Cholesterol transfer at the plasma membrane

  • Markus Axmann
    Upper Austria University of Applied Sciences, Campus Linz, Garnisonstrasse 21, 4020, Linz, Austria

    Medical University of Vienna, Center for Pathobiochemistry and Genetics, Institute of Medical Chemistry, Vienna, 1090, Austria
    Search for articles by this author
  • Witta Monika Strobl
    Medical University of Vienna, Center for Pathobiochemistry and Genetics, Institute of Medical Chemistry, Vienna, 1090, Austria
    Search for articles by this author
  • Birgit Plochberger
    Upper Austria University of Applied Sciences, Campus Linz, Garnisonstrasse 21, 4020, Linz, Austria
    Search for articles by this author
  • Herbert Stangl
    Corresponding author. Medical University of Vienna, Center for Pathobiochemistry and Genetics, Institute of Medical Chemistry, Währingerstrasse 10, Vienna, 1090, Austria.
    Medical University of Vienna, Center for Pathobiochemistry and Genetics, Institute of Medical Chemistry, Vienna, 1090, Austria
    Search for articles by this author


      • Free cholesterol transfer from lipoprotein particles to the plasma membrane occurs in mammals.
      • Amphiphilic lipid transfer occurs upon contact of lipoprotein particles to the plasma membrane.
      • Both transfer mechanisms are driven by a concentration gradient.
      • They are independent of the apolipoprotein/protein composition of the lipoprotein particle.
      • Close proximity of lipoprotein particles to the membrane yields immediate transfer of cholesterol.


      Cholesterol homeostasis is of central importance for life. Therefore, cells have developed a divergent set of pathways to meet their cholesterol needs. In this review, we focus on the direct transfer of cholesterol from lipoprotein particles to the cell membrane. More molecular details on the transfer of lipoprotein-derived lipids were gained by recent studies using phospholipid bilayers. While amphiphilic lipids are transferred right after contact of the lipoprotein particle with the membrane, the transfer of core lipids is restricted. Amphiphilic lipid transfer gains special importance in genetic diseases impairing lipoprotein metabolism like familial hypercholesterolemia. Taken together, these data indicate that there is a constant exchange of amphiphilic lipids between lipoprotein particles and the cell membrane.

      Graphical abstract


      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Atherosclerosis
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Lange Y.
        Disposition of intracellular cholesterol in human fibroblasts.
        J. Lipid Res. 1991; 32: 329-339
        • Warnock D.E.
        • Roberts C.
        • Lutz M.S.
        • et al.
        Determination of plasma membrane lipid mass and composition in cultured Chinese hamster ovary cells using high gradient magnetic affinity chromatography.
        J. Biol. Chem. 1993; 268: 10145-10153
        • Schroeder R.
        • London E.
        • Brown D.
        Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior.
        Proc. Natl. Acad. Sci. U.S.A. 1994; 91: 12130-12134
        • Simons K.
        • Ikonen E.
        Functional rafts in cell membranes.
        Nature. 1997; 387: 569-572
        • Das A.
        • Brown M.S.
        • Anderson D.D.
        • et al.
        Three pools of plasma membrane cholesterol and their relation to cholesterol homeostasis.
        Elife. 2014; 3e02882
        • Infante R.E.
        • Radhakrishnan A.
        Continuous transport of a small fraction of plasma membrane cholesterol to endoplasmic reticulum regulates total cellular cholesterol.
        Elife. 2017; 6e25466
        • Lange Y.
        • Cutler H.B.
        • Steck T.L.
        The effect of cholesterol and other intercalated amphipaths on the contour and stability of the isolated red cell membrane.
        J. Biol. Chem. 1980; 255: 9331-9337
        • Lange Y.
        • Tabei S.M.
        • Ye J.
        • et al.
        Stability and stoichiometry of bilayer phospholipid-cholesterol complexes: relationship to cellular sterol distribution and homeostasis.
