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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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BackgroundCombined Statin and Niacin Therapy Remodels the High-Density Lipoprotein Proteome
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An Immune Response Network Associated with Blood Lipid Levels
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“These results indicate that the nature of the amphipathic helical domains present in the exchangeable apolipoproteins and the protein composition of HDL may be important factors that determine the atherogenic or antiatherogenic properties of HDL (19).”
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Respiratory uncoupling in skeletal muscle delays death and diminishes age-related disease
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“It has been reported as the most abundant protein in HDL isolated from atherosclerotic lesions [89], indicating an important role of apoE in atherosclerosis pathophysiology.”
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“The proteins associated with HDL can be classified in six major categories and include proteins involved in lipid, lipoprotein, and HDL biogenesis and metabolism, acute phase proteins, protease inhibitors, complement regulatory proteins, and a few others (albumin, fibrinogen a chain platelet basic protein) (Vaisar et…”
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BackgroundAltered high-density lipoprotein composition and functions during severe COVID-19
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“[51] took a proteomics approach to profile protein composition of HDL particles isolated from human subjects.”
Antiatherogenic Functionality of High Density Lipoprotein: How Much versus How Gooden-subtitle=
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“This equation normalizes relative protein expression to a value between 21 and +1 [38].”
BackgroundSelf-citationDistinct Proteomic Signatures in 16 HDL (High-Density Lipoprotein) Subspecies
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“proteins are associated with HDL, many of which are related to antiinflammatory and anti-oxidative functions [117,118].”
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“Increased levels of HDL associated complement C3 and HDL associated hemoglobin and haptoglobin were identified in patients with CAD, psoriasis and rheumatoid arthritis [75,80,83,84,86].”
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“Proteomics techniques recently applied to HDL and to the HDL3 subclass of a group of coronary artery disease patients and controls showed significant differences in the distribution of conventional apolipoproteins, acute-phase response proteins, proteinase inhibitors, and members of the complement activation (10).”
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“There is remarkable overlap with a recently reported set of proteins complexed to hDL [30].”
BackgroundHDL and cardiovascular disease
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“have identified 1-antitrypsin in HDL2 and HDL3 fractions (3, 4).”
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“HDL can also function as a transport vehicle for a number of physiologically important proteins identified by proteomic analyses (75, 76).”
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“Insulin resistance often clusters with elevated blood pressure, obesity, central obesity, elevated TG, and low HDL-C.”
BackgroundInfluentialThe role of complement system in adipose tissue-related inflammation
Vlaicu, S. I., Tatomir, A., Boodhoo, D., Vesa, Ș. C., Mircea, P. A., & Rus, H. (2016) · Immunologic Research · doi:10.1007/s12026-015-8783-5 · Cited by 95
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“These include endotoxin [20] complement factors [21] or enzymes such as myeloperoxidase [22,23 ] that if catalytically active can oxidize proteins that then become pro-inflammatory.”
BackgroundReverse Cholesterol Transport Revisited
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Monocyte-to-Macrophage Differentiation
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“For this analysis, the following criteria were used to identify proteins (42): (a) a high peptide identification score according to PeptideProphet (p 0.”
MethodSelf-citationQuantification of HDL Particle Concentration by Calibrated Ion Mobility Analysis
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Self-citationProteomics of Apolipoproteins and Associated Proteins From Plasma High-Density Lipoproteins
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“proteolysis, complement activation, and coagulation, suggesting a key role for HDL cargo in inflammation (1, 89, 109).”
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High-density lipoprotein and the acute phase response
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Apolipoproteins E and CIII interact to regulate HDL metabolism and coronary heart disease risk
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“higher concentrations of apoE in a small and dense subfraction of HDL (HDL3) from 7 patients with CAD compared with HDL3 of 6 healthy controls (37).”
MMP-9 Sheds the β2 Integrin Subunit (CD18) from Macrophages
Vaisar, T., Kassim, S. Y., Gomez, I. G., Green, P. S., Hargarten, S., Gough, P. J., Parks, W. C., Wilson, C. L., Raines, E. W., & Heinecke, J. W. (2008) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m800449-mcp200 · Cited by 91
“LC-MS—Peptides were separated with a 2D LC system (Surveyor HPLC, Thermo Fisher) and then introduced into an ion trap mass spectrometer (Deca XP Plus, Thermo Fisher) using ESI (35).”
MethodSelf-citationRegulation of ABCA1 functions by signaling pathways
Liu, Y., & Tang, C. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.08.015 · Cited by 93
“ApoA-I is found in all serum HDL particles, while the other proteins are found only in some of the particles [5, 6].”
