Reconstituted Discoidal High-Density Lipoproteins: Bioinspired Nanodiscs with Many Unexpected Applications

Current Atherosclerosis Reports - Tập 20 Số 12 - 2018
Maki Tsujita1, Anna Wolska2, Daniel A.P. Gutmann3, Alan T. Remaley2
1Department of Biochemistry, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan
2Lipoprotein Metabolism Laboratory, Translational Vascular Medicine Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, USA
3University of Tübingen, Tübingen, Germany

Tóm tắt

Từ khóa


Tài liệu tham khảo

Forte T, Norum KR, Glomset JA, Nichols AV. Plasma lipoproteins in familial lecithin: cholesterol acyltransferase deficiency: structure of low and high density lipoproteins as revealed by elctron microscopy. J Clin Invest. 1971;50(5):1141–8. https://doi.org/10.1172/JCI106586 .

Forte TM, Nichols AV, Gong EL, Levy RI, Lux S. Electron microscopic study on reassembly of plasma high density apoprotein with various lipids. Biochim Biophys Acta. 1971;248(2):381–6.

Tall AR, Small DM, Shipley GG, Lees RS. Apoprotein stability and lipid-protein interactions in human plasma high density lipoproteins. Proc Natl Acad Sci U S A. 1975;72(12):4940–2.

Andrews AL, Atkinson D, Barratt MD, Finer EG, Hauser H, Henry R, et al. Interaction of apoprotein from porcine high-density lipoprotein with dimyristoly lecithin. 2. Nature of lipid-protein interaction. European journal of biochemistry / FEBS. 1976;64(2):549–63.

Segrest JP. Amphipathic helixes and plasma lipoproteins: thermodynamic and geometric considerations. Chem Phys Lipids. 1977;18(1):7–22.

Segrest JP, Feldmann RJ. Amphipathic helixes and plasma lipoproteins: a computer study. Biopolymers. 1977;16(9):2053–65. https://doi.org/10.1002/bip.1977.360160916 .

Wlodawer A, Segrest JP, Chung BH, Chiovetti R Jr, Weinstein JN. High-density lipoprotein recombinants: evidence for a bicycle tire micelle structure obtained by neutron scattering and electron microscopy. FEBS Lett. 1979;104(2):231–5.

Mendez AJ, Anantharamaiah GM, Segrest JP, Oram JF. Synthetic amphipathic helical peptides that mimic apolipoprotein A-I in clearing cellular cholesterol. J Clin Invest. 1994;94(4):1698–705. https://doi.org/10.1172/JCI117515 .

Kane JP, Malloy MJ. Prebeta-1 HDL and coronary heart disease. Curr Opin Lipidol. 2012;23(4):367–71. https://doi.org/10.1097/MOL.0b013e328353eef1 .

Kunitake ST, La Sala KJ, Kane JP. Apolipoprotein A-I-containing lipoproteins with pre-beta electrophoretic mobility. J Lipid Res. 1985;26(5):549–55.

Norum KR, Glomset JA, Nichols AV, Forte T. Plasma lipoproteins in familial lecithin: cholesterol acyltransferase deficiency: physical and chemical studies of low and high density lipoproteins. J Clin Invest. 1971;50(5):1131–40. https://doi.org/10.1172/JCI106585 .

Ishida BY, Frolich J, Fielding CJ. Prebeta-migrating high density lipoprotein: quantitation in normal and hyperlipidemic plasma by solid phase radioimmunoassay following electrophoretic transfer. J Lipid Res. 1987;28(7):778–86.

Castro GR, Fielding CJ. Early incorporation of cell-derived cholesterol into pre-beta-migrating high-density lipoprotein. Biochemistry. 1988;27(1):25–9.

Hara H, Yokoyama S. Interaction of free apolipoproteins with macrophages. Formation of high density lipoprotein-like lipoproteins and reduction of cellular cholesterol. J Biol Chem. 1991;266(5):3080–6.

