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Annual Review of Physiology

Volume 80, 2018

SR-B1: A Unique Multifunctional Receptor for Cholesterol Influx and Efflux

Abstract

The scavenger receptor, class B type 1 (SR-B1), is a multiligand membrane receptor protein that functions as a physiologically relevant high-density lipoprotein (HDL) receptor whose primary role is to mediate selective uptake or influx of HDL-derived cholesteryl esters into cells and tissues. SR-B1 also facilitates the efflux of cholesterol from peripheral tissues, including macrophages, back to liver. As a regulator of plasma membrane cholesterol content, SR-B1 promotes the uptake of lipid soluble vitamins as well as viral entry into host cells. These collective functions of SR-B1 ultimately affect programmed cell death, female fertility, platelet function, vasculature inflammation, and diet-induced atherosclerosis and myocardial infarction. SR-B1 has also been identified as a potential marker for cancer diagnosis and prognosis. Finally, the SR-B1–linked selective HDL-cholesteryl ester uptake pathway is now being evaluated as a gateway for the delivery of therapeutic and diagnostic agents. In this review, we focus on the regulation and functional significance of SR-B1 in mediating cholesterol movement into and out of cells.

Keyword(s): HDL, HDL receptor, reverse cholesterol transport, selective cholesterol uptake
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/content/journals/10.1146/annurev-physiol-021317-121550
2018-02-10
2024-04-23
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Literature Cited

  1. Ikonen E.1.  2008. Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell. Biol. 9:125–38 [Google Scholar]
  2. Cooper G.2.  2000. The Cell: A Molecular Approach Cary, NC: Sinauer Assoc
  3. Incardona JP, Eaton S. 3.  2000. Cholesterol in signal transduction. Curr. Opin. Cell Biol. 12:193–203 [Google Scholar]
  4. Carmena R, Duriez P, Fruchart JC. 4.  2004. Atherogenic lipoprotein particles in atherosclerosis. Circulation 109:III2–7 [Google Scholar]
  5. Rosenson RS, Brewer HB Jr., Davidson WS, Fayad ZA, Fuster V. 5.  et al. 2012. Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation 125:1905–19 [Google Scholar]
  6. Shen WJ, Azhar S, Kraemer FB. 6.  2016. ACTH regulation of adrenal SR-B1. Front. Endocrinol. 7:42 [Google Scholar]
  7. Shen WJ, Azhar S, Kraemer FB. 7.  2016. Lipid droplets and steroidogenic cells. Exp. Cell Res. 340:209–14 [Google Scholar]
  8. Kraemer FB, Shen WJ, Harada K, Patel S, Osuga J. 8.  et al. 2004. Hormone-sensitive lipase is required for high-density lipoprotein cholesteryl ester-supported adrenal steroidogenesis. Mol. Endocrinol. 18:549–57 [Google Scholar]
  9. Kraemer FB, Shen WJ, Natu V, Patel S, Osuga J. 9.  et al. 2002. Adrenal neutral cholesteryl ester hydrolase: identification, subcellular distribution, and sex differences. Endocrinology 143:801–6 [Google Scholar]
  10. Lin Y, Hou X, Shen WJ, Hanssen R, Khor VK. 10.  et al. 2016. SNARE-mediated cholesterol movement to mitochondria supports steroidogenesis in rodent cells. Mol. Endocrinol. 30:234–47 [Google Scholar]
  11. Freeman DA.11.  1987. Regulation of the cholesterol ester cycle of cultured Leydig tumor cells. Eur. J. Biochem. 164:351–56 [Google Scholar]
  12. Rader DJ, Alexander ET, Weibel GL, Billheimer J, Rothblat GH. 12.  2009. The role of reverse cholesterol transport in animals and humans and relationship to atherosclerosis. J. Lipid Res. 50:S189–94 [Google Scholar]
  13. Annema W, Tietge UJ. 13.  2012. Regulation of reverse cholesterol transport—a comprehensive appraisal of available animal studies. Nutr. Metab. 9:25 [Google Scholar]
  14. Ono K.14.  2012. Current concept of reverse cholesterol transport and novel strategy for atheroprotection. J. Cardiol. 60:339–43 [Google Scholar]
  15. Phillips MC.15.  2014. Molecular mechanisms of cellular cholesterol efflux. J. Biol. Chem. 289:24020–29 [Google Scholar]
  16. Calvo D, Vega MA. 16.  1993. Identification, primary structure, and distribution of CLA-1, a novel member of the CD36/LIMPII gene family. J. Biol. Chem. 268:18929–35 [Google Scholar]
  17. Acton SL, Scherer PE, Lodish HF, Krieger M. 17.  1994. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J. Biol. Chem. 269:21003–9 [Google Scholar]
  18. Duggan A, Marie R, Callard I. 18.  2002. Expression of SR-BI (Scavenger Receptor Class B Type I) in turtle (Chrysemys picta) tissues and other nonmammalian vertebrates. J. Exp. Zool. 292:430–34 [Google Scholar]
