Advertisement
Review article| Volume 315, P111-125, December 2020

Transendothelial transport of lipoproteins

  • Erika Jang
    Affiliations
    Keenan Centre for Biomedical Research, St. Michael's Hospital, Toronto, Canada

    Department of Laboratory Medicine and Pathobiology, University of Toronto, Canada
    Search for articles by this author
  • Jerome Robert
    Affiliations
    Institute of Clinical Chemistry, University of Zurich and University Hospital of Zurich, Switzerland
    Search for articles by this author
  • Lucia Rohrer
    Affiliations
    Institute of Clinical Chemistry, University of Zurich and University Hospital of Zurich, Switzerland
    Search for articles by this author
  • Arnold von Eckardstein
    Correspondence
    Corresponding author. University Hospital Zurich, Institute of Clinical Chemistry, Raemistrasse 100, CH 8091, ZURICH, Switzerland.
    Affiliations
    Institute of Clinical Chemistry, University of Zurich and University Hospital of Zurich, Switzerland
    Search for articles by this author
  • Warren L. Lee
    Correspondence
    Corresponding author. Keenan Centre for Biomedical Research, St. Michael's Hospital, 30 Bond St, Toronto, Ontario, Canada.
    Affiliations
    Keenan Centre for Biomedical Research, St. Michael's Hospital, Toronto, Canada

    Department of Laboratory Medicine and Pathobiology, University of Toronto, Canada

    Interdepartmental Division of Critical Care, Department of Medicine, University of Toronto, Canada

    Department of Biochemistry, University of Toronto, Canada

    Institute of Medical Science, University of Toronto, Canada
    Search for articles by this author

      Highlights

      • The endothelium limits the entry and exit of lipoproteins into and from the arterial wall, respectively.
      • SR-BI, activin like kinase 1, and caveolin-1 as well as GPER and sphingosine-1-phosphate regulate the transcytosis of LDL.
      • SR-BI, ABCG1, endothelial lipase, the ecto-ATPase/P2Y-receptor axis, VEGF, IL-6/17, and S1P regulate HDL transcytosis.

      Abstract

      The accumulation of low-density lipoproteins (LDL) in the arterial wall plays a pivotal role in the initiation and pathogenesis of atherosclerosis. Conversely, the removal of cholesterol from the intima by cholesterol efflux to high density lipoproteins (HDL) and subsequent reverse cholesterol transport shall confer protection against atherosclerosis. To reach the subendothelial space, both LDL and HDL must cross the intact endothelium. Traditionally, this transit is explained by passive filtration. This dogma has been challenged by the identification of several rate-limiting factors namely scavenger receptor SR-BI, activin like kinase 1, and caveolin-1 for LDL as well as SR-BI, ATP binding cassette transporter G1, and endothelial lipase for HDL. In addition, estradiol, vascular endothelial growth factor, interleukins 6 and 17, purinergic signals, and sphingosine-1-phosphate were found to regulate transendothelial transport of either LDL or HDL. Thorough understanding of transendothelial lipoprotein transport is expected to elucidate new therapeutic targets for the treatment or prevention of atherosclerotic cardiovascular disease and the development of strategies for the local delivery of drugs or diagnostic tracers into diseased tissues including atherosclerotic lesions.

      Graphical abstract

      Keywords

      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:

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

      References

        • Martel C.
        • et al.
        Lymphatic vasculature mediates macrophage reverse cholesterol transport in mice.
        J. Clin. Invest. 2013; 123: 1571-1579
        • Williams K.J.
        • Tabas I.
        The response-to-retention hypothesis of early atherogenesis.
        Arterioscler. Thromb. Vasc. Biol. 1995; 15: 551-562
        • Fung K.Y.Y.
        • Fairn G.D.
        • Lee W.L.
        Transcellular vesicular transport in epithelial and endothelial cells: challenges and opportunities.
        Traffic. 2018; 19: 5-18
        • Rippe B.
        • Haraldsson B.
        Transport of macromolecules across microvascular walls: the two-pore theory.
        Physiol. Rev. 1994; 74: 163-219
        • Michel C.C.
        • Curry F.E.
        Microvascular permeability.
        Physiol. Rev. 1999; 79: 703-761
        • Aird W.C.
        Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms.
        Circ. Res. 2007; 100: 158-173
        • Aird W.C.
        Phenotypic heterogeneity of the endothelium: II. Representative vascular beds.
        Circ. Res. 2007; 100: 174-190
      1. Andreone, B. J. et al. Blood-brain barrier permeability is regulated by lipid transport-dependent suppression of caveolae-mediated transcytosis. Neuron 94, 581–594 (3027).