Hara H, Hara H, Komaba A, Yokoyama S. Alpha-helical requirements for free apolipoproteins to generate HDL and to induce cellular lipid efflux. Lipids. 1992;27(4):302–4.

Hara H, Yokoyama S. Role of apolipoproteins in cholesterol efflux from macrophages to lipid microemulsion: proposal of a putative model for the pre-beta high-density lipoprotein pathway. Biochemistry. 1992;31(7):2040–6.

Tsujita M, Yokoyama S. Selective inhibition of free apolipoprotein-mediated cellular lipid efflux by probucol. Biochemistry. 1996;35(40):13011–20. https://doi.org/10.1021/bi960734h .

Tsujita M, Tomimoto S, Okumura-Noji K, Okazaki M, Yokoyama S. Apolipoprotein-mediated cellular cholesterol/phospholipid efflux and plasma high density lipoprotein level in mice. Biochim Biophys Acta. 2000;1485(2–3):199–213.

Bodzioch M, Orso E, Klucken J, Langmann T, Bottcher A, Diederich W, et al. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet. 1999;22(4):347–51. https://doi.org/10.1038/11914 .

Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, et al. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet. 1999;22(4):336–45. https://doi.org/10.1038/11905 .

Rust S, Rosier M, Funke H, Real J, Amoura Z, Piette JC, et al. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet. 1999;22(4):352–5. https://doi.org/10.1038/11921 .

Qian H, Zhao X, Cao P, Lei J, Yan N, Gong X. Structure of the human lipid exporter ABCA1. Cell. 2017;169(7):1228–39 e10. https://doi.org/10.1016/j.cell.2017.05.020 .

Francis GA, Knopp RH, Oram JF. Defective removal of cellular cholesterol and phospholipids by apolipoprotein A-I in Tangier disease. J Clin Invest. 1995;96(1):78–87. https://doi.org/10.1172/JCI118082 .

Oram JF. Tangier disease and ABCA1. Biochim Biophys Acta. 2000;1529(1–3):321–30.

Huang LH, Elvington A, Randolph GJ. The role of the lymphatic system in cholesterol transport. Front Pharmacol. 2015;6:182. https://doi.org/10.3389/fphar.2015.00182 .

Koppaka V, Silvestro L, Engler JA, Brouillette CG, Axelsen PH. The structure of human lipoprotein A-I. Evidence for the “belt” model. J Biol Chem. 1999;274(21):14541–4.

Phillips JC, Wriggers W, Li Z, Jonas A, Schulten K. Predicting the structure of apolipoprotein A-I in reconstituted high-density lipoprotein disks. Biophys J. 1997;73(5):2337–46. https://doi.org/10.1016/S0006-3495(97)78264-X .

Segrest JP, Jones MK, Klon AE, Sheldahl CJ, Hellinger M, De Loof H, et al. A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein. J Biol Chem. 1999;274(45):31755–8.

Davidson WS, Hilliard GM. The spatial organization of apolipoprotein A-I on the edge of discoidal high density lipoprotein particles: a mass specrometry study. J Biol Chem. 2003;278(29):27199–207. https://doi.org/10.1074/jbc.M302764200 .

Davidson WS, Silva RA. Apolipoprotein structural organization in high density lipoproteins: belts, bundles, hinges and hairpins. Curr Opin Lipidol. 2005;16(3):295–300.

Shih AY, Denisov IG, Phillips JC, Sligar SG, Schulten K. Molecular dynamics simulations of discoidal bilayers assembled from truncated human lipoproteins. Biophys J. 2005;88(1):548–56. https://doi.org/10.1529/biophysj.104.046896 .

Wu Z, Wagner MA, Zheng L, Parks JS, Shy JM 3rd, Smith JD, et al. The refined structure of nascent HDL reveals a key functional domain for particle maturation and dysfunction. Nat Struct Mol Biol. 2007;14(9):861–8. https://doi.org/10.1038/nsmb1284 .

Shih AY, Sligar SG, Schulten K. Molecular models need to be tested: the case of a solar flares discoidal HDL model. Biophys J. 2008;94(12):L87–9. https://doi.org/10.1529/biophysj.108.131581 .

