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PMID: 10430941 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 96 ·No. 16 ·1999-08-03 ·Pages 9322-7

Trigatti B, Rayburn H, Viñals M, Braun A, Miettinen H, Penman M, Hertz M, Schrenzel M, Amigo L, Rigotti A, Krieger M

Abstract

The high density lipoprotein (HDL) receptor SR-BI (scavenger receptor class B type I) mediates the selective uptake of plasma HDL cholesterol by the liver and steroidogenic tissues. As a consequence, SR-BI can influence plasma HDL cholesterol levels, HDL structure, biliary cholesterol concentrations, and the uptake, storage, and utilization of cholesterol by steroid hormone-producing cells. Here we used homozygous null SR-BI knockout mice to show that SR-BI is required for maintaining normal biliary cholesterol levels, oocyte development, and female fertility. We also used SR-BI/apolipoprotein E double homozygous knockout mice to show that SR-BI can protect against early-onset atherosclerosis. Although the mechanisms underlying the effects of SR-BI loss on reproduction and atherosclerosis have not been established, potential causes include changes in (i) plasma lipoprotein levels and/or structure, (ii) cholesterol flux into or out of peripheral tissues (ovary, aortic wall), and (iii) reverse cholesterol transport, as indicated by the significant reduction of gallbladder bile cholesterol levels in SR-BI and SR-BI/apolipoprotein E double knockout mice relative to controls. If SR-BI has similar activities in humans, it may become an attractive target for therapeutic intervention in a variety of diseases.

MeSH Terms
Animals Apolipoprotein A-I/blood Apolipoproteins E/deficiency,genetics,metabolism Arteriosclerosis/genetics,pathology,physiopathology Bile/physiology CD36 Antigens/genetics,physiology Cholesterol/blood,metabolism Cholesterol, HDL/blood Female Homozygote Humans Lipoproteins/blood Membrane Proteins Mice Mice, Inbred C57BL Mice, Inbred Strains Mice, Knockout Organ Specificity Receptors, Immunologic Receptors, Lipoprotein/physiology Receptors, Scavenger Reference Values Scavenger Receptors, Class B Sinus of Valsalva/pathology
Chemicals
Apolipoprotein A-I Apolipoproteins E CD36 Antigens Cholesterol, HDL Lipoproteins Membrane Proteins Receptors, Immunologic Receptors, Lipoprotein Receptors, Scavenger SCARB1 protein, human Scarb1 protein, mouse Scavenger Receptors, Class B Cholesterol
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Trigatti B
Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
Rayburn H
Viñals M
Braun A
Miettinen H
Penman M
Hertz M
Schrenzel M
Amigo L
Rigotti A
Krieger M
References (62)
62 references, click to expand
  1. Apolipoprotein A-I is required for cholesteryl ester accumulation in steroidogenic cells and for normal adrenal steroid production.
    J Clin Invest. 1996 Jun 1;97(11):2660-71 PMID: 8647961
  2. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells.
    Cell. 1992 Oct 16;71(2):343-53 PMID: 1423598
  3. Two-dimensional nondenaturing electrophoresis of lipoproteins: applications to high-density lipoprotein speciation.
    Methods Enzymol. 1996;263:251-9 PMID: 8749012
  4. Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat.
    J Clin Invest. 1996 Aug 15;98(4):984-95 PMID: 8770871
  5. 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. 1996 Aug 30;271(35):21001-4 PMID: 8798380
  6. Disruption of the acyl-CoA:cholesterol acyltransferase gene in mice: evidence suggesting multiple cholesterol esterification enzymes in mammals.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):14041-6 PMID: 8943057
  7. 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. 1996 Dec 27;271(52):33545-9 PMID: 8969220
  8. Apolipoprotein-mediated removal of cellular cholesterol and phospholipids.
    J Lipid Res. 1996 Dec;37(12):2473-91 PMID: 9017501
  9. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection.
    Nature. 1997 Mar 20;386(6622):292-6 PMID: 9069289
  10. Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acylated and colocalizes with plasma membrane caveolae.
    J Biol Chem. 1997 May 16;272(20):13242-9 PMID: 9148942
  11. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels.
    Nature. 1997 May 22;387(6631):414-7 PMID: 9163428
  12. Cloning, characterization, and cellular distribution of rat scavenger receptor class B type I (SRBI) in the ovary.
    Biochem Biophys Res Commun. 1997 May 19;234(2):499-505 PMID: 9177301
  13. ApoA-I knockout mice: characterization of HDL metabolism in homozygotes and identification of a post-RNA mechanism of apoA-I up-regulation in heterozygotes.