  19. Shen WJ, Hu J, Hu Z, Kraemer FB, Azhar S. 19.  2014. Scavenger receptor class B type I (SR-BI): a versatile receptor with multiple functions and actions. Metabolism 63:875–86 [Google Scholar]
  20. Means TK.20.  2010. Fungal pathogen recognition by scavenger receptors in nematodes and mammals. Virulence 1:37–41 [Google Scholar]
  21. Herboso L, Talamillo A, Pérez C, Barrio R. 21.  2011. Expression of the Scavenger Receptor Class B type I (SR-BI) family in Drosophila melanogaster. Int. J. Dev. Biol. 55:603–11 [Google Scholar]
  22. Sakudoh T, Kuwazaki S, Iizuka T, Narukawa J, Yamamoto K. 22.  et al. 2013. CD36 homolog divergence is responsible for the selectivity of carotenoid species migration to the silk gland of the silkworm Bombyx mori. J. Lipid Res. 54:482–95 [Google Scholar]
  23. Nichols Z, Vogt RG. 23.  2008. The SNMP/CD36 gene family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem. Mol. Biol 38:398–415 [Google Scholar]
  24. Kiefer C, Sumser E, Wernet MF, von Lintig J. 24.  2002. A class B scavenger receptor mediates the cellular uptake of carotenoids. PNAS 99:10581–86 [Google Scholar]
  25. Tabunoki H, Sugiyama H, Tanaka Y, Fujui H, Banno Y. 25.  et al. 2002. Isolation, characterization, and cDNA sequence of a carotenoid binding protein from the silk gland of Bombyx mori. J. Biol. Chem. 277:32133–40 [Google Scholar]
  26. Sakudoh T, Iizuka T, Narukawa J, Sezutsu H, Kobayashi I. 26.  et al. 2010. A CD36-related transmembrane protein is coordinated with an intracellular lipid-binding protein in selective carotenoid transport for cocoon coloration. J. Biol. Chem. 285:7739–51 [Google Scholar]
  27. Brown MS, Goldstein JL. 27.  1986. A receptor-mediated pathway for cholesterol homeostasis. Science 232:34–47 [Google Scholar]
  28. Pittman RC, Knecht TP, Rosenbaum MS, Taylor CA Jr.. 28.  1987. A nonendocytotic mechanism for the selective uptake of high density lipoprotein-associated cholesterol esters. J. Biol. Chem. 262:2443–50 [Google Scholar]
  29. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. 29.  1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271:518–20 [Google Scholar]
  30. Varban ML, Rinninger F, Wang N, Fairchild-Huntress V, Dunmore JH. 30.  et al. 1998. Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of high density lipoprotein cholesterol. PNAS 95:4619–24 [Google Scholar]
  31. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, Krieger M. 31.  1997. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. PNAS 94:12610–15 [Google Scholar]
  32. Van Eck M, Twisk J, Hoekstra M, Van Rij BT, Van der Lans CA. 32.  et al. 2003. Differential effects of scavenger receptor BI deficiency on lipid metabolism in cells of the arterial wall and in the liver. J. Biol. Chem. 278:23699–705 [Google Scholar]
  33. Kozarsky KF, Donahee MH, Rigotti A, Iqbal SN, Edelman ER, Krieger M. 33.  1997. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 387:414–17 [Google Scholar]
  34. Ueda Y, Royer L, Gong E, Zhang J, Cooper PN. 34.  et al. 1999. Lower plasma levels and accelerated clearance of high density lipoprotein (HDL) and non-HDL cholesterol in scavenger receptor class B type I transgenic mice. J. Biol. Chem. 274:7165–71 [Google Scholar]
  35. Wang N, Arai T, Ji Y, Rinninger F, Tall AR. 35.  1998. Liver-specific overexpression of scavenger receptor BI decreases levels of very low density lipoprotein ApoB, low density lipoprotein ApoB, and high density lipoprotein in transgenic mice. J. Biol. Chem. 273:32920–26 [Google Scholar]
  36. During A, Dawson H, Harrison E. 36.  2005. Carotenoid transport is decreased and expression of the lipid transporters SR-BI, NPC1L1, and ABCA1 is downregulated in Caco-2 cells treated with ezetimibe. J. Nutr. 135:2305–12 [Google Scholar]
  37. Reboul E, Klein A, Bietrix F, Gleize B, Malezet-Desmoulins C. 37.  et al. 2006. Scavenger receptor class B type I (SR-BI) is involved in vitamin E transport across the enterocyte. J. Biol. Chem. 281:4739–45 [Google Scholar]
  38. Rigotti A, Acton S, Krieger M. 38.  1995. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J. Biol. Chem. 270:16221–24 [Google Scholar]
  39. Saddar S, Carriere V, Lee W, Tanigaki K, Yuhanna I. 39.  et al. 2013. Scavenger Receptor Class B Type I (SR-BI) is a plasma membrane cholesterol sensor. Circ. Res. 112:140–51 [Google Scholar]
  40. Tsugita M, Morimoto N, Tashiro M, Kinoshita K, Nakayama M. 40.  2017. SR-B1 is a silica receptor that mediates canonical inflammasome activation. Cell Rep 18:1298–311 [Google Scholar]
