J Nutrigenet Nutrigenomics 2014;7:48–60 DOI: 10.1159/000363137 Received: October 15, 2013 Accepted after revision: April 18, 2014 Published online: July 4, 2014

© 2014 S. Karger AG, Basel 1661–6499/14/0071–0048$39.50/0 www.karger.com/jnn

Original Paper

Effect of an Isoenergetic Traditional Mediterranean Diet on the High-Density Lipoprotein Proteome in Men with the Metabolic Syndrome Caroline Richard a Patrick Couture a Sophie Desroches a Benjamin Nehmé b Sylvie Bourassa b Arnaud Droit b Benoît Lamarche a a

Institute of Nutrition and Functional Foods, Laval University, and b Proteomics Platform, CHU de Quebec Research Center, Quebec City, Que., Canada

Key Words Diet · High-density lipoprotein · Proteome · Metabolic syndrome · Functionality Abstract Background/Aims: The objective of this preliminary study was to examine the impact of the Mediterranean diet (MedDiet) on the high-density lipoprotein (HDL) proteome in men with the metabolic syndrome (MetS). Methods: Twenty-six men with the MetS first consumed a standardized baseline North American isoenergetic control diet (5 weeks) and then consumed an isoenergetic MedDiet (5 weeks), both in full feeding condition. The HDL fraction was isolated by ultracentrifugation at the end of each diet and the HDL proteome assessed by isobaric tags for relative and absolute quantitation and mass spectrometry. Results: Of all proteins identified within HDL, only 3 showed significant changes in relative abundance after the MedDiet versus the control diet, including a reduction in inflammation-related inter-α-trypsin inhibitor heavy chain H4 (fold change: 0.62) and hemoglobin subunits α (fold change: 0.40) and β (fold change: 0.46). Other HDL-bound proteins associated with functions related to lipid metabolism/cholesterol homeostasis, oxidation, coagulation, complement activation and immunity were unchanged after consumption of the MedDiet for 5 weeks. Conclusions: Changes in the HDL proteome may explain, at least partly, the well-known anti-inflammatory effect ascribed to the MedDiet. Otherwise, short-term consumption of the MedDiet seems to have little impact on other features of the HDL proteome in men with the MetS. © 2014 S. Karger AG, Basel

Benoît Lamarche Institute of Nutrition and Functional Foods Laval University, 2440 Boulevard Hochelaga Quebec, QC G1V 0A6 (Canada) E-Mail Benoit.Lamarche @ fsaa.ulaval.ca

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The study is registered at ClinicalTrial.gov, registration No. NCT00988650; http://clinicaltrials.gov/ct2/ show/NCT00988650?term=NCT00988650&rank=1.

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J Nutrigenet Nutrigenomics 2014;7:48–60 DOI: 10.1159/000363137

© 2014 S. Karger AG, Basel www.karger.com/jnn

Richard et al.: Effect of an Isoenergetic Traditional Mediterranean Diet on the HighDensity Lipoprotein Proteome in Men with the Metabolic Syndrome

Background

Reduced high-density lipoprotein cholesterol (HDL-C) concentrations are associated with an increased coronary heart disease (CHD) risk [1]. While the low-HDL-C phenotype may explain part of the increased CHD risk seen in the metabolic syndrome (MetS), it has been proposed that HDL functionality may be a better predictor of CHD risk than plasma HDL-C concentrations per se [2, 3]. Indeed, HDL has been shown to exert several biological activities including anti-oxidative [4], anti-inflammatory [2] and anti-thrombotic activities [5] as well as regulation of the immune response and the complement system [6]. Perturbations in these anti-atherogenic functions of HDL may also contribute to the risk of CHD in patients with low HDL-C concentrations such as obese and MetS patients. Adherence to the Mediterranean diet (MedDiet) has been shown to have little impact on plasma HDL-C concentrations [7–9]. We have also shown recently that consumption of the MedDiet in the absence of weight loss had no effect on the rate of clearance and production of apolipoprotein (apo)A-I, the protein moiety of HDL [10]. To our knowledge, no study has yet investigated the impact of the MedDiet on the HDL proteome as a surrogate for numerous anti-atherogenic functions of HDL. In this study, we provide preliminary data examining how consumption of the MedDiet versus a control North American diet impacts the HDL proteome in men with the MetS. We hypothesized that the consumption of an isoenergetic MedDiet, despite having no mean effect on HDL-C concentrations, leads to significant alterations in proteins related to anti-inflammatory and anti-oxidant functions of HDL.

