SUPPLEMENTAL FILE MATERIALS AND METHODS. Effects of extended-release nicotinic acid on apolipoprotein (a) kinetics in. hypertriglyceridemic patients
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1 SUPPLEMENTAL FILE MATERIALS AND METHODS Effects of extended-release nicotinic acid on apolipoprotein (a) kinetics in hypertriglyceridemic patients Mikaël Croyal, Khadija Ouguerram, Maxime Passard, Véronique Ferchaud-Roucher, Maud Chétiveaux, Stéphanie Billon-Crossouard, Gilles Lambert, Michel Krempf and Estelle Nobécourt. 1 1
2 MATERIAL AND METHODS Patients Patients that met inclusion criteria (male, age to years, plasma triglyceride concentration to 00 mg/gl, high-density lipoprotein cholesterol (HDL-C) below 0 mg/dl, waist circumference > cm and body mass index to kg/m ) were included in a double blind, placebo controlled cross-over week study. These criteria were selected according to the European definition of the metabolic syndrome from the International Diabetes Federation (1) and also according to the ERN guidelines for prescription (). Patients diagnosed with cancer, diabetes mellitus, hepatic, renal, or digestive disorders, and hypertension and those that received chronic medical treatment that interfered with lipid metabolism were excluded form the study. Each subject received extended-release nicotinic acid (ERN, Niaspan, Merck Clevenot, France) and placebo in a random order for eight weeks. A two-week interval was included between the two treatments. To minimize flushing effects, the daily dose of ERN was gradually increased from 0. to.0 g/day in the first four weeks, then kept constant at.0 g/day during the last four weeks and associated in both arms with 00 mg/day of lysine acetylsalicylate). Regular phone calls and intermediate visit ( weeks) were organized to control for treatment compliance. At the end of each treatment phase, ERN or placebo were given after an overnight fast, and subjects received a µm/kg bolus injection of [,,- H ]- L-Leucine immediately followed by constant infusion of [,,- H ]-L-Leucine ( µm/kg/h) for 1 hours. Subjects were only allowed to drink water until the end of the tracer infusion. Blood samples were collected at 0, 1, 0,, 0, 0,,, and 0 minutes then at,,,, 1 and 1 hours. The Ethics Committee of Nantes University Hospital approved the clinical protocol, and a written informed consent was obtained from each subject (reference trial number: NCT0). Sample collection and preparation Blood samples were collected in EDTA tubes (Venoject, Paris, France), and plasma was separated by centrifugation at C for 0 minutes and stored at -0 C until analysis. Lipoproteins fractions, including very low-density lipoprotein (VLDL, <1.00 g/ml), intermediate density lipoprotein (IDL, 1.00 to 1.01 g/ml), low-density lipoprotein (LDL, 1.01 to 1.0 g/ml) and high-density lipoprotein (HDL, 1.0 to 1. g/ml), were separated by density gradient ultracentrifugation as described previously (, ) and stored at -0 C until analysis. Chemicals UPLC/MS-grade acetonitrile, water, and % formic acid were purchased from Biosolve (Valkenswaard, Netherlands). Ammonium bicarbonate (AB), dithiothreitol (DTT), iodoacetamide (IA), sodium deoxycholate (SDC), trypsin, ammonium hydroxide (NaOH), and % hydrochloric acid (HCl) were obtained from Sigma Aldrich (Saint-Quentin Fallavier, France). Synthetic peptides LFLEPTQADIALLK, [,,- H ]L-FLEPTQADIALLK, LFLEPTQADIALL-[ 1 C 1 N ]K, GTYSTTVTGR, and GTYSTTVTG-[ 1 C 1 N ]R were purchased from Thermo Scientific Biopolymers (Einsteinstrasse, Germany). Measures of plasma concentrations of the lipid and glucose parameters Cholesterol and triglyceride concentrations were measured using enzymatic test kits from Boehringer Mannheim GmbH (Mannheim, Germany). ApoA-I concentrations were measured by immunonephelemetry (Behring, Rueil Malmaison, France), and ApoB0 concentrations were obtained using selective precipitation and mass spectrometry (). Plasma PCSK concentrations were measured by ELISA (R&D Systems, Lille, France). Fasting blood glucose and insulin concentrations were measured as previously reported as well as the HOMA-IR index calculation (). Measurement of ApoB0 Leucine enrichment
