly complex lipoprotein that has likely mor e than 70 associated proteins, as identified by proteomics analysis (10) and consists likely of more than 1000 different lipid species (Figure).”
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Self-citationHigh-density lipoprotein metabolism and endothelial function
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“5) Time spent on sport activities (h/week) 0 (0, 2) 1 (0, 2) Time spent cycling (h/week) 1 (0, 3) 1 (0, 3) Time spent walking (h/week) 3 (1, 5) 3 (2, 5) Time spent gardening (h/week) 2 (1, 4) 1 (0, 3) Smoking status Never smoker 477 (20.”
Hepatic Syndecan-1 Changes Associate With Dyslipidemia After Renal Transplantation
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“Although this finding do not prove a direct physical association between syndecan-1 and HDL particles, we speculate that shed syndecan-1 is largely deglycanated and, via core-protein interaction, binds with HDL proteins such as a1-antitrypsin, which, by proteomic analysis, have been found in HDL fractions (49) and bin…”
BackgroundProteomics in Gerontology: Current Applications and Future Aspects – A Mini-Review
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“Vaisar et al. [ 48 ] used LC-MS/MS shotgun proteomics to profile HDL composition.”
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“…such as CAD, diabetes, chronic kidney disease, rheumatoid arthritis, and cardiac surgery (Besler et al., 2011; Honda et al., 2017; Huang et al., 2013; Khine et al., 2017; Li et al., 2020; Miki et al., 2019; O ’ Reilly et al., 2016; Rohatgi et al., 2014; Shao et al., 2014; Vaisar et al., 2007).”
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“Az egyedi funkcionális és összhatás azonban még ismeretlen [24].”
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Native–Native 2D Gel Electrophoresis for HDL Subpopulation Analysis
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“APOE protein is also thought to have a role in atherogenesis (47).”
BackgroundGauthamadasa, K., Vaitinadin, N. S., Dressman, J. L., Macha, S. F., Homan, R., Greis, K. D., & Silva, R. A. G. D. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.291070 · Cited by 16
“Although recent mass spectrometry identifications reported HDL to contain up to 70 different proteins (8, 9), 90% of HDL protein content is made up of two major apolipoproteins (apos), apoA-I and apoA-II.”
BackgroundReconstituted HDL: a therapy for atherosclerosis and beyond
Murphy, A. J., Chin-Dusting, J. P. F., & Sviridov, D. (2009) · Clinical Lipidology · doi:10.2217/clp.09.68 · Cited by 16
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Genetic and Structure-Function Studies of Missense Mutations in Human Endothelial Lipase
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“However, in addition to absolute plasma levels, recent data suggest that the biological functions of HDL are important in assessing the role of HDL in CHD and major cardiovascular events [2,3].”
BackgroundIncreasing High-Density Lipoprotein as a Therapeutic Target in Atherothrombotic Disease
Badimón, J. J., & Ibáñez, B. (2010) · Revista Española de Cardiología (English Edition) · doi:10.1016/s1885-5857(10)70065-7 · Cited by 17
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“[37] Answers to this controversy can only come from designing and developing better and more specific assays of HDL functionality.”
BackgroundClinical proteomics: Current techniques and potential applications in the elderly
Siwy, J., Vlahou, A., Zimmerli, L., Zürbig, P., & Schiffer, E. (2010) · Maturitas · doi:10.1016/j.maturitas.2010.11.001 · Cited by 15
Sontag, T. J., Carnemolla, R., Vaisar, T., Reardon, C. A., & Getz, G. S. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m021154 · Cited by 15
Self-citationPulmonary surfactant protein B carried by HDL predicts incident CVD in patients with type 1 diabetes
Shao, B., Snell‐Bergeon, J. K., Pyle, L. L., Thomas, K. E., de Boer, I. H., Kothari, V. M., Segrest, J. P., Davidson, W. S., Bornfeldt, K., & Heinecke, J. W. (2022) · Journal of Lipid Research · doi:10.1016/j.jlr.2022.100196 · Cited by 15
“and complement regulation (13), suggesting that its”
Self-citationActivation of intracellular signaling systems by high-density lipoproteins
Toth, P. P. (2010) · Journal of clinical lipidology · doi:10.1016/j.jacl.2010.08.011 · Cited by 15
Aragonès, G., Beltrán‐Debón, R., Rull, A., Rodríguez-Sanabria, F., Fernández-Sénder, L., Camps, J., Joven, J., & Alonso‐Villaverde, C. (2010) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2010.218 · Cited by 15
“HDL particles contain a wide array of proteins that mediate these properties, and their binding affinities may depend on HDL particle size and distribution (6).”