        Biochemistry. 2013; 52: 6950-6959
        • Chapman M.J.
        Animal lipoproteins: chemistry, structure, and comparative aspects.
        J. Lipid Res. 1980; 21: 789-853
        • Brown D.A.
        • London E.
        Structure and function of sphingolipid- and cholesterol-rich membrane rafts.
        J. Biol. Chem. 2000; 275: 17221-17224
        • London E.
        • Brown D.A.
        Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts).
        Biochim. Biophys. Acta. 2000; 1508: 182-195
        • Iaea D.B.
        • Maxfield F.R.
        Cholesterol trafficking and distribution.
        Essays Biochem. 2015; 57: 43-55
        • Maxfield F.R.
        • van Meer G.
        Cholesterol, the central lipid of mammalian cells.
        Curr. Opin. Cell Biol. 2010; 22: 422-429
        • Kobayashi T.
        • Menon A.K.
        Transbilayer lipid asymmetry.
        Curr. Biol. 2018; 28: R386-R391
        • Steck T.L.
        • Lange Y.
        Transverse distribution of plasma membrane bilayer cholesterol: picking sides.
        Traffic. 2018; 19: 750-760
        • Courtney K.C.
        • Fung K.Y.
        • Maxfield F.R.
        • et al.
        Comment on 'Orthogonal lipid sensors identify transbilayer asymmetry of plasma membrane cholesterol'.
        Elife. 2018; 7
        • Browning K.L.
        • Lind T.K.
        • Maric S.
        • et al.
        Human lipoproteins at model cell membranes: effect of lipoprotein class on lipid exchange.
        Sci. Rep. 2017; 7: 7478
        • Meyer J.M.
        • Graf G.A.
        • van der Westhuyzen D.R.
        New developments in selective cholesteryl ester uptake.
        Curr. Opin. Lipidol. 2013; 24: 386-392
        • Acton S.
        • Rigotti A.
        • Landschulz K.T.
        • et al.
        Identification of scavenger receptor SR-BI as a high density lipoprotein receptor.
        Science (New York, N.Y). 1996; 271: 518-520
        • Brown M.S.
        • Goldstein J.L.
        A receptor-mediated pathway for cholesterol homeostasis.
        Science (New York, N.Y). 1986; 232: 34-47
        • Heeren J.
        • Beisiegel U.
        • Grewal T.
        Apolipoprotein E recycling: implications for dyslipidemia and atherosclerosis.
        Arterioscler. Thromb. Vasc. Biol. 2006; 26: 442-448
        • Mahley R.W.
        • Ji Z.S.
        Remnant lipoprotein metabolism: key pathways involving cell-surface heparan sulfate proteoglycans and apolipoprotein E.
        J. Lipid Res. 1999; 40: 1-16
        • Willnow T.E.
        • Hammes A.
        • Eaton S.
        Lipoproteins and their receptors in embryonic development: more than cholesterol clearance.
        Development. 2007; 134: 3239-3249
        • Lillis A.P.
        • Van Duyn L.B.
        • Murphy-Ullrich J.E.
        • et al.
        LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies.
        Physiol. Rev. 2008; 88: 887-918
        • Zhang X.
        • Sessa W.C.
        • Fernandez-Hernando C.
        Endothelial transcytosis of lipoproteins in atherosclerosis.
        Front. Cardiovasc. Med. 2018; 5: 130
        • Rohrl C.
        • Meisslitzer-Ruppitsch C.
        • Bittman R.
        • et al.
        Combined light and electron microscopy using diaminobenzidine photooxidation to monitor trafficking of lipids derived from lipoprotein particles.
        Curr. Pharmaceut. Biotechnol. 2012; 13: 331-340
        • Rohrl C.
        • Pagler T.A.
        • Strobl W.
        • et al.
        Characterization of endocytic compartments after holo-high density lipoprotein particle uptake in HepG2 cells.