        • Armstrong S.M.
        • et al.
        A novel assay uncovers an unexpected role for SR-BI in LDL transcytosis.
        Cardiovasc. Res. 2015; 108: 268-277
        • Huang L.
        • et al.
        SR-B1 drives endothelial cell LDL transcytosis via DOCK4 to promote atherosclerosis.
        Nature. 2019; 569: 565-569
        • Dehouck B.
        • et al.
        A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier.
        J. Cell Biol. 1997; 138: 877-889
        • Miranda C.H.
        • de Carvalho Borges M.
        • Schmidt A.
        • Marin-Neto J.A.
        • Pazin-Filho A.
        Evaluation of the endothelial glycocalyx damage in patients with acute coronary syndrome.
        Atherosclerosis. 2016; 247: 184-188
        • Yang Y.
        • Schmidt E.
        The endothelial glycocalyx: an important regulator of the pulmonary vascular barrier.
        Tissue Barriers. 2013; 1e23494
        • Skålén K.
        • et al.
        Subendothelial retention of atherogenic lipoproteins in early atherosclerosis.
        Nature. 2002; 417: 750-754
        • Sprague E.A.
        • Steinbach B.L.
        • Nerem R.M.
        • Schwartz C.J.
        Influence of a laminar steady-state fluid-imposed wall shear stress on the binding, internalization, and degradation of low-density lipoproteins by cultured arterial endothelium.
        Circulation. 1987; 76: 648-656
        • Pappenheimer J.R.
        • Renkin E.M.
        • Borrero L.M.
        Filtration, diffusion and molecular sieving through peripheral capillary membranes: a contribution to the Pore Theory of capillary permeability.
        Am. J. Physiol. 1951; 167: 13-46
        • Rippe B.
        • Rosengren B.I.
        • Carlsson O.
        • Venturoli D.
        Transendothelial transport: the vesicle controversy.
        J. Vasc. Res. 2002; 39: 375-390
        • Grotte G.
        Passage of dextran molecules across the blood-lymph barrier.
        Acta Chir. Scand. 1956; 211: 1-84
        • Rippe B.
        • Kamiya A.
        • Folkow B.
        Transcapillary passage of albumin, effects of tissue cooling and of increases in filtration and plasma colloid osmotic pressure.
        Acta Physiol. Scand. 1979; 105: 171-187
        • Stender S.
        • Zilversmit D.B.
        Transfer of plasma lipoprotein components and of plasma proteins into aortas of cholesterol-fed rabbits. Molecular size as a determinant of plasma lipoprotein influx.
        Arteriosclerosis. 1981; 1: 38-49
        • Nordestgaard B.G.
        • Hjelms E.
        • Stender S.
        • Kjeldsen K.
        Different efflux pathways for high and low density lipoproteins from porcine aortic intima.
        Arterioscler. Thromb. Vasc. Biol. 1990; 10: 477-485
        • Nordestgaard B.G.
        • Tybjaerg-Hansen A.
        • Lewis B.
        Influx in vivo of low density, intermediate density, and very low density lipoproteins into aortic intimas of genetically hyperlipidemic rabbits: roles of plasma concentration, extent of aortic lesion, and lipoprotein particle size as determinants.
        Arterioscler. Thromb. 1992; 12: 6-18
        • 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
        • Shaikh M.
        • et al.
        Quantitative studies of transfer in vivo of low density, Sf 12-60, and Sf 60-400 lipoproteins between plasma and arterial intima in humans.
        Arterioscler. Thromb. 1991; 11: 569-577
        • Björnheden T.
        • Babyi A.
        • Bondjers G.
        • Wiklund O.
        Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system.
        Atherosclerosis. 1996; : 123 43-56
        • Michel C.C.
        • Nanjee M.N.
        • Olszewski W.L.
        • Miller N.E.
        LDL and HDL transfer rates across peripheral microvascular endothelium agree with those predicted for passive ultrafiltration in humans.
        J. Lipid Res. 2015; 56: 122-128
        • Simionescu M.
        • Simionescu N.
        • Palade G.E.
        Morphometric data on the endothelium of blood capillaries.
        J. Cell Biol. 1974; 60: 128-152
        • Palade G.E.
        • Bruns R.R.
        Structural modulations of plasmalemmal vesicles.
        J. Cell Biol. 1968; 37: 633-649
        • Bruns R.R.
        • Palade G.E.
        Studies on blood capillaries. II. Transport of ferritin molecules across the wall of muscle capillaries.
        J. Cell Biol. 1968; 37: 277-299
        • Simionescu N.
        • Simionescu M.
        • Palade G.E.
        Permeability of muscle capillaries to small heme-peptides.
        J. Cell Biol. 1975; 64: 586-607
        • Vasile E.
        • Simionescu M.
        • Simionescu N.
        Visualization of the binding, endocytosis, and transcytosis of low-density lipoprotein in the arterial endothelium in situ.
        J. Cell Biol. 1983; 96: 1677-1689
        • Wilson D.W.
        • et al.
        A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast.
        Nature. 1989; 339: 355-359
        • Snelting-Havinga I.
        • et al.
        Immunoelectron microscopic visualization of the transcytosis of low density lipoproteins in perfused rat arteries.
        Eur. J. Cell Biol. 1989; 48: 27-36
        • Cancel L.M.
        • Fitting A.
        • Tarbell J.M.
        In vitro study of LDL transport under pressurized (convective) conditions.
        Am. J. Physiol. Heart Circ. Physiol. 2007; 293: 126-132
        • Lin S.J.
        • Jan K.M.
        • Chien S.
        Role of dying endothelial cells in transendothelial macromolecular transport.
        Arterioscler. Thromb. Vasc. Biol. 1990; 10: 703-709
        • Lin S.-J.
        • Jan K.-M.
        • Weinbaum S.
        • Chien S.
        Transendothelial transport of low density lipoprotein in association with cell mitosis in rat aorta.
        Arteriosclerosis. 1989; 9: 230-236
        • Cancel L.M.
        • Tarbell J.M.
        The role of mitosis in LDL transport through cultured endothelial cell monolayers.
        Am. J. Physiol. Heart Circ. Physiol. 2011; 300: H769-H776
        • Taylor K.E.
        • Glagov S.
        • Zarins C.Z.
        Preservation and structural adaptation of endothelium over experimental foam cell lesions.
        Quantitative ultrastructural study. Arteriosclerosis. 1989; 9: 881-894
        • Chang M.Y.
        • Lees A.M.
        • Lees R.S.
        Time course of 125I-labeled LDL accumulation in the healing, balloon-deendothelialized rabbit aorta.
        Arterioscler. Thromb. 1992; 12: 1088-1098
        • Minick C.R.
        • Stemerman M.B.
        • Insull W.
        Effect of regenerated endothelium on lipid accumulation in the arterial wall.
        Proc. Natl. Acad. Sci. U.S.A. 1977; 74: 1724-1728