BackgroundAlipour, A., van Oostrom, A. J. H. H. M., van Wijk, J. P. H., Verseijden, C., Plokker, H. W. M., Jukema, J. W., Rabelink, T. J., & Cabezas, M. C. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.03.007 · Cited by 15
Importance of high-density lipoprotein quality
Kon, V., Ikizler, T. A., & Fazio, S. (2013) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0b013e32835fe47f · Cited by 15
Cholesterol and cognitive performance among community volunteers from the Czech Republic
Chanti‐Ketterl, M., Andel, R., Lerch, O., Laczó, J., & Hort, J. (2015) · International Psychogeriatrics · doi:10.1017/s1041610215000320 · Cited by 15
Li, B., McIntyre, M. K., Gandhi, C. D., Halabi, M., Long, A., Hoof, A. V., Afridi, A., Schmidt, M. H., Cole, C. D., Santarelli, J. G., et al. (2020) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2020.106062 · Cited by 15
Miarka, P., Idzior−Waluś, B., Kuźniewski, M., Waluś‐Miarka, M., Klupa, T., & Sułowicz, W. (2011) · Clinical and Experimental Nephrology · doi:10.1007/s10157-011-0409-1 · Cited by 16
“ered to be potentially anti-inflammatory and anti-atherogenic [6, 7].”
BackgroundVivanco, F., Mas, S., Dardé, V. M., de la Cuesta, F., Álvarez‐Llamas, G., & Barderas, M. G. (2007) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.200700190 · Cited by 15
Is high HDL cholesterol always good?
OLSSON, A. G. (2008) · Annals of Medicine · doi:10.1080/07853890802609534 · Cited by 15
“HDL is also enriched in several proteins involved in the complement cascade, as well as in a variety of protease inhibitors, supporting the concept that HDL plays a role in innate immunity and in the regulation of proteolytic cascades involved in inflammatory and coagulation processes (11).”
Backgroundde Boer, I. H., & Brunzell, J. D. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2014010062 · Cited by 15
Self-citationPig and Mouse Models of Hyperlipidemia and Atherosclerosis
Getz, G. S., & Reardon, C. A. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-1924-7_24 · Cited by 14
Proteomic and functional analysis of HDL subclasses in humans and rats: a proof-of-concept study
Huang, C., Zhang, J., Huang, J., Li, H., Wen, K., Bao, J., Wu, X., Sun, R., Abudukeremu, A., Wang, Y., et al. (2023) · Lipids in Health and Disease · doi:10.1186/s12944-023-01829-9 · Cited by 14
Guillas, I., Lhomme, M., Pionneau, C., Mathéron, L., Ponnaiah, M., Galier, S., Lebreton, S., Delbos, M., Ma, F., Darabi, M., et al. (2023) · Basic Research in Cardiology · doi:10.1007/s00395-023-01004-2 · Cited by 14
“1 Characterisation of pre-beta-HDL purified from healthy normolipidic subjects.”
Bae, S. S., Chang, L. C., Merkin, S. S., Elashoff, D. A., Ishigami, J., Matsushita, K., & Charles‐Schoeman, C. (2020) · The American Journal of Medicine · doi:10.1016/j.amjmed.2020.07.022 · Cited by 14
“HDL are immunomodulatory particles containing proteins involved in complement activation and the acute inflammatory response (12, 21).”
BackgroundSadana, P., Lin, L., Aghayev, M., Ilchenko, S., & Kasumov, T. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207472 · Cited by 14
“identified albumin as an HDL-associated protein [38-40].”
Wilkens, T. L., Sørensen, H., Jensen, M. K., Furtado, J. D., Dragsted, L. O., & Mukamal, K. J. (2022) · Current Problems in Cardiology · doi:10.1016/j.cpcardiol.2022.101395 · Cited by 14
“18,19,43 On the other hand, the apoE concentration in HDL has been associated with higher CHD risk, 44 and proteomics analyses have shown apoE enrichment of HDL 3 in patients with established CHD compared with controls.”