        Histochem. Cell Biol. 2010; 133: 261-272
        • Huang L.
        • Chambliss K.L.
        • Gao X.
        • et al.
        SR-B1 drives endothelial cell LDL transcytosis via DOCK4 to promote atherosclerosis.
        Nature. 2019 May; 569: 565-569
        • Phillips M.C.
        Molecular mechanisms of cellular cholesterol efflux.
        J. Biol. Chem. 2014; 289: 24020-24029
        • Raal F.J.
        • Hovingh G.K.
        • Catapano A.L.
        Familial hypercholesterolemia treatments: guidelines and new therapies.
        Atherosclerosis. 2018; 277: 483-492
        • Fuller M.
        • Dadoo O.
        • Serkis V.
        • et al.
        The effects of diet on occlusive coronary artery atherosclerosis and myocardial infarction in scavenger receptor class B, type 1/low-density lipoprotein receptor double knockout mice.
        Arterioscler. Thromb. Vasc. Biol. 2014; 34: 2394-2403
        • Liao J.
        • Gao M.
        • Wang M.
        • et al.
        Spontaneous and diet-aggravated hemolysis and its correction by probucol in SR-BI knockout mice with LDL-R deficiency.
        Biochem. Biophys. Res. Commun. 2015; 463: 48-53
        • Liao J.
        • Guo X.
        • Wang M.
        • et al.
        Scavenger receptor class B type 1 deletion led to coronary atherosclerosis and ischemic heart disease in low-density lipoprotein receptor knockout mice on modified western-type diet.
        J. Atheroscler. Thromb. 2017; 24: 133-146
        • Guo X.
        • Liao J.
        • Huang X.
        • et al.
        Reversal of adipose tissue loss by probucol in mice with deficiency of both scavenger receptor class B type 1 and LDL receptor on high fat diet.
        Biochem. Biophys. Res. Commun. 2018; 497: 930-936
        • Goldstein J.L.
        • Brown M.S.
        • Anderson R.G.
        • et al.
        Receptor-mediated endocytosis: concepts emerging from the LDL receptor system.
        Annu. Rev. Cell Biol. 1985; 1: 1-39
        • Goldstein J.L.
        • Brown M.S.
        The LDL receptor.
        Arterioscler. Thromb. Vasc. Biol. 2009; 29: 431-438
        • Heybrock S.
        • Kanerva K.
        • Meng Y.
        • et al.
        Lysosomal integral membrane protein-2 (LIMP-2/SCARB2) is involved in lysosomal cholesterol export.
        Nat. Commun. 2019; 10: 3521
        • Glass C.
        • Pittman R.C.
        • Civen M.
        • et al.
        Uptake of high-density lipoprotein-associated apoprotein A-I and cholesterol esters by 16 tissues of the rat in vivo and by adrenal cells and hepatocytes in vitro.
        J. Biol. Chem. 1985; 260: 744-750
        • Glass C.
        • Pittman R.C.
        • Weinstein D.B.
        • et al.
        Dissociation of tissue uptake of cholesterol ester from that of apoprotein A-I of rat plasma high density lipoprotein: selective delivery of cholesterol ester to liver, adrenal, and gonad.
        Proc. Natl. Acad. Sci. U.S.A. 1983; 80: 5435-5439
        • Ikonen E.
        Cellular cholesterol trafficking and compartmentalization.
        Nat. Rev. Mol. Cell Biol. 2008; 9: 125-138
        • Sandhu J.
        • Li S.
        • Fairall L.
        • et al.
        Aster proteins facilitate nonvesicular plasma membrane to ER cholesterol transport in mammalian cells.
        Cell. 2018; 175: 514-529 e520
        • Horenkamp F.A.
        • Valverde D.P.
        • Nunnari J.
        • et al.
        Molecular basis for sterol transport by StART-like lipid transfer domains.
        EMBO J. 2018; 37
        • Kutyavin V.I.
        • Chawla A.
