SR-B1 and PDZK1: Partners in HDL regulation

Current Opinion in Lipidology

Volumn 28, Issue 2, 2017, Pages 201-208

  Trigatti, Bernardo L ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b HAMILTON HEALTH SCIENCES   (Canada)

Author keywords

atherosclerosis; genetics; HDL; PDZK1; SR B1

Indexed keywords

ADAPTOR PROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PDZ PROTEIN; POSTSYNAPTIC DENSITY 95 DISKS LARGE ZO 1 DOMAIN K1 PROTEIN; SCAVENGER RECEPTOR BI; UNCLASSIFIED DRUG; CARRIER PROTEIN; HIGH DENSITY LIPOPROTEIN; SCAVENGER RECEPTOR B;

ATHEROSCLEROSIS; CHOLESTEROL LIVER LEVEL; CHOLESTEROL TRANSPORT; GENE MUTATION; HUMAN; METABOLIC REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MUTATION;

ANIMALS; CARRIER PROTEINS; HUMANS; LIPOPROTEINS, HDL; MUTATION; SCAVENGER RECEPTORS, CLASS B;

EID: 85010977231     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0000000000000396     Document Type: Review

References (76)

1. Prabhudas M, Bowdish D, Drickamer K, et al. Standardizing scavenger receptor nomenclature. J Immunol 2014; 192:1997-2006.
2. Acton S, Rigotti A, Landschulz KT, et al. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 1996; 271:518-520.
3. Le Jossec M, Wambach T, Labuda D, et al. Genetic diversity patterns in the SR-BI/II locus can be explained by a recent selective sweep. Mol Biol Evol 2004; 21:760-769.
4. Webb NR, de Villiers WJ, Connell PM, et al. Alternative forms of the scavenger receptor BI (SR-BI). J Lipid Res 1997; 38:1490-1495.
5. Kocher O, Krieger M. Role of the adaptor protein PDZK1 in controlling the HDL receptor SR-BI. Curr Opin Lipidol 2009; 20:236-241.
6. Webb NR, Connell PM, Graf GA, et al. 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 1998; 273:15241-15248.
7. Pal R, Ke Q, Pihan GA, et al. C-Terminal deletion of the HDL receptor reduces receptor levels in liver and steroidogenic tissues, induces hypercholesterolemia and causes fatal heart disease. Am J Physiol Heart Circ Physiol 2016; 311:H1392-H1408.
8. Kocher O, Birrane G, Tsukamoto K, et al. In vitro and in vivo analysis of the binding of the C terminus of the HDL receptor scavenger receptor class B, type I (SR-BI), to the PDZ1 domain of its adaptor protein PDZK1. J Biol Chem 2010; 285:34999-35010.
9. Kocher O, Birrane G, Yesilaltay A, et al. Identification of the PDZ3 domain of the adaptor protein PDZK1 as a second, physiologically functional binding site for the C terminus of the high density lipoprotein receptor scavenger receptor class B type I. J Biol Chem 2011; 286:25171-25186.
10. Tsukamoto K, Wales TE, Daniels K, et al. Noncanonical role of the PDZ4 domain of the adaptor protein PDZK1 in the regulation of the hepatic high density lipoprotein receptor scavenger receptor class B, type I (SR-BI). J Biol Chem 2013; 288:19845-19860.
11. Al-Jarallah A, Chen X, Gonzalez L, Trigatti BL. High density lipoprotein stimulated migration of macrophages depends on the scavenger receptor class B, type I, PDZK1 and Akt1 and is blocked by sphingosine 1 phosphate receptor antagonists. PloS One 2014; 9:e106487.
12. Kocher O, Yesilaltay A, Cirovic C, et al. 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 2003; 278:52820-52825.
13. Kocher O, Yesilaltay A, Shen CH, et al. Influence of PDZK1 on lipoprotein metabolism and atherosclerosis. Biochimica et biophysica acta 2008; 1782:310-316.
14. Zhu W, Saddar S, Seetharam D, et al. The scavenger receptor class B type I adaptor protein PDZK1 maintains endothelial monolayer integrity. Circ Res 2008; 102:480-487.
15. Al-Jarallah A, Trigatti BL. A role for the scavenger receptor, class B type I in high density lipoprotein dependent activation of cellular signaling pathways. Biochimica et biophysica acta 2010; 1801:1239-1248.