3 Isolation and measurement of Leucine enrichment in ApoB0 were described previously (). Briefly, ApoB0-containing lipoprotein fractions were isolated by sodium dodecyl sulfate polyacrylamide gel electrophoresis and then hydrolyzed with HCl. Amino acids were purified by cation exchange chromatography, derivatized (N-Propanol-acetylchlorid and heptafluorobutyric acid), and analyzed by gas chromatography-mass spectrometry to determine [,,- H ]-L-Leucine enrichment. Selection of proteotypic Apo(a) peptides Apo(a) sequences were Blast searched using the UNIPROT tool ( and theoretical proteotypic peptides were searched using the free software peptide mass calculator ( Peptide candidates were selected to maximize sensitivity, specificity, and stability. Peptides containing methionine and cysteine were not considered due to potential oxidation. As described by Lassman et al. () and Zhou et al. (), LFLEPTQADIALLK was selected for Apo(a) quantification and kinetic measurements, and GTYSTTVTGR was selected for Apo(a) size characterization. The LFLEPTQADIALLK and GTYSTTVTGR peptides are located in the Peptidase S1 and kringle IV domains, respectively. Sample preparation for Apo(a) quantitation and size characterization in plasma LFLEPTQADIALLK, LFLEPTQADIALL-[ 1 C 1 N ]K, GTYSTTVTGR, and GTYSTTVTG- [ 1 C 1 N ]R synthetic peptides were dissolved in a water/acetonitrile mixture (0/0, v/v) containing 0.1% formic acid at a concentration of 0 µm and were stored at -0 C in aliquots of 0 µl. Stock solutions of LFLEPTQADIALLK and GTYSTTVTGR were then mixed and diluted in 0.% SDC to produce seven X standard solutions ranging from.0 to 0.0 µm and 0.0 to 0. µm for LFLEPTQADIALLK and GTYSTTVTGR, respectively. Plasma samples ( µl) were mixed and diluted with 1 µl of 0.% SDC. LFLEPTQADIALL- [ 1 C 1 N ]K and GTYSTTVTG-[ 1 C 1 N ]R were used as internal standards (ISs). Ten microliters ( µl) of each IS stock solution were extemporaneously added to,0 µl of a reduction buffer (ph ) containing mm AB, 0.% SDC, and. mm DTT. Twenty microliters of X standard solutions and diluted plasma samples were added to 0 µl of reduction buffer containing both ISs. Final concentrations of AB, DTT, and ISs were 0 mm, mm, and 0 nm, respectively. The final concentrations of standard solutions were from 00 to nm and from 000 to 0 nm for LFLEPTQADIALLK and GTYSTTVTGR, respectively. Samples were reduced for 0 minutes at 0 C then alkylated with µl of fresh IA solution (1 M in 1 M NaOH) for 0 minutes at room temperature (protected from light). Samples were digested overnight with µl of trypsin solution (0.1 mg/ml in 1 mm HCl), and µl of 0% formic acid were added to stop the reaction and to precipitate the SDC. Samples were centrifuged for 1 minutes at 0,000 g, C and 0 µl of supernatants were transferred to LC vials for LC-MS/MS analyses. Sample preparation for Apo(a) kinetic measurements in lipoprotein fractions To recover the major Lp(a) particles, 0 µl of LDL and HDL lipoprotein fractions were combined () and desalted and concentrated with ml of 0 mm AB buffer (ph ) and a - kda molecular weight cut-off filter. Concentrated samples (0 µl) were mixed with µl of 0 mm AB buffer (ph ), µl of % SDC, and µl of 00 mm DTT and reduced at 0 C for 0 minutes. Samples were then treated as described in the previous section. LFLEPTQADIALLK and [,,- H ]L-FLEPTQADIALLK synthetic peptides were dissolved in a water/acetonitrile mixture (0/0, v/v) containing 0.1% formic acid to reach a final concentration of 00 nm. To evaluate accuracy, labeled peptide solution was diluted in unlabeled peptide solutions to reach theoretical enrichments ranging from 0 to % (0, 0.1, 0., 0., 1.0,.0, and.0%, n = /point). Control samples were prepared with the same method at % enrichment and for concentrations of 00, 0, 0, 0, 0 and nm (n = /point). Analytical parameters