        Aster: A new star in cholesterol trafficking.
        Cell. 2018; 175: 307-309
        • Yancey P.G.
        • Bortnick A.E.
        • Kellner-Weibel G.
        • et al.
        Importance of different pathways of cellular cholesterol efflux.
        Arterioscler. Thromb. Vasc. Biol. 2003; 23: 712-719
        • Wustner D.
        • Mondal M.
        • Huang A.
        • et al.
        Different transport routes for high density lipoprotein and its associated free sterol in polarized hepatic cells.
        J. Lipid Res. 2004; 45: 427-437
        • Bravo E.
        • Botham K.M.
        • Mindham M.A.
        • et al.
        Evaluation in vivo of the differential uptake and processing of high-density lipoprotein unesterified cholesterol and cholesteryl ester in the rat.
        Biochim. Biophys. Acta. 1994; 1215: 93-102
        • Nestler J.E.
        • Bamberger M.
        • Rothblat G.H.
        • et al.
        Metabolism of high density lipoproteins reconstituted with [3H]cholesteryl ester and [14C]cholesterol in the rat, with special reference to the ovary.
        Endocrinology. 1985; 117: 502-510
        • Robins S.J.
        • Fasulo J.M.
        • Leduc R.
        • et al.
        The transport of lipoprotein cholesterol into bile: a reassessment of kinetic studies in the experimental animal.
        Biochim. Biophys. Acta. 1989; 1004: 327-331
        • Wustner D.
        Mathematical analysis of hepatic high density lipoprotein transport based on quantitative imaging data.
        J. Biol. Chem. 2005; 280: 6766-6779
        • Bamberger M.
        • Lund-Katz S.
        • Phillips M.C.
        • et al.
        Mechanism of the hepatic lipase induced accumulation of high-density lipoprotein cholesterol by cells in culture.
        Biochemistry. 1985; 24: 3693-3701
        • Brundert M.
        • Heeren J.
        • Greten H.
        • et al.
        Hepatic lipase mediates an increase in selective uptake of HDL-associated cholesteryl esters by cells in culture independent from SR-BI.
        J. Lipid Res. 2003; 44: 1020-1032
        • Rajan V.P.
        • Menon K.M.
        Differential uptake and metabolism of free and esterified cholesterol from high-density lipoproteins in the ovary.
        Biochim. Biophys. Acta. 1988; 959: 206-213
        • Schwartz C.C.
        • Zech L.A.
        • VandenBroek J.M.
        • et al.
        Cholesterol kinetics in subjects with bile fistula. Positive relationship between size of the bile acid precursor pool and bile acid synthetic rate.
        J. Clin. Investig. 1993; 91: 923-938
        • Schwartz C.C.
        • Halloran L.G.
        • Vlahcevic Z.R.
        • et al.
        Preferential utilization of free cholesterol from high-density lipoproteins for biliary cholesterol secretion in man.
        Science (New York, N.Y). 1978; 200: 62-64
        • Turner S.
        • Voogt J.
        • Davidson M.
        • et al.
        Measurement of reverse cholesterol transport pathways in humans: in vivo rates of free cholesterol efflux, esterification, and excretion.
        J. Am. Heart Assoc. 2012; 1e001826
        • Goodman D.S.
        • Noble R.P.
        • Dell R.B.
        Three-pool model of the long-term turnover of plasma cholesterol in man.
        J. Lipid Res. 1973; 14: 178-188
        • Schwartz C.C.
        • Berman M.
        • Vlahcevic Z.R.
        • et al.
        Multicompartmental analysis of cholesterol metabolism in man. Characterization of the hepatic bile acid and biliary cholesterol precursor sites.
        J. Clin. Investig. 1978; 61: 408-423
        • Schwartz C.C.
        • VandenBroek J.M.
        • Cooper P.S.
        Lipoprotein cholesteryl ester production, transfer, and output in vivo in humans.