Gogonea V. Structural insights into high density lipoprotein: old models and new facts. Front Pharmacol. 2015;6:318. https://doi.org/10.3389/fphar.2015.00318 .

Cooke AL, Morris J, Melchior JT, Street SE, Jerome WG, Huang R, et al. A thumbwheel mechanism for APOA1 activation of LCAT activity in HDL. J Lipid Res. 2018;59:1244–55. https://doi.org/10.1194/jlr.M085332 .

Murray SC, Gillard BK, Ludtke SJ, Pownall HJ. Direct measurement of the structure of reconstituted high-density lipoproteins by Cryo-EM. Biophys J. 2016;110(4):810–6. https://doi.org/10.1016/j.bpj.2015.10.028 .

Brainard JR, Knapp RD, Morrisett JD, Pownall HJ. 13C NMR studies of the thermal properties of a model high density lipoprotein. Apolipoprotein A-I-dimyristoylphosphatidylcholine complex. J Biol Chem. 1984;259(16):10340–7.

Gilman T, Kauffman JW, Pownall HJ. Raman spectroscopy of the thermal properties of reassembled high-density lipoprotein: apolipoprotein A-I complexes of dimyristoylphosphatidylcholine. Biochemistry. 1981;20(3):656–61.

Jonas A. Reconstitution of high-density lipoproteins. Methods Enzymol. 1986;128:553–82.

Bayburt TH, Sligar SG. Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc Natl Acad Sci U S A. 2002;99(10):6725–30. https://doi.org/10.1073/pnas.062565599 .

Carlson JW, Jonas A, Sligar SG. Imaging and manipulation of high-density lipoproteins. Biophys J. 1997;73(3):1184–9. https://doi.org/10.1016/S0006-3495(97)78150-5 .

Bayburt TH, Carlson JW, Sligar SG. Reconstitution and imaging of a membrane protein in a nanometer-size phospholipid bilayer. J Struct Biol. 1998;123(1):37–44. https://doi.org/10.1006/jsbi.1998.4007 .

Bayburt TH, Carlson JW, Sligar SG. Single molecule height measurements on a membrane protein in nanometer-scale phospholipid bilayer disks. Langmuir : the ACS journal of surfaces and colloids. 2000;16(14):5993–7. https://doi.org/10.1021/la991449c .

Bayburt TH, Grinkova YV, Sligar SG. Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett. 2002;2(8):853–6. https://doi.org/10.1021/nl025623k .

Baas BJ, Denisov IG, Sligar SG. Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch Biochem Biophys. 2004;430(2):218–28. https://doi.org/10.1016/j.abb.2004.07.003 .

Hagn F, Nasr ML, Wagner G. Assembly of phospholipid nanodiscs of controlled size for structural studies of membrane proteins by NMR. Nat Protoc. 2018;13(1):79–98. https://doi.org/10.1038/nprot.2017.094 .

Lee AG. Lipid-protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta. 2003;1612(1):1–40.

Khatri Y, Gregory MC, Grinkova YV, Denisov IG, Sligar SG. Active site proton delivery and the lyase activity of human CYP17A1. Biochem Biophys Res Commun. 2014;443(1):179–84. https://doi.org/10.1016/j.bbrc.2013.11.094 .

Bavishi K, Laursen T, Martinez KL, Moller BL, Della Pia EA. Application of nanodisc technology for direct electrochemical investigation of plant cytochrome P450s and their NADPH P450 oxidoreductase. Sci Rep. 2016;6:29459. https://doi.org/10.1038/srep29459 .

Denisov IG, Grinkova YV, Lazarides AA, Sligar SG. Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J Am Chem Soc. 2004;126(11):3477–87. https://doi.org/10.1021/ja0393574 .

Hagn F, Etzkorn M, Raschle T, Wagner G. Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J Am Chem Soc. 2013;135(5):1919–25. https://doi.org/10.1021/ja310901f .