BackgroundZhang, W., Wang, J., Jia, J., Chen, L., Wu, Z., & Liu, J. (2015) · Journal of Pharmacy & Pharmaceutical Sciences · doi:10.18433/j3531x · Cited by 14
“Although apoA-I is the most abundant protein (roughly 70% of the HDL protein mass) (16) component of HDLs, other apos in HDLs such as apoA-II, apoE also play an essential role in HDL-therapy of coronary artery disease (17, 18).”
BackgroundLeduc, M. S., Blair, R. H., Verdugo, R. A., Tsaih, S., Walsh, K., Churchill, G. A., & Paigen, B. J. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m025833 · Cited by 12
HDL functionality in South Asians as compared to white Caucasians
Bakker, L. E. H., Boon, M. R., Annema, W., Dikkers, A., van Eyk, H. J., Verhoeven, A., Mayboroda, O. A., Jukema, J. W., Havekes, L. M., Meinders, A. E., et al. (2016) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2016.02.010 · Cited by 16
“Recent studies suggest that the HDL proteome is implicated in HDL functionality [29,30].”
HDL: o yin-yang da doença cardiovascular
Leança, C. C., Passarelli, M., Nakandakare, E. R., & Quintão, E. C. R. (2010) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302010000900002 · Cited by 14
The Susceptibility to Diet-Induced Atherosclerosis Is Exacerbated with Aging in C57B1/6 Mice
Simo, O. K., Berrougui, H., Fülöp, T., & Khalil, A. (2021) · Biomedicines · doi:10.3390/biomedicines9050487 · Cited by 13
“In addition, reports of marked heterogeneity in the particle composition and biological properties of HDL pointed to a need for validated assays to measure HDL function [10].”
BackgroundSacks, F. M., & Andraski, A. B. (2021) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000809 · Cited by 13
Rodríguez‐Carrio, J., Alpéri, M., López, P., Pérez-Álvarez, Á. I., Robinson, G., Alonso-Castro, S., Amigó, N., Atzeni, F., & Suárez, A. (2023) · Lara D. Veeken · doi:10.1093/rheumatology/kead009 · Cited by 13
Metadata
- Authors
- Vaisar, T., Pennathur, S., Green, P. S., Gharib, S. A., Hoofnagle, A. N., Cheung, M. C., Byun, J., Vuletic, S., Kassim, S., Singh, P., Chea, H., Knopp, R. H., Brunzell, J., Geary, R., Chait, A., Zhao, X.-Q., Elkon, K., Marcovina, S., Ridker, P., Oram, J. F., & Heinecke, J. W.
- Affiliations
- University of Washington (US)
- Wake Forest University (US)
- Harvard University (US)
- Corresponding author
- Heinecke, Jay W.
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2007-03-01
- Volume
- 117
- Issue
- 3
- Pages
- 746-756
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC1804352
- OpenAlex
- W2083315579
- Cited by
- 942
- References
- 70
- Citations by year
- 2026: 16 · 2025: 20 · 2024: 19 · 2023: 25 · 2022: 36 · 2021: 28 · 2020: 35 · 2019: 36 · 2018: 45 · 2017: 31 · 2016: 51 · 2015: 69 · 2014: 58 · 2013: 81 · 2012: 79
- FWCI
- 79.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Washington (P30ES07033)
- National Institutes of Health (P30ES07033, DK017047)
- National Heart, Lung, and Blood Institute (HL086798, P01HL030086, HL-078527, K08HL074223, HL-57557, HL074223, R01HL086798, R01HL057557, R01HL078527)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK017047, DK 02456, P01DK002456, P30DK017047)
- National Institute of Environmental Health Sciences (P30 ES-07033, P30ES007033)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
- Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
- Keywords
- HDL cholesterol, HDL proteome, complement regulation, serpins, protease inhibition, anti-inflammatory activity, coronary artery disease, HDL3, apolipoprotein E, acute phase proteins, atherosclerosis, cardiovascular disease
- MeSH terms
- Amino Acid Sequence, Chromatography, Liquid, Complement Activation, Coronary Artery Disease, Humans, Inflammation, Lipoproteins, HDL, Microscopy, Electron, Scanning, Molecular Sequence Data, Peptide Hydrolases, Mass Spectrometry, Proteomics, Lipid Metabolism
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