        J. Lipid Res. 2004; 45: 1594-1607
        • van de Pas N.C.
        • Woutersen R.A.
        • van Ommen B.
        • et al.
        A physiologically based in silico kinetic model predicting plasma cholesterol concentrations in humans.
        J. Lipid Res. 2012; 53: 2734-2746
        • Axmann M.
        • Sezgin E.
        • Karner A.
        • et al.
        Receptor-independent transfer of low density lipoprotein cargo to biomembranes.
        Nano Lett. 2019; 19: 2562-2567
        • Plochberger B.
        • Axmann M.
        • Rohrl C.
        • et al.
        Direct observation of cargo transfer from HDL particles to the plasma membrane.
        Atherosclerosis. 2018; 277: 53-59
        • Plochberger B.
        • Rohrl C.
        • Preiner J.
        • et al.
        HDL particles incorporate into lipid bilayers - a combined AFM and single molecule fluorescence microscopy study.
        Sci. Rep. 2017; 7: 15886
        • Marques P.E.
        • Nyegaard S.
        • Collins R.F.
        • et al.
        Multimerization and retention of the scavenger receptor SR-B1 in the plasma membrane.
        Dev. Cell. 2019; 50: 283-295 e285
        • Ikonen E.
        • Kanerva K.
        Shuttling HDL cholesterol to the membrane via metastable receptor multimers.
        Dev. Cell. 2019; 50: 257-258
        • Zimetti F.
        • Weibel G.K.
        • Duong M.
        • et al.
        Measurement of cholesterol bidirectional flux between cells and lipoproteins.
        J. Lipid Res. 2006; 47: 605-613
        • Stangl H.
        • Hyatt M.
        • Hobbs H.H.
        Transport of lipids from high and low density lipoproteins via scavenger receptor-BI.
        J. Biol. Chem. 1999; 274: 32692-32698
        • Ji Y.
        • Jian B.
        • Wang N.
        • et al.
        Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux.
        J. Biol. Chem. 1997; 272: 20982-20985
        • Ji Y.
        • Wang N.
        • Ramakrishnan R.
        • et al.
        Hepatic scavenger receptor BI promotes rapid clearance of high density lipoprotein free cholesterol and its transport into bile.
        J. Biol. Chem. 1999; 274: 33398-33402
        • Ji A.
        • Meyer J.M.
        • Cai L.
        • et al.
        Scavenger receptor SR-BI in macrophage lipid metabolism.
        Atherosclerosis. 2011; 217: 106-112
        • de la Llera-Moya M.
        • Rothblat G.H.
        • Connelly M.A.
        • et al.
        Scavenger receptor BI (SR-BI) mediates free cholesterol flux independently of HDL tethering to the cell surface.
        J. Lipid Res. 1999; 40: 575-580
        • Stangl H.
        • Cao G.
        • Wyne K.L.
        • et al.
        Scavenger receptor, class B, type I-dependent stimulation of cholesterol esterification by high density lipoproteins, low density lipoproteins, and nonlipoprotein cholesterol.
        J. Biol. Chem. 1998; 273: 31002-31008
        • Rigotti A.
        • Acton S.L.
        • Krieger M.
        The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids.
        J. Biol. Chem. 1995; 270: 16221-16224
        • Gu X.
        • Lawrence R.
        • Krieger M.
        Dissociation of the high density lipoprotein and low density lipoprotein binding activities of murine scavenger receptor class B type I (mSR-BI) using retrovirus library-based activity dissection.
        J. Biol. Chem. 2000; 275: 9120-9130
        • Storey S.M.
        • McIntosh A.L.
        • Huang H.
        • et al.
        Intracellular cholesterol-binding proteins enhance HDL-mediated cholesterol uptake in cultured primary mouse hepatocytes.
        Am. J. Physiol. Gastrointest. Liver Physiol. 2012; 302: G824-G839
        • Scanu A.M.
        Structure of human serum lipoproteins.
