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Significance of Cholesterol-Binding Motifs in ABCA1, ABCG1, and SR-B1 Structure

  • Alexander D. Dergunov
  • Eugeny V. Savushkin
  • Liudmila V. Dergunova
  • Dmitry Y. Litvinov
Article
  • 27 Downloads

Abstract

ABCA1, ABCG1 transporters, and SR-B1 receptor are the major proteins involved in cholesterol efflux from cells. We superposed in silico the location of putative cholesterol (Chol)-binding motifs CRAC/CARC and CCM in human ABCA1, ABCG1, and SR-B1 with (1) transmembrane protein topology, (2) a profile of structural order of protein, and (3) with an influence of single amino acid substitutions on protein structure and function. ABCA1, ABCG1, and SR-B1 molecules contain 50, 19, and 13 Chol-binding motifs, respectively, that are localized either in membrane helices, or at membrane–water interface, or in water-exposed protein regions. Arginine residues in motifs that coincide with molecular recognition features within intrinsically disordered regions of the transporters are suggested to be important in cholesterol binding; cholesterol–arginine interaction may result in the induction of local order in protein structure. Chol-binding motifs in membrane helices may immobilize cholesterol, while motifs at membrane–water interface may be involved into the efflux of “active” cholesterol. Cholesterol may interfere with ATP binding in both nucleotide-binding domains of ABCA1 structure. For ABCA1 and ABCG1, but not for SR-B1, the presence of mirror code as a CARC–CRAC vector couple in the C-terminal helices controlling protein–cholesterol interactions in the outer and inner membrane leaflets was evidenced. We propose the role of Chol-binding motifs with different immersion in membrane in transport of different cholesterol pools by ABCA1 and ABCG1.

Keywords

ABCA1 ABCG1 SR-B1 ApoA-I Cholesterol-binding domains 

Abbreviations

apoA-I

Apolipoprotein A-I

CARC

Inverted CRAC

CCM

Cholesterol consensus motif

Chol

Cholesterol

CRAC

Cholesterol recognition/interaction amino acid consensus

HDL

High-density lipoproteins

HDL-C

HDL cholesterol

HGMD

Human gene mutation database

MoRF

Molecular recognition feature

NBD

Nucleotide-binding domain

SNP

Single-nucleotide polymorphism

TM

Transmembrane

TMD

Transmembrane domain

Notes

Funding

This study was funded by the grants 16-04-00067 and 17-04-00217 from the Russian Fund for Basic Research.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research Involving Human and Animal Participants