  41. Burlone M, Budkowska A. 41.  2009. Hepatitis C virus cell entry: role of lipoproteins and cellular receptors. J. Gen. Virol. 90:1055–70 [Google Scholar]
  42. Barth H, Schnober E, Neumann-Haefelin C, Thumann C, Zeisel M. 42.  et al. 2008. Scavenger receptor class B is required for hepatitis C virus uptake and cross-presentation by human dendritic cells. J. Virol. 82:3466–79 [Google Scholar]
  43. Osada Y, Sunatani T, Kim I, Nakanishi Y, Shiratsuchi A. 43.  2009. Signalling pathway involving GULP, MAPK and Rac1 for SR-BI-induced phagocytosis of apoptotic cells. J. Biochem. 145:387–94 [Google Scholar]
  44. Miettinen H, Rayburn H, Krieger M. 44.  2001. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J. Clin. Investig. 108:1717–22 [Google Scholar]
  45. Ma Y, Ashraf M, Podrez E. 45.  2010. Scavenger receptor BI modulates platelet reactivity and thrombosis in dyslipidemia. Blood 116:1932–41 [Google Scholar]
  46. Zimman A, Podrez E. 46.  2010. Regulation of platelet function by class B scavenger receptors in hyperlipidemia. Arterioscler. Thromb. Vasc. Biol. 30:2350–56 [Google Scholar]
  47. Al-Jarallah A, Trigatti B. 47.  2010. A role for the scavenger receptor, class B type I in high density lipoprotein dependent activation of cellular signaling pathways. Biochim. Biophys. Acta 1801:1239–49 [Google Scholar]
  48. Saddar S MC, Shaul PW. 48.  2010. Signaling by the high-affinity HDL receptor B type I. Arterioscler. Thromb. Vasc. Biol. 30:144–50 [Google Scholar]
  49. Pei Y, Chen X, Aboutouk D, Fuller M, Dadoo O. 49.  et al. 2013. SR-BI in bone marrow derived cells protects mice from diet induced coronary artery atherosclerosis and myocardial infarction. PLOS ONE 8:e72492 [Google Scholar]
  50. Webb NR, de Villiers WJ, Connell PM, de Beer FC, van der Westhuyzen DR. 50.  1997. Alternative forms of the scavenger receptor BI (SR-BI). J. Lipid Res. 38:1490–95 [Google Scholar]
  51. Trigatti BL.51.  2017. SR-B1 and PDZK1: partners in HDL regulation. Curr. Opin. Lipidol. 28:201–8 [Google Scholar]
  52. Webb NR, Connell PM, Graf GA, Smart EJ, de Villiers WJ. 52.  et al. 1998. SR-BII, an isoform of the scavenger receptor BI containing an alternate cytoplasmic tail, mediates lipid transfer between high density lipoprotein and cells. J. Biol. Chem. 273:15241–48 [Google Scholar]
  53. Carithers LJ, Moore HM. 53.  2015. The Genotype-Tissue Expression (GTEx) Project. Biopreserv. Biobank. 13:307–8 [Google Scholar]
  54. Chen R, Jiang X, Sun D, Han G, Wang F. 54.  et al. 2009. Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J. Proteome Res. 8:651–61 [Google Scholar]
  55. Viñals M, Xu S, Vasile E, Krieger M. 55.  2003. Identification of the N-linked glycosylation sites on the high density lipoprotein (HDL) receptor SR-BI and assessment of the effects on HDL binding and selective lipid uptake. J. Biol. Chem. 278:5325–32 [Google Scholar]
  56. Bian Y, Song C, Cheng K, Dong M, Wang F. 56.  et al. 2014. An enzyme assisted RP-RPLC approach for in-depth analysis of human liver phosphoproteome. J. Proteom. 96:253–62 [Google Scholar]
  57. Gaidukov L, Nager A, Xu S, Penman M, Krieger M. 57.  2011. Glycine dimerization motif in the N-terminal transmembrane domain of the high density lipoprotein receptor SR-BI required for normal receptor oligomerization and lipid transport. J. Biol. Chem. 286:18452–64 [Google Scholar]
  58. Neculai D, Schwake M, Ravichandran M, Zunke F, Collins RF. 58.  et al. 2013. Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature 504:172–76 [Google Scholar]
  59. Rasmussen JT, Berglund L, Rasmussen MS, Petersen TE. 59.  1998. Assignment of disulfide bridges in bovine CD36. Eur. J. Biochem. 257:488–94 [Google Scholar]
  60. Yu M, Lau TY, Carr SA, Krieger M. 60.  2012. Contributions of a disulfide bond and a reduced cysteine side chain to the intrinsic activity of the high-density lipoprotein receptor SR-BI. Biochemistry 51:10044–55 [Google Scholar]
  61. Hu J, Zhang Z, Shen WJ, Nomoto A, Azhar S. 61.  2011. Differential roles of cysteine residues in the cellular trafficking, dimerization, and function of the high-density lipoprotein receptor, SR-BI. Biochemistry 50:10860–75 [Google Scholar]
  62. Yu M, Romer KA, Nieland TJ, Xu S, Saenz-Vash V. 62.  et al. 2011. Exoplasmic cysteine Cys384 of the HDL receptor SR-BI is critical for its sensitivity to a small-molecule inhibitor and normal lipid transport activity. PNAS 108:12243–48 [Google Scholar]