        Ann. N. Y. Acad. Sci. 1972; 195: 390-406
        • Hevonoja T.
        • Pentikainen M.O.
        • Hyvonen M.T.
        • et al.
        Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL.
        Biochim. Biophys. Acta. 2000; 1488: 189-210
        • Lund-Katz S.
        • Phillips M.C.
        Packing of cholesterol molecules in human low-density lipoprotein.
        Biochemistry. 1986; 25: 1562-1568
        • Edge S.B.
        • Hoeg J.M.
        • Triche T.
        • et al.
        Cultured human hepatocytes. Evidence for metabolism of low density lipoproteins by a pathway independent of the classical low density lipoprotein receptor.
        J. Biol. Chem. 1986; 261: 3800-3806
        • Havel R.J.
        • Hamilton R.L.
        Hepatocytic lipoprotein receptors and intracellular lipoprotein catabolism.
        Hepatology. 1988; 8: 1689-1704
        • Fielding C.J.
        • Fielding P.E.
        Role of an N-ethylmaleimide-sensitive factor in the selective cellular uptake of low-density lipoprotein free cholesterol.
        Biochemistry. 1995; 34: 14237-14244
        • Fielding P.E.
        • Fielding C.J.
        Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae.
        Biochemistry. 1996; 35: 14932-14938
        • Fielding P.E.
        • Fielding C.J.
        Plasma membrane caveolae mediate the efflux of cellular free cholesterol.
        Biochemistry. 1995; 34: 14288-14292
        • Fong B.S.
        • Angel A.
        Transfer of free and esterified cholesterol from low-density lipoproteins and high-density lipoproteins to human adipocytes.
        Biochim. Biophys. Acta. 1989; 1004: 53-60
        • Slotte J.P.
        • Chait A.
        • Bierman E.L.
        Cholesterol accumulation in aortic smooth muscle cells exposed to low density lipoproteins. Contribution of free cholesterol transfer.
        Arteriosclerosis. 1988; 8: 750-758
        • Calvo D.
        • Gomez-Coronado D.
        • Lasuncion M.A.
        • et al.
        CLA-1 is an 85-kD plasma membrane glycoprotein that acts as a high-affinity receptor for both native (HDL, LDL, and VLDL) and modified (OxLDL and AcLDL) lipoproteins.
        Arterioscler. Thromb. Vasc. Biol. 1997; 17: 2341-2349
        • Calvo D.
        • Gomez-Coronado D.
        • Suarez Y.
        • et al.
        Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL.
        J. Lipid Res. 1998; 39: 777-788
        • Hu L.
        • van der Hoogt C.C.
        • Espirito Santo S.M.
        • et al.
        The hepatic uptake of VLDL in lrp-ldlr-/-vldlr-/- mice is regulated by LPL activity and involves proteoglycans and SR-BI.
        J. Lipid Res. 2008; 49: 1553-1561
        • Nordestgaard B.G.
        • Wootton R.
        • Lewis B.
        Selective retention of VLDL, IDL, and LDL in the arterial intima of genetically hyperlipidemic rabbits in vivo. Molecular size as a determinant of fractional loss from the intima-inner media.
        Arterioscler. Thromb. Vasc. Biol. 1995; 15: 534-542
        • Rohrl C.
        • Fruhwurth S.
        • Schreier S.M.
        • et al.
        Scavenger receptor, Class B, Type I provides an alternative means for beta-VLDL uptake independent of the LDL receptor in tissue culture.
        Biochim. Biophys. Acta. 2010; 1801: 198-204
        • Tabas I.
        • Lim S.
        • Xu X.X.
        • et al.
        Endocytosed beta-VLDL and LDL are delivered to different intracellular vesicles in mouse peritoneal macrophages.
        J. Cell Biol. 1990; 111: 929-940
        • Van Eck M.
        • Hoekstra M.
        • Out R.
        • et al.
        Scavenger receptor BI facilitates the metabolism of VLDL lipoproteins in vivo.