4 Analyses were performed on an LC-MS/MS system consisting of a Xevo Triple-Quadrupole mass spectrometer (Waters Corporation, Milford, MA, USA) equipped with an electrospray ionization (ESI) interface and an Acquity H-Class UPLC TM device (Waters Corporation, Milford, MA, USA). Data acquisition and analyses were performed using MassLynx and TargetLynx software, respectively (version.1, Waters Corporation, Milford, MA, USA). Labeled and unlabeled peptides were separated on an Acquity BEH C column (.1 0 mm, 1. µm, Waters) at 0 C with a linear gradient of mobile phase B (acetonitrile containing 0.1% formic acid) in mobile phase A (% acetonitrile in water containing 0.1% formic acid) and at a flow rate of 00 µl/min. Mobile phase B was linearly increased from 1 to 0% for minutes, kept constant for 1 min, returned to the initial condition in 1 min, and kept constant for 1 min before the next injection. Ten microliters of each sample were injected into the LC column. Labeled and unlabeled peptides were then detected by the mass spectrometer equipped with an ESI interface operating in the positive ion mode. The multiple reaction monitoring (MRM) mode was applied for MS/MS detection. Selected MRM transitions, cone voltages, and collision energies are described in Supplemental Table I (supplemental material). Note that each precursor ion was detected as a doubly charged ion leading to the formation of singly charged product ions (y + for LFLEPTQADIALLK and labeled analogues and y + for GTYSTTVTGR and labeled analogue). Apo(a) data management Chromatographic peak area ratios between target peptides and their respective ISs constituted detector responses. Standard solutions were used to plot calibration curves for quantification of both peptides (Supplemental Figure I in supplemental material). A linear regression model was used for peptide quantification ( concentration levels, n = ), and the linearity of the method was confirmed (r² at 0. and 0. for LFLEPTQADIALLK and GTYSTTVTGR, respectively). Each plasma sample was assayed three times, and the coefficients of variation did not exceed.% and 1.% for LFLEPTQADIALLK and GTYSTTVTGR, respectively. As targeted peptide LFLEPTQADIALLK is unique in Apo(a), 1 mole of Apo(a) was assumed to be equal to 1 mole of this peptide. As the target peptide GTYSTTVTGR is repeated in the kringle IV 1, IV, IV and IV regions but not in the IV, IV, IV, IV, IV and IV regions, the total number of kringle IV was equal to (([GTYSTTVTGR]/[LFLEPTQADIALLK]) + ) taking into account that the result expressed the average Apo(a) size of the two circulating isoforms. For Apo(a) enrichment measurements, M/M0 ratios were calculated using chromatographic peak areas; M corresponded to the [,,- H ]-L-Leucine labeled peptide and M0 to the unlabeled peptide. As the selected peptide contains Leucines and isotopomers of M can be formed (Supplemental Table I), the sum of MRM transitions used for the M detection allowed detection of all the isotopomers. Thus, M/M0 ratios measured in biological samples were corrected by dividing the primary result by, as described by Brunengraber et al. (). Correction was not applied in standard