        • Von Eckardstein A.
        • Rohrer L.
        Transendothelial lipoprotein transport and regulation of endothelial permeability and integrity by lipoproteins.
        Curr. Opin. Lipidol. 2009; 20: 197-205
        • Kontush A.
        HDL particle number and size as predictors of cardiovascular disease.
        Front. Pharmacol. 2015; 6: 1-6
        • Christoffersen C.
        • et al.
        Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M.
        Proc. Natl. Acad. Sci. U.S.A. 2011; 108: 9613-9618
        • Christensen P.M.
        • et al.
        Impaired endothelial barrier function in apolipoprotein M-deficient mice is dependent on sphingosine-1-phosphate receptor 1.
        Faseb. J. 2016; 30: 2351-2359
        • Janiurek M.M.
        • Soylu-Kucharz R.
        • Christoffersen C.
        • Kucharz K.
        • Lauritzen M.
        Apolipoprotein M-bound sphingosine-1-phosphate regulates blood–brain barrier paracellular permeability and transcytosis.
        Elife. 2019; 8: 1-22
        • Del Gaudio I.
        • et al.
        Circulating cord blood HDL-S1P complex preserves the integrity of the feto-placental vasculature.
        Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2020; 1865
        • Schnitzer J.E.
        • Oh P.
        • Pinney E.
        • Allard J.
        Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules.
        J. Cell Biol. 1994; 127: 1217-1232
        • Schnitzer J.E.
        • Allard J.
        • Oh P.
        NEM inhibits transcytosis, endocytosis, and capillary permeability: implication of caveolae fusion in endothelia.
        Am. J. Physiol. Heart Circ. Physiol. 1995; 268: 48-55
        • Carlsson O.
        • Rosengren B.I.
        • Rippe B.
        Transcytosis inhibitor N-ethylmaleimide increases microvascular permeability in rat muscle.
        Am. J. Physiol. Heart Circ. Physiol. 2001; 281: 1728-1733
        • Drab M.
        • et al.
        Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice.
        Science. 2001; 293: 2449-2452
        • Schubert W.
        • et al.
        Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo.
        J. Biol. Chem. 2001; 276: 48619-48622
        • Schubert W.
        • et al.
        Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice.
        J. Biol. Chem. 2002; 277: 40091-40098
        • Frank P.G.
        • Pavlides S.
        • Cheung M.W.C.
        • Daumer K.
        • Lisanti M.P.
        Role of caveolin-1 in the regulation of lipoprotein metabolism.
        Am. J. Physiol. Cell Physiol. 2008; 295: 242-248
        • Frank P.G.
        • et al.
        Genetic ablation of caveolin-1 confers protection against atherosclerosis.
        Arterioscler. Thromb. Vasc. Biol. 2004; 24: 98-105
        • Fernández-Hernando C.
        • Yu J.
        • Dávalos A.
        • Prendergast J.
        • Sessa W.C.
        Endothelial-specific overexpression of caveolin-1 accelerates atherosclerosis in apolipoprotein E-deficient mice.
        Am. J. Pathol. 2010; 177: 998-1003
        • Sobal G.
        • Resch U.
        • Sinzinger H.
        Modification of low-density lipoprotein by different radioiodination methods.
        Nucl. Med. Biol. 2004; 31: 381-388
        • Fung K.Y.
        • et al.
        SR-BI mediated transcytosis of HDL in brain microvascular endothelial cells is independent of caveolin, clathrin, and PDZK1.
        Front. Physiol. 2017; 8: 1-16
        • Rohrer L.
        • et al.
        High-density lipoprotein transport through aortic endothelial cells involves scavenger receptor BI and ATP-binding cassette transporter G1.
        Circ. Res. 2009; 104: 1142-1150
        • Kraehling J.R.
        • et al.
        Genome-wide RNAi screen reveals ALK1 mediates LDL uptake and transcytosis in endothelial cells.
        Nat. Commun. 2016; 7: 1-15
        • Lim H.Y.
        • et al.
        Lymphatic vessels are essential for the removal of cholesterol from peripheral tissues by SR-BI-Mediated transport of HDL.
        Cell Metabol. 2013; 17: 671-684
        • Mulligan-Kehoe M.J.
        The vasa vasorum in diseased and nondiseased arteries.
        Am. J. Physiol. Heart Circ. Physiol. 2010; 298: 295-305
        • Bratzler R.L.
        • Chisolm G.M.
        • Colton C.K.
        • Smith K.A.
        • Lees R.S.
        The distribution of labeled low-density lipoproteins across the rabbit thoracic aorta in vivo.
        Atherosclerosis. 1977; 28: 289-307
        • Adams C.W.
        • Virág S.
        • Morgan R.S.
        • Orton C.C.
        Dissociation of [3H]cholesterol and 125I-labelled plasma protein influx in normal and atheromatous rabbit aorta. A quantitative histochemical study.
        J. Atherosclerosis Res. 1968; 8: 679-696
        • John T.A.
        • Vogel S.M.
        • Tiruppathi C.
        • Malik A.B.
        • Minshall R.D.
        Quantitative analysis of albumin uptake and transport in the rat microvessel endothelial monolayer.
        Am. J. Physiol. Lung Cell Mol. Physiol. 2003; 284: 187-196
        • Raheel H.
        • et al.
        CD36 mediates albumin transcytosis by dermal but not lung microvascular endothelial cells: role in fatty acid delivery.
        Am. J. Physiol. Lung Cell Mol. Physiol. 2019; 316: L740-L750
        • Azizi P.M.
        • et al.
        Clathrin-dependent entry and vesicle-mediated exocytosis define insulin transcytosis across microvascular endothelial cells.
        Mol. Biol. Cell. 2015; 26: 740-750
        • Goldstein J.L.
        • Brown M.S.
        A century of cholesterol and coronaries: from plaques to genes to statins.
        Cell. 2015; 161: 161-172
        • Ramkumar S.
        • Raghunath A.
        • Raghunath S.
        Statin therapy: review of safety and potential side effects.
        Acta Cardiol. Sin. 2016; 32: 631-639
        • Scandinavian Simvastatin Survival Study Group
        Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S).
        Lancet. 1994; 344: 1383-1389
        • Sever P.S.
        • et al.
        Prevention of coronary and stroke events with atorvastatin in hypertensive patients who have average or lower-than-average cholesterol concentrations, in the Anglo-Scandinavian Cardiac Outcomes Trial - lipid Lowering Arm (ASCOT-LLA): a multicentre randomi.
        Lancet. 2003; 361: 1149-1158
        • Ross R.
        • Glomset J.
        • Harker L.
        Response to injury and atherogenesis.
        Am. J. Pathol. 1977; 86: 675-684
        • Hjelms E.
        • Stender S.
        Accelerated cholesterol accumulation in homologous arterial transplants in cholesterol-fed rabbits: a surgical model to study transplantation atherosclerosis.