Methods

Study Design and Isoenergetic Experimental Diets In this fixed-sequence study, the participants’ diet was first standardized to a control diet reflecting current averages in macronutrient intake in North American men [12]. Food was provided under isoenergetic conditions over a 5-week period to maintain a constant body weight. This controlled lead-in feeding period was included in the protocol to minimize inter-individual variations attributed to each participant’s usual diet. The participants were then fed a MedDiet (5 weeks) that was formulated to be concordant with characteristics of the traditional Mediterranean eating pattern, again in isoenergetic conditions to maintain the body weight constant [13]. Seven-day menus and daily servings of various food categories for the control diet and the MedDiet were developed for the study and have been described previously [8]. The mean nutritional compositions of the control diet and the MedDiet are presented in table 1. All meals, foods and beverages including red wine were provided to the participants at the clinical investigation unit of the Institute of Nutrition and Functional Foods. Most of the men ate their lunch (40% of daily energy intake) at the clinical investigation unit and dinners and breakfasts at home. The participants were instructed to consume only the meals provided and to report any deviation from the prescribed protocol on checklists. The use of vitamin supplements, anti-inflammatory medications (NSAIDs) and natural health products was strictly forbidden during the entire experimental period. None of the subjects was on lipidlowering or hypertension medication prior to being enrolled in the study. Medication without anti-inflammatory effect (e.g. acetaminophen) was provided to participants if needed, except during the 3 days prior to

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Population Details of the study design have previously been provided [8]. Briefly, 29 men with the MetS according to NCEP-ATP III [11] were recruited for the study. The participants were nonsmokers, had no history of CHD or type 2 diabetes, and were not using lipid-lowering or anti-hypertensive medication. Their body weight had to have been stable for at least 6 months prior to the start of the study. The use of vitamin supplements or natural health products and an aversion to specific components of the MedDiet were exclusion criteria. The study procedures were approved by the Research Ethics Committee of Laval University, and written informed consent was obtained from all participants prior to their enrolment in the study.

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DOI: 10.1159/000363137

Richard et al.: Effect of an Isoenergetic Traditional Mediterranean Diet on the HighDensity Lipoprotein Proteome in Men with the Metabolic Syndrome

Table 1. Mean nutritional composition of the control diet and the MedDiet

Control diet Energy, kJ Lipids, g/day SFA, g/day MUFA, g/day PUFA, g/day TFA, g/day Cholesterol, mg/day Carbohydrates, g/day Total fibers, g/day Soluble fibers, g/day Proteins, g/day Alcohol, g/day Sodium, mg/day

13,179 ± 1,936 119.0 ± 17.5 45.5 ± 6.7 46.0 ± 6.8 18.2 ± 2.7 7.0 ± 1.0 414.1 ± 60.8 380.9 ± 56.0 25.2 ± 3.7 9.2 ± 1.4 133.8 ± 19.7 9.0 ± 1.3 4,406 ± 647

MedDiet (–) (34.0%) (13.0%) (13.2%) (5.2%) (2.0%) (–) (48.4%) (–) (–) (17.0%) (2.0%) (–)

13,270 ± 1,856 112.7 ± 15.8 23.7 ± 3.3 63.8 ± 8.9 16.7 ± 2.3 1.2 ± 0.2 367.3 ± 51.4 396.4 ± 55.5 53.6 ± 7.5 15.4 ± 2.2 134.7 ± 18.8 22.7 ± 3.2 3,853 ± 539

p (–) (32.0%) (6.7%) (18.1%) (4.7%) (0.3%) (–) (50.0%) (–) (–) (17.0%) (5.0%) (–)