enrichment samples prepared with one standard isotopomer (Supplemental Figure I). Agreement was observed at 00 nm between the measured and expected ratio of [,,- H ]-L-Leucine labeled peptide (M) and unlabeled peptide (M0) over seven enrichment levels (n = ). The slope and r² of the linear regression were 0. and 1.0, respectively. To gain confidence in the ratio measurements, a theoretical enrichment at % was performed over six distinct concentrations of LFLEPTQADIALLK (n = ). No significant variation was observed from to 00 nm. The coefficients of variation calculated over the six replicates did not exceed.%, and the mean difference calculated between theoretical and measured enrichments was below.0%. Apo(a) and ApoB0 kinetic modeling Apo(a) fractional catabolic rate (FCR) was estimated on the 1 hour samples and using the SAAM II modeling program (Epsilon Group, Charlottesville, VA, USA) and fitting a mono exponential curve (mono compartmental model), as suggested for proteins with slow turnover rates (). Apo(a) was assumed to have the corresponding VLDL-ApoB0 leucine plateau enrichment as a precursor pool. According to this steady state model, the FCR was
5 considered equivalent to the fractional synthetic rate (FSR). Kinetic parameters of VLDL and LDL ApoB0 were calculated from the same plasma samples and using a three compartmental model as described previously for a 1 hours of a tracer constant infusion (). Individual kinetic data are shown in supplemental Table II (supplemental material). Statistical analyses Statistical analyses were performed with GraphPad Prism software (version.0, GraphPad Software Inc., La Jolla, CA, USA) using the nonparametric Wilcoxon matched-pairs signed rank test. Results are expressed as mean ± standard deviation (SD) or mean ± standard error of the mean (SEM). Differences between ERN and placebo treatment were considered statistically significant at p <0.0 (two-tailed or otherwise specified). REFERENCES 1. Zimmet P, Magliano D, Matsuzawa Y, Alberti G, Shaw J. The metabolic syndrome: a global public health problem and a new definition. J Atheroscler Thromb. 00:1: McCormack PL, Keating GM. Prolonged-release nicotinic acid: a review of its use in the treatment of dyslipidaemia. Drugs. 00::1-0.. Maugeais C, Ouguerram K, Krempf M, Maugeais P, Gardette J, Bigot E, Magot T. A minimal model using stable isotopes to study the metabolism of apolipoprotein B- containing lipoproteins in humans. Diabetes Metab. 1::-. Bailhache E, Briand F, Nguyen P, Krempf M, Magot T, Ouguerram K. Metabolism of cholesterol ester of apolipoprotein B0-containing lipoproteins in dogs: evidence for disregarding cholesterol ester transfer. Eur J Clin Invest. 00::-.. Beghin L, Duhal N, Poulain P, Hauw P, Lacroix B, Lecerf JM, Bonte JP, Fruchart JC, Luc G. Measurement of apolipoprotein B concentration in plasma lipoproteins by combining selective precipitation and mass spectrometry. J Lipid Res. 000:1:-.. Blond E, Rieusset J, Alligier M et.al. Nicotinic acid effects on insulin sensitivity and hepatic lipid metabolism: an in vivo to in vitro study. Horm Metab Res. 01:: 0-.. Lassman ME, McLaughlin TM, Zhou H, Pan Y, Marcovina SM, Laterza O, Roddy TP. Simultaneous quantitation and size characterization of apolipoprotein(a) by ultraperformance liquid chromatography/mass spectrometry. Rapid Commun Mass Spectrom. 01:: Zhou H, Castro-Perez J, Lassman ME et.al. Measurement of apo(a) kinetics in human subjects using a microfluidic device with tandem mass spectrometry. Rapid Commun Mass Spectrom. 01::1-... Brunengraber H, Kelleher JK, Des Rosiers C. Applications of mass isotopomer analysis to nutrition research. Annu Rev Nutr. 1::-.
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