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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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BackgroundInfluentialCholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis
Khera, A. V., Cuchel, M., de la Llera-Moya, M., Rodrigues, A., Burke, M. F., Jafri, K., French, B. C., Phillips, J. A., Mucksavage, M. L., Wilensky, R. L., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1001689 · Cited by 1,943
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“This suggests that the term “HDL” refers to a constellation of distinct protein and lipid constructs that share a similar density (20,21), but may vary widely in function (22), as originally suggested by Alaupovic and colleagues (23).”
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BackgroundHDL and cardiovascular disease: atherogenic and atheroprotective mechanisms
Navab, M., Reddy, S. T., Lenten, B. J. V., & Fogelman, A. M. (2011) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2010.222 · Cited by 666
“With the use of mass-spectrometry-based proteomics, Vaisar and colleagues identified 48 different proteins in HDL isolated from healthy individuals and patients with CHD”
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Bays, H. E., Toth, P. P., Kris-Etherton, P. M., Abate, N., Aronne, L. J., Brown, W. V., Gonzalez-Campoy, J. M., Jones, S. R., Kumar, R., La Forge, R., et al. (2013) · Journal of Clinical Lipidology · doi:10.1016/j.jacl.2013.04.001 · Cited by 521
“The HDL proteome comprises more than 70 distinct proteins.(114) The apoproteins, enzymes, globulins, microribonucleic acids, sphingolipids, and complement components comprising HDL’s proteome confer a remarkable range of biochemical functions to these lipoproteins.”
BackgroundTranslating molecular discoveries into new therapies for atherosclerosis
Rader, D. J., & Daugherty, A. (2008) · Nature · doi:10.1038/nature06796 · Cited by 515
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Biological activities of HDL subpopulations and their relevance to cardiovascular disease
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Duivenvoorden, R., Tang, J., Cormode, D. P., Mieszawska, A. J., Izquierdo‐Garcia, D., Ozcan, C., Otten, M. J., Zaidi, N., Lobatto, M. E., van Rijs, S. M., et al. (2014) · Nature Communications · doi:10.1038/ncomms4065 · Cited by 448
“In addition to HDL’s ability to remove excess cholesterol from atherosclerotic plaques, native HDL also transports proteins involved in inflammation, coagulation, complement activation 27 , and endogenous micro RNAs, and delivers them to recipient cells 28 .”
BackgroundDavidson, W. S., Silva, R. A. G. D., Chantepie, S., Lagor, W. R., Chapman, M. J., & Kontush, A. (2009) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.109.186031 · Cited by 415
High-Density Lipoprotein Modulates Glucose Metabolism in Patients With Type 2 Diabetes Mellitus
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“Although the magnitude of the plasma glucose reduction might be considered modest, it is likely of clinical significance given ( 1 ) that patients were fasted, (2) the short-term nature of the stimulus, and (3) the numerous homeostatic pathways controlling blood glucose.”
Inflammation Impairs Reverse Cholesterol Transport In Vivo
McGillicuddy, F. C., Moya, M. D. L. L., Hinkle, C. C., Joshi, M. R., Chiquoine, E. H., Billheimer, J. T., Rothblat, G. H., & Reilly, M. P. (2009) · Circulation · doi:10.1161/circulationaha.108.810721 · Cited by 392
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“Fewer than half subserve lipid metabolism.(68) Brain cerebrospinal fluid, embryologically equivalent to the subretinal space, also harbors HDL-like lipoproteins containing apoE.”
BackgroundYuana, Y., Levels, J. H. M., Grootemaat, A. E., Sturk, A., & Nieuwland, R. (2014) · Journal of Extracellular Vesicles · doi:10.3402/jev.v3.23262 · Cited by 380
“(10), which shows proteomics of HDL isolated by using KBr-density gradient centrifugation, showed the”
BackgroundSHAH, A. S., Tan, L., Long, J. L., & Davidson, W. S. (2013) · Journal of Lipid Research · doi:10.1194/jlr.r035725 · Cited by 359
“were the first to compare HDL proteomic profiles between normolipidemic subjects and patients with documented coronary artery disease (CAD) (23;75;76).”