        Arterioscler. Thromb. Vasc. Biol. 1992; 12: 771-779
        • Schwenke D.C.
        • Zilversmit D.B.
        Enhanced accumulation and turnover of esterified cholesterol in injured rabbit aorta.
        Arteriosclerosis. 1987; 7: 367-377
        • Schwenke D.C.
        • Zilversmit D.B.
        The arterial barrier to lipoprotein influx in the hypercholesterolemic rabbit. 2. Long-term studies in deendothelialized and reendothelialized aortas.
        Atherosclerosis. 1989; 77: 105-115
        • Katsuda S.
        • Boyd H.C.
        • Fligner C.
        • Ross R.
        • Gown A.M.
        Human atherosclerosis: III. Immunocytochemical analysis of the cell composition of lesions of young adults.
        Am. J. Pathol. 1992; 140: 907-914
        • Tabas I.
        • Williams K.J.
        • Borén J.
        Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications.
        Circulation. 2007; 116: 1832-1844
        • Schwenke D.C.
        • Carew T.E.
        Initiation of atherosclerotic lesions in cholesterol-fed rabbits. I. Focal increases in arterial LDL concentration precede development of fatty streak lesions.
        Arteriosclerosis. 1989; 9: 895-907
        • Schwenke D.C.
        • Carew T.E.
        Initiation of atherosclerotic lesions in cholesterol-fed rabbits. II. Selective retention of LDL vs. selective increases in LDL permeability in susceptible sites of arteries.
        Arteriosclerosis. 1989; 9: 908-918
        • Proctor S.D.
        • Vine D.F.
        • Mamo J.C.L.
        Arterial permeability and efflux of apolipoprotein B-containing lipoproteins assessed by in situ perfusion and three-dimensional quantitative confocal microscopy.
        Arterioscler. Thromb. Vasc. Biol. 2004; 24: 2162-2167
        • Tolleshaug H.
        • Hobgood K.K.
        • Brown M.S.
        • Goldstein J.L.
        The LDL receptor locus in familial hypercholesterolemia: multiple mutations disrupt transport and processing of a membrane receptor.
        Cell. 1983; 32: 941-951
        • Davis C.G.
        • et al.
        The J. D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors.
        Cell. 1986; 45: 15-24
        • Calvo D.
        • Gómez-Coronado D.
        • Lasunción M.A.
        • Vega M.A.
        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
        • Vaisman B.L.
        • et al.
        Endothelial expression of scavenger receptor class B, type I protects against development of atherosclerosis in mice.
        BioMed Res. Int. 2015; 1–13 (2015)
        • Westerterp M.
        • et al.
        Deficiency of ATP-binding cassette transporters A1 and G1 in endothelial cells accelerates atherosclerosis in mice.
        Arterioscler. Thromb. Vasc. Biol. 2016; 36: 1328-1337
        • Calvo D.
        • Gómez-Coronado D.
        • Suárez Y.
        • Lasunción M.A.
        • Vega M.A.
        Human CD36 is a high affinity receptor for the native lipoproteins HDL, LDL, and VLDL.
        J. Lipid Res. 1998; 39: 777-788
        • Adachi H.
        • Tsujimoto M.
        Endothelial scavenger receptors.
        Prog. Lipid Res. 2006; 45: 379-404
        • Mineo C.
        • Shaul P.W.
        Role of high-density lipoprotein and scavenger receptor B type I in the promotion of endothelial repair.
        Trends Cardiovasc. Med. 2007; 17: 156-161
        • Wang D.
        • et al.
        SR-BI as a target of natural products and its significance in cancer.
        Semin. Canc. Biol. 2020; https://doi.org/10.1016/j.semcancer.2019.12.025
        • Tan J.T.M.
        • et al.
        High-density lipoproteins rescue diabetes-impaired angiogenesis via scavenger receptor Class B Type i.
        Diabetes. 2016; 65: 3091-3103
        • Zhu W.
        • et al.
        PDZK1 Maintains Endothelial Monolayer Integrity.
        2008: 480-487https://doi.org/10.1161/CIRCRESAHA.107.159079
        • Lu S.M.
        • Fairn G.D.
        Mesoscale organization of domains in the plasma membrane–beyond the lipid raft.
        Crit. Rev. Biochem. Mol. Biol. 2018; 53: 192-207
        • Palade G.E.
        Blood capillaries of the heart and other organs.
        Circulation. 1961; 24: 368-384
        • Santibanez J.F.
        • et al.
        Caveolin-1 interacts and cooperates with the transforming growth factor-β type I receptor ALK1 in endothelial caveolae.
        Cardiovasc. Res. 2008; 77: 791-799
        • Briand O.
        • et al.
        SR-BI does not require raft/caveola localisation for cholesteryl ester selective uptake in the human adrenal cell line NCI-H295R.
        Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2003; 1631: 42-50
        • Wang D.-X.
        • Pan Y.-Q.
        • Liu B.
        • Dai L.
        Cav-1 promotes atherosclerosis by activating JNK-associated signaling.
        Biochem. Biophys. Res. Commun. 2018; 503: 513-520
        • Fernández-Hernando C.
        • et al.
        Genetic evidence supporting a critical role of endothelial caveolin-1 during the progression of atherosclerosis.
        Cell Metabol. 2009; 10: 48-54
        • Ramírez C.M.
        • et al.
        Caveolin-1 regulates atherogenesis by attenuating low-density lipoprotein transcytosis and vascular inflammation independently of endothelial nitric oxide synthase activation.
        Circulation. 2019; 140: 225-239
        • Armstrong S.M.
        • et al.
        Co-regulation of transcellular and paracellular leak across microvascular endothelium by dynamin and Rac.
        Am. J. Pathol. 2012; 180: 1308-1323
        • Couet J.
        • Li S.
        • Okamoto T.
        • Ikezu T.
        • Lisanti M.P.
        Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins.
        J. Biol. Chem. 1997; 272: 6525-6533
        • Pol A.
        • Ortega D.
        • Enrich C.
        Identification of cytoskeleton-associated proteins in isolated rat liver endosomes.
        Biochem. J. 1997; 327: 741-746
        • Lisanti M.P.
        • et al.
        Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease.
        J. Cell Biol. 1994; 126: 111-126
        • Sverdlov M.
        • Shinin V.
        • Place A.T.
        • Castellon M.
        • Minshall R.D.
        Filamin A regulates caveolae internalization and trafficking in endothelial cells.
        Mol. Biol. Cell. 2009; 20: 4531-4540
        • Tuma P.L.
        • Hubbard A. L. Transcytosis
        Crossing cellular barriers.
        Physiol. Rev. 2003; 83: 871-932
        • Villaseñor R.
        • Schilling M.
        • Sundaresan J.
        • Lutz Y.
        • Collin L.
        Sorting tubules regulate blood-brain barrier transcytosis.
        Cell Rep. 2017; 21: 3256-3270