16. Mineo C, Shaul PW. Regulation of signal transduction by HDL. J Lipid Res 2013; 54:2315-2324.
17. Nofer JR. Signal transduction by HDL: Agonists, receptors, and signaling cascades. Handbook of Exp Pharmacol 2015; 224:229-256.
18. Gaidukov L, Nager AR, Xu S, et al. 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 2011; 286:18452-18464.
19. Sahoo D, Peng Y, Smith JR, et al. Scavenger receptor class B, type I (SR-BI) homo-dimerizes via its C-Terminal region: fluorescence resonance energy transfer analysis. Biochimica et biophysica acta 2007; 1771:818-829.
20. Thuahnai ST, Lund-Katz S, Williams DL, Phillips MC. 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 2001; 276:43801-43808.
21. Chadwick AC, Jensen DR, Peterson FC, et al. Expression, purification and reconstitution of the C-Terminal transmembrane domain of scavenger receptor BI into detergent micelles for NMR analysis. Protein Expr Purif 2015; 107:35-42.
22. Neculai D, Schwake M, Ravichandran M, et al. Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature 2013; 504:172-176.
23. Brundert M, Ewert A, Heeren J, et al. Scavenger receptor class B type I mediates the selective uptake of high-density lipoprotein-Associated cholesteryl ester by the liver in mice. Arterioscler Thromb Vasc Biol 2005; 25:143-148.
24. Hoekstra M, Ye D, Hildebrand RB, et al. Scavenger receptor class B type Imediated uptake of serum cholesterol is essential for optimal adrenal glucocorticoid production. J Lipid Res 2009; 50:1039-1046.
25. Kozarsky KF, Donahee MH, Rigotti A, et al. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 1997; 387:414-417.
26. Out R, Hoekstra M, Spijkers JA, et al. Scavenger receptor class B type I is solely responsible for the selective uptake of cholesteryl esters from HDL by the liver and the adrenals in mice. J Lipid Res 2004; 45:2088-2095.
27. Rigotti A, Trigatti BL, Penman M, et al. 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. Proc Natl Acad Sci U S A 1997; 94:12610-12615.
28. Temel RE, Trigatti B, DeMattos RB, et al. 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. Proc Natl Acad Sci U S A 1997; 94:13600-13605.
29. Trigatti B, Rayburn H, Vinals M, et al. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A 1999; 96:9322-9327.
30. Ueda Y, Royer L, Gong E, et al. 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 1999; 274:7165-7171.
31. Wang N, Arai T, Ji Y, et al. 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 1998; 273:32920-32926.
32. Huby T, Doucet C, Dachet C, et al. Knockdown expression and hepatic deficiency reveal an atheroprotective role for SR-BI in liver and peripheral tissues. J Clin Invest 2006; 116:2767-2776.
33. Mardones P, Quinones V, Amigo L, et al. Hepatic cholesterol and bile acid metabolism and intestinal cholesterol absorption in scavenger receptor class B type I-deficient mice. J Lipid Res 2001; 42:170-180.
34. Stylianou IM, Svenson KL, VanOrman SK, et al. Novel ENU-induced point mutation in scavenger receptor class B, member 1, results in liver specific loss of SCARB1 protein. PloS One 2009; 4:e6521.
35. Zhang Y, Da Silva JR, ReillyM, et al. Hepatic expression of scavenger receptor class B type I (SR-BI) is a positive regulator of macrophage reverse cholesterol transport in vivo. J Clin Invest 2005; 115:2870-2874.
36. Covey SD, Krieger M, Wang W, et al. Scavenger receptor class B type Imediated protection against atherosclerosis in LDL receptor-negative mice involves its expression in bone marrow-derived cells. Arterioscler Thromb Vasc Biol 2003; 23:1589-1594.
37. Huszar D, Varban ML, Rinninger F, et al. Increased LDL cholesterol and atherosclerosis in LDL receptor-deficient mice with attenuated expression of scavenger receptor B1. Arterioscler Thromb Vasc Biol 2000; 20:1068-1073.