Zoghbi ME, Cooper RS, Altenberg GA. The lipid bilayer modulates the structure and function of an ATP-binding cassette exporter. J Biol Chem. 2016;291(9):4453–61. https://doi.org/10.1074/jbc.M115.698498 .

Zoghbi ME, Mok L, Swartz DJ, Singh A, Fendley GA, Urbatsch IL, et al. Substrate-induced conformational changes in the nucleotide-binding domains of lipid bilayer-associated P-glycoprotein during ATP hydrolysis. J Biol Chem. 2017;292(50):20412–24. https://doi.org/10.1074/jbc.M117.814186 .

Kawai T, Caaveiro JM, Abe R, Katagiri T, Tsumoto K. Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett. 2011;585(22):3533–7. https://doi.org/10.1016/j.febslet.2011.10.015 .

Fiori MC, Jiang Y, Zheng W, Anzaldua M, Borgnia MJ, Altenberg GA, et al. Polymer nanodiscs: discoidal amphiphilic block copolymer membranes as a new platform for membrane proteins. Sci Rep. 2017;7(1):15227. https://doi.org/10.1038/s41598-017-15151-9 .

Rouck JE, Krapf JE, Roy J, Huff HC, Das A. Recent advances in nanodisc technology for membrane protein studies (2012-2017). FEBS Lett. 2017;591(14):2057–88. https://doi.org/10.1002/1873-3468.12706 .

Yang Z, Wang C, Zhou Q, An J, Hildebrandt E, Aleksandrov LA, et al. Membrane protein stability can be compromised by detergent interactions with the extramembranous soluble domains. Protein science : a publication of the Protein Society. 2014;23(6):769–89. https://doi.org/10.1002/pro.2460 .

Li D, Gordon S, Schwendeman A, Remaley AT. Apolipoprotein mimetics in the Management of Human Disease. New York: Springer International Publishing; 2015.

Ahuja S, Jahr N, Im SC, Vivekanandan S, Popovych N, Le Clair SV, et al. A model of the membrane-bound cytochrome b5-cytochrome P450 complex from NMR and mutagenesis data. J Biol Chem. 2013;288(30):22080–95. https://doi.org/10.1074/jbc.M112.448225 .

Yamamoto K, Gildenberg M, Ahuja S, Im SC, Pearcy P, Waskell L, et al. Probing the transmembrane structure and topology of microsomal cytochrome-p450 by solid-state NMR on temperature-resistant bicelles. Sci Rep. 2013;3:2556. https://doi.org/10.1038/srep02556 .

Yamamoto K, Durr UH, Xu J, Im SC, Waskell L, Ramamoorthy A. Dynamic interaction between membrane-bound full-length cytochrome P450 and cytochrome b5 observed by solid-state NMR spectroscopy. Sci Rep. 2013;3:2538. https://doi.org/10.1038/srep02538 .

Yamamoto K, Caporini MA, Im S, Waskell L, Ramamoorthy A. Shortening spin-lattice relaxation using a copper-chelated lipid at low-temperatures - a magic angle spinning solid-state NMR study on a membrane-bound protein. J Magn Reson. 2013;237:175–81. https://doi.org/10.1016/j.jmr.2013.10.017 .

Yamamoto K, Caporini MA, Im SC, Waskell L, Ramamoorthy A. Transmembrane interactions of full-length mammalian bitopic cytochrome-P450-cytochrome-b5 complex in lipid bilayers revealed by sensitivity-enhanced dynamic nuclear polarization solid-state NMR spectroscopy. Sci Rep. 2017;7(1):4116. https://doi.org/10.1038/s41598-017-04219-1 .

Counsell RE, Pohland RC. Lipoproteins as potential site-specific delivery systems for diagnostic and therapeutic agents. J Med Chem. 1982;25(10):1115–20.

Schouten D, van der Kooij M, Muller J, Pieters MN, Bijsterbosch MK, van Berkel TJ. Development of lipoprotein-like lipid particles for drug targeting: neo-high density lipoproteins. Mol Pharmacol. 1993;44(2):486–92.