InfluentialHigh-density lipoproteins: A consensus statement from the National Lipid Association
Toth, P. P., Barter, P. J., Rosenson, R. S., Boden, W. E., Chapman, M. J., Cuchel, M., D'Agostino, R. B., Davidson, M. H., Davidson, W. S., Heinecke, J. W., et al. (2013) · Journal of Clinical Lipidology · doi:10.1016/j.jacl.2013.08.001 · Cited by 336
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“Similarly, by using TUNEL staining, we observed that HDL Healthy and delipidated HDL Healthy signifi- cantly reduced the number of apoptotic endothelial cells (22.2±8.0% and 19.0±14.1% versus control 37.6±10.2%, P<0.05), that was not observed with apoA-I or rHDL alone (29.0±8.7% and 25.3±10.4%, respectively; P=0.11 an…”
BackgroundInfluentialThe emerging role of HDL in glucose metabolism
Drew, B. G., Rye, K.-A., Duffy, S. J., Barter, P., & Kingwell, B. A. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.235 · Cited by 307
“HDL represents a vehicle for accepting cholesterol, phospholipids and perhaps protein”
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“Indeed, recent proteomic analyses of HDL have revealed the presence of up to 75 distinct proteins.(28,29)”
BackgroundAntiatherogenic function of HDL particle subpopulations: focus on antioxidative activities
Kontush, A., & Chapman, M. J. (2010) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e32833bcdc1 · Cited by 294
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“Furthermore, HDL particles isolated from atherosclerotic lesions were very similar to the ones isolated from CAD patients’ plasma (Vaisar et al., 2007).”
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“HDL particles carry >80 different proteins and hundreds of lipid species.(19,22) Most recently, even microRNAs have been found in HDL particles,(23) although a relevant uptake of microRNAs from HDL into vascular cells was not observed.”
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“…debris (Grindle and Marshall, 1978) or by stress-related basolateral secretion We omit from this section clusterin, a widely expressed, multifunctional 70 kDa glycoprotein whose strong association with plasma HDL earned it the name of apolipoprotein J (de Silva et al., 1990; Vaisar et al., 2007).”
Structure of HDL: Particle Subclasses and Molecular Components
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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].”
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“…provides a logical explanation for why these two apparently distant regions on the APOA1 polypeptide chain support PON1 interaction — they are predicted to be directly adjacent to one another on the two anti-parallel APOA1 chains within HDL (Figures 3 and 7, and Supple-mental Figures 12 and 13).”
InfluentialUremia Alters HDL Composition and Function
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“recently diagnosed with CHD, but not yet treated with statins, have a unique protein cargo, compared to HDL found in healthy control subjects.(365,387) There are many molecular mechanisms through which HDL may become dysfunctional, including changes in protein composition, change in antioxidant activity, overexpressio…”
BackgroundHigh-density lipoproteins, reverse cholesterol transport and atherogenesis
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“For example, in coronary artery disease (CAD) C3 and complement C4 were elevated in the HDL fraction compared to controls while clusterin was reduced, suggesting that under specific conditions the inflammatory profile of HDL particle can change (Vaisar et al., 2007).”
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“Proteomic studies underlined the diversity of HDLassociated proteins in normal conditions [9].”
BackgroundHigh-Density Lipoprotein Particle Size and Concentration and Coronary Risk
Harchaoui, K. E., Arsenault, B. J., Franssen, R., Després, J., Hovingh, G. K., Stroes, E. S. G., Otvos, J. D., Wareham, N. J., Kastelein, J. J. P., Khaw, K., et al. (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-150-2-200901200-00006 · Cited by 231
“In fact, HDL particles were recently shown to carry a wide array of proteins that mediate these properties (6).”