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248–249CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alrasadi K, Ruel IL, Marcil M, Genest J (2006) Functional mutations of the ABCA1 gene in subjects of French-Canadian descent with HDL deficiency. Atherosclerosis 188:281–291CrossRefGoogle Scholar
  3. Assanasen C, Mineo C, Seetharam D, Yuhanna IS, Marcel YL, Connelly MA, Williams DL, Llera-Moya M, Shaul PW, Silver DL (2005) Cholesterol binding, efflux, and a PDZ-interacting domain of scavenger receptor-BI mediate HDL-initiated signaling. J Clin Investig 115:969–977CrossRefGoogle Scholar
  4. Baier CJ, Fantini J, Barrantes FJ (2011) Disclosure of cholesterol recognition motifs in transmembrane domains of the human nicotinic acetylcholine receptor. Sci Rep 1:69CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beis K (2015) Structural basis for the mechanism of ABC transporters. Biochem Soc Trans 43:889–893CrossRefGoogle Scholar
  6. Berge KE, Leren TP (2010) Mutations in APOA-I and ABCA1 in Norwegians with low levels of HDL cholesterol. Clin Chim Acta 411:2019–2023CrossRefGoogle Scholar
  7. Bi C, Wu J, Jiang T, Liu Q, Cai W, Yu P, Cai T, Zhao M, Jiang YH, Sun ZS (2012) Mutations of ANK3 identified by exome sequencing are associated with autism susceptibility. Hum Mutat 33:1635–1638CrossRefGoogle Scholar
  8. Bochem AE, van Wijk DF, Holleboom AG, Duivenvoorden R, Motazacker MM, Dallinga-Thie GM, de Groot E, Kastelein JJ, Nederveen AJ, Hovingh GK, Stroes ES (2013) ABCA1 mutation carriers with low high-density lipoprotein cholesterol are characterized by a larger atherosclerotic burden. Eur Heart J 34:286–291CrossRefGoogle Scholar
  9. Brunham LR, Tietjen I, Bochem AE, Singaraja RR, Franchini PL, Radomski C, Mattice M, Legendre A, Hovingh GK, Kastelein JJ, Hayden MR (2011) Novel mutations in scavenger receptor BI associated with high HDL cholesterol in humans. Clin Genet 79:575–581CrossRefGoogle Scholar
  10. Cameron J, Ranheim T, Halvorsen B, Kulseth MA, Leren TP, Berge KE (2010) Tangier disease caused by compound heterozygosity for ABCA1 mutations R282X and Y1532C. Atherosclerosis 209:163–166CrossRefPubMedGoogle Scholar
  11. Candini C, Schimmel AW, Peter J, Bochem AE, Holleboom AG, Vergeer M, Dullaart RP, Dallinga-Thie GM, Hovingh GK, Khoo KL, Fasano T, Bocchi L, Calandra S, Kuivenhoven JA, Motazacker MM (2010) Identification and characterization of novel loss of function mutations in ATP-binding cassette transporter A1 in patients with low plasma high-density lipoprotein cholesterol. Atherosclerosis 213:492–498CrossRefPubMedGoogle Scholar
  12. Chadwick AC, Sahoo D (2012) Functional characterization of newly-discovered mutations in human SR-BI. PLoS ONE 7:e45660CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cohen JC, Kiss RS, Pertsemlidis A, Marcel YL, McPherson R, Hobbs HH (2004) Multiple rare alleles contribute to low plasma levels of HDL cholesterol. Science 305:869–872CrossRefPubMedGoogle Scholar
  14. Connelly MA, Llera-Moya M, Monzo P, Yancey PG, Drazul D, Stoudt G, Fournier N, Klein SM, Rothblat GH, Williams DL (2001) Analysis of chimeric receptors shows that multiple distinct functional activities of scavenger receptor, class B, type I (SR-BI), are localized to the extracellular receptor domain. Biochemistry 40:5249–5259CrossRefPubMedGoogle Scholar
  15. Dergunov AD (2013) Mutation mapping of apolipoprotein A-I structure assisted with the putative cholesterol recognition regions. Biochim Biophys Acta 1834:2030–2035CrossRefPubMedGoogle Scholar
  16. Dergunov AD, Garaeva EA, Savushkin EV, Litvinov DY (2017) Significance of lipid-free and lipid-associated ApoA-I in cellular cholesterol efflux. Curr Prot Pept Sci 18:92–99CrossRefGoogle Scholar