0.506 90% (41/44) of the proteins identified within the HDL fraction. The absence of a mean change in proteins related to lipid and cholesterol metabolism in the whole study sample is not entirely surprising, since the mean plasma HDL-C concentrations were also unchanged after consumption of the MedDiet for 5 weeks [10]. Despite the well-characterized anti-oxidant [23] and anti-thrombotic properties [24] of some of its specific components such as virgin olive oil, short-term consumption of the MedDiet had no apparent impact on the proteins related to blood coagulation and anti-oxidant activities within the HDL fraction. On the other hand, MedDiet consumption led to significant reductions in the relative abundance of inter-α-trypsin inhibitor heavy chain H4 and of hemoglobin subunits α and β compared with the control North American diet. Levels of inter-α-trypsin inhibitor heavy chain H4 have been shown to be increased in acute-phase processes such as in acute ischemic stroke and unstable angina [25]. HDL-associated hemoglobin has also been associated with pro-inflammatory HDL in both mouse models and in humans [26], and CHD patients present more hemoglobin associated with HDL than healthy patients [26, 27]. The lowering of the relative abundance of these HDL-bound pro-inflammatory proteins after the MedDiet is consistent with the observed reduction in C-reactive protein concentrations in the same sample of subjects [28]. This suggests that the anti-inflammatory effects of the MedDiet may be mediated, at least partly, through enhanced anti-inflammatory properties of HDL. This hypothesis needs to be formally tested and validated using more specific models and functional tests. As shown previously, the individual HDL-C response to short-term consumption of the MedDiet is highly variable [8]. Changes in HDL proteins related to acute-phase and immune responses were also inconsistent in our study. HDL-bound SAA4 levels were higher among the subjects who showed an increase in plasma HDL-C after consumption of the MedDiet. It must be emphasized that, unlike other proteins of the SAA family, SAA4 is specifically considered a constitutive protein that is not induced during the acute-phase response [29]. Thus, an increase in HDL-bound SAA4 with the MedDiet may not reflect a pro-inflammatory change. On the other hand, cathelicidin antimicrobial peptide, a component of the innate immune system, has been negatively associated with serum HDL-C levels in men [30]. This is contrary to our results showing an increase in relative abundance of cathelicidin antimicrobial peptide in the participants with the greatest increase in HDL-C concentrations in response to the MedDiet. The implication of such a change in immune response proteins within HDL needs to be replicated and further investigated. Unsurprisingly, subanalyses indicated that the participants in whom HDL-C concentrations were increased with the MedDiet showed a parallel increase in the relative abundance of proteins related to cholesterol homeostasis/lipid metabolism, namely apoF, apoC-II and apoE. ApoF is a lipid transfer inhibitor protein known to inhibit cholesteryl ester transfer protein [31]. Although an overexpression of apoF has been shown to reduce HDL-C concentrations in mice [32], knocking out the apoF gene in mice had no effect on HDL-C concentra-