  63. Rigotti A, Edelman ER, Seifert P, Iqbal SN, DeMattos RB. 63.  et al. 1996. Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogenic cells of the murine adrenal gland. J. Biol. Chem. 271:33546–49 [Google Scholar]
  64. Azhar S, Nomoto A, Reaven E. 64.  2002. Hormonal regulation of adrenal microvillar channel formation. J. Lipid Res. 43:861–71 [Google Scholar]
  65. Rigotti A, Edelmann E, Seifert P, Iqbal S, DeMattos R. 65.  et al. 1996. Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogenic cells of the murine adrenal gland. J. Biol. Chem. 271:33545–49 [Google Scholar]
  66. Wang N, Weng W, Breslow JL, Tall AR. 66.  1996. Scavenger receptor BI (SR-BI) is up-regulated in adrenal gland in apolipoprotein A-I and hepatic lipase knock-out mice as a response to depletion of cholesterol stores. In vivo evidence that SR-BI is a functional high density lipoprotein receptor under feedback control. J. Biol. Chem. 271:21001–4 [Google Scholar]
  67. Hu Z, Hu J, Shen WJ, Kraemer FB, Azhar S. 67.  2015. A novel role of salt-inducible kinase 1 (SIK1) in the post-translational regulation of scavenger receptor class B type 1 activity. Biochemistry 54:6917–30 [Google Scholar]
  68. Sun Y, Wang N, Tall AR. 68.  1999. Regulation of adrenal scavenger receptor-BI expression by ACTH and cellular cholesterol pools. J. Lipid Res. 40:1799–805 [Google Scholar]
  69. Liu J, Voutilainen R, Heikkila P, Kahri AI. 69.  1997. Ribonucleic acid expression of the CLA-1 gene, a human homolog to mouse high density lipoprotein receptor SR-BI, in human adrenal tumors and cultured adrenal cells. J. Clin. Endocrinol. Metab. 82:2522–27 [Google Scholar]
  70. Martin G, Pilon A, Albert C, Valle M, Hum DW. 70.  et al. 1999. Comparison of expression and regulation of the high-density lipoprotein receptor SR-BI and the low-density lipoprotein receptor in human adrenocortical carcinoma NCI-H295 cells. Eur. J. Biochem. 261:481–91 [Google Scholar]
  71. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs HH. 71.  1996. Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J. Clin. Investig. 98:984–95 [Google Scholar]
  72. Azhar S, Nomoto A, Leers-Sucheta S, Reaven E. 72.  1998. Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model. J. Lipid Res. 39:1616–28 [Google Scholar]
  73. Reaven E, Nomoto A, Leers-Sucheta S, Temel R, Williams DL, Azhar S. 73.  1998. Expression and microvillar localization of scavenger receptor, class B, type I (a high density lipoprotein receptor) in luteinized and hormone-desensitized rat ovarian model. Endocrinology 139:2847–56 [Google Scholar]
  74. Reaven E, Zhan L, Nomoto A, Leers-Sucheta S, Azhar S. 74.  2000. Expression and microvillar localization of scavenger receptor class B, type I (SR-BI) and selective cholesteryl ester uptake in Leydig cells from rat testis. J. Lipid Res. 41:343–56 [Google Scholar]
  75. Ljunggren SA, Levels JH, Hovingh K, Holleboom AG, Vergeer M. 75.  et al. 2015. Lipoprotein profiles in human heterozygote carriers of a functional mutation P297S in scavenger receptor class B1. Biochim. Biophys. Acta 1851:1587–95 [Google Scholar]
  76. Vergeer M, Korporaal SJ, Franssen R, Meurs I, Out R. 76.  et al. 2011. Genetic variant of the scavenger receptor BI in humans. N. Engl. J. Med. 364:136–45 [Google Scholar]
  77. Lopez D, McLean MP. 77.  1999. Sterol regulatory element-binding protein-1a binds to cis elements in the promoter of the rat high density lipoprotein receptor SR-BI gene. Endocrinology 140:5669–81 [Google Scholar]
  78. Cao G, Garcia CK, Wyne KL, Schultz RA, Parker KL, Hobbs HH. 78.  1997. Structure and localization of the human gene encoding SR-BI/CLA-1. Evidence for transcriptional control by steroidogenic factor 1. J. Biol. Chem. 272:33068–76 [Google Scholar]
  79. Malerød L, Juvet LK, Hanssen-Bauer A, Eskild W, Berg T. 79.  2002. Oxysterol-activated LXRα/RXR induces hSR-BI-promoter activity in hepatoma cells and preadipocytes. Biochem. Biophys. Res. Commun. 299:916–23 [Google Scholar]
  80. Lopez D, McLean MP. 80.  2006. Activation of the rat scavenger receptor class B type I gene by PPARα. Mol. Cell Endocrinol. 251:67–77 [Google Scholar]
  81. Schoonjans K, Annicotte JS, Huby T, Botrugno OA, Fayard E. 81.  et al. 2002. Liver receptor homolog 1 controls the expression of the scavenger receptor class B type I. EMBO Rep 3:1181–87 [Google Scholar]
  82. Lopez D, Sanchez MD, Shea-Eaton W, McLean MP. 82.  2002. Estrogen activates the high-density lipoprotein receptor gene via binding to estrogen response elements and interaction with sterol regulatory element binding protein-1A. Endocrinology 143:2155–68 [Google Scholar]