Lacko AG, Sabnis NA, Nagarajan B, McConathy WJ. HDL as a drug and nucleic acid delivery vehicle. Front Pharmacol. 2015;6:247. https://doi.org/10.3389/fphar.2015.00247 .

Kuai R, Li D, Chen YE, Moon JJ, Schwendeman A. High-density lipoproteins: nature’s multifunctional nanoparticles. ACS Nano. 2016;10(3):3015–41. https://doi.org/10.1021/acsnano.5b07522 .

Swaney JB. Mechanisms of protein-lipid interaction. Association of apolipoproteins A-I and A-II with binary phospholipid mixtures. J Biol Chem. 1980;255(18):8791–7.

Foit L, Giles FJ, Gordon LI, Thaxton CS. Synthetic high-density lipoprotein-like nanoparticles for cancer therapy. Expert Rev Anticancer Ther. 2015;15(1):27–34. https://doi.org/10.1586/14737140.2015.990889 .

Raut S, Dasseux JL, Sabnis NA, Mooberry L, Lacko A. Lipoproteins for therapeutic delivery: recent advances and future opportunities. Ther Deliv. 2018;9(4):257–68. https://doi.org/10.4155/tde-2017-0122 .

Oda MN, Hargreaves PL, Beckstead JA, Redmond KA, van Antwerpen R, Ryan RO. Reconstituted high density lipoprotein enriched with the polyene antibiotic amphotericin B. J Lipid Res. 2006;47(2):260–7. https://doi.org/10.1194/jlr.D500033-JLR200 .

Redmond KA, Nguyen TS, Ryan RO. All-trans-retinoic acid nanodisks. Int J Pharm. 2007;339(1–2):246–50. https://doi.org/10.1016/j.ijpharm.2007.02.033 .

Ghosh M, Ryan RO. ApoE enhances nanodisk-mediated curcumin delivery to glioblastoma multiforme cells. Nanomedicine (Lond). 2014;9(6):763–71. https://doi.org/10.2217/nnm.13.35 .

Singh AT, Ghosh M, Forte TM, Ryan RO, Gordon LI. Curcumin nanodisk-induced apoptosis in mantle cell lymphoma. Leuk Lymphoma. 2011;52(8):1537–43. https://doi.org/10.3109/10428194.2011.584253 .

Ghosh M, Singh AT, Xu W, Sulchek T, Gordon LI, Ryan RO. Curcumin nanodisks: formulation and characterization. Nanomedicine. 2011;7(2):162–7. https://doi.org/10.1016/j.nano.2010.08.002 .

Wang J, Jia J, Liu J, He H, Zhang W, Li Z. Tumor targeting effects of a novel modified paclitaxel-loaded discoidal mimic high density lipoproteins. Drug Deliv. 2013;20(8):356–63. https://doi.org/10.3109/10717544.2013.834418 .

Song Q, Huang M, Yao L, Wang X, Gu X, Chen J, et al. Lipoprotein-based nanoparticles rescue the memory loss of mice with Alzheimer’s disease by accelerating the clearance of amyloid-beta. ACS Nano. 2014;8(3):2345–59. https://doi.org/10.1021/nn4058215 .

Song Q, Song H, Xu J, Huang J, Hu M, Gu X, et al. Biomimetic ApoE-reconstituted high density lipoprotein nanocarrier for blood-brain barrier penetration and amyloid beta-targeting drug delivery. Mol Pharm. 2016;13(11):3976–87. https://doi.org/10.1021/acs.molpharmaceut.6b00781 .

Perez-Medina C, Tang J, Abdel-Atti D, Hogstad B, Merad M, Fisher EA, et al. PET imaging of tumor-associated macrophages with 89Zr-labeled high-density lipoprotein nanoparticles. J Nucl Med. 2015;56(8):1272–7. https://doi.org/10.2967/jnumed.115.158956 .

Sviridov D, Remaley AT. High-density lipoprotein mimetics: promises and challenges. The Biochemical journal. 2015;472(3):249–59. https://doi.org/10.1042/BJ20150832 .

