Scavenger receptor class B type I-mediated uptake of serum cholesterol is essential for optimal adrenal glucocorticoid production

Journal of Lipid Research

Volumn 50, Issue 6, 2009, Pages 1039-1046

  Hoekstra, Menno ^a   Ye, Dan ^a   Hildebrand, Reeni B ^a   Zhao, Ying ^a   Lammers, Bart ^a   Stitzinger, Miranda ^a   Kuiper, Johan ^a   Van Berkel, Theo J C ^a   Van Eck, Miranda ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Adrenals; Cholesteryl ester transfer protein; Cholesterylester; Corticosterone; Highdensity lipoprotein; Inflammation; Low density lipoprotein

Indexed keywords

CHOLESTEROL ESTER TRANSFER PROTEIN; GLUCOCORTICOID; LIPOPOLYSACCHARIDE; SCAVENGER RECEPTOR BI; TUMOR NECROSIS FACTOR ALPHA;

ADRENAL CORTEX; ADRENAL FUNCTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; GENE EXPRESSION; HORMONE SYNTHESIS; HUMAN; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; STEROIDOGENESIS; TRANSGENE;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CHOLESTEROL; CHOLESTEROL ESTER TRANSFER PROTEINS; CHOLESTEROL ESTERS; CORTICOSTERONE; DNA PRIMERS; GLUCOCORTICOIDS; HUMANS; LIPOPROTEINS, HDL; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RECOMBINANT PROTEINS; RNA, MESSENGER; SCAVENGER RECEPTORS, CLASS B;

EID: 67650517085     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800410-JLR200     Document Type: Article

References (38)