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Chapman, M. J., Redfern, J. S., McGovern, M. E., & Giral, P. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.01.008 · Cited by 227
Urinary Proteomic Biomarkers in Coronary Artery Disease
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“Several groups have reported on the application of proteomics techniques to analyze tissue or plaque specimens to study cardiovascular disease or arteriosclerosis (44-48).”
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“Mass spectrometry studies have revealed that the HDL particles carry a multiplicity of proteins, which not only affect lipid metabolism but are also involved in complement regulation, acute-phase response and proteinase inhibition [19].”
BackgroundLipid parameters for measuring risk of cardiovascular disease
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“The principal apolipoprotein on HDL particles is apo A-I; however, HDL also contains many other components, including apo A-II”
BackgroundTranslation of High-Density Lipoprotein Function Into Clinical Practice
Rosenson, R. S., Brewer, H. B., Ansell, B. J., Barter, P. J., Chapman, M. J., Heinecke, J. W., Kontush, A., Tall, A. R., & Webb, N. R. (2013) · Circulation · doi:10.1161/circulationaha.113.000962 · Cited by 225
“The ability of HDL to promote efflux of cholesterol from macrophages in the artery wall is the best known of the potentially cardioprotective functions of HDL.2 However, HDL particles have additional properties with the potential to protect against vascular disease, some of which are related and others are unrelated t…”
BackgroundMethodInfluentialSelf-citationThe role of dysfunctional HDL in atherosclerosis
Navab, M., Reddy, S. T., Lenten, B. J. V., Anantharamaiah, G. M., & Fogelman, A. M. (2008) · Journal of Lipid Research · doi:10.1194/jlr.r800036-jlr200 · Cited by 222
The HDL hypothesis: does high-density lipoprotein protect from atherosclerosis?
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“Recent proteomics studies have identified between 28 and 67 HDL-associated proteins using liquid chromatography–electro-spray ionization tandem mass spectrometry (LC-ESI-MS/MS) (Davidson et al, 2009; Vaisar et al, 2007).”
McMahon, M. A., Grossman, J. M., Skaggs, B. J., FitzGerald, J. D., Sahakian, L., Ragavendra, N., Charles‐Schoeman, C., Watson, K. E., Wong, W. K., Volkmann, E. R., et al. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24677 · Cited by 216
“in patients with coronary artery disease [34].”
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“We chose proteins, peptides, and transitions based on the shotgun proteomic experiments and a previous study [27].”
BackgroundMethodInfluentialSelf-citationThe Structure of Apolipoprotein A-I in High Density Lipoproteins
Davidson, W. S., & Thompson, T. B. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.r700014200 · Cited by 211
Inflammatory remodeling of the HDL proteome impairs cholesterol efflux capacity
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Self-citationStructure of apolipoprotein A-I in spherical high density lipoproteins of different sizes
Silva, R. A. G. D., Huang, R., Morris, J. C., Fang, J., Gracheva, E. O., Ren, G., Kontush, A., Jerome, W. G., Rye, K., & Davidson, W. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803626105 · Cited by 206
“Furthermore, recent proteomics studies indicate that up to 50 additional proteins can associate with HDL in widely varying abundances (28).”
BackgroundHDL and endothelial protection
Tran‐Dinh, A., Diallo, D., Delbosc, S., Varela, L. M., Dang, Q., Lapergue, B., Burillo, E., Michel, J., Levoye, A., Martı́n-Ventura, J. L., et al. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12174 · Cited by 212
Multiple actions of high-density lipoprotein
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Serum Amyloid A in Uremic HDL Promotes Inflammation
Weichhart, T., Kopecky, C., Kubicek, M., Haidinger, M., Döller, D., Katholnig, K., Suarna, C., Eller, P., Tölle, M., Gerner, C., et al. (2012) · Journal of the American Society of Nephrology · doi:10.1681/asn.2011070668 · Cited by 201
The HDL proteome in acute coronary syndromes shifts to an inflammatory profile
Al-Waili, K., Bailey, D., Awan, Z. A., Bailey, S. D., Ruel, I. L., Hafiane, A., Krimbou, L., LaBoissière, S., & Genest, J. J. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2011.07.013 · Cited by 198
“Contents lists available at ScienceDirect Biochimica et Biophysica Acta j ourna l homepage: www.e lsev ie r.com/ locate /bba l ip The HDL proteome in acute coronary syndromes shifts to an inflammatory profile☆ Khalid Alwaili a,1, Dana Bailey a,⁎,1, Zuhier Awan c, Swneke D. Bailey a, Isabelle Ruel a, Anouar Hafiane a,…”
BackgroundInfluentialAnti-inflammatory and Antioxidant Properties of HDLs Are Impaired in Type 2 Diabetes
Morgantini, C., Natali, A., Boldrini, B., Imaizumi, S., Navab, M., Fogelman, A. M., Ferrannini, E., & Reddy, S. T. (2011) · Diabetes · doi:10.2337/db11-0378 · Cited by 200
Novel methodologies for biomarker discovery in atherosclerosis
Hoefer, I. E., Steffens, S., Ala‐Korpela, M., Bäck, M., Badimón, L., Bochaton‐Piallat, M., Boulanger, C. M., Caligiuri, G., Dimmeler, S., Egido, J., et al. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv236 · Cited by 206
Lipid and Lipoprotein Metabolism
Feingold, K. R. (2022) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2022.02.008 · Cited by 229
High density lipoproteins: Measurement techniques and potential biomarkers of cardiovascular risk
Hafiane, A., & Genest, J. J. (2015) · BBA Clinical · doi:10.1016/j.bbacli.2015.01.005 · Cited by 204
Metabolic and functional relevance of HDL subspecies
Asztalos, B. F., Tani, M., & Schaefer, E. J. (2011) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e3283468061 · Cited by 201
Emerging role of high density lipoproteins as a player in the immune system
Norata, G. D., Pirillo, A., Ammirati, E., & Catapano, A. L. (2011) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2011.06.045 · Cited by 195
Sphingosine 1-phosphate levels in plasma and HDL are altered in coronary artery disease
Sattler, K., Elbasan, Ş., Keul, P., Elter-Schulz, M., Bode, C., Gräler, M. H., Bröcker‐Preuß, M., Budde, T., Erbel, R., Heusch, G., et al. (2010) · Basic Research in Cardiology · doi:10.1007/s00395-010-0112-5 · Cited by 192
“Such modifications comprise enrichment of HDL from CAD patients with a different ‘‘set’’ of proteins than HDL from healthy individuals [ 27 ] as well as biochemical modifications of different HDL constituents [28].”
BackgroundEffects of Dietary Flavonoids on Reverse Cholesterol Transport, HDL Metabolism, and HDL function
Millar, C. L., Duclos, Q., & Blesso, C. N. (2017) · Advances in Nutrition · doi:10.3945/an.116.014050 · Cited by 208
“Much of the biological activity of HDL is due to its protein content, with it carrying >50 distinct proteins with known functions in inflammation, oxidation, protease inhibition, complement regulation, and innate immunity (44).”
BackgroundLaboratory Assessment of HDL Heterogeneity and Function
Movva, R., & Rader, D. J. (2008) · Clinical Chemistry · doi:10.1373/clinchem.2007.101923 · Cited by 190
HDL-mediated mechanisms of protection in cardiovascular disease
Kontush, A. (2014) · Cardiovascular Research · doi:10.1093/cvr/cvu147 · Cited by 198
“Such an anti-elastase action can be related to the presence in HDL of serpin peptidase inhibitors, including alpha-1-antitrypsin.(80)”
BackgroundEffects of curcumin on HDL functionality
Ganjali, S., Blesso, C. N., Banach, M., Pirro, M., Majeed, M., & Sahebkar, A. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.02.008 · Cited by 186
Myeloperoxidase: An Oxidative Pathway for Generating Dysfunctional High-Density Lipoprotein
Shao, B., Oda, M. N., Oram, J. F., & Heinecke, J. W. (2009) · Chemical Research in Toxicology · doi:10.1021/tx9003775 · Cited by 189
“Moreover, recent proteomics studies have revealed that HDL carries proteins that might play a previously unsuspected role in its anti-inflammatory properties (26,27).”