        • Goldstein J.L.
        • Brown M.S.
        History of Discovery : the LDL receptor.
        Arterioscler. Thromb. Vasc. Biol. 2010; 29: 431-438
        • Steinberg D.
        The LDL modification hypothesis of atherogenesis: an update.
        J. Lipid Res. 2009; 50: S376-S381
        • Parthasarathy S.
        • Steinbrecher U.P.
        • Barnett J.
        • Witztum J.L.
        • Steinberg D.
        Essential role of phospholipase A2 activity in endothelial cell-induced modification of low density lipoprotein.
        Proc. Natl. Acad. Sci. U.S.A. 1985; 82: 3000-3004
        • Yoshida H.
        • Kisugi R.
        Mechanisms of LDL oxidation.
        Clin. Chim. Acta. 2010; 411: 1875-1882
        • Steinbrecher U.P.
        • Parthasarathy S.
        • Leake D.S.
        • Witztum J.L.
        • Steinberg D.
        Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids.
        Proc. Natl. Acad. Sci. U.S.A. 1984; 81: 3883-3887
        • Kuner T.
        • Li Y.
        • Gee K.R.
        • Bonewald L.F.
        • Augustine G.J.
        Photolysis of a caged peptide reveals rapid action of N-ethylmaleimide sensitive factor before neurotransmitter release.
        Proc. Natl. Acad. Sci. U.S.A. 2008; 105: 347-352
        • Predescu S.A.
        • Predescu D.N.
        • Palade G.E.
        Endothelial transcytotic machinery involves supramolecular protein – lipid complexes.
        Mol. Biol. Cell. 2001; 12: 1019-1033
        • Lee W.
        • Cheung A.
        • Cape D.
        • Zinman B.
        Impact of diabetes on coronary artery disease in women and men: a meta-analysis of prospective studies.
        Diabetes Care. 2000; 23: 962-968
        • Barrett-Connor E.
        • Bush T.L.
        Estrogen and coronary heart disease in women.
        J. Am. Med. Assoc. 1991; 265: 1861-1867
        • Bush T.L.
        • et al.
        Cardiovascular mortality and noncontraceptive use of estrogen in women: results from the lipid research clinics program follow-up study.
        Circulation. 1987; 75: 1102-1109
        • Billon-Galés A.
        • et al.
        Endothelial estrogen receptor-α plays a crucial role in the atheroprotective action of 17β-estradiol in low-density lipoprotein receptor-deficient mice.
        Circulation. 2009; 120: 2567-2576
        • Wagner J.D.
        • et al.
        Estrogen and progesterone replacement therapy reduces low density lipoprotein accumulation in the coronary arteries of surgically postmenopausal cynomolgus monkeys.
        J. Clin. Invest. 1991; 88: 1995-2002
        • Ghaffari S.
        • Nabi F.N.
        • Sugiyama M.G.
        • Lee W.L.
        Estrogen inhibits LDL (low-density lipoprotein) transcytosis by human coronary artery endothelial cells via GPER (G-protein-coupled estrogen receptor) and SR-BI (scavenger receptor class B type 1).
        Arterioscler. Thromb. Vasc. Biol. 2018; 38: 2283-2294
        • Jensen J.S.
        • et al.
        Transendothelial lipoprotein exchange and microalbuminuria.
        Cardiovasc. Res. 2004; 63: 149-154
        • Kornerup K.
        • et al.
        Transendothelial exchange of low-density lipoprotein is unaffected by the presence of severe atherosclerosis.
        Cardiovasc. Res. 2004; 64: 337-345
        • Meyer G.
        • Merval R.
        • Tedgui A.
        Effects of pressure-induced stretch and convection on low-density lipoprotein and albumin uptake in the rabbit aortic wall.
        Circ. Res. 1996; 79: 532-540
        • Chobanian A.V.
        • et al.
        Influence of hypertension on aortic atherosclerosis in the Watanabe rabbit.
        Hypertension. 1989; 14: 203-209
        • Bartels E.D.
        • Christoffersen C.
        • Lindholm M.W.
        • Nielsen L.B.
        Altered metabolism of LDL in the arterial wall precedes atherosclerosis regression.
        Circ. Res. 2015; 117: 933-942
        • Bai X.
        • et al.
        CAV1-CAVIN1-LC3B-mediated autophagy regulates high glucose-stimulated LDL transcytosis.
        Autophagy. 2019; https://doi.org/10.1080/15548627.2019.1659613
        • Torisu K.
        • et al.
        Intact endothelial autophagy is required to maintain vascular lipid homeostasis.
        Aging Cell. 2016; 15: 187-191
        • Zhang X.
        • et al.
        Cav-1 (Caveolin-1) deficiency increases autophagy in the endothelium and attenuates vascular inflammation and atherosclerosis.
        Arterioscler. Thromb. Vasc. Biol. 2020; 40: 1510-1522
        • Zhang Y.
        • et al.
        TNF-α promotes early atherosclerosis by increasing transcytosis of LDL across endothelial cells: crosstalk between NF-κB and PPAR-γ.
        J. Mol. Cell. Cardiol. 2014; 72: 85-94
        • Bian F.
        • et al.
        C-reactive protein promotes atherosclerosis by increasing LDL transcytosis across endothelial cells.
        Br. J. Pharmacol. 2014; 171: 2671-2684
        • Bian F.
        • Yang X.-Y.
        • Xu G.
        • Zheng T.
        • Jin S.
        CRP-Induced NLRP3 inflammasome activation increases LDL transcytosis across endothelial cells.
        Front. Pharmacol. 2019; 9: 1-11
        • Li C.
        • et al.
        CTRP5 promotes transcytosis and oxidative modification of low-density lipoprotein and the development of atherosclerosis.
        Atherosclerosis. 2018; 278: 197-209
        • Cartier A.
        • Hla T.
        Sphingosine 1-phosphate: lipid signaling in pathology and therapy.
        Science. 2019; 80–: 366
        • Feuerborn R.
        • et al.
        Elevating endogenous sphingosine-1-phosphate (S1P) levels improves endothelial function and ameliorates atherosclerosis in low density lipoprotein receptor-deficient (LDL-R -/-) mice.
        Thromb. Haemostasis. 2018; 118: 1470-1480
        • Velagapudi V.
        • et al.
        DIFFERERENTIAL AND ANTAGONISTIC REGULATION OF TRANSENDOTHELIAL TRANSPORT OF HDL AND LDL BY SPHINGOSINE-1-PHOSPHATE RECEPTORS 1 AND 3.
        ATHEROSCLEROSIS, 2018 (Meeting abstract LB1:2 E3–E3)
        • Gilibert S.
        • et al.
        Adrenocortical scavenger receptor class B type I deficiency exacerbates endotoxic shock and precipitates sepsis-induced mortality in mice.
        J. Immunol. 2014; 193: 817-826
        • Walley K.R.
        • et al.
        The central role of proprotein convertase subtilisin/kexin type 9 in septic pathogen lipid transport and clearance.
        Am. J. Respir. Crit. Care Med. 2015; 192: 1275-1286
        • Walley K.R.
        • et al.
        PCSK9 is a critical regulator of the innate immune response and septic shock outcome.
        Sci. Transl. Med. 2014; 6: 258ra143
        • März W.
        • et al.