    J Lipid Res. 1997 May;38(5):1033-47 PMID: 9186920
  14. Disruption of the murine lecithin:cholesterol acyltransferase gene causes impairment of adrenal lipid delivery and up-regulation of scavenger receptor class B type I.
    J Biol Chem. 1997 Jun 20;272(25):15777-81 PMID: 9188474
  15. Scavenger receptor BI--a cell surface receptor for high density lipoprotein.
    Curr Opin Lipidol. 1997 Jun;8(3):181-8 PMID: 9211067
  16. Characterization of CLA-1, a human homologue of rodent scavenger receptor BI, as a receptor for high density lipoprotein and apoptotic thymocytes.
    J Biol Chem. 1997 Jul 11;272(28):17551-7 PMID: 9211901
  17. Apolipoproteins of HDL can directly mediate binding to the scavenger receptor SR-BI, an HDL receptor that mediates selective lipid uptake.
    J Lipid Res. 1997 Jul;38(7):1289-98 PMID: 9254056
  18. 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. 1997 Aug;82(8):2522-7 PMID: 9253328
  19. Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux.
    J Biol Chem. 1997 Aug 22;272(34):20982-5 PMID: 9261096
  20. 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 Nov 11;94(23):12610-5 PMID: 9356497
  21. 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 Dec 9;94(25):13600-5 PMID: 9391072
  22. Sequence of the bovine HDL-receptor (SR-BI) cDNA and changes in receptor mRNA expression during granulosa cell luteinization in vivo and in vitro.
    Mol Cell Endocrinol. 1997 Oct 31;134(1):59-67 PMID: 9406850
  23. Structure and localization of the human gene encoding SR-BI/CLA-1. Evidence for transcriptional control by steroidogenic factor 1.
    J Biol Chem. 1997 Dec 26;272(52):33068-76 PMID: 9407090
  24. 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 Nov;17(11):2341-9 PMID: 9409200
  25. In vivo regulation of scavenger receptor BI and the selective uptake of high density lipoprotein cholesteryl esters in rat liver parenchymal and Kupffer cells.
    J Biol Chem. 1998 Apr 3;273(14):8434-8 PMID: 9525955
  26. Temporal and spatial pattern of expression of the HDL receptor SR-BI during murine embryogenesis.
    J Lipid Res. 1998 Mar;39(3):495-508 PMID: 9548583
  27. Transport of maternal LDL and HDL to the fetal membranes and placenta of the Golden Syrian hamster is mediated by receptor-dependent and receptor-independent processes.
    J Lipid Res. 1998 Mar;39(3):518-30 PMID: 9548585
  28. Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of high density lipoprotein cholesterol.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4619-24 PMID: 9539787
  29. Expression and microvillar localization of scavenger receptor, class B, type I (a high density lipoprotein receptor) in luteinized and hormone-desensitized rat ovarian models.
    Endocrinology. 1998 Jun;139(6):2847-56 PMID: 9607793
  30. In situ hybridization of high density lipoprotein (scavenger, type 1) receptor messenger ribonucleic acid (mRNA) during folliculogenesis and luteinization: evidence for mRNA expression and induction by human chorionic gonadotropin specifically in cell types that use cholesterol for steroidogenesis.
    Endocrinology. 1998 Jul;139(7):3043-9 PMID: 9645674
  31. Biliary cholesterol excretion: a novel mechanism that regulates dietary cholesterol absorption.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10194-9 PMID: 9707623
  32. 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. 1998 Aug;39(8):1616-28 PMID: 9717722
  33. 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. 1998 Oct 9;273(41):26338-48 PMID: 9756864
  34. Scavenger receptor, class B, type I-dependent stimulation of cholesterol esterification by high density lipoproteins, low density lipoproteins, and nonlipoprotein cholesterol.
    J Biol Chem. 1998 Nov 20;273(47):31002-8 PMID: 9812997
  35. Mouse models of ovarian failure.
    Rev Reprod. 1998 Sep;3(3):183-95 PMID: 9829553
  36. 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 Dec 4;273(49):32920-6 PMID: 9830042
  37. Decreased atherosclerosis in heterozygous low density lipoprotein receptor-deficient mice expressing the scavenger receptor BI transgene.