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tions, size and protein content [33]. In humans, apoF has also been positively associated with HDL-C concentrations in normolipidemic men [34]. The apparent increase in the relative abundance of HDL-bound apoF with the MedDiet is therefore consistent with these observations. The primary role of apoC-II is to activate lipoprotein lipase. CHD patients have significantly lower serum apoC-II concentrations than normal subjects [35]. Although excess apoC-II has been associated with a smaller HDL particle size [36], the increase in the relative abundance of HDL-bound apoC-II in the participants in whom HDL-C concentrations were increased with the MedDiet may reflect an overall enhanced capacity of lipolysis of triglyceride-rich lipoproteins. Further studies are needed to confirm this hypothesis. Participants in whom HDL-C levels were reduced with the MedDiet also showed concurrent reductions in the relative abundance of proteins related to cholesterol homeostasis/lipid metabolism, namely apoC-I, apoC-III and apoA-II. Elevated apoC-III concentrations have been associated with an increased risk of cardiovascular diseases [37, 38], and a study has shown that the presence of apoC-III in HDL inhibits cholesterol efflux [39]. ApoA-II in HDL3 has also been shown to inhibit cholesterol efflux from rat hepatoma cells [40]. The reduction in the relative abundance of HDL-bound apoC-III and A-II in the participants who showed a reduction in plasma HDL-C concentrations after the MedDiet therefore suggests an unaltered and perhaps even enhanced capacity for cholesterol efflux. An elevation in HDLassociated apoC-I has been shown to inhibit the scavenger receptor BI in mice, suggesting a reduced uptake of cholesteryl esters by hepatocytes [41]. ApoC-I has also been shown to inhibit cholesteryl ester transfer protein [42]. The extent to which the reduction in the relative abundance of HDL-bound apoC-I in the participants in whom HDL-C concentrations were reduced with the MedDiet may reflect improved HDL lipid metabolism needs to be formally tested in future studies. HDL-bound apoE was significantly increased in both subgroups of participants, i.e. irrespective of the increase or reduction in HDL-C concentrations with the MedDiet. ApoE plays a pivotal role in cholesterol homeostasis and atherosclerosis by facilitating the clearance of remnant lipoproteins [43] but also by promoting cholesterol efflux from macrophages [44, 45]. Cholesterol-loaded macrophages secrete more apoE in the presence of HDL3 particles, and this has been purported to reflect a more effective clearance of peripheral cholesterol by the liver [46]. This increase in the relative abundance of HDL-bound apoE with the MedDiet may therefore reflect an enhanced cholesterol efflux capacity in response to the MedDiet, irrespective of HDL-C variations. We stress that the increase in HDL-bound apoE in the entire group of subjects did not quite reach our a priori defined statistical significance criteria, and thus more studies are warranted to validate this hypothesis. This study encompasses several strengths and limitations. It was a fixed-sequence study that did not include a control group to document changes over time (i.e. independently of the intervention). However, the participants served as their own controls, having been measured on repeated occasions during the study. Baseline ‘control’ values were also obtained following 5 weeks of a controlled feeding period on a North American diet, which is a significant strength. The pooling of samples ensures that the final sample contained all proteins potentially present in the entire sample. It also averages the protein profiles for each group or treatment phase, hence highlighting major differences between the study phases. The use of pooled samples has been shown to be a valid method for iTRAQ protein quantification [47]. However, this approach does not allow correlating individual changes in protein levels to individual changes in cardiometabolic risk factors. The study diets were fed over relatively short periods of time, and we cannot rule out the possibility of longer-term effects of the MedDiet on the HDL proteome and functions. We stress that these preliminary analyses were not designed a priori to study changes in the HDL proteome, and the results should be interpreted in that context. We also stress that

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© 2014 S. Karger AG, Basel www.karger.com/jnn

Richard et al.: Effect of an Isoenergetic Traditional Mediterranean Diet on the HighDensity Lipoprotein Proteome in Men with the Metabolic Syndrome

the purported change in HDL-bound proteins in the proteome of subjects with an increase or decrease in HDL-C concentrations after the MedDiet is based on a small sample size, and this finding will need to be replicated in studies with more subjects. Conclusions

The data suggest that changes in the HDL proteome may explain, at least partly, the wellknown anti-inflammatory effects of the MedDiet. Otherwise, a short-term consumption of the MedDiet seems to have little impact on other features of the HDL proteome in men with the MetS. Acknowledgements Provigo-Loblaws provided the funds used to supply the study foods through their support of the Chair in Nutrition and Cardiovascular Health. We thank the staff of the metabolic kitchen, nurses and the laboratory staff of the Institute of Nutrition and Functional Foods for their technical assistance and the expert care provided to the participants. We also express our gratitude to the participants, without whom the study would not have been possible. B.L. holds a Chair in Nutrition and Cardiovascular Health; S.D. is a Canadian Institutes of Health Research (CIHR) New Investigator and a Fonds de la recherche en santé du Québec (FRSQ) Junior 1 Scholar; C.R. is a recipient of doctoral scholarships from the CIHR and FRSQ. This study was supported by an operating grant from the CIHR (MOP-68866).

Disclosure Statement The authors report no conflict of interest in relation with this study.