        HDL cholesterol: reappraisal of its clinical relevance.
        Clin. Res. Cardiol. 2017; 106: 663-675
        • Annema W.
        • von Eckardstein A.
        High-density lipoproteins. Multifunctional but vulnerable protections from atherosclerosis.
        Circ. J. 2013; 77: 2432-2448
        • Karjalainen M.K.
        • et al.
        Apolipoprotein A-I concentrations and risk of coronary artery disease: a Mendelian randomization study.
        Atherosclerosis. 2020; 299: 56-63
        • Richardson T.G.
        • et al.
        Evaluating the relationship between circulating lipoprotein lipids and apolipoproteins with risk of coronary heart disease: a multivariable Mendelian randomisation analysis.
        PLoS Med. 2020; 17e1003062
        • Randolph G.J.
        • Miller N.E.
        Lymphatic transport of high-density lipoproteins and chylomicrons.
        J. Clin. Invest. 2014; 124: 929-935
        • Mackness B.
        • Hunt R.
        • Durrington P.N.
        • Mackness M.I.
        Increased immunolocalization of paraoxonase, clusterin, and apolipoprotein A-I in the human artery wall with the progression of atherosclerosis.
        Arterioscler. Thromb. Vasc. Biol. 1997; 17: 1233-1238
        • Huang Y.
        • et al.
        An abundant dysfunctional apolipoprotein A1 in human atheroma.
        Nat. Med. 2014; 20: 193-203
        • Ishikawa Y.
        • et al.
        Immunolocalization of apolipoproteins in aortic atherosclerosis in American youths and young adults: findings from the PDAY study.
        Atherosclerosis. 2001; 158: 215-225
        • Nordestgaard B.G.
        • Hjelms E.
        • Stender S.
        • Kjeldsen K.
        Different efflux pathways for high and low density lipoproteins from porcine aortic intima.
        Arteriosclerosis. 1990; 10: 477-485
        • Cavelier C.
        • Rohrer L.
        • Von Eckardstein A.
        ATP-binding cassette transporter A1 modulates apolipoprotein A-I transcytosis through aortic endothelial cells.
        Circ. Res. 2006; 99: 1060-1066
        • Cavelier C.
        • Ohnsorg P.M.
        • Rohrer L.
        • von Eckardstein A.
        The beta-chain of cell surface F(0)F(1) ATPase modulates apoA-I and HDL transcytosis through aortic endothelial cells.
        Arterioscler. Thromb. Vasc. Biol. 2012; 32: 131-139
        • Robert J.
        • et al.
        Interleukin 6 stimulates endothelial binding and transport of high-density lipoprotein through induction of endothelial lipase.
        Arterioscler. Thromb. Vasc. Biol. 2013; 33: 2699-2706
        • Ohnsorg P.M.
        • et al.
        Carboxyl terminus of apolipoprotein A-I (ApoA-I) is necessary for the transport of lipid-free ApoA-I but not prelipidated ApoA-I particles through aortic endothelial cells.
        J. Biol. Chem. 2011; 286: 7744-7754
        • Huang L.-H.
        • et al.
        Interleukin-17 drives interstitial entrapment of tissue lipoproteins in experimental psoriasis.
        Cell Metabol. 2019; 29 (e7): 475-487
        • Velagapudi S.
        • et al.
        VEGF-A regulates cellular localization of SR-BI as well as transendothelial transport of HDL but Not LDL.
        Arterioscler. Thromb. Vasc. Biol. 2017; 37: 794-803
        • Stukas S.
        • et al.
        Intravenously injected human apolipoprotein A-I rapidly enters the central nervous system via the choroid plexus.
        J Am Hear. Assoc. 2014; 3e001156
        • Koch S.
        • et al.
        Characterization of four lipoprotein classes in human cerebrospinal fluid.
        J. Lipid Res. 2001; 42: 1143-1151
        • Borghini I.
        • Barja F.
        • Pometta D.
        • James R.W.
        Characterization of subpopulations of lipoprotein particles isolated from human cerebrospinal fluid.
        Biochim. Biophys. Acta. 1995; 1255: 192-200
        • Manousopoulou A.
        • et al.
        Systems proteomic analysis reveals that Clusterin and Tissue Inhibitor of Metalloproteinases 3 increase in leptomeningeal arteries affected by cerebral amyloid angiopathy.
        Neuropathol. Appl. Neurobiol. 2017; 43: 492-504
        • Button E.B.
        • et al.
        HDL from an Alzheimer's disease perspective.
        Curr. Opin. Lipidol. 2019; 30
        • Ladu M.J.
        • et al.
        Lipoproteins in the central nervous system.
        Ann. N. Y. Acad. Sci. 2000; 903: 167-175
        • Linton M.F.
        • et al.
        Phenotypes of apolipoprotein B and apolipoprotein E after liver transplantation.
        J. Clin. Invest. 1991; 88: 270-281
        • Koch M.
        • et al.
        Apolipoproteins and their subspecies in human cerebrospinal fluid and plasma.
        Alzheimer’s Dement. Diagnosis, Assess. Dis. Monit. 2017; 6: 182-187
        • Zhou A.L.
        • et al.
        Apolipoprotein A-I crosses the blood-brain barrier through clathrin-independent and cholesterol-mediated endocytosis.
        J. Pharmacol. Exp. Therapeut. 2019; 369: 1-32
        • Rohrer L.
        • et al.
        Binding, internalization and transport of apolipoprotein A-I by vascular endothelial cells.
        Biochim. Biophys. Acta. 2006; 1761: 186-194
        • Perisa D.
        • Rohrer L.
        • Kaech A.
        • von Eckardstein A.
        Itinerary of high density lipoproteins in endothelial cells.
        Biochim. Biophys. Acta. 2016; 1861: 98-107
        • Vuilleumier N.
        • Dayer J.-M.
        • von Eckardstein A.
        • Roux-Lombard P.
        Pro- or anti-inflammatory role of apolipoprotein A-1 in high-density lipoproteins?.
        Swiss Med. Wkly. 2013; 143: w13781
        • Zamanian-Daryoush M.
        • et al.
        Site-specific 5-hydroxytryptophan incorporation into apolipoprotein A-I impairs cholesterol efflux activity and high-density lipoprotein biogenesis.
        J. Biol. Chem. 2020; 295: 4836-4848
        • DiDonato J.A.
        • et al.
        Site-specific nitration of apolipoprotein A-I at tyrosine 166 is both abundant within human atherosclerotic plaque and dysfunctional.
        J. Biol. Chem. 2014; 289: 10276-10292
        • Zanoni P.
        • Velagapudi S.
        • Yalcinkaya M.
        • Rohrer L.
        • von Eckardstein A.
        Endocytosis of lipoproteins.
        Atherosclerosis. 2018; 275: 273-295
        • Linton M.F.
        • Tao H.
        • Linton E.F.
        • Yancey P.G.
        SR-BI: a multifunctional receptor in cholesterol homeostasis and atherosclerosis.
        Trends Endocrinol. Metabol. 2017; 28: 461-472
      2. Ljungström, K. G., Strandberg, O. & Sandstedt, B. Infarction of the small bowel caused by giant cell arteritis. Case report. Acta Chir. Scand. 155, 361–363.