  17. Di Scala C, Fantini J, Yahi N, Barrantes FJ, Chahinian H (2018) Anandamide revisited: how cholesterol and ceramides control receptor-dependent and receptor-independent signal transmission pathways of a lipid neurotransmitter. Biomolecules 8:31CrossRefPubMedCentralGoogle Scholar
  18. Disfani FM, Hsu WL, Mizianty MJ, Oldfield CJ, Xue B, Dunker AK, Uversky VN, Kurgan L (2012) MoRFpred, a computational tool for sequence-based prediction and characterization of short disorder-to-order transitioning binding regions in proteins. Bioinformatics 28:i75–i83CrossRefPubMedPubMedCentralGoogle Scholar
  19. Epand RM, Sayer BG, Epand RF (2005) Caveolin scaffolding region and cholesterol-rich domains in membranes. J Mol Biol 345:339–350CrossRefPubMedGoogle Scholar
  20. Estronca LM, Moreno MJ, Laranjinha JA, Almeida LM, Vaz WL (2005) Kinetics and thermodynamics of lipid amphiphile exchange between lipoproteins and albumin in serum. Biophys J 88:557–565CrossRefPubMedGoogle Scholar
  21. Fantini J, Barrantes FJ (2013) How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front Physiol 4:31PubMedPubMedCentralGoogle Scholar
  22. Fantini J, Carlus D, Yahi N (2011) The fusogenic tilted peptide (67–78) of alpha-synuclein is a cholesterol binding domain. Biochim Biophys Acta 1808:2343–2351CrossRefPubMedGoogle Scholar
  23. Fantini J, Di SC, Evans LS, Williamson PT, Barrantes FJ (2016) A mirror code for protein-cholesterol interactions in the two leaflets of biological membranes. Sci Rep 6:21907CrossRefPubMedPubMedCentralGoogle Scholar
  24. Frikke-Schmidt R, Nordestgaard BG, Schnohr P, Steffensen R, Tybjaerg-Hansen A (2005) Mutation in ABCA1 predicted risk of ischemic heart disease in the Copenhagen City Heart Study Population. J Am Coll Cardiol 46:1516–1520CrossRefPubMedGoogle Scholar
  25. Frikke-Schmidt R, Nordestgaard BG, Stene MC, Sethi AA, Remaley AT, Schnohr P, Grande P, Tybjaerg-Hansen A (2008) Association of loss-of-function mutations in the ABCA1 gene with high-density lipoprotein cholesterol levels and risk of ischemic heart disease. JAMA 299:2524–2532CrossRefPubMedGoogle Scholar
  26. Fukushima D, Yokoyama S, Kezdy FJ, Kaiser ET (1981) Binding of amphiphilic peptides to phospholipid/cholesterol unilamellar vesicles: a model for protein–cholesterol interaction. Proc Natl Acad Sci USA 78:2732–2736CrossRefPubMedGoogle Scholar
  27. Gater DL, Saurel O, Iordanov I, Liu W, Cherezov V, Milon A (2014) Two classes of cholesterol binding sites for the beta2AR revealed by thermostability and NMR. Biophys J 107:2305–2312CrossRefPubMedPubMedCentralGoogle Scholar
  28. Gulshan K, Brubaker G, Conger H, Wang S, Zhang R, Hazen SL, Smith JD (2016) PI(4,5)P2 is translocated by ABCA1 to the cell surface where it mediates apolipoprotein A1 binding and nascent HDL assembly. Circ Res 119:827–838CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gutierrez-Pajares JL, Ben HC, Chevalier S, Frank PG (2016) SR-BI: linking cholesterol and lipoprotein metabolism with breast and prostate cancer. Front Pharmacol 7:338CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola VP, Chien EY, Velasquez J, Kuhn P, Stevens RC (2008) A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16:897–905CrossRefPubMedPubMedCentralGoogle Scholar
  31. Ho HS, Rhyne J, Zeller K, Miller M (2002) Novel ABCA1 compound variant associated with HDL cholesterol deficiency. Biochim Biophys Acta 1587:60–64CrossRefGoogle Scholar
  32. Hong SH, Rhyne J, Miller M (2003) Novel polypyrimidine variation (IVS46: del T -39…) in ABCA1 causes exon skipping and contributes to HDL cholesterol deficiency in a family with premature coronary disease. Circ Res 93:1006–1012CrossRefGoogle Scholar
  33. Huang W, Moriyama K, Koga T, Hua H, Ageta M, Kawabata S, Mawatari K, Imamura T, Eto T, Kawamura M, Teramoto T, Sasaki J (2001) Novel mutations in ABCA1 gene in Japanese patients with Tangier disease and familial high density lipoprotein deficiency with coronary heart disease. Biochim Biophys Acta 1537:71–78CrossRefGoogle Scholar