38. Picataggi A, Lim GF, Kent AP, et al. A coding variant in SR-BI (I179N) significantly increases atherosclerosis in mice. Mammalian Genome 2013; 24:257-265.
39. Van Eck M, Twisk J, Hoekstra M, et al. Differential effects of scavenger receptor BI deficiency on lipid metabolism in cells of the arterial wall and in the liver. J Biol Chem 2003; 278:23699-23705.
40. Gonzalez L, Yu P, Trigatti BL. Mouse models of coronary artery atherosclerosis. J Cardiovasc Disord 2016; 3:id1021.
41. Trigatti BL, Fuller M. HDL signaling and protection against coronary artery atherosclerosis in mice. J Biomed Res 2015; 30:94-100.
42. Braun A, Trigatti BL, Post MJ, et al. Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ Res 2002; 90:270-276.
43. Fuller M, Dadoo O, Serkis V, et al. The effects of diet on occlusive coronary artery atherosclerosis and myocardial infarction in scavenger receptor class B, type 1/low-density lipoprotein receptor double knockout mice. Arterioscler Thromb Vasc Biol 2014; 34:2394-2403.
44. Liao J, Guo X, Wang M, et al. Scavenger receptor class B type 1 deletion led to coronary atherosclerosis and ischemic heart disease in low-density lipoprotein receptor knockout mice on modified western-Type diet. J Atheroscler Thromb 2016. 23 (in press).
45. Zhang S, Picard MH, Vasile E, et al. Diet-induced occlusive coronary atherosclerosis, myocardial infarction, cardiac dysfunction, and premature death in scavenger receptor class B type I-deficient, hypomorphic apolipoprotein ER61 mice. Circulation 2005; 111:3457-3464.
46. Nakagawa-Toyama Y, Zhang S, Krieger M. Dietary manipulation and social isolation alter disease progression in a murine model of coronary heart disease. PloS One 2012; 7:e47965.
47. Braun A, Rigotti A, Trigatti BL. Myocardial infarction following atherosclerosis in murine models. Curr Drug Targets 2008; 9:217-223.
48. Hermann S, Kuhlmann MT, Starsichova A, et al. Imaging reveals the connection between spontaneous coronary plaque ruptures, atherothrombosis, and myocardial infarctions in hypoe/SRBI-/-mice. J Nucl Med 2016; 57:1420-1427.
49. Yesilaltay A, Daniels K, Pal R, et al. Loss of PDZK1 causes coronary artery occlusion and myocardial infarction in Paigen diet-fed apolipoprotein E deficient mice. PloS One 2009; 4:e8103.
50. Pei Y, Chen X, Aboutouk D, et al. SR-BI in bone marrow derived cells protects mice from diet induced coronary artery atherosclerosis and myocardial infarction. PloS ONe 2013; 8:e72492.
51. Tao H, Yancey PG, Babaev VR, et al. Macrophage SR-BI mediates efferocytosis via Src/PI3K/Rac1 signaling and reduces atherosclerotic lesion necrosis. J Lipid Res 2015; 56:1449-1460.
52. Van Eck M, Bos IS, Hildebrand RB, et al. Dual role for scavenger receptor class B, type I on bone marrow-derived cells in atherosclerotic lesion development. Am J Pathol 2004; 165:785-794.
53. Zhang W, Yancey PG, Su YR, et al. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2003; 108:2258-2263.
54. Braun A, Zhang S, Miettinen HE, et al. Probucol prevents early coronary heart disease and death in the high-density lipoprotein receptor SR-BI/apolipoprotein E double knockout mouse. Proc Natl Acad Sci U S A 2003; 100:7283-7288.
55. Dole VS, Matuskova J, Vasile E, et al. Thrombocytopenia and platelet abnormalities in high-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2008; 28:1111-1116.
56. Holm TM, Braun A, Trigatti BL, et al. Failure of red blood cell maturation in mice with defects in the high-density lipoprotein receptor SR-BI. Blood 2002; 99:1817-1824.
