Cited by 944Cholesterol and Lipid MetabolismLipoproteins and Cardiovascular HealthAtherosclerosis and Cardiovascular Diseases

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Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL

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Vaisar, Tomas, Pennathur, Subramaniam, Green, Pattie S., Gharib, Sina A., Hoofnagle, Andrew N., Cheung, Marian C., Byun, Jaeman, Vuletic, Simona, Kassim, Sean, Singh, Pragya, Chea, Helen, Knopp, Robert H., Brunzell, John, Geary, Randolph, Chait, Alan, Zhao, Xue-Qiao, Elkon, Keith, Marcovina, Santica, Ridker, Paul, Oram, John F., Heinecke, Jay W.·2007·Journal of Clinical Investigation

DOI 10.1172/jci26206PMC PMC1804352

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Abstract

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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BackgroundInfluential
Reconstituted High-Density Lipoprotein Attenuates Cholesterol Crystal–Induced Inflammatory Responses by Reducing Complement Activation
Niyonzima, N., Samstad, E. O., Aune, M. H., Ryan, L., Bakke, S. S., Rokstad, A. M., Wright, S. D., Damås, J. K., Mollnes, T. E., Latz, E., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1403044 · Cited by 37
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Vitamin E therapy results in a reduction in HDL function in individuals with diabetes and the haptoglobin 2-1 genotype
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Albuminuria, the High-Density Lipoprotein Proteome, and Coronary Artery Calcification in Type 1 Diabetes Mellitus
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“In a cross-sectional study of 191 subjects enrolled in the DCCT (Diabetes Control and Complications Trial)/EDIC study (Epidemiology of Diabetes Interventions and Complications), we used isotope dilution tandem mass spectrometry to quantify 46 proteins in HDL. Stringent statistical analysis demonstrated that 8 proteins…”
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Complement activation in polycystic ovary syndrome occurs in the postprandial and fasted state and is influenced by obesity and insulin sensitivity
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Understanding the Exchange of Systemic HDL Particles Into the Brain and Vascular Cells Has Diagnostic and Therapeutic Implications for Neurodegenerative Diseases
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Overexpression of apolipoprotein O does not impact on plasma HDL levels or functionality in human apolipoprotein A-I transgenic mice
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“Interestingly, apoO was not detected in a comprehensive proteomics study aiming at the identification of HDLassociated proteins (7), conceivably because the abundance of this apolipoprotein is low.”
Background
The human HDL proteome displays high inter-individual variability and is altered dynamically in response to angioplasty-induced atheroma plaque rupture
Jorge, I., Burillo, E., Mesa, R., Baila-Rueda, L., Moreno, M., Trevisán-Herraz, M., Silla-Castro, J. C., Camafeita, E., Ortega‐Muñoz, M., Bonzón‐Kulichenko, E., et al. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.04.010 · Cited by 34
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Mapping Atheroprotective Functions and Related Proteins/Lipoproteins in Size Fractionated Human Plasma
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“Several previous studies have detected fibrinogen associated with lipoprotein particles (12, 15, 16, 65, 66), but it is unclear whether the association is specific, or is simply because of the abundance of the fibrinogen complex non-specifically sticking to the lipoprotein particles.”
Background
Shotgun proteomic analysis reveals proteome alterations in HDL of patients with cholesteryl ester transfer protein deficiency
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Good Cholesterol Gone Bad? HDL and COVID-19
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Biological Properties of Apolipoprotein A-I Mimetic Peptides
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Reduction of paraoxonase-1 activity may contribute the qualitative impairment of HDL particles in patients with type 2 diabetes
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“[7] Vaisar T, Pennathur S, Green PS, Gharib SA, Hoofnagle AN, Cheung MC, et al.”
BackgroundMethod
Distribution and determinants of circulating complement factor H concentration determined by a high-throughput immunonephelometric assay
Sofat, R., Mangione, P. P., Gallimore, J. R., Hakobyan, S., Hughes, T. R., Shah, T., Goodship, T. H. J., D’Aiuto, F., Langenberg, C., Wareham, N. J., et al. (2013) · Journal of Immunological Methods · doi:10.1016/j.jim.2013.01.009 · Cited by 34
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Carboxyl-Terminal Cleavage of Apolipoprotein A-I by Human Mast Cell Chymase Impairs Its Anti-Inflammatory Properties
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Development of an MRM assay panel with application to biobank samples from patients with myocardial infarction
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BackgroundResult
HDL structure and function is profoundly affected when stored frozen in the absence of cryoprotectants
Holzer, M., Kern, S., Trieb, M., Trakaki, A., & Marsche, G. (2017) · Journal of Lipid Research · doi:10.1194/jlr.d075366 · Cited by 35
Novel serum paraoxonase activity assays are associated with coronary artery disease
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“On this basis, we speculate that under proatherogenic conditions there could be a compensatory increase of PON1 lactonase activity stimulation by HDL, possibly due to CAD-related changes in HDL composition (40).”
Background
Age-related macular degeneration and coronary heart disease: Evaluation of genetic and environmental associations
Keilhauer, C. N., Fritsche, L. G., Guthoff, R., Haubitz, I., & Weber, B. H. F. (2012) · European Journal of Medical Genetics · doi:10.1016/j.ejmg.2012.10.005 · Cited by 32
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“It is important to recognize that HDL is not a simple complex of apolipoproteins and lipids, but also carries a large number of enzymes, biologically active proteins and miRNAs [3, 4] that regulate various aspects of cellular and systemic metabolism independently from reverse cholesterol transport.”
Background
Computational studies of plasma lipoprotein lipids
Pan, L., & Segrest, J. P. (2016) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2016.03.010 · Cited by 37
Cyclooxygenase-2 Expression, Prostacyclin Production and Endothelial Protection of High-density Lipoprotein
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Cholesteryl Ester Transfer Protein Inhibition in Cardiovascular Risk Management: Ongoing Trials will End the Confusion
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Identification of Critical Paraoxonase 1 Residues Involved in High Density Lipoprotein Interaction
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Paraoxonases
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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: Pennathur, Subramaniam
Gharib, Sina A.
Hoofnagle, Andrew N.
Kassim, Sean
Singh, Pragya
Brunzell, John
Chait, Alan
Elkon, Keith
Marcovina, Santica
Ridker, Paul
Heinecke, Jay W.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2007-03-01
Volume: 117
Issue: 3
Pages: 746-756
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci26206
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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Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL

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