  34. Hulce JJ, Cognetta AB, Niphakis MJ, Tully SE, Cravatt BF (2013) Proteome-wide mapping of cholesterol-interacting proteins in mammalian cells. Nat Methods 10:259–264CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jafurulla M, Tiwari S, Chattopadhyay A (2011) Identification of cholesterol recognition amino acid consensus (CRAC) motif in G-protein coupled receptors. Biochem Biophys Res Commun 404:569–573CrossRefGoogle Scholar
  36. Jones PM, George AM (2014) A reciprocating twin-channel model for ABC transporters. Q Rev Biophys 47:189–220CrossRefGoogle Scholar
  37. Klucken J, Buchler C, Orso E, Kaminski WE, Porsch-Ozcurumez M, Liebisch G, Kapinsky M, Diederich W, Drobnik W, Dean M, Allikmets R, Schmitz G (2000) ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc Natl Acad Sci USA 97:817–822CrossRefGoogle Scholar
  38. Lange Y, Steck TL (2008) Cholesterol homeostasis and the escape tendency (activity) of plasma membrane cholesterol. Prog Lipid Res 47:319–332CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lapicka-Bodzioch K, Bodzioch M, Krull M, Kielar D, Probst M, Kiec B, Andrikovics H, Bottcher A, Hubacek J, Aslanidis C, Suttorp N, Schmitz G (2001) Homogeneous assay based on 52 primer sets to scan for mutations of the ABCA1 gene and its application in genetic analysis of a new patient with familial high-density lipoprotein deficiency syndrome. Biochim Biophys Acta 1537:42–48CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lawn RM, Wade DP, Garvin MR, Wang X, Schwartz K, Porter JG, Seilhamer JJ, Vaughan AM, Oram JF (1999) The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J Clin Investig 104:R25–R31CrossRefPubMedGoogle Scholar
  41. Lee JY, Kinch LN, Borek DM, Wang J, Wang J, Urbatsch IL, Xie XS, Grishin NV, Cohen JC, Otwinowski Z, Hobbs HH, Rosenbaum DM (2016) Crystal structure of the human sterol transporter ABCG5/ABCG8. Nature 533:561–564CrossRefPubMedPubMedCentralGoogle Scholar
  42. Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P (2009) Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 25:2744–2750CrossRefPubMedPubMedCentralGoogle Scholar
  43. Li H, Papadopoulos V (1998) Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139:4991–4997CrossRefPubMedGoogle Scholar
  44. Manna M, Niemela M, Tynkkynen J, Javanainen M, Kulig W, Muller DJ, Rog T, Vattulainen I (2016) Mechanism of allosteric regulation of beta2-adrenergic receptor by cholesterol. Elife 5:e18432CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mantaring M, Rhyne J, Ho HS, Miller M (2007) Genotypic variation in ATP-binding cassette transporter-1 (ABCA1) as contributors to the high and low high-density lipoprotein-cholesterol (HDL-C) phenotype. Transl Res 149:205–210CrossRefPubMedGoogle Scholar
  46. Mizianty MJ, Stach W, Chen K, Kedarisetti KD, Disfani FM, Kurgan L (2010) Improved sequence-based prediction of disordered regions with multilayer fusion of multiple information sources. Bioinformatics 26:i489–i496CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mohan A, Oldfield CJ, Radivojac P, Vacic V, Cortese MS, Dunker AK, Uversky VN (2006) Analysis of molecular recognition features (MoRFs). J Mol Biol 362:1043–1059CrossRefPubMedGoogle Scholar
  48. Nagata KO, Nakada C, Kasai RS, Kusumi A, Ueda K (2013) ABCA1 dimer-monomer interconversion during HDL generation revealed by single-molecule imaging. Proc Natl Acad Sci USA 110:5034–5039CrossRefGoogle Scholar
  49. Phillips MC (2014) Molecular mechanisms of cellular cholesterol efflux. J Biol Chem 289:24020–24029CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pisciotta L, Bocchi L, Candini C, Sallo R, Zanotti I, Fasano T, Chakrapani A, Bates T, Bonardi R, Cantafora A, Ball S, Watts G, Bernini F, Calandra S, Bertolini S (2009) Severe HDL deficiency due to novel defects in the ABCA1 transporter. J Intern Med 265:359–372CrossRefPubMedGoogle Scholar