BackgroundThe impact of protein corona on the biological behavior of targeting nanomedicines
Farshbaf, M., Valizadeh, H., Panahi, Y., Fatahi, Y., Chen, M., Zarebkohan, A., & Gao, H. (2022) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2022.121458 · Cited by 95
Progranulin: at the interface of neurodegenerative and metabolic diseases
Nguyen, A. D., Nguyen, T. A., Martens, L. H., Mitic, L. L., & Farese, R. V. (2013) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2013.08.003 · Cited by 90
“However, subsequent studies using several methods of HDL isolation [18] and two proteomic studies [79, 80] did not detect progranulin in human or mouse HDL.”
ResultEnhanced atherogenesis and altered high density lipoprotein in patients with Crohn's disease
van Leuven, S. I., Hezemans, R., Levels, J. H. M., Snoek, S., Stokkers, P. C. F., Hovingh, G. K., Kastelein, J. J. P., Stroes, E. S. G., de Groot, E., & Hommes, D. W. (2007) · Journal of Lipid Research · doi:10.1194/jlr.m700176-jlr200 · Cited by 89
“Simultaneously, HDL protein profiling has emerged as a promising tool to unravel the biochemical composition of HDL (11, 48, 49), with which functional characteristics are intertwined.”
BackgroundJoshi, P. H., Toth, P. P., Lirette, S. T., Griswold, M. E., Massaro, J. M., Martin, S. S., Blaha, M. J., Kulkarni, K. R., Khokhar, A. A., Correa, A., et al. (2014) · European Journal of Preventive Cardiology · doi:10.1177/2047487314543890 · Cited by 91
High-density lipoprotein synthesis and metabolism (Review)
Zhou, L., Li, C., Gao, L., & Wang, A. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3930 · Cited by 94
“In addition to apoAI, several other apolipoproteins (for example, apoAII, apoAIV, apoB, apoCI and apoCII) contribute to the composition of HDL (1-3).”
Yang, M., Yang, Y.-H., Lu, C.-Y., Jong, S.-B., Chen, L.-J., Lin, Y., Wu, S.-J., Chu, P., Chung, T., & Tyan, Y. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.04.017 · Cited by 88
High-density lipoprotein metabolism and the human embryo
Fujimoto, V. Y., Kane, J. P., Ishida, B. Y., Bloom, M. S., & Browne, R. W. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp029 · Cited by 90
“Mass spectrometric analysis has revealed at least 50 protein species in human HDL (Vaisar et al., 2007).”
BackgroundMazur, M. T., Cardasis, H. L., Spellman, D. S., Liaw, A., Yates, N. A., & Hendrickson, R. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910776107 · Cited by 87
“The routine analysis of mixtures of tryptic peptides by tandem mass spectrometry has resulted in the publication of a wide variety of bottom-up applications that include sequence analysis of complete genomes (4, 5) by multidimensional protein identification using strong cation exchange or isoelectric focusing, composi…”
MethodHoofnagle, A. N., Wu, M., Gosmanova, A. K., Becker, J. O., Wijsman, E. M., Brunzell, J. D., Kahn, S. E., Knopp, R. H., Lyons, T. J., & Heinecke, J. W. (2010) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.110.212894 · Cited by 87
Self-citationEdmondson, A. C., Braund, P. S., Stylianou, I. M., Khera, A. V., Nelson, C. P., Wolfe, M. L., DerOhannessian, S. L., Keating, B. J., Qu, L., He, J., et al. (2011) · Circulation Cardiovascular Genetics · doi:10.1161/circgenetics.110.957563 · Cited by 87
Determinants of variation in human serum paraoxonase activity
Rainwater, D. L., Rutherford, S., Dyer, T. D., Rainwater, E., Cole, S. A., VandeBerg, J. L., Almasy, L. A., Blangero, J., MacCluer, J. W., & Mahaney, M. C. (2008) · Heredity · doi:10.1038/hdy.2008.110 · Cited by 86
“2001), though at much reduced levels compared to PON1 (Draganov, 2007; Vaisar et al., 2007).”
InfluentialMorris, G., Puri, B. K., Bortolasci, C. C., Carvalho, A., Berk, M., Walder, K., Moreira, E. G., & Maes, M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.037 · Cited by 84
Qiu, C., Zhao, X., Zhou, Q., & Zhang, Z. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-017-0604-5 · Cited by 89
“HDLs comprise various subspecies and vary widely in particle size, as well as the lipid and protein composition [18].”
BackgroundSelf-citationSequence conservation of apolipoprotein A-I affords novel insights into HDL structure-function
Bashtovyy, D., Jones, M. K., Anantharamaiah, G. M., & Segrest, J. P. (2010) · Journal of Lipid Research · doi:10.1194/jlr.r012658 · Cited by 86
HDL and cholesterol: life after the divorce?