  83. Lopez D, Sandhoff TW, McLean MP. 83.  1999. Steroidogenic factor-1 mediates cyclic 3′,5′-adenosine monophosphate regulation of the high density lipoprotein receptor. Endocrinology 140:3034–44 [Google Scholar]
  84. Shea-Eaton W, Lopez D, McLean MP. 84.  2001. Yin yang 1 protein negatively regulates high-density lipoprotein receptor gene transcription by disrupting binding of sterol regulatory element binding protein to the sterol regulatory element. Endocrinology 142:49–58 [Google Scholar]
  85. Sporstol M, Tapia G, Malerod L, Mousavi SA, Berg T. 85.  2005. Pregnane X receptor-agonists down-regulate hepatic ATP-binding cassette transporter A1 and scavenger receptor class B type I. Biochem. Biophys. Res. Commun. 331:1533–41 [Google Scholar]
  86. Temel RE, Trigatti B, DeMattos RB, Azhar S, Krieger M, Williams DL. 86.  1997. Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells. PNAS 94:13600–5 [Google Scholar]
  87. Cao G, Zhao L, Stangl H, Hasegawa T, Richardson J. 87.  et al. 1999. Developmental and hormonal regulation of murine scavenger receptor, class B, type 1. Mol. Endocrinol. 13:1460–73 [Google Scholar]
  88. Vieira-van Bruggen D, Kalkman I, van Gent T, van Tol A, Jansen H. 88.  1998. Induction of adrenal scavenger receptor BI and increased high density lipoprotein-cholesteryl ether uptake by in vivo inhibition of hepatic lipase. J. Biol. Chem. 273:32038–41 [Google Scholar]
  89. Mavridou S, Venihaki M, Rassouli O, Tsatsanis C, Kardassis D. 89.  2010. Feedback inhibition of human scavenger receptor class B type I gene expression by glucocorticoid in adrenal and ovarian cells. Endocrinology 151:3214–24 [Google Scholar]
  90. Wang L, Jia XJ, Jiang HJ, Du Y, Yang F. 90.  et al. 2013. MicroRNAs 185, 96, and 223 repress selective high-density lipoprotein cholesterol uptake through posttranscriptional inhibition. Mol. Cell. Biol. 33:1956–64 [Google Scholar]
  91. Hu Z, Shen WJ, Kraemer FB, Azhar S. 91.  2012. MicroRNAs 125a and 455 repress lipoprotein-supported steroidogenesis by targeting scavenger receptor class B type I in steroidogenic cells. Mol. Cell. Biol. 32:5035–45 [Google Scholar]
  92. Gu X, Trigatti B, Xu S, Acton S, Babitt J, Krieger M. 92.  1998. The efficient cellular uptake of high density lipoprotein lipids via scavenger receptor class B type I requires not only receptor-mediated surface binding but also receptor-specific lipid transfer mediated by its extracellular domain. J. Biol. Chem. 273:26338–48 [Google Scholar]
  93. Nieland TJ, Xu S, Penman M, Krieger M. 93.  2011. Negatively cooperative binding of high-density lipoprotein to the HDL receptor SR-BI. Biochemistry 50:1818–30 [Google Scholar]
  94. Thuahnai ST, Lund-Katz S, Dhanasekaran P, de la Llera-Moya M, Connelly MA. 94.  et al. 2004. Scavenger receptor class B type I-mediated cholesteryl ester-selective uptake and efflux of unesterified cholesterol. Influence of high density lipoprotein size and structure. J. Biol. Chem. 279:12448–55 [Google Scholar]
  95. Bocharov A, Baranova I, Vishnyakova T, Remaley A, Csako G. 95.  et al. 2004. Targeting of scavenger receptor class B type I by synthetic amphipathic α-helical-containing peptides blocks lipopolysaccharide (LPS) uptake and LPS-induced pro-inflammatory cytokine responses in THP-1 monocyte cells. J. Biol. Chem. 279:36072–82 [Google Scholar]
  96. Thuahnai S, Lund-Katz S, Anantharamaiah G, Williams D, Phillips M. 96.  2003. A quantitative analysis of apolipoprotein binding to SR-BI: multiple binding sites for lipid-free and lipid-associated apolipoproteins. J. Lipid Res. 44:1132–42 [Google Scholar]
  97. Connelly M, Klein S, Azhar S, Abumrad N, Williams D. 97.  1999. Comparison of class B scavenger receptors, CD36 and scavenger receptor BI (SR-BI), shows that both receptors mediate high density lipoprotein-cholesteryl ester selective uptake but SR-BI exhibits a unique enhancement of cholesteryl ester uptake. J. Biol. Chem. 274:41–47 [Google Scholar]
  98. Sun B, Boyanovsky B, Connelly M, Shridas P, van der Westhuyzen D, Webb N. 98.  2007. Distinct mechanisms for OxLDL uptake and cellular trafficking by class B scavenger receptors CD36 and SR-BI. J. Lipid Res. 48:2560–70 [Google Scholar]
  99. Reaven E, Leers-Sucheta S, Nomoto A, Azhar S. 99.  2001. Expression of scavenger receptor class B type 1 (SR-BI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system. PNAS 98:1613–18 [Google Scholar]
  100. Reaven E, Nomoto A, Cortez Y, Azhar S. 100.  2006. Consequences of over-expression of rat scavenger receptor, SR-BI, in an adrenal cell model. Nutr. Metab. 3:43 [Google Scholar]