Remaley AT, Thomas F, Stonik JA, Demosky SJ, Bark SE, Neufeld EB, et al. Synthetic amphipathic helical peptides promote lipid efflux from cells by an ABCA1-dependent and an ABCA1-independent pathway. J Lipid Res. 2003;44(4):828–36. https://doi.org/10.1194/jlr.M200475-JLR200 .

Schwendeman A, Sviridov DO, Yuan W, Guo Y, Morin EE, Yuan Y, et al. The effect of phospholipid composition of reconstituted HDL on its cholesterol efflux and anti-inflammatory properties. J Lipid Res. 2015;56(9):1727–37. https://doi.org/10.1194/jlr.M060285 .

Gao Y, Fang H, Fang L, Liu D, Liu J, Su M, et al. The modification and design of antimicrobial peptide. Curr Pharm Des. 2018;24:904–10. https://doi.org/10.2174/1381612824666180213130318 .

Sethi AA, Stonik JA, Thomas F, Demosky SJ, Amar M, Neufeld E, et al. Asymmetry in the lipid affinity of bihelical amphipathic peptides. A structural determinant for the specificity of ABCA1-dependent cholesterol efflux by peptides. J Biol Chem. 2008;283(47):32273–82. https://doi.org/10.1074/jbc.M804461200 .

Bielicki JK, Zhang H, Cortez Y, Zheng Y, Narayanaswami V, Patel A, et al. A new HDL mimetic peptide that stimulates cellular cholesterol efflux with high efficiency greatly reduces atherosclerosis in mice. J Lipid Res. 2010;51(6):1496–503. https://doi.org/10.1194/jlr.M003665 .

Islam RM, Pourmousa M, Sviridov D, Gordon SM, Neufeld EB, Freeman LA, et al. Structural properties of apolipoprotein A-I mimetic peptides that promote ABCA1-dependent cholesterol efflux. Sci Rep. 2018;8(1):2956. https://doi.org/10.1038/s41598-018-20965-2 .

Guo Y, Yuan W, Yu B, Kuai R, Hu W, Morin EE, et al. Synthetic high-density lipoprotein-mediated targeted delivery of liver X receptors agonist promotes atherosclerosis regression. EBioMedicine. 2018;28:225–33. https://doi.org/10.1016/j.ebiom.2017.12.021 .

Diditchenko S, Gille A, Pragst I, Stadler D, Waelchli M, Hamilton R, et al. Novel formulation of a reconstituted high-density lipoprotein (CSL112) dramatically enhances ABCA1-dependent cholesterol efflux. Arterioscler Thromb Vasc Biol. 2013;33(9):2202–11. https://doi.org/10.1161/ATVBAHA.113.301981 .

Easton R, Gille A, D’Andrea D, Davis R, Wright SD, Shear C. A multiple ascending dose study of CSL112, an infused formulation of ApoA-I. J Clin Pharmacol. 2014;54(3):301–10. https://doi.org/10.1002/jcph.194 .

Gille A, Easton R, D’Andrea D, Wright SD, Shear CL. CSL112 enhances biomarkers of reverse cholesterol transport after single and multiple infusions in healthy subjects. Arterioscler Thromb Vasc Biol. 2014;34(9):2106–14. https://doi.org/10.1161/ATVBAHA.114.303720 .

Tardif JC, Ballantyne CM, Barter P, Dasseux JL, Fayad ZA, Guertin MC, et al. Effects of the high-density lipoprotein mimetic agent CER-001 on coronary atherosclerosis in patients with acute coronary syndromes: a randomized trial. Eur Heart J. 2014;35(46):3277–86. https://doi.org/10.1093/eurheartj/ehu171 .

Tardy C, Goffinet M, Boubekeur N, Ackermann R, Sy G, Bluteau A, et al. CER-001, a HDL-mimetic, stimulates the reverse lipid transport and atherosclerosis regression in high cholesterol diet-fed LDL-receptor deficient mice. Atherosclerosis. 2014;232(1):110–8. https://doi.org/10.1016/j.atherosclerosis.2013.10.018 .