        • Trigatti B.L.
        SR-B1 and PDZK1: partners in HDL regulation.
        Curr. Opin. Lipidol. 2017; 28: 201-208
        • Mineo C.
        Lipoprotein receptor signalling in atherosclerosis.
        Cardiovasc. Res. 2020; 116: 1254-1274
        • Frambach S.J.C.M.
        • et al.
        Brothers in arms: ABCA1- and ABCG1-mediated cholesterol efflux as promising targets in cardiovascular disease treatment.
        Pharmacol. Rev. 2020; 72: 152-190
        • Kober A.C.
        • et al.
        Implications of cerebrovascular ATP-binding cassette transporter G1 (ABCG1) and apolipoprotein M in cholesterol transport at the blood-brain barrier.
        Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2017; 1862: 573-588
        • Tarling E.J.
        • Edwards P.A.
        Intracellular localization of endogenous mouse ABCG1 is mimicked by both ABCG1-l550 and ABCG1-P550-brief report.
        Arterioscler. Thromb. Vasc. Biol. 2016; 36: 1323-1327
        • Yu J.E.
        • Han S.-Y.
        • Wolfson B.
        • Zhou Q.
        The role of endothelial lipase in lipid metabolism, inflammation, and cancer.
        Histol. Histopathol. 2018; 33: 1-10
        • Riederer M.
        • et al.
        Endothelial lipase (EL) and EL-generated lysophosphatidylcholines promote IL-8 expression in endothelial cells.
        Atherosclerosis. 2011; 214: 338-344
        • Tatematsu S.
        • et al.
        Endothelial lipase is a critical determinant of high-density lipoprotein-stimulated sphingosine 1-phosphate-dependent signaling in vascular endothelium.
        Arterioscler. Thromb. Vasc. Biol. 2013; 33: 1788-1794
        • Fruhwürth S.
        • et al.
        High-density lipoprotein endocytosis in endothelial cells.
        World J. Biol. Chem. 2013; 4: 131-140
        • Hessvik N.P.
        • Llorente A.
        Current knowledge on exosome biogenesis and release.
        Cell. Mol. Life Sci. 2018; 75: 193-208
        • Schillemans M.
        • Karampini E.
        • Kat M.
        • Bierings R.
        Exocytosis of Weibel-Palade bodies: how to unpack a vascular emergency kit.
        J. Thromb. Haemostasis. 2019; 17: 6-18
        • Balazs Z.
        • et al.
        Uptake and transport of high-density lipoprotein (HDL) and HDL-associated alpha-tocopherol by an in vitro blood-brain barrier model.
        J. Neurochem. 2004; 89: 939-950
        • Burnstock G.
        Purinergic signaling in the cardiovascular system.
        Circ. Res. 2017; 120: 207-228
        • Vanhoutte P.M.
        • Zhao Y.
        • Xu A.
        • Leung S.W.S.
        Thirty years of saying NO: sources, fate, actions, and misfortunes of the endothelium-derived vasodilator mediator.
        Circ. Res. 2016; 119: 375-396
        • Förstermann U.
        • Xia N.
        • Li H.
        Roles of vascular oxidative stress and nitric oxide in the pathogenesis of atherosclerosis.
        Circ. Res. 2017; 120: 713-735
        • Pi X.
        • Xie L.
        • Patterson C.
        Emerging roles of vascular endothelium in metabolic homeostasis.
        Circ. Res. 2018; 123: 477-494
        • Jansen F.
        • Li Q.
        • Pfeifer A.
        • Werner N.
        Endothelial- and immune cell-derived extracellular vesicles in the regulation of cardiovascular health and disease.
        JACC. Basic to Transl. Sci. 2017; 2: 790-807
        • Martinez L.O.
        • Najib S.
        • Perret B.
        • Cabou C.
        • Lichtenstein L.
        Ecto-F1-ATPase/P2Y pathways in metabolic and vascular functions of high density lipoproteins.
        Atherosclerosis. 2015; 238: 89-100
        • Fabre A.C.
        • et al.
        P2Y13 receptor is critical for reverse cholesterol transport.
        Hepatology. 2010; 52: 1477-1483
        • Cabou C.
        • et al.
        Pharmacological inhibition of the F1 -ATPase/P2Y1 pathway suppresses the effect of apolipoprotein A1 on endothelial nitric oxide synthesis and vasorelaxation.
        Acta Physiol. 2019; 226e13268
        • Velagapudi S.
        • et al.
        Scavenger receptor BI promotes cytoplasmic accumulation of lipoproteins in clear-cell renal cell carcinoma.
        J. Lipid Res. 2018; 59: 2188-2201
        • Wang D.
        • Rohrer L.
        • Eckardstein A. von
        Sphingosine-1-phosphate Receptors 1 and 3 Regulate the Expression of Scavenger Receptor B1 in Human Aortic Endothelial Cells.
        2020
        • Huang J.
        • Wang D.
        • Huang L.-H.
        • Huang H.
        Roles of reconstituted high-density lipoprotein nanoparticles in cardiovascular disease: a new paradigm for drug discovery.
        Int. J. Mol. Sci. 2020; 21
        • Nicholls S.J.
        • et al.
        Effect of serial infusions of CER-001, a pre-β High-density lipoprotein mimetic, on coronary atherosclerosis in patients following acute coronary syndromes in the CER-001 atherosclerosis regression acute coronary syndrome trial: a randomized clinical tria.
        JAMA Cardiol. 2018; 3: 815-822
        • Nicholls S.J.
        • et al.