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Boden WE: High-density lipoprotein cholesterol as an independent risk factor in cardiovascular disease: assessing the data from Framingham to the Veterans Affairs High-Density Lipoprotein Intervention Trial. Am J Cardiol 2000;86:19L–22L. Ansell BJ, Navab M, Hama S, Kamranpour N, Fonarow G, Hough G, Rahmani S, Mottahedeh R, Dave R, Reddy ST, Fogelman AM: Inflammatory/antiinflammatory properties of high-density lipoprotein distinguish patients from control subjects better than high-density lipoprotein cholesterol levels and are favorably affected by simvastatin treatment. Circulation 2003;108:2751–2756. Fisher EA, Feig JE, Hewing B, Hazen SL, Smith JD: High-density lipoprotein function, dysfunction, and reverse cholesterol transport. Arterioscler Thromb Vasc Biol 2012;32:2813–2820. Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM, Navab M: Protective effect of high density lipoprotein associated paraoxonase: inhibition of the biological activity of minimally oxidized low density lipoprotein. J Clin Invest 1995;96:2882–2891. Mineo C, Deguchi H, Griffin JH, Shaul PW: Endothelial and antithrombotic actions of HDL. Circ Res 2006;98: 1352–1364. Shah AS, Tan L, Long JL, Davidson WS: The proteomic diversity of high density lipoproteins: our emerging understanding of its importance in lipid transport and beyond. J Lipid Res 2013;54:2575–2585. Bedard A, Riverin M, Dodin S, Corneau L, Lemieux S: Sex differences in the impact of the Mediterranean diet on cardiovascular risk profile. Br J Nutr 2012;108:1428–1434. Richard C, Couture P, Desroches S, Charest A, Lamarche B: Effect of the Mediterranean diet with and without weight loss on cardiovascular risk factors in men with the metabolic syndrome. Nutr Metab Cardiovasc Dis 2011;21:628–635. Nordmann AJ, Suter-Zimmermann K, Bucher HC, Shai I, Tuttle KR, Estruch R, Briel M: Meta-analysis comparing Mediterranean to low-fat diets for modification of cardiovascular risk factors. Am J Med 2011;124:841–851e2. Richard C, Couture P, Desroches S, Lichtenstein AH, Lamarche B: Effect of an isoenergetic traditional Mediterranean diet on apolipoprotein A-I kinetic in men with metabolic syndrome. Nutr J 2013;12:76.