  101. Reaven E, Cortez Y, Leers-Sucheta S, Nomoto A, Azhar S. 101.  2004. Dimerization of the scavenger receptor class B type I: formation, function, and localization in diverse cells and tissues. J. Lipid Res. 45:513–28 [Google Scholar]
  102. Kocher O, Yesilaltay A, Cirovic C, Pal R, Rigotti A, Krieger M. 102.  2003. Targeted disruption of the PDZK1 gene in mice causes tissue-specific depletion of the high density lipoprotein receptor scavenger receptor class B type I and altered lipoprotein metabolism. J. Biol. Chem. 278:52820–25 [Google Scholar]
  103. Hu Z, Hu J, Zhang Z, Shen W, Yun C. 103.  et al. 2013. Regulation of expression and function of scavenger receptor class B, type I (SR-BI) by Na+/H+ exchanger regulatory factors (NHERFs). J. Biol. Chem. 288:11416–35 [Google Scholar]
  104. Thuahnai ST, Lund-Katz S, Williams DL, Phillips MC. 104.  2001. Scavenger receptor class B, type I-mediated uptake of various lipids into cells. Influence of the nature of the donor particle interaction with the receptor. J. Biol. Chem. 276:43801–8 [Google Scholar]
  105. Rodrigueza WV, Thuahnai ST, Temel RE, Lund-Katz S, Phillips MC, Williams DL. 105.  1999. Mechanism of scavenger receptor class B type I-mediated selective uptake of cholesteryl esters from high density lipoprotein to adrenal cells. J. Biol. Chem. 274:20344–50 [Google Scholar]
  106. Silver DL, Wang N, Xiao X, Tall AR. 106.  2001. High density lipoprotein (HDL) particle uptake mediated by scavenger receptor class B type 1 results in selective sorting of HDL cholesterol from protein and polarized cholesterol secretion. J. Biol. Chem. 276:25287–93 [Google Scholar]
  107. Reaven E, Tsai L, Azhar S. 107.  1996. Intracellular events in the “selective” transport of lipoprotein-derived cholesteryl esters. J. Biol. Chem. 271:16208–17 [Google Scholar]
  108. Di Angelantonio E, Sarwar N, Perry P, Kaptoge S, Ray KK. 108.  et al. 2009. Major lipids, apolipoproteins, and risk of vascular disease. JAMA 302:1993–2000 [Google Scholar]
  109. Lewington S, Whitlock G, Clarke R, Sherliker P, Emberson J. 109.  et al. 2007. Blood cholesterol and vascular mortality by age, sex, and blood pressure: a meta-analysis of individual data from 61 prospective studies with 55,000 vascular deaths. Lancet 370:1829–39 [Google Scholar]
  110. Hu J, Zhang Z, Shen WJ, Azhar S. 110.  2010. Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr. Metab. 7:47 [Google Scholar]
  111. De la Llera-Moya M, Rothblat GH, Connelly MA, Kellner-Weibel G, Sakr SW. 111.  et al. 1999. Scavenger receptor BI (SR-BI) mediates free cholesterol flux independently of HDL tethering to the cell surface. J. Lipid Res. 40:575–80 [Google Scholar]
  112. Yancey PG, de la Llera-Moya M, Swarnakar S, Monzo P, Klein SM. 112.  et al. 2000. High density lipoprotein phospholipid composition is a major determinant of the bi-directional flux and net movement of cellular free cholesterol mediated by scavenger receptor BI. J. Biol. Chem. 275:36596–604 [Google Scholar]
  113. Kellner-Weibel G, de la Llera-Moya M, Connelly MA, Stoudt G, Christian AE. 113.  et al. 2000. Expression of scavenger receptor BI in COS-7 cells alters cholesterol content and distribution. Biochemistry 39:221–29 [Google Scholar]
  114. Larrede S, Quinn CM, Jessup W, Frisdal E, Olivier M. 114.  et al. 2009. Stimulation of cholesterol efflux by LXR agonists in cholesterol-loaded human macrophages is ABCA1-dependent but ABCG1-independent. Arterioscler. Thromb. Vasc. Biol. 29:1930–36 [Google Scholar]
  115. Badeau RM, Metso J, Wahala K, Tikkanen MJ, Jauhiainen M. 115.  2009. Human macrophage cholesterol efflux potential is enhanced by HDL-associated 17β-estradiol fatty acyl esters. J. Steroid Biochem. Mol. Biol. 116:44–49 [Google Scholar]
  116. Linton MF, Tao H, Linton EF, Yancey PG. 116.  2017. SR-BI: A multifunctional receptor in cholesterol homeostasis and atherosclerosis. Trends Endocrinol. Metab. 28:461–72 [Google Scholar]
  117. Williams DL, Temel RE, Connelly MA. 117.  2000. Roles of scavenger receptor BI and APO A-I in selective uptake of HDL cholesterol by adrenal cells. Endocr. Res. 26:639–51 [Google Scholar]
  118. Williams D, Wong J, Hamilton R. 118.  2002. SR-BI is required for microvillar channel formation and the localization of HDL particles to the surface of adrenocortical cells in vivo. J. Lipid Res. 43:544 [Google Scholar]