  51. Pisciotta L, Hamilton-Craig I, Tarugi P, Bellocchio A, Fasano T, Alessandrini P, Bon GB, Siepi D, Mannarino E, Cattin L, Averna M, Cefalu AB, Cantafora A, Calandra S, Bertolini S (2004) Familial HDL deficiency due to ABCA1 gene mutations with or without other genetic lipoprotein disorders. Atherosclerosis 172:309–320CrossRefPubMedGoogle Scholar
  52. Probst MC, Thumann H, Aslanidis C, Langmann T, Buechler C, Patsch W, Baralle FE, Dallinga-Thie GM, Geisel J, Keller C, Menys VC, Schmitz G (2004) Screening for functional sequence variations and mutations in ABCA1. Atherosclerosis 175:269–279CrossRefPubMedGoogle Scholar
  53. PyMOL Molecular Graphics System. [1.3]. 2010. Schrodinger, LLCGoogle Scholar
  54. Qian H, Zhao X, Cao P, Lei J, Yan N, Gong X (2017) Structure of the human lipid exporter ABCA1. Cell 169:1228–1239CrossRefPubMedGoogle Scholar
  55. Quazi F, Molday RS (2013) Differential phospholipid substrates and directional transport by ATP-binding cassette proteins ABCA1, ABCA7, and ABCA4 and disease-causing mutants. J Biol Chem 288:34414–34426CrossRefPubMedPubMedCentralGoogle Scholar
  56. Reboul E, Dyka FM, Quazi F, Molday RS (2013) Cholesterol transport via ABCA1: new insights from solid-phase binding assay. Biochimie 95:957–961CrossRefPubMedGoogle Scholar
  57. Rosenhouse-Dantsker A (2017) Insights into the molecular requirements for cholesterol binding to ion channels. Curr Top Membr 80:187–208CrossRefPubMedGoogle Scholar
  58. Rosenhouse-Dantsker A, Noskov S, Durdagi S, Logothetis DE, Levitan I (2013) Identification of novel cholesterol-binding regions in Kir2 channels. J Biol Chem 288:31154–31164CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sankaranarayanan S, Oram JF, Asztalos BF, Vaughan AM, Lund-Katz S, Adorni MP, Phillips MC, Rothblat GH (2009) Effects of acceptor composition and mechanism of ABCG1-mediated cellular free cholesterol efflux. J Lipid Res 50:275–284CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sano O, Ito S, Kato R, Shimizu Y, Kobayashi A, Kimura Y, Kioka N, Hanada K, Ueda K, Matsuo M (2014) ABCA1, ABCG1, and ABCG4 are distributed to distinct membrane meso-domains and disturb detergent-resistant domains on the plasma membrane. PLoS ONE 9:e109886CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sharpe LJ, Rao G, Jones PM, Glancey E, Aleidi SM, George AM, Brown AJ, Gelissen IC (2015) Cholesterol sensing by the ABCG1 lipid transporter: Requirement of a CRAC motif in the final transmembrane domain. Biochim Biophys Acta 1851:956–964CrossRefPubMedGoogle Scholar
  62. Shintre CA, Pike AC, Li Q, Kim JI, Barr AJ, Goubin S, Shrestha L, Yang J, Berridge G, Ross J, Stansfeld PJ, Sansom MS, Edwards AM, Bountra C, Marsden BD, von Delft F, Bullock AN, Gileadi O, Burgess-Brown NA, Carpenter EP (2013) Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states. Proc Natl Acad Sci USA 110:9710–9715CrossRefPubMedGoogle Scholar
  63. Slatter TL, Jones GT, Williams MJ, van Rij AM, McCormick SP (2008) Novel rare mutations and promoter haplotypes in ABCA1 contribute to low-HDL-C levels. Clin Genet 73:179–184CrossRefPubMedGoogle Scholar
  64. Slatter TL, Williams MJ, Frikke-Schmidt R, Tybjaerg-Hansen A, Morison IM, McCormick SP (2006) Promoter haplotype of a new ABCA1 mutant influences expression of familial hypoalphalipoproteinemia. Atherosclerosis 187:393–400CrossRefPubMedGoogle Scholar
  65. Song Y, Kenworthy AK, Sanders CR (2014) Cholesterol as a co-solvent and a ligand for membrane proteins. Prot Sci 23:1–22CrossRefGoogle Scholar
  66. Stenson PD, Ball EV, Mort M, Phillips AD, Shiel JA, Thomas NS, Abeysinghe S, Krawczak M, Cooper DN (2003) Human gene mutation database (HGMD): 2003 update. Hum Mutat 21:577–581CrossRefPubMedGoogle Scholar