BackgroundSelf-citationAnnema, W., & von Eckardstein, A. (2013) · Circulation Journal · doi:10.1253/circj.cj-13-1025 · Cited by 185
Lecithin:cholesterol acyltransferase: old friend or foe in atherosclerosis?
Kunnen, S., & Eck, M. V. (2012) · Journal of Lipid Research · doi:10.1194/jlr.r024513 · Cited by 181
New insights into the determination of HDL structure by apolipoproteins
Phillips, M. C. (2012) · Journal of Lipid Research · doi:10.1194/jlr.r034025 · Cited by 172
Sattler, K., & Levkau, B. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvp070 · Cited by 179
HDL dysfunction in diabetes: causes and possible treatments
Farbstein, D., & Levy, A. P. (2012) · Expert Review of Cardiovascular Therapy · doi:10.1586/erc.11.182 · Cited by 178
Psoriasis alters HDL composition and cholesterol efflux capacity
Holzer, M., Wolf, P., Ćurčić, S., Birner‐Gruenberger, R., Weger, W., Inzinger, M., El‐Gamal, D., Wadsack, C., Heinemann, Á., & Marsche, G. (2012) · Journal of Lipid Research · doi:10.1194/jlr.m027367 · Cited by 175
HDL biogenesis and functions: Role of HDL quality and quantity in atherosclerosis
Tsompanidi, E. M., Brinkmeier, M. S., Fotiadou, E. H., Giakoumi, S. M., & Kypreos, K. E. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.05.034 · Cited by 171
“[65] Vaisar T, Pennathur S, Green PS, et al.”
The HDL proteome: a marker–and perhaps mediator–of coronary artery disease
Heinecke, J. W. (2008) · Journal of Lipid Research · doi:10.1194/jlr.r800097-jlr200 · Cited by 170
“Our proteomic analyses suggested that apoE was enriched in HDL3 isolated from CAD subjects ( 20 ).”
BackgroundMethodInfluentialSelf-citationSepúlveda, D., Rojas‐Rivera, D., Rodríguez, D. A., Groenendyk, J., Kohler, A., Lebeaupin, C., Ito, S., Urra, H., Carreras‐Sureda, A., Hazari, Y., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2017.12.028 · Cited by 163
Self-citationHigh-density lipoproteins, inflammation and oxidative stress
Tabet, F., & Rye, K. (2008) · Clinical Science · doi:10.1042/cs20080106 · Cited by 165
Host-derived oxidized phospholipids and HDL regulate innate immunity in human leprosy
Cruz, D., Watson, A. D., Miller, C. S., Montoya, D. J., Ochoa, M. T., Sieling, P. A., Gutierrez, M. A., Navab, M., Reddy, S. T., Witztum, J. L., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34189 · Cited by 162
Dysfunctional HDL as a Diagnostic and Therapeutic Target
Smith, J. D. (2009) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.179226 · Cited by 157
Anti‐oxidant properties of high‐density lipoprotein and atherosclerosis
Podrez, E. A. (2010) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2010.05380.x · Cited by 154
“system and complement factors, coagulation and hormone binding.(6,7) In a more recent study, plasma HDL was subfractionated into five physicochemically defined particle subpopulations by isopycnic density gradient ultracentrifugation and the protein composition of the subfractions was assessed by mass spectrometry.”
MethodSoran, H., Hama, S., Yadav, R., & Durrington, P. N. (2012) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e328355ca25 · Cited by 155
Charles‐Schoeman, C., Watanabe, J., Lee, Y. Y., Fürst, D. E., Amjadi, S., Elashoff, D. A., Park, G. S. H., McMahon, M. A., Paulus, H. E., Fogelman, A. M., et al. (2009) · Arthritis & Rheumatism · doi:10.1002/art.24802 · Cited by 150
Rono, M. K., Whitten, M. M. A., Oulad‐Abdelghani, M., Levashina, E. A., & Marois, É. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000434 · Cited by 150
“Interestingly, human HDL has been shown to host a fraction of complement factor C3 [21] as well as trypanosome-killing protein complexes [22].”