  119. Peng Y, Akmentin W, Connelly M, Lund-Katz S, Phillips M, Williams D. 119.  2004. Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasma membrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein. Mol. Biol. Cell 15:384–96 [Google Scholar]
  120. Yesilaltay A, Morales MG, Amigo L, Zanlungo S, Rigotti A. 120.  et al. 2006. Effects of hepatic expression of the high-density lipoprotein receptor SR-BI on lipoprotein metabolism and female fertility. Endocrinology 147:1577–88 [Google Scholar]
  121. Kozarsky KF, Donahee MH, Glick JM, Krieger M, Rader DJ. 121.  2000. Gene transfer and hepatic overexpression of the HDL receptor SR-BI reduces atherosclerosis in the cholesterol-fed LDL receptor-deficient mouse. Arterioscler. Thromb. Vasc. Biol. 20:721–27 [Google Scholar]
  122. Zhang Y, Da Silva JR, Reilly M, Billheimer JT, Rothblat GH, Rader DJ. 122.  2005. Hepatic expression of scavenger receptor class B type I (SR-BI) is a positive regulator of macrophage reverse cholesterol transport in vivo. J. Clin. Investig. 115:2870–74 [Google Scholar]
  123. Zhang W, Yancey PG, Su YR, Babaev VR, Zhang Y. 123.  et al. 2003. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 108:2258–63 [Google Scholar]
  124. Zanoni P, Khetarpal SA, Larach DB, Hancock-Cerutti WF, Millar JS. 124.  et al. 2016. Rare variant in scavenger receptor BI raises HDL cholesterol and increases risk of coronary heart disease. Science 351:1166–71 [Google Scholar]
  125. Lim HY, Thiam CH, Yeo KP, Bisoendial R, Hii CS. 125.  et al. 2013. Lymphatic vessels are essential for the removal of cholesterol from peripheral tissues by SR-BI-mediated transport of HDL. Cell Metab 17:671–84 [Google Scholar]
  126. Zhu W, Saddar S, Seetharam D, Chambliss KL, Longoria C. 126.  et al. 2008. The scavenger receptor class B type I adaptor protein PDZK1 maintains endothelial monolayer integrity. Circ. Res. 102:480–87 [Google Scholar]
  127. Ouimet M, Franklin V, Mak E, Liao X, Tabas I, Marcel YL. 127.  2011. Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab 13:655–67 [Google Scholar]
  128. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K. 128.  et al. 2012. Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab 15:545–53 [Google Scholar]
  129. Pfeiler S, Khandagale AB, Magenau A, Nichols M, Heijnen HF. 129.  et al. 2016. Distinct surveillance pathway for immunopathology during acute infection via autophagy and SR-BI. Sci. Rep. 6:34440 [Google Scholar]
  130. Ahras M, Naing T, McPherson R. 130.  2008. Scavenger receptor class B type I localizes to a late endosomal compartment. J. Lipid Res. 49:1569–76 [Google Scholar]
  131. Jager S, Bucci C, Tanida I, Ueno T, Kominami E. 131.  et al. 2004. Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117:4837–48 [Google Scholar]
  132. McCarthy JJ, Lehner T, Reeves C, Moliterno DJ, Newby LK. 132.  et al. 2003. Association of genetic variants in the HDL receptor, SR-B1, with abnormal lipids in women with coronary artery disease. J. Med. Genet. 40:453–58 [Google Scholar]
  133. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM. 133.  et al. 2010. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466:707–13 [Google Scholar]
  134. Yang X, Sethi A, Yanek LR, Knapper C, Nordestgaard BG. 134.  et al. 2016. SCARB1 gene variants are associated with the phenotype of combined high high-density lipoprotein cholesterol and high lipoprotein (a). Circ. Cardiovasc. Genet. 9:408–18 [Google Scholar]
  135. Hayashi AA, Webb J, Choi J, Baker C, Lino M. 135.  et al. 2011. Intestinal SR-BI is upregulated in insulin-resistant states and is associated with overproduction of intestinal apoB48-containing lipoproteins. Am. J. Physiol. Gastrointest. Liver Physiol. 301:G326–37 [Google Scholar]
  136. Masson D, Koseki M, Ishibashi M, Larson CJ, Miller SG. 136.  et al. 2009. Increased HDL cholesterol and apoA-I in humans and mice treated with a novel SR-BI inhibitor. Arterioscler. Thromb. Vasc. Biol. 29:2054–60 [Google Scholar]
  137. Syder AJ, Lee H, Zeisel MB, Grove J, Soulier E. 137.  et al. 2011. Small molecule scavenger receptor BI antagonists are potent HCV entry inhibitors. J. Hepatol. 54:48–55 [Google Scholar]
  138. Zhu YZ, Qian XJ, Zhao P, Qi ZT. 138.  2014. How hepatitis C virus invades hepatocytes: the mystery of viral entry. World J. Gastroenterol. 20:3457–67 [Google Scholar]
  139. Li Y, Kakinami C, Li Q, Yang B, Li H. 139.  2013. Human apolipoprotein A-I is associated with dengue virus and enhances virus infection through SR-BI. PLOS ONE 8:e70390 [Google Scholar]
  140. Gutierrez-Pajares JL, Ben Hassen C, Chevalier S, Frank PG. 140.  2016. SR-BI: Linking cholesterol and lipoprotein metabolism with breast and prostate cancer. Front. Pharmacol. 7:338 [Google Scholar]