  67. Takahashi K, Kimura Y, Kioka N, Matsuo M, Ueda K (2006) Purification and ATPase activity of human ABCA1. J Biol Chem 281:10760–10768CrossRefPubMedGoogle Scholar
  68. Tamehiro N, Park MH, Hawxhurst V, Nagpal K, Adams ME, Zannis VI, Golenbock DT, Fitzgerald ML (2015) LXR agonism upregulates the macrophage ABCA1/syntrophin protein complex that can bind ApoA-I and stabilized ABCA1 protein, but complex loss does not inhibit lipid efflux. Biochemistry 54:6931–6941CrossRefPubMedPubMedCentralGoogle Scholar
  69. Tarling EJ, Edwards PA (2011) ATP binding cassette transporter G1 (ABCG1) is an intracellular sterol transporter. Proc Natl Acad Sci USA 108:19719–19724CrossRefPubMedGoogle Scholar
  70. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2:42–49CrossRefGoogle Scholar
  71. Tietjen I, Hovingh GK, Singaraja R, Radomski C, McEwen J, Chan E, Mattice M, Legendre A, Kastelein JJ, Hayden MR (2012) Increased risk of coronary artery disease in Caucasians with extremely low HDL cholesterol due to mutations in ABCA1, APOA1, and LCAT. Biochim Biophys Acta 1821:416–424CrossRefGoogle Scholar
  72. Trigatti B, Rigotti A, Krieger M (2000) The role of the high-density lipoprotein receptor SR-BI in cholesterol metabolism. Curr Opin Lipidol 11:123–131CrossRefGoogle Scholar
  73. Vaughan AM, Tang C, Oram JF (2009) ABCA1 mutants reveal an interdependency between lipid export function, apoA-I binding activity, and Janus kinase 2 activation. J Lipid Res 50:285–292CrossRefPubMedPubMedCentralGoogle Scholar
  74. Vedhachalam C, Duong PT, Nickel M, Nguyen D, Dhanasekaran P, Saito H, Rothblat GH, Lund-Katz S, Phillips MC (2007) Mechanism of ATP-binding cassette transporter A1-mediated cellular lipid efflux to apolipoprotein A-I and formation of high density lipoprotein particles. J Biol Chem 282:25123–25130CrossRefGoogle Scholar
  75. Wiersma H, Gatti A, Nijstad N, Oude Elferink RP, Kuipers F, Tietge UJ (2009) Scavenger receptor class B type I mediates biliary cholesterol secretion independent of ATP-binding cassette transporter g5/g8 in mice. Hepatology 50:1263–1272CrossRefGoogle Scholar
  76. Wustner D, Solanko K (2015) How cholesterol interacts with proteins and lipids during its intracellular transport. Biochim Biophys Acta 1848:1908–1926CrossRefGoogle Scholar
  77. Xue XH, Wang N, Lin Y, Zhao GX, Fang L, Murong S, Wu ZY (2008) Novel mutation in the ABCA1 gene identified in a chinese patient with dementia and atherothrombotic cerebral infarction. Dement Geriatr Cogn Disord 26:234–238CrossRefGoogle Scholar
  78. Yamauchi Y, Abe-Dohmae S, Yokoyama S (2002) Differential regulation of apolipoprotein A-I/ATP binding cassette transporter A1-mediated cholesterol and phospholipid release. Biochim Biophys Acta 1585:1–10CrossRefGoogle Scholar
  79. Yamauchi Y, Iwamoto N, Rogers MA, Abe-Dohmae S, Fujimoto T, Chang CC, Ishigami M, Kishimoto T, Kobayashi T, Ueda K, Furukawa K, Chang TY, Yokoyama S (2015) Deficiency in the lipid exporter ABCA1 impairs retrograde sterol movement and disrupts sterol sensing at the endoplasmic reticulum. J Biol Chem 290:23464–23477CrossRefPubMedPubMedCentralGoogle Scholar
  80. Yamauchi Y, Yokoyama S, Chang TY (2016) ABCA1-dependent sterol release: sterol molecule specificity and potential membrane domain for HDL biogenesis. J Lipid Res 57:77–88CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zhang T, Faraggi E, Xue B, Dunker AK, Uversky VN, Zhou Y (2012) SPINE-D: accurate prediction of short and long disordered regions by a single neural-network based method. J Biomol Struct Dyn 29:799–813CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.National Research Centre for Preventive MedicineMoscowRussia
  2. 2.Institute of Molecular Genetics of the Russian Academy of Sciences2 Kurchatov Square, MoscowRussia

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