BackgroundThe macrophage: the intersection between HIV infection and atherosclerosis
Crowe, S. M., Westhorpe, C. L. V., Mukhamedova, N., Jaworowski, A., Sviridov, D., & Bukrinsky, M. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0809580 · Cited by 149
“, transport of serum amyloid A and complement components by HDL, and accumulation of lipoproteins in the subendothelial space is associated with accumulation of pro- or anti-inflammatory proteins [139, 140].”
BackgroundSuzuki, M., Pritchard, D. K., Becker, L., Hoofnagle, A. N., Tanimura, N., Bammler, T. K., Beyer, R. P., Bumgarner, R. E., Vaisar, T., de Beer, M. C., et al. (2010) · Circulation · doi:10.1161/circulationaha.110.961193 · Cited by 145
Self-citationGordon, S. M., Li, H., Zhu, X., SHAH, A. S., Lu, L. J., & Davidson, W. S. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00213 · Cited by 150
Jensen, M. K., Rimm, E. B., Furtado, J. D., & Sacks, F. M. (2012) · Journal of the American Heart Association · doi:10.1161/jaha.111.000232 · Cited by 142
Hoofnagle, A. N., Becker, J. O., Oda, M. N., Cavigiolio, G., Mayer, P., & Vaisar, T. (2012) · Clinical Chemistry · doi:10.1373/clinchem.2011.173856 · Cited by 140
Self-citationCorrection of HDL Dysfunction in Individuals With Diabetes and the Haptoglobin 2-2 Genotype
Asleh, R., Blum, S., Kalet-Litman, S., Alshiek, J. A., Miller‐Lotan, R., Asaf, R., Rock, W., Aviram, M., Milman, U., Shapira, C., et al. (2008) · Diabetes · doi:10.2337/db08-0450 · Cited by 140
“Hp has been shown by some but not all investigators to be a HDL associated protein (24,27-29).”
BackgroundMethodDelles, C., Schiffer, E., Mühlen, C. V. Z., Peter, K., Rossing, P. R., Parving, H., Dymott, J. A., Neisius, U., Zimmerli, L., Snell‐Bergeon, J. K., et al. (2010) · Journal of Hypertension · doi:10.1097/hjh.0b013e32833d81b7 · Cited by 138
The HDL proteome watch: compilation of studies leads to new insights on HDL function
Davidson, W. S., Shah, A. S., Sexmith, H., & Gordon, S. M. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2021.159072 · Cited by 107
“Interestingly, APOA4 was statistically different in four studies, but two reported higher [98,52] and three reported lower concentrations [97,46].”
BackgroundResultHDL Remodeling During the Acute Phase Response
Jahangiri, A., de Beer, M. C., Noffsinger, V. P., Tannock, L. R., Ramaiah, C., Webb, N. R., van der Westhuyzen, D. R., & de Beer, F. C. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.108.178681 · Cited by 135
High‐density lipoprotein: A potent inhibitor of inflammation
Murphy, A. J., & Woollard, K. J. (2009) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2009.05338.x · Cited by 139
“(apoA-I) exhibiting the potential to carry many other proteins and lipids.(8) ‘‘largely related to inhibition of inflammation’’”
BackgroundYetukuri, L., Söderlund, S., Koivuniemi, A., Seppänen‐Laakso, T., Niemelä, P. S., Hyvönen, M., Taskinen, M., Vattulainen, I., Jauhiainen, M., & Orešič, M. (2010) · Journal of Lipid Research · doi:10.1194/jlr.m006494 · Cited by 134
Trinder, M., Walley, K. R., Boyd, J. H., & Brunham, L. R. (2019) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313381 · Cited by 126
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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