Barbaras R. Non-clinical development of CER-001. Front Pharmacol. 2015;6:220. https://doi.org/10.3389/fphar.2015.00220 .

Hovingh GK, Smits LP, Stefanutti C, Soran H, Kwok S, de Graaf J, et al. The effect of an apolipoprotein A-I-containing high-density lipoprotein-mimetic particle (CER-001) on carotid artery wall thickness in patients with homozygous familial hypercholesterolemia: the Modifying Orphan Disease Evaluation (MODE) study. Am Heart J. 2015;169(5):736–42 e1. https://doi.org/10.1016/j.ahj.2015.01.008 .

Kootte RS, Smits LP, van der Valk FM, Dasseux JL, Keyserling CH, Barbaras R, et al. Effect of open-label infusion of an apoA-I-containing particle (CER-001) on RCT and artery wall thickness in patients with FHA. J Lipid Res. 2015;56(3):703–12. https://doi.org/10.1194/jlr.M055665 .

Marsche G. It’s time to reassess the high-density lipoprotein (HDL) hypothesis: CSL112, a novel promising reconstituted HDL formulation. J Am Heart Assoc. 2015;4(8):e002371. https://doi.org/10.1161/JAHA.115.002371 .

Tardy C, Goffinet M, Boubekeur N, Cholez G, Ackermann R, Sy G, et al. HDL and CER-001 inverse-dose dependent inhibition of atherosclerotic plaque formation in apoE-/ mice: evidence of ABCA1 down-regulation. PLoS One. 2015;10(9):e0137584. https://doi.org/10.1371/journal.pone.0137584 .

Tricoci P, D’Andrea DM, Gurbel PA, Yao Z, Cuchel M, Winston B, et al. Infusion of reconstituted high-density lipoprotein, CSL112, in patients with atherosclerosis: safety and pharmacokinetic results from a phase 2a randomized clinical trial. J Am Heart Assoc. 2015;4(8):e002171. https://doi.org/10.1161/JAHA.115.002171 .

Didichenko SA, Navdaev AV, Cukier AM, Gille A, Schuetz P, Spycher MO, et al. Enhanced HDL functionality in small HDL species produced upon remodeling of HDL by reconstituted HDL, CSL112: effects on cholesterol efflux. Anti-Inflammatory and Antioxidative Activity Circulation research. 2016;119(6):751–63. https://doi.org/10.1161/CIRCRESAHA.116.308685 .

Gibson CM, Korjian S, Tricoci P, Daaboul Y, Alexander JH, Steg PG, et al. Rationale and design of Apo-I Event Reduction in Ischemic Syndromes I (AEGIS-I): a phase 2b, randomized, placebo-controlled, dose-ranging trial to investigate the safety and tolerability of CSL112, a reconstituted, infusible, human apoA-I, after acute myocardial infarction. Am Heart J. 2016;180:22–8. https://doi.org/10.1016/j.ahj.2016.06.017 .

Michael Gibson C, Korjian S, Tricoci P, Daaboul Y, Yee M, Jain P, et al. Safety and tolerability of CSL112, a reconstituted, infusible, plasma-derived apolipoprotein A-I, after acute myocardial infarction: the AEGIS-I trial (ApoA-I Event Reducing in Ischemic Syndromes I). Circulation. 2016;134(24):1918–30. https://doi.org/10.1161/CIRCULATIONAHA.116.025687 .

Zheng KH, van der Valk FM, Smits LP, Sandberg M, Dasseux JL, Baron R, et al. HDL mimetic CER-001 targets atherosclerotic plaques in patients. Atherosclerosis. 2016;251:381–8. https://doi.org/10.1016/j.atherosclerosis.2016.05.038 .

Andrews J, Janssan A, Nguyen T, Pisaniello AD, Scherer DJ, Kastelein JJ, et al. Effect of serial infusions of reconstituted high-density lipoprotein (CER-001) on coronary atherosclerosis: rationale and design of the CARAT study. Cardiovasc Diagn Ther. 2017;7(1):45–51. https://doi.org/10.21037/cdt.2017.01.01 .