        Effect of infusion of high-density lipoprotein mimetic containing recombinant apolipoprotein A-I Milano on coronary disease in patients with an acute coronary syndrome in the MILANO-PILOT trial: a randomized clinical trial.
        JAMA Cardiol. 2018; 3: 806-814
        • Ducroux C.
        • et al.
        Protective effect of ApoA1 (apolipoprotein a1)-milano in a rat model of large vessel occlusion stroke.
        Stroke. 2020; 51: 1886-1890
        • Lapergue B.
        • et al.
        Protective effect of high-density lipoprotein-based therapy in a model of embolic stroke.
        Stroke. 2010; 41: 1536-1542
        • Wang X.
        • et al.
        ApoA-I mimetic peptide reduces vascular and white matter damage after stroke in type-2 diabetic mice.
        Front. Neurosci. 2019; 13: 1127
        • Cui X.
        • Chopp M.
        • Zacharek A.
        • Cui C.
        D-4F Decreases White Matter Damage after Stroke in Mice.
        2015: 214-220https://doi.org/10.1161/STROKEAHA.115.011046
        • Robert J.
        • et al.
        Reconstituted high-density lipoproteins acutely reduce soluble brain Aβ levels in symptomatic APP/PS1 mice.
        Biochim. Biophys. Acta. 2015; 1862
        • Fernández-de Retana S.
        • et al.
        Intravenous treatment with human recombinant ApoA-I Milano reduces beta amyloid cerebral deposition in the APP23-transgenic mouse model of Alzheimer's disease.
        Neurobiol. Aging. 2017; 60: 116-128
        • Handattu S.P.
        • et al.
        Oral apolipoprotein A-I mimetic peptide improves cognitive function and reduces amyloid burden in a mouse model of Alzheimer's disease.
        Neurobiol. Dis. 2009; 34: 525-534
        • Schnitzler J.G.
        • Dzobo K.E.
        • Nurmohamed N.S.
        • Stroes E.S.G.
        • Kroon J.
        Surmounting the endothelial barrier for delivery of drugs and imaging tracers.
        Atherosclerosis. 2020; https://doi.org/10.1016/j.atherosclerosis.2020.04.025
        • Kratzer I.
        • et al.
        Apolipoprotein A-I coating of protamine-oligonucleotide nanoparticles increases particle uptake and transcytosis in an in vitro model of the blood-brain barrier.
        J. Contr. Release. 2007; 117: 301-311
        • Li J.
        • et al.
        Sterically stabilized recombined HDL composed of modified apolipoprotein A-I for efficient targeting toward glioma cells.
        Drug Deliv. 2020; 27: 530-541
        • Song Q.
        • et al.
        Biomimetic ApoE-reconstituted high density lipoprotein nanocarrier for blood-brain barrier penetration and amyloid beta-targeting drug delivery.
        Mol. Pharm. 2016; 13: 3976-3987
        • Huang J.-L.
        • et al.
        Lipoprotein-biomimetic nanostructure enables efficient targeting delivery of siRNA to Ras-activated glioblastoma cells via macropinocytosis.
        Nat. Commun. 2017; 8: 15144
        • Kadiyala P.
        • et al.
        High-density lipoprotein-mimicking nanodiscs for chemo-immunotherapy against glioblastoma multiforme.
        ACS Nano. 2019; 13: 1365-1384
        • Lee Y.T.
        • et al.
        Mouse models of atherosclerosis: a historical perspective and recent advances.
        Lipids Health Dis. 2017; 16: 1-11
        • Zadelaar S.
        • et al.
        Mouse models for atherosclerosis and pharmaceutical modifiers.
        Arterioscler. Thromb. Vasc. Biol. 2007; 27: 1706-1721
        • Daugherty A.
        Mouse models of atherosclerosis.
        Am. J. Med. Sci. 2002; 323: 3-10
        • Song Q.
        • 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: 2345-2359
        • Kuwahara H.
        • et al.
        Efficient in vivo delivery of siRNA into brain capillary endothelial cells along with endogenous lipoprotein.
        Mol. Ther. 2011; 19: 2213-2221
        • Oliver G.
        • Detmar M.
        The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature.
        Genes Dev. 2002; 16: 773-783
        • Pepper M.S.
        • Skobe M.
        Lymphatic endothelium: morphological, molecular and functional properties.
        J. Cell Biol. 2003; 163: 209-213
        • Gotloib L.
        • Shustak A.
        • Bar-Sella P.
        • Eiali V.
        Fenestrated capillaries in human parietal and rabbit diaphragmatic peritoneum.
        Nephron. 1985; 41: 200-202
        • Rosengren B.I.
        • Carlsson O.
        • Venturoli D.
        • Al Rayyes O.
        • Rippe B.
        Transvascular passage of macromolecules into the peritoneal cavity of normo- and hypothermic rats in vivo: active or passive transport?.
        J. Vasc. Res. 2004; 41: 123-130
        • Moriyama T.
        • Sasaki K.
        • Karasawa K.
        • Uchida K.
        • Nitta K.
        Intracellular transcytosis of albumin in glomerular endothelial cells after endocytosis through caveolae.
        J. Cell. Physiol. 2017; 232: 3565-3573
        • Naito M.
        • Wisse E.
        Filtration effect of endothelial fenestrations on chylomicron transport in neonatal rat liver sinusoids.
        Cell Tissue Res. 1978; 190: 371-382
        • Smedsrod B.
        • Pertoft H.
        • Gustafson S.
        • Laurent T.C.
        Scavenger functions of the liver endothelial cell.
        Biochem. J. 1990; 266: 313-327