1. Van Eck, M., M. Pennings, M. Hoekstra, R. Out, and T. J. Van Berkel. 2005. Scavenger receptor BI and ATP-binding cassette transporter A1 in reverse cholesterol transport and atherosclerosis. Curr. Opin. Lipidol. 16: 307-315.
2. Lewis, G. F., and D. J. Rader. 2005. New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ. Res. 96: 1221-1232.
3. Acton, S., A. Rigotti, K. T. Landschulz, S. Xu, H. H. Hobbs, and M. Krieger. 1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 271: 518-520.
4. Out, R., M. Hoekstra, J. A. Spijkers, J. K. Kruijt, M. Van Eck, I. S. Bos, J. Twisk, and T. J. Van Berkel. 2004. 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. 45: 2088-2095.
5. Hoekstra, M., I. Meurs, M. Koenders, R. Out, R. B. Hildebrand, J. K. Kruijt, M. Van Eck, and T. J. Van Berkel. 2008. Absence of HDL cholesterol ester uptake in mice via SR-BI impairs an adequate adrenal glucocorticoid-mediated stress response to fasting. J. Lipid Res. 49: 738-745.
6. Cai, L., A. Ji, F. C.deBeer,L. R.Tannock, andD. R. van der Westhuyzen. 2008. SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance. J. Clin. Invest. 118: 364-375.
7. Nagashima, M., J. W. McLean, and R. M. Lawn. 1988. Cloning and mRNA tissue distribution of rabbit cholesteryl ester transfer protein. J. Lipid Res. 29: 1643-1649.
8. Drayna, D., A. S. Jarnagin, J. McLean, W. Henzel, W. Kohr, C. Fielding, and R. Lawn. 1987. Cloning and sequencing of human cholesteryl ester transfer protein cDNA. Nature. 327: 632-634.
9. Pape, M. E., E. F. Rehberg, K. R. Marotti, and G. W. Melchior. 1991. Molecular cloning, sequence, and expression of cynomolgus monkey cholesteryl ester transfer protein. Inverse correlation between hepatic cholesteryl ester transfer protein mRNA levels and plasma high density lipoprotein levels. Arterioscler. Thromb. 11: 1759-1771.
10. Van Eck, M., D. Ye, R. B. Hildebrand, J. Kar Kruijt, W. de Haan, M. Hoekstra, P. C. Rensen, C. Ehnholm, M. Jauhiainen, and T. J. Van Berkel. 2007. Important role for bonemarrow-derived cholesteryl ester transfer protein in lipoprotein cholesterol redistribution and atherosclerotic lesion development in LDL receptor knockout mice. Circ. Res. 100: 678-685.
11. Tall, A. R. 1993. Plasma cholesteryl ester transfer protein. J. Lipid Res. 34: 1255-1274.
12. Windler, E. E., P. T. Kovanen, Y. S. Chao, M. S. Brown, R. J. Havel, and J. L. Goldstein. 1980. The estradiol-stimulated lipoprotein receptor of rat liver. A binding site that membrane mediates the uptake of rat lipoproteins containing apoproteins B and E. J. Biol. Chem. 255: 10464-10471.
13. Kovanen, P. T., J. R. Faust, M. S. Brown, and J. L. Goldstein. 1979. Low density lipoprotein receptors in bovine adrenal cortex. I. Receptor-mediated uptake of low density lipoprotein and utilization of its cholesterol for steroid synthesis in cultured adrenocortical cells. Endocrinology. 104: 599-609.
14. Kita, T., U. Beisiegel, J. L. Goldstein, W. J. Schneider, and M. S. Brown. 1981. Antibody against low density lipoprotein receptor blocks uptake of low density lipoprotein (but not high density lipoprotein) by the adrenal gland of the mouse in vivo. J. Biol. Chem. 256: 4701-4703.
15. Fong, L. G., E. Bonney, J. C. Kosek, and A. D. Cooper. 1989. Immunohistochemical localization of low density lipoprotein receptors in adrenal gland, liver, and intestine. J. Clin. Invest. 84: 847-856.
16. Rigotti, A., B. L. Trigatti, M. Penman, H. Rayburn, J. Herz, and M. Krieger. 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. Proc. Natl. Acad. Sci. USA. 94: 12610-12615.
17. Jiang, X. C., L. B. Agellon, A. Walsh, J. L. Breslow, and A. Tall. 1992. Dietary cholesterol increases transcription of the human cholesteryl ester transfer protein gene in transgenic mice. Dependence on natural flanking sequences. J. Clin. Invest. 90: 1290-1295.
18. Hoekstra, M., J. K. Kruijt, M. Van Eck, and T. J. Van Berkel. 2003. Specific gene expression of ATP-binding cassette transporters and nuclear hormone receptors in rat liver parenchymal, endothelial, and Kupffer cells. J. Biol. Chem. 278: 25448-25453.
19. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