Kataoka Y, Andrews J, Duong M, Nguyen T, Schwarz N, Fendler J, et al. Regression of coronary atherosclerosis with infusions of the high-density lipoprotein mimetic CER-001 in patients with more extensive plaque burden. Cardiovasc Diagn Ther. 2017;7(3):252–63. https://doi.org/10.21037/cdt.2017.02.01 .

Keyserling CH, Barbaras R, Benghozi R, Dasseux JL. Development of CER-001: preclinical dose selection through to phase I clinical findings. Clin Drug Investig. 2017;37(5):483–91. https://doi.org/10.1007/s40261-017-0506-3 .

Gille A, D’Andrea D, Tortorici MA, Hartel G, Wright SD. CSL112 (apolipoprotein A-I [human]) enhances cholesterol efflux similarly in healthy individuals and stable atherosclerotic disease patients. Arterioscler Thromb Vasc Biol. 2018;38(4):953–63. https://doi.org/10.1161/ATVBAHA.118.310538 .

Gurbel PA, Tantry US, D’Andrea D, Chung T, Alexander JH, Bliden KP, et al. Evaluation of potential antiplatelet effects of CSL112 (apolipoprotein A-I [human]) in patients with atherosclerosis: results from a phase 2a study. J Thromb Thrombolysis. 2018;45(4):469–76. https://doi.org/10.1007/s11239-018-1644-z .

Navab M, Anantharamaiah GM, Reddy ST, Fogelman AM. Apolipoprotein A-I mimetic peptides and their role in atherosclerosis prevention. Nat Clin Pract Cardiovasc Med. 2006;3(10):540–7. https://doi.org/10.1038/ncpcardio0661 .

Navab M, Anantharamaiah GM, Reddy ST, Van Lenten BJ, Datta G, Garber D, et al. Potential clinical utility of high-density lipoprotein-mimetic peptides. Curr Opin Lipidol. 2006;17(4):440–4. https://doi.org/10.1097/01.mol.0000236371.27508.d4 .

Kroenke MA, Weeraratne DK, Deng H, Sloey B, Subramanian R, Wu B, et al. Clinical immunogenicity of the d-amino acid peptide therapeutic etelcalcetide: method development challenges and anti-drug antibody clinical impact assessments. J Immunol Methods. 2017;445:37–44. https://doi.org/10.1016/j.jim.2017.03.005 .

Sacks FM, Bray GA, Carey VJ, Smith SR, Ryan DH, Anton SD, et al. Comparison of weight-loss diets with different compositions of fat, protein, and carbohydrates. N Engl J Med. 2009;360(9):859–73. https://doi.org/10.1056/NEJMoa0804748 .

Waksman R, Torguson R, Kent KM, Pichard AD, Suddath WO, Satler LF, et al. A first-in-man, randomized, placebo-controlled study to evaluate the safety and feasibility of autologous delipidated high-density lipoprotein plasma infusions in patients with acute coronary syndrome. J Am Coll Cardiol. 2010;55(24):2727–35. https://doi.org/10.1016/j.jacc.2009.12.067 .

Pollock NL, Lee SC, Patel JH, Gulamhussein AA, Rothnie AJ. Structure and function of membrane proteins encapsulated in a polymer-bound lipid bilayer. Biochim Biophys Acta. 2018;1860(4):809–17. https://doi.org/10.1016/j.bbamem.2017.08.012 .

Le Bon C, Marconnet A, Masscheleyn S, Popot JL, Zoonens M. Folding and stabilizing membrane proteins in amphipol A8-35. Methods. 2018;147:95–105. https://doi.org/10.1016/j.ymeth.2018.04.012 .

Ahn SI, Park H-J, Yom J, Kim T, Kim YT. High-density lipoprotein mimetic nanotherapeutics for cardiovascular and neurodegenerative diseases. Nano Res. 2018;11:5130–43. https://doi.org/10.1007/s12274-018-2101-1 .