        J. Lipid Res. 2008; 49: 136-146
        • McLean L.R.
        • Phillips M.C.
        Mechanism of cholesterol and phosphatidylcholine exchange or transfer between unilamellar vesicles.
        Biochemistry. 1981; 20: 2893-2900
        • Lange Y.
        • Molinaro A.L.
        • Chauncey T.R.
        • et al.
        On the mechanism of transfer of cholesterol between human erythrocytes and plasma.
        J. Biol. Chem. 1983; 258: 6920-6926
        • Nishida H.I.
        • Nishida T.
        Phospholipid transfer protein mediates transfer of not only phosphatidylcholine but also cholesterol from phosphatidylcholine-cholesterol vesicles to high density lipoproteins.
        J. Biol. Chem. 1997; 272: 6959-6964
        • Kuwano T.
        • Bi X.
        • Cipollari E.
        • et al.
        Overexpression and deletion of phospholipid transfer protein reduce HDL mass and cholesterol efflux capacity but not macrophage reverse cholesterol transport.
        J. Lipid Res. 2017; 58: 731-741
        • Cuchel M.
        • Raper A.C.
        • Conlon D.M.
        • et al.
        A novel approach to measuring macrophage-specific reverse cholesterol transport in vivo in humans.
        J. Lipid Res. 2017; 58: 752-762
        • Ho Y.K.
        • Brown M.S.
        • Goldstein J.L.
        Hydrolysis and excretion of cytoplasmic cholesteryl esters by macrophages: stimulation by high density lipoprotein and other agents.
        J. Lipid Res. 1980; 21: 391-398
        • Nikolic M.
        • Stanic D.
        • Antonijevic N.
        • et al.
        Cholesterol bound to hemoglobin in normal human erythrocytes: a new form of cholesterol in circulation?.
        Clin. Biochem. 2004; 37: 22-26
        • Reinhart W.H.
        • Usami S.
        • Schmalzer E.A.
        • et al.
        Evaluation of red blood cell filterability test: influences of pore size, hematocrit level, and flow rate.
        J. Lab. Clin. Med. 1984; 104: 501-516
        • Frohlich J.
        • Godin D.V.
        Erythrocyte membrane alterations and plasma lipids in patients with chylomicronemia and in Tangier disease.
        Clin. Biochem. 1986; 19: 229-234
        • van Zwieten R.
        • Bochem A.E.
        • Hilarius P.M.
        • et al.
        The cholesterol content of the erythrocyte membrane is an important determinant of phosphatidylserine exposure.
        Biochim. Biophys. Acta. 2012; 1821: 1493-1500
        • Hung K.T.
        • Berisha S.Z.
        • Ritchey B.M.
        • et al.
        Red blood cells play a role in reverse cholesterol transport.
        Arterioscler. Thromb. Vasc. Biol. 2012; 32: 1460-1465
        • Sanchez S.A.
        • Tricerri M.A.
        • Ossato G.
        • et al.
        Lipid packing determines protein-membrane interactions: challenges for apolipoprotein A-I and high density lipoproteins.
        Biochim. Biophys. Acta. 2010; 1798: 1399-1408
        • Thomas P.D.
        • Poznansky M.J.
        Effect of surface curvature on the rate of cholesterol transfer between lipid vesicles.
        Biochem. J. 1988; 254: 155-160
        • Massey J.B.
        • Gotto A.M.
        • Pownall H.J.
        Kinetics and mechanism of the spontaneous transfer of fluorescent phospholipids between apolipoprotein-phospholipid recombinants - effect of the polar headgroup.
        J. Biol. Chem. 1982; 257: 5444-5448
        • Estronca L.M.
        • Filipe H.A.
        • Salvador A.
        • et al.
        Homeostasis of free cholesterol in the blood: a preliminary evaluation and modeling of its passive transport.
        J. Lipid Res. 2014; 55: 1033-1043