20. Redgrave, T. G., D. C. Roberts, and C. E. West. 1975. Separation of plasma lipoproteins by density-gradient ultracentrifugation. Anal. Biochem. 65: 42-49.
21. Fluiter, K., H. Vietsch, E. A. Biessen, G. M. Kostner, T. J. van Berkel, and W. Sattler. 1996. Increased selective uptake in vivo and in vitro of oxidized cholesteryl esters from high-density lipoprotein by rat liver parenchymal cells. Biochem. J. 319: 471-476.
22. Ho, M. M., and G. P. Vinson. 1997. Peptide growth factors and the adrenal cortex. Microsc. Res. Tech. 36: 558-568.
23. Heikkilä, P., J. Arola, J. Liu, and A. I. Kahri. 1998. ACTH regulates LDL receptor and CLA-1 mRNA in the rat adrenal cortex. Endocr. Res. 24: 591-593.
24. Kovanen, P. T., J. L. Goldstein, D. A. Chappell, and M. S. Brown. 1980. Regulation of low density lipoprotein receptors by adrenocorticotropin in the adrenal gland of mice and rats in vivo. J. Biol. Chem. 255: 5591-5598.
25. Kraemer, F. B. 2007. Adrenal cholesterol utilization. Mol. Cell. Endocrinol. 265-266: 42-45.
26. Martin, G., A. Pilon, C. Albert, M. Vallé, D. W. Hum, J. C. Fruchart, J. Najib, V. Clavey, and B. Staels. 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: 481-491.
27. Pilon, A., G. Martin, S. Bultel-Brienne, D. Junquero, A. Delhon, J. C. Fruchart, B. Staels, and V. Clavey. 2003. Regulation of the scavenger receptor BI and the LDL receptor by activators of aldosterone production, angiotensin II and PMA, in the human NCI-H295R adrenocortical cell line. Biochim. Biophys. Acta. 1631: 218-228.
28. Liu, J., P. Heikkila, Q. H. Meng, A. I. Kahri, M. J. Tikkanen, and R. Voutilainen. 2000. Expression of low and high density lipoprotein receptor genes in human adrenals. Eur. J. Endocrinol. 142: 677-682.
29. Sun, Y., N. Wang, and A. R. Tall. 1999. Regulation of adrenal scavenger receptor-BI expression by ACTH and cellular cholesterol pools. J. Lipid Res. 40: 1799-1805.
30. Rigotti, A., E. R. Edelman, P. Seifert, S. N. Iqbal, R. B. DeMattos, R. E. Temel, M. Krieger, and D. L. Williams. 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: 33545-33549.
31. Murao, K., V. Terpstra, S. R. Green, N. Kondratenko, D. Steinberg, and O. Quehenberger. 1997. 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. 272: 17551-17557.
32. Harder, C., P. Lau, A. Meng, S. C. Whitman, and R. McPherson. 2007. Cholesteryl ester transfer protein (CETP) expression protects against diet induced atherosclerosis in SR-BI deficient mice. Arterioscler. Thromb. Vasc. Biol. 27: 858-864.
33. Kraemer, F. B.,W. J. Shen, S. Patel, J. Osuga, S. Ishibashi, and S. Azhar. 2007. The LDL receptor is not necessary for acute adrenal steroidogenesis in mouse adrenocortical cells. Am. J. Physiol. Endocrinol. Metab. 292: E408-E412.
34. Temel, R. E., B. Trigatti, R. B. DeMattos, S. Azhar, M. Krieger, and D. L. Williams. 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. Proc. Natl. Acad. Sci. USA. 94: 13600-13605.
35. Hsu, L. A., Y. L. Ko, S. Wu, M. S. Teng, T. Y. Peng, C. F. Chen, C. F. Chen, and Y. S. Lee. 2003. Association between a novel 11-base pair deletion mutation in the promoter region of the scavenger receptor class B type I gene and plasma HDL cholesterol levels in Taiwanese Chinese. Arterioscler. Thromb. Vasc. Biol. 23: 1869-1874.
36. Morabia, A., B. M. Ross, M. C. Costanza, E. Cayanis, M. S. Flaherty, G. B. Alvin, K. Das, R. James, A. S. Yang, O. Evagrafov, et al. 2004. Population-based study of SR-BI genetic variation and lipid profile. Atherosclerosis. 175: 159-168.
37. Osgood, D., D. Corella, S. Demissie, L. A. Cupples, P. W. Wilson, J. B. Meigs, E. J. Schaefer, O. Coltell, and J. M. Ordovas. 2003. Genetic variation at the scavenger receptor class B type I gene locus determines plasma lipoprotein concentrations and particle size and interacts with type 2 diabetes: the framinghamstudy. J. Clin. Endocrinol. Metab. 88: 2869-2879.
38. Acton, S., D. Osgood, M. Donoghue, D. Corella, M. Pocovi, A. Cenarro, P. Mozas, J. Keilty, S. Squazzo, E. A. Woolf, et al. 1999. Association of polymorphisms at the SR-BI gene locus with plasma lipid levels and body mass index in a white population. Arterioscler. Thromb. Vasc. Biol. 19: 1734-1743.