57. Korporaal SJ, Meurs I, Hauer AD, et al. Deletion of the high-density lipoprotein receptor scavenger receptor BI in mice modulates thrombosis susceptibility and indirectly affects platelet function by elevation of plasma free cholesterol. Arterioscler Thromb Vasc Biol 2011; 31:34-42.
58. Hoekstra M, van der Sluis RJ, Van Eck M, Van Berkel TJ. Adrenal-specific scavenger receptor BI deficiency induces glucocorticoid insufficiency and lowers plasma very-low-density and low-density lipoprotein levels in mice. Arterioscler Thromb Vasc Biol 2013; 33:e39-e46.
59. Brunham LR, Tietjen I, Bochem AE, et al. Novel mutations in scavenger receptor BI associated with high HDL cholesterol in humans. Clin Genet 2011; 79:575-581.
60. Chadwick AC, Sahoo D. Functional characterization of newly-discovered mutations in human SR-BI. PloS One 2012; 7:e45660.
61. Vergeer M, Korporaal SJ, Franssen R, et al. Genetic variant of the scavenger receptor BI in humans. N Engl J Med 2011; 364:136-145.
62. Vinals M, Xu S, Vasile E, Krieger M. Identification of the N-linked glycosylation sites on the high density lipoprotein (HDL) receptor SR-BI and assessment of their effects on HDL binding and selective lipid uptake. J Biol Chem 2003; 278:5325-5332.
63. Trigatti BL, Hegele RA. Rare genetic variants and high-density lipoprotein: marching to a different drum. Arterioscler Thromb Vasc Biol 2016; 36:e53-e55.
64. Zanoni P, Khetarpal SA, Larach DB, et al. Rare variant in scavenger receptor BI raises HDL cholesterol and increases risk of coronary heart disease. Science 2016; 351:1166-1171
65. Yang X, Sethi A, Yanek LR, et al. SCARB1 gene variants are associated with the phenotype of combined high high-density lipoprotein cholesterol and high lipoprotein (a) circulation. Cardiovasc Genet 2016; 9:408-418.
66. Yang XP, Amar MJ, Vaisman B, et al. Scavenger receptor-BI is a receptor for lipoprotein(a). J Lipid Res 2013; 54:2450-2457.
67. Kartz GA, Holme RL, Nicholson K, Sahoo D. SR-BI/CD36 chimeric receptors define extracellular subdomains of SR-BI critical for cholesterol transport. Biochemistry 2014; 53:6173-6182.
68. Papale GA, Nicholson K, Hanson PJ, et al. Extracellular hydrophobic regions in scavenger receptor BI play a key role in mediating HDL-cholesterol transport. Arch Biochem Biophys 2010; 496:132-139.
69. Lek M, Karczewski KJ, Minikel EV, et al. Analysis of protein-coding genetic variation in 60 706 humans. Nature 2016; 536:285-291.
70. Parathath S, Sahoo D, Darlington YF, et al. Glycine 420 near the C-Terminal transmembrane domain of SR-BI is critical for proper delivery and metabolismof high density lipoprotein cholesteryl ester. J Biol Chem 2004; 279:24976-24985.
71. Nakamura T, Shibata N, Nishimoto-Shibata T, et al. Regulation of SR-BI protein levels by phosphorylation of its associated protein, PDZK1. Proc Natl Acad Sci U S A 2005; 102:13404-13409.
72. Fenske SA, Yesilaltay A, Pal R, et al. Normal hepatic cell surface localization of the high density lipoprotein receptor, scavenger receptor class B, type I, depends on all four PDZ domains of PDZK1. J Biol Chem 2009; 284:5797-5806.
73. Fenske SA, Yesilaltay A, Pal R, et al. Overexpression of the PDZ1 domain of PDZK1 blocks the activity of hepatic scavenger receptor, class B, type I by altering its abundance and cellular localization. J Biol Chem 2008; 283: 22097-22104.
74. Claperon A, Mergey M, Fouassier L. Roles of the scaffolding proteins NHERF in liver biology. Clin Res Hepatol Gastroenterol 2011; 35: 176-181.
75. Lee WR, Sacharidou A, Behling-Kelly E, et al. PDZK1 prevents neointima formation via suppression of breakpoint cluster region kinase in vascular smooth muscle. PloS One 2015; 10:e0124494.
76. Vickers KC, Rodriguez A. Human scavenger receptor class B type I variants, lipid traits, and cardiovascular disease. Circ Cardiovasc Genet 2014; 7:735-737.