  141. Schörghofer D, Kinslechner K, Preitschopf A, Schütz B, Röhrl C. 141.  et al. 2015. The HDL receptor SR-BI is associated with human prostate cancer progression and plays a possible role in establishing androgen independence. Reprod. Biol. Endocrinol. 13:88 [Google Scholar]
  142. Yuan B, Wu C, Wang X, Wang D, Liu H. 142.  et al. 2016. High scavenger receptor class B type I expression is related to tumor aggressiveness and poor prognosis in breast cancer. Tumor Biol 37:3581–88 [Google Scholar]
  143. Cao WM, Murao K, Imachi H, Yu X, Abe H. 143.  et al. 2004. A mutant high-density lipoprotein receptor inhibits proliferation of human breast cancer cells. Cancer Res 64:1515–21 [Google Scholar]
  144. Shahzad MM, Mangala LS, Han HD, Lu C, Bottsford-Miller J. 144.  et al. 2011. Targeted delivery of small interfering RNA using reconstituted high-density lipoprotein nanoparticles. Neoplasia 13:309–19 [Google Scholar]
  145. Zheng Y, Liu Y, Jin H, Pan S, Qian Y. 145.  et al. 2013. Scavenger receptor B1 is a potential biomarker of human nasopharyngeal carcinoma and its growth is inhibited by HDL-mimetic nanoparticles. Theranostics 3:477–86 [Google Scholar]
  146. Mooberry LK, Sabnis NA, Panchoo M, Nagarajan B, Lacko AG. 146.  2016. Targeting the SR-B1 receptor as a gateway for cancer therapy and imaging. Front. Pharmacol. 7:466 [Google Scholar]
  147. Mooberry LK, Nair M, Paranjape S, McConathy WJ, Lacko AG. 147.  2010. Receptor mediated uptake of paclitaxel from a synthetic high density lipoprotein nanocarrier. J. Drug Target. 18:53–58 [Google Scholar]
  148. Yang S, Damiano MG, Zhang H, Tripathy S, Luthi AJ. 148.  et al. 2013. Biomimetic, synthetic HDL nanostructures for lymphoma. PNAS 110:2511–16 [Google Scholar]
  149. Farokhzad OC, Langer R. 149.  2009. Impact of nanotechnology on drug delivery. ACS Nano 3:16–20 [Google Scholar]
  150. Counsell RE, Pohland RC. 150.  1982. Lipoproteins as potential site-specific delivery systems for diagnostic and therapeutic agents. J. Med. Chem. 25:1115–20 [Google Scholar]
  151. Kader A, Pater A. 151.  2002. Loading anticancer drugs into HDL as well as LDL has little affect on properties of complexes and enhances cytotoxicity to human carcinoma cells. J. Control. Release 80:29–44 [Google Scholar]
  152. Wu M, Frieboes HB, McDougall SR, Chaplain MA, Cristini V, Lowengrub J. 152.  2013. The effect of interstitial pressure on tumor growth: coupling with the blood and lymphatic vascular systems. J. Theor. Biol. 320:131–51 [Google Scholar]
  153. Bricarello DA, Smilowitz JT, Zivkovic AM, German JB, Parikh AN. 153.  2011. Reconstituted lipoprotein: a versatile class of biologically-inspired nanostructures. ACS Nano 5:42–57 [Google Scholar]
  154. Lacko AG, Sabnis NA, Nagarajan B, McConathy WJ. 154.  2015. HDL as a drug and nucleic acid delivery vehicle. Front. Pharmacol. 6:247 [Google Scholar]
  155. Lou B, Liao XL, Wu MP, Cheng PF, Yin CY, Fei Z. 155.  2005. High-density lipoprotein as a potential carrier for delivery of a lipophilic antitumoral drug into hepatoma cells. World J. Gastroenterol. 11:954–59 [Google Scholar]
  156. Sabnis N, Nair M, Israel M, McConathy WJ, Lacko AG. 156.  2012. Enhanced solubility and functionality of valrubicin (AD-32) against cancer cells upon encapsulation into biocompatible nanoparticles. Int. J. Nanomed. 7:975–83 [Google Scholar]
  157. Frias JC, Williams KJ, Fisher EA, Fayad ZA. 157.  2004. Recombinant HDL-like nanoparticles: a specific contrast agent for MRI of atherosclerotic plaques. J. Am. Chem. Soc. 126:16316–17 [Google Scholar]
  158. Cormode DP, Briley-Saebo KC, Mulder WJ, Aguinaldo JG, Barazza A. 158.  et al. 2008. An ApoA-I mimetic peptide high-density-lipoprotein-based MRI contrast agent for atherosclerotic plaque composition detection. Small 4:1437–44 [Google Scholar]
  159. Skajaa T, Cormode DP, Falk E, Mulder WJ, Fisher EA, Fayad ZA. 159.  2010. High-density lipoprotein-based contrast agents for multimodal imaging of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 30:169–76 [Google Scholar]
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SR-B1: A Unique Multifunctional Receptor for Cholesterol Influx and Efflux
Annual Review of Physiology 80, 95 (2018); https://doi.org/10.1146/annurev-physiol-021317-121550
/content/journals/10.1146/annurev-physiol-021317-121550
/content/journals/10.1146/annurev-physiol-021317-121550
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