Downloaded by: University of Pittsburgh 198.143.32.66 - 6/18/2015 5:34:53 PM

References

59

J Nutrigenet Nutrigenomics 2014;7:48–60 DOI: 10.1159/000363137

© 2014 S. Karger AG, Basel www.karger.com/jnn

11 12 13 14 15 16 17 18 19 20 21 22

23 24 25 26

27 28 29 30 31 32 33 34 35

Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C: Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 2004;109:433–438. Gray-Donald K, Jacobs-Starkey L, Johnson-Down L: Food habits of Canadians: reduction in fat intake over a generation. Can J Public Health 2000;91:381–385. Willett WC, Sacks F, Trichopoulou A, Drescher G, Ferro-Luzzi A, Helsing E, Trichopoulos D: Mediterranean diet pyramid: a cultural model for healthy eating. Am J Clin Nutr 1995;61:1402S–1406S. Havel RJ, Eder H, Bragdon J: The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 1955;34:1345–1353. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA: The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics 2007;6:1638–1655. Tang WH, Shilov IV, Seymour SL: Nonlinear fitting method for determining local false discovery rates from decoy database searches. J Proteome Res 2008;7:3661–3667. Mange A, Goux A, Badiou S, Patrier L, Canaud B, Maudelonde T, Cristol JP, Solassol J: HDL proteome in hemodialysis patients: a quantitative nanoflow liquid chromatography-tandem mass spectrometry approach. PLoS One 2012;7:e34107. Alwaili K, Bailey D, Awan Z, Bailey SD, Ruel I, Hafiane A, Krimbou L, Laboissiere S, Genest J: The HDL proteome in acute coronary syndromes shifts to an inflammatory profile. Biochim Biophys Acta 2012;1821:405–415. Burillo E, Mateo-Gallego R, Cenarro A, Fiddyment S, Bea AM, Jorge I, Vazquez J, Civeira F: Beneficial effects of omega-3 fatty acids in the proteome of high-density lipoprotein proteome. Lipids Health Dis 2012;11:116. Davidson WS, Silva RA, Chantepie S, Lagor WR, Chapman MJ, Kontush A: Proteomic analysis of defined HDL subpopulations reveals particle-specific protein clusters: relevance to antioxidative function. Arterioscler Thromb Vasc Biol 2009;29:870–876. Gordon SM, Deng J, Lu LJ, Davidson WS: Proteomic characterization of human plasma high density lipoprotein fractionated by gel filtration chromatography. J Proteome Res 2010;9:5239–5249. Vaisar T, Pennathur S, Green PS, Gharib SA, Hoofnagle AN, Cheung MC, Byun J, Vuletic S, Kassim S, Singh P, Chea H, Knopp RH, Brunzell J, Geary R, Chait A, Zhao XQ, Elkon K, Marcovina S, Ridker P, Oram JF, Heinecke JW: Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J Clin Invest 2007;117:746–756. Martin-Pelaez S, Covas MI, Fito M, Kusar A, Pravst I: Health effects of olive oil polyphenols: recent advances and possibilities for the use of health claims. Mol Nutr Food Res 2013;57:760–771. Carluccio MA, Massaro M, Scoditti E, de Caterina R: Vasculoprotective potential of olive oil components. Mol Nutr Food Res 2007;51:1225–1234. Pineiro M, Alava MA, Gonzalez-Ramon N, Osada J, Lasierra P, Larrad L, Pineiro A, Lampreave F: ITIH4 serum concentration increases during acute-phase processes in human patients and is up-regulated by interleukin-6 in hepatocarcinoma HepG2 cells. Biochem Biophys Res Commun 1999;263:224–229. Watanabe J, Chou KJ, Liao JC, Miao Y, Meng HH, Ge H, Grijalva V, Hama S, Kozak K, Buga G, Whitelegge JP, Lee TD, Farias-Eisner R, Navab M, Fogelman AM, Reddy ST: Differential association of hemoglobin with proinflammatory high density lipoproteins in atherogenic/hyperlipidemic mice: a novel biomarker of atherosclerosis. J Biol Chem 2007;282:23698–23707. Watanabe J, Grijalva V, Hama S, Barbour K, Berger FG, Navab M, Fogelman AM, Reddy ST: Hemoglobin and its scavenger protein haptoglobin associate with apoA-1-containing particles and influence the inflammatory properties and function of high density lipoprotein. J Biol Chem 2009;284:18292–18301. Richard C, Couture P, Desroches S, Lamarche B: Effect of the Mediterranean diet with and without weight loss on markers of inflammation in men with metabolic syndrome. Obesity (Silver Spring) 2013;21:51–57. Whitehead AS, de Beer MC, Steel DM, Rits M, Lelias JM, Lane WS, de Beer FC: Identification of novel members of the serum amyloid A protein superfamily as constitutive apolipoproteins of high density lipoprotein. J Biol Chem 1992;267:3862–3867. Benachour H, Zaiou M, Samara A, Herbeth B, Pfister M, Lambert D, Siest G, Visvikis-Siest S: Association of human cathelicidin (hCAP-18/LL-37) gene expression with cardiovascular disease risk factors. Nutr Metab Cardiovasc Dis 2009;19:720–728. Wang X, Driscoll DM, Morton RE: Molecular cloning and expression of lipid transfer inhibitor protein reveals its identity with apolipoprotein F. J Biol Chem 1999;274:1814–1820. Lagor WR, Brown RJ, Toh SA, Millar JS, Fuki IV, de la Llera-Moya M, Yuen T, Rothblat G, Billheimer JT, Rader DJ: Overexpression of apolipoprotein F reduces HDL cholesterol levels in vivo. Arterioscler Thromb Vasc Biol 2009;29:40–46. Lagor WR, Fields DW, Khetarpal SA, Kumaravel A, Lin W, Weintraub N, Wu K, Hamm-Alvarez SF, DrazulSchrader D, de la Llera-Moya M, Rothblat GH, Rader DJ: The effects of apolipoprotein F deficiency on high density lipoprotein cholesterol metabolism in mice. PLoS One 2012;7:e31616. Morton RE, Gnizak HM, Greene DJ, Cho KH, Paromov VM: Lipid transfer inhibitor protein (apolipoprotein F) concentration in normolipidemic and hyperlipidemic subjects. J Lipid Res 2008;49:127–135. Liu BW, Shao MZ, Yuan HJ, Wu ZF, Zhang ZH, Fu MD, Zhang RJ, Fan P: Serum lipids and apolipoproteins AI, B100, CI, CII, and CIII in 142 patients with coronary heart disease (in Chinese). Hua Xi Yi Ke Da Xue Xue Bao 1989;20:119–122.