    J Biol Chem. 1999 Jan 22;274(4):2366-71 PMID: 9891004
  38. Identification of a receptor mediating absorption of dietary cholesterol in the intestine.
    Biochemistry. 1998 Dec 22;37(51):17843-50 PMID: 9922151
  39. Charting the fate of the "good cholesterol": identification and characterization of the high-density lipoprotein receptor SR-BI.
    Annu Rev Biochem. 1999;68:523-58 PMID: 10872459
  40. Separate mechanisms for the uptake of high and low density lipoproteins by mouse adrenal gland in vivo.
    J Biol Chem. 1979 Jun 25;254(12):5498-505 PMID: 221472
  41. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  42. The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands.
    Endocr Rev. 1982 Summer;3(3):299-329 PMID: 6288367
  43. A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology.
    Biol Reprod. 1982 Sep;27(2):327-39 PMID: 6889895
  44. Dissociation of tissue uptake of cholesterol ester from that of apoprotein A-I of rat plasma high density lipoprotein: selective delivery of cholesterol ester to liver, adrenal, and gonad.
    Proc Natl Acad Sci U S A. 1983 Sep;80(17):5435-9 PMID: 6412229
  45. Identification, primary structure, and distribution of CLA-1, a novel member of the CD36/LIMPII gene family.
    J Biol Chem. 1993 Sep 5;268(25):18929-35 PMID: 7689561
  46. Plasma cholesteryl ester transfer protein.
    J Lipid Res. 1993 Aug;34(8):1255-74 PMID: 8409761
  47. In vitro and in vivo evidence for the role of HDL in reverse cholesterol transport.
    Biochim Biophys Acta. 1994 Jan 11;1225(2):125-34 PMID: 8280780
  48. Expression cloning of SR-BI, a CD36-related class B scavenger receptor.
    J Biol Chem. 1994 Aug 19;269(33):21003-9 PMID: 7520436
  49. Diet-induced atherosclerosis in mice heterozygous and homozygous for apolipoprotein E gene disruption.
    J Clin Invest. 1994 Sep;94(3):937-45 PMID: 8083379
  50. Molecular physiology of reverse cholesterol transport.
    J Lipid Res. 1995 Feb;36(2):211-28 PMID: 7751809
  51. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids.
    J Biol Chem. 1995 Jul 7;270(27):16221-4 PMID: 7541795
  52. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor.
    Science. 1996 Jan 26;271(5248):518-20 PMID: 8560269
  53. 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 Mar 12;274(11):7165-71 PMID: 10066776
  54. Myocardial infarction mediated by endothelin receptor signaling in hypercholesterolemic mice.
    Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6920-4 PMID: 10359814
  55. Uptake of high-density lipoprotein-associated apoprotein A-I and cholesterol esters by 16 tissues of the rat in vivo and by adrenal cells and hepatocytes in vitro.
    J Biol Chem. 1985 Jan 25;260(2):744-50 PMID: 3918032
  56. How do the polyene macrolide antibiotics affect the cellular membrane properties?
    Biochim Biophys Acta. 1986 Dec 22;864(3-4):257-304 PMID: 3539192
  57. Quantitative assessment of atherosclerotic lesions in mice.
    Atherosclerosis. 1987 Dec;68(3):231-40 PMID: 3426656
  58. High-density lipoprotein--the clinical implications of recent studies.
    N Engl J Med. 1989 Nov 9;321(19):1311-6 PMID: 2677733
  59. Interconversion of prebeta-migrating lipoproteins containing apolipoprotein A-I and HDL.
    J Lipid Res. 1990 Feb;31(2):227-36 PMID: 2109030
  60. Cholesterol transport between cells and high-density lipoproteins.
    Biochim Biophys Acta. 1991 Oct 1;1085(3):273-98 PMID: 1911862
  61. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E.
    Science. 1992 Oct 16;258(5081):468-71 PMID: 1411543
  62. Modulation of intrahepatic cholesterol trafficking: evidence by in vivo antisense treatment for the involvement of sterol carrier protein-2 in newly synthesized cholesterol transport into rat bile.
    Biochem J. 1996 Aug 1;317 ( Pt 3):681-7 PMID: 8760350
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.96.16.9322
Published
1999-08-03
Pages
9322-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC17781
Subset
IM
Grants
NHLBI NIH HHS · HL41484 · United States
External Links
PubMed source DOI: 10.1073/pnas.96.16.9322 PMC Full Text View journal details
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