Vickers, K. C., & Remaley, A. T. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r035964 · Cited by 87
Ma, F., Darabi, M., Tubeuf, E., Canicio, A., Lhomme, M., Frisdal, É., Lebreton, S., Mathéron, L., Rached, F. H., Ponnaiah, M., et al. (2019) · European Journal of Preventive Cardiology · doi:10.1177/2047487319894114 · Cited by 88
Shao, B. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.11.011 · Cited by 84
“Moreover, proteins carried by HDL play key roles in the acute-phase response, proteolysis, and the complement system, strongly linking the lipoprotein to modulation of inflammation [53].”
The Effects of Type 2 Diabetes on Lipoprotein Composition and Arterial Stiffness in Male Youth
Gordon, S. M., Davidson, W. S., Urbina, E. M., Dolan, L. M., Heink, A., Zang, H., Lu, L. J., & SHAH, A. S. (2013) · Diabetes · doi:10.2337/db12-1753 · Cited by 86
“proteins across fractions between groups (16).”
The role of complement in atherosclerosis
Haskard, D. O., Boyle, J. J., & Mason, J. C. (2008) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e32830f4a06 · Cited by 81
Higher HDL Cholesterol Is Associated with Better Cognitive Function: the Maine-Syracuse Study
Crichton, G. E., Elias, M. F., Davey, A., Sullivan, K., & Robbins, M. A. (2014) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617714000885 · Cited by 82
“…from the cells, and transports it back to the liver to be disposed through the bile, thereby preventing atherosclerosis and protecting the arteries (Felix-Redondo, Grau, & Fernandez-Berges, 2013), in addition to anti-in fl ammatory (Vaisar et al., 2007) and antioxidant effects (Elsoe et al., 2012).”
Crystal Structures of Cholesteryl Ester Transfer Protein in Complex with Inhibitors
Liu, S., Mistry, A., Reynolds, J. M., Lloyd, D. B., Griffor, M. C., Perry, D. A., Ruggeri, R. B., Clark, R. W., & Qiu, X. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.380063 · Cited by 81
Lehti, S., Nguyen, S. D., Belevich, I., Vihinen, H., Heikkilä, H. M., Soliymani, R., Käkelä, R., Saksi, J., Jauhiainen, M., Grabowski, G. A., et al. (2018) · The American Journal of Pathology · doi:10.1016/j.ajpath.2017.09.019 · Cited by 79
“57 Moreover, immunoglobulins were found to be associated with the extracellular lipoprotein particles, a fi nding suggesting local formation of immunocomplexes, such as those that have been reported for oxidized LDL in human atherosclerotic lesions.”
BackgroundHDL in humans with cardiovascular disease exhibits a proteomic signature
Vaisar, T., Mayer, P. S., Nilsson, E. J., Zhao, X. Q., Knopp, R. H., & Prazen, B. J. (2010) · Clinica Chimica Acta · doi:10.1016/j.cca.2010.03.023 · Cited by 80
“Features were identified using high mass accuracy of the MALDI-TOF spectra and relatively low complexity of HDL proteome (40–60 proteins typically identified in shotgun proteomics analysis) [5] allowed us to target these features in the LC-MALDI-MS/MS experiment.”
BackgroundMethodResultInfluentialSelf-citationStructure/Function Relationships of Apolipoprotein A-I Mimetic Peptides
D’Souza, W., Stonik, J. A., Murphy, A. J., Demosky, S. J., Sethi, A. A., Moore, X. L., Chin-Dusting, J. P. F., Remaley, A. T., & Sviridov, D. (2010) · Circulation Research · doi:10.1161/circresaha.110.216507 · Cited by 80
High-Density Lipoproteins and the Immune System
Kaji, H. (2013) · Journal of Lipids · doi:10.1155/2013/684903 · Cited by 81
Moore, N. H., Costa, L. G., Shaffer, S. A., Goodlett, D. R., & Guizzetti, M. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05836.x · Cited by 77
“2) have been recently reported to be associated with blood high-density lipoprotein and to be implicated in the anti-inflammatory properties of lipoproteins (Vaisar et al. 2007).”
A Macrophage Sterol-Responsive Network Linked to Atherogenesis
Becker, L., Gharib, S. A., Irwin, A. D., Wijsman, E. M., Vaisar, T., Oram, J. F., & Heinecke, J. W. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.01.003 · Cited by 79
Self-citationGourgari, E., Ma, J., Playford, M. P., Mehta, N. N., Goldman, R., Remaley, A. T., & Gordon, S. M. (2019) · Cardiovascular Diabetology · doi:10.1186/s12933-019-0846-9 · Cited by 76
Sphingomyelin in High-Density Lipoproteins: Structural Role and Biological Function
Martínez‐Beamonte, R., Lou-Bonafonte, J. M., Martínez-Gracia, M. V., & Osada, J. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14047716 · Cited by 77
“HDL also transport enzymes such as lecithin–cholesterol acyltransferase (LCAT), paraoxonase 1 and 3 and platelet-activating factor acetylhydrolase, and proteins involved in regulating the complement system and protecting tissue from proteolysis [1].”
Background
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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