Downloaded by: University of Pittsburgh 198.143.32.66 - 6/18/2015 5:34:53 PM

Richard et al.: Effect of an Isoenergetic Traditional Mediterranean Diet on the HighDensity Lipoprotein Proteome in Men with the Metabolic Syndrome

60

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© 2014 S. Karger AG, Basel www.karger.com/jnn

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37 38 39 40

41 42 43 44 45 46 47

Tian L, Xu Y, Fu M, Jia L, Yang Y: Influence of apolipoprotein CII concentrations on HDL subclass distribution. J Atheroscler Thromb 2009;16:611–620. Sacks FM, Alaupovic P, Moye LA, Cole TG, Sussex B, Stampfer MJ, Pfeffer MA, Braunwald E: VLDL, apolipoproteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation 2000;102:1886–1892. Zheng C, Khoo C, Furtado J, Sacks FM: Apolipoprotein C-III and the metabolic basis for hypertriglyceridemia and the dense low-density lipoprotein phenotype. Circulation 2010;121:1722–1734. Holzer M, Birner-Gruenberger R, Stojakovic T, El-Gamal D, Binder V, Wadsack C, Heinemann A, Marsche G: Uremia alters HDL composition and function. J Am Soc Nephrol 2011;22:1631–1641. Lagrost L, Dengremont C, Athias A, de Geitere C, Fruchart JC, Lallemant C, Gambert P, Castro G: Modulation of cholesterol efflux from Fu5AH hepatoma cells by the apolipoprotein content of high density lipoprotein particles: particles containing various proportions of apolipoproteins A-I and A-II. J Biol Chem 1995; 270: 13004–13009. de Haan W, Out R, Berbee JF, van der Hoogt CC, van Dijk KW, van Berkel TJ, Romijn JA, Jukema JW, Havekes LM, Rensen PC: Apolipoprotein CI inhibits scavenger receptor BI and increases plasma HDL levels in vivo. Biochem Biophys Res Commun 2008;377:1294–1298. Shachter NS: Apolipoproteins C-I and C-III as important modulators of lipoprotein metabolism. Curr Opin Lipidol 2001;12:297–304. Mahley RW, Ji ZS: Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E. J Lipid Res 1999;40:1–16. Lin CY, Duan H, Mazzone T: Apolipoprotein E-dependent cholesterol efflux from macrophages: kinetic study and divergent mechanisms for endogenous versus exogenous apolipoprotein E. J Lipid Res 1999; 40: 1618– 1627. Tall AR: Cholesterol efflux pathways and other potential mechanisms involved in the athero-protective effect of high density lipoproteins. J Intern Med 2008;263:256–273. Dory L: Regulation of apolipoprotein E secretion by high density lipoprotein 3 in mouse macrophages. J Lipid Res 1991;32:783–792. Song X, Bandow J, Sherman J, Baker JD, Brown PW, McDowell MT, Molloy MP: iTRAQ experimental design for plasma biomarker discovery. J Proteome Res 2008;7:2952–2958.

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Effect of an isoenergetic traditional Mediterranean diet on the high-density lipoprotein proteome in men with the metabolic syndrome.

The objective of this preliminary study was to examine the impact of the Mediterranean diet (MedDiet) on the high-density lipoprotein (HDL) proteome i...
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