High density lipoprotein as a source of cholesterol for adrenal steroidogenesis: A study in individuals with low plasma HDL-C

Journal of Lipid Research

Volumn 54, Issue 6, 2013, Pages 1698-1704

  Bochem, Andrea E ^a   Holleboom, Adriaan G ^a   Romijn, Johannes A ^a   Hoekstra, Menno ^b   Dallinga Thie, Geesje M ^a   Motazacker, Mahdi M ^a   Hovingh, G Kees ^a   Kuivenhoven, Jan A ^c   Stroes, Erik S G ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

17 OXOSTEROID; ABC TRANSPORTER A1; CORTICOTROPIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE;

ADRENAL CORTEX FUNCTION; ADULT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; GENE MUTATION; HETEROZYGOTE; HUMAN; LIPID ANALYSIS; MALE; PRIORITY JOURNAL; STEROIDOGENESIS; URINARY EXCRETION;

CORTISOL; DYSLIPIDEMIA; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYPOALPHALIPOPROTEINEMIA; STEROID HORMONES;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ADULT; AGED; ATP-BINDING CASSETTE TRANSPORTERS; CHOLESTEROL, HDL; HUMANS; MALE; MIDDLE AGED; PHOSPHATIDYLCHOLINE-STEROL O-ACYLTRANSFERASE; STEROIDS;

EID: 84877889801     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.P033449     Document Type: Article

References (34)

1. Hu, J., Z. Zhang, W. J. Shen, and S. Azhar. 2010. Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr. Metab. (Lond.). 7: 47.
2. Borkowski, A., C. Delcroix, and S. Levin. 1972. Metabolism of adrenal cholesterol in man. I. In vivo studies. J. Clin. Invest. 51:1664-1678.
3. Borkowski, A. J., S. Levin, C. Delcroix, A. Mahler, and V. Verhas. 1967. Blood cholesterol and hydrocortisone production in man: quantitative aspects of the utilization of circulating cholesterol by the adrenals at rest and under adrenocorticotropin stimulation. J. Clin. Invest. 46: 797-811.
4. Illingworth, D. R., A. M. Lees, and R. S. Lees. 1983. Adrenal cortical function in homozygous familial hypercholesterolemia. Metabolism.32: 1045-1052. (Pubitemid 13022151)
5. Illingworth, D. R., N. A. Alam, and S. Lindsey. 1984. Adrenocortical response to adrenocorticotropin in heterozygous familial hypercholesterolemia. J. Clin. Endocrinol. Metab. 58: 206-211. (Pubitemid 14220540)
6. Illingworth, D. R., T. A. Kenny, and E. S. Orwoll. 1982. Adrenal function in heterozygous and homozygous hypobetalipoproteinemia. J. Clin. Endocrinol. Metab. 54: 27-33. (Pubitemid 13242129)
7. van der Voort, P. H., R. T. Gerritsen, A. J. Bakker, E. C. Boerma, M. A. Kuiper, and L. de Heide. 2003. HDL-cholesterol level and cortisol response to synacthen in critically ill patients. Intensive Care Med. 29: 2199-2203.
8. Marik, P. E., T. Gayowski, and T. E. Starzl. 2005. The hepatoadrenal syndrome: a common yet unrecognized clinical condition. Crit. Care Med. 33: 1254-1259. (Pubitemid 40827374)
9. Yaguchi, H., K. Tsutsumi, K. Shimono, M. Omura, H. Sasano, and T. Nishikawa. 1998. Involvement of high density lipoprotein as substrate cholesterol for steroidogenesis by bovine adrenal fasciculoreticularis cells. Life Sci. 62: 1387-1395. (Pubitemid 28143981)
10. Azhar, S., and E. Reaven. 2002. Scavenger receptor class BI and selective cholesteryl ester uptake: partners in the regulation of steroidogenesis. Mol. Cell. Endocrinol. 195: 1-26. (Pubitemid 35291178)
11. Azhar, S., S. Leers-Sucheta, and E. Reaven. 2003. Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and 'selective' pathway connection. Front. Biosci. 8: s998-s1029. (Pubitemid 38925366)
12. Reaven, E., Y. D. Chen, M. Spicher, and S. Azhar. 1984. Morphological evidence that high density lipoproteins are not internalized by steroid-producing cells during in situ organ perfusion. J. Clin. Invest. 74: 1384-1397. (Pubitemid 15206835)
13. Azhar, S., D. Stewart, and E. Reaven. 1989. Utilization of cholesterol-rich lipoproteins by perfused rat adrenals. J. Lipid Res. 30:1799-1810. (Pubitemid 20024859)
14. 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 cholesteryl ester uptake in mice via SR-BI impairs an adequate adrenal glucocorticoid-mediated stress response to fasting. J. Lipid Res. 49:738-745.
15. Hoekstra, M., D. Ye, R. B. Hildebrand, Y. Zhao, B. Lammers, M. Stitzinger, J. Kuiper, T. J. Van Berkel, and M. van Eck. 2009. Scavenger receptor class B type I-mediated uptake of serum cholesterol is essential for optimal adrenal glucocorticoid production. J. Lipid Res. 50: 1039-1046.
16. Vergeer, M., S. J. Korporaal, R. Franssen, I. Meurs, R. Out, G. K. Hovingh, M. Hoekstra, J. A. Sierts, G. M. Dallinga-Thie, M. M. Motazacker, et al. 2011. Genetic variant of the scavenger receptor BI in humans. N. Engl. J. Med. 364: 136-145.
17. Candini, C., A. W. Schimmel, J. Peter, A. E. Bochem, A. G. Holleboom, M. Vergeer, R. P. Dullaart, G. M. Dallinga-Thie, G. K. Hovingh, K. L. Khoo, et al. 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: 492-498.
18. Duivenvoorden, R., E. de Groot, B. M. Elsen, J. S. Lameris, R. J. van der Geest, E. S. Stroes, J. J. Kastelein, and A. J. Nederveen. 2009. In vivo quantification of carotid artery wall dimensions: 3.0-Tesla MRI versus B-mode ultrasound imaging. Circ. Cardiovasc. Imaging.2: 235-242.
19. Duivenvoorden, R., A. G. Holleboom, B. van den Bogaard, A. J. Nederveen, E. de Groot, B. A. Hutten, A. W. Schimmel, G. K. Hovingh, J. J. Kastelein, J. A. Kuivenhoven, et al. 2011. Cholesterol acyltransferase gene mutations have accelerated atherogenesis as assessed by carotid 3.0-T magnetic resonance imaging. J. Am. Coll. Cardiol.58: 2481-2487.
20. van Dam, M. J., E. de Groot, S. M. Clee, G. K. Hovingh, R. Roelants, A. Brooks-Wilson, A. H. Zwinderman, A. J. Smit, A. H. Smelt, A. K. Groen, et al. 2002. Association between increased arterial-wall thickness and impairment in ABCA1-driven cholesterol efflux: an observational study. Lancet. 359: 37-42.
21. Holleboom, A. G., J. A. Kuivenhoven, F. Peelman, A. W. Schimmel, J. Peter, J. C. Defesche, J. J. Kastelein, G. K. Hovingh, E. S. Stroes, and M. M. Motazacker. 2011. High prevalence of mutations in LCAT in patients with low HDL cholesterol levels in The Netherlands: identification and characterization of eight novel mutations. Hum. Mutat. 32: 1290-1298.
22. van de Calseyde, J. F., R. J. Scholtis, N. A. Schmidt, and C. J. Leijten. 1972. Profiling urinary steroids. A reliable procedure. Clin. Chim. Acta. 38: 103-111.
23. Weykamp, C. W., T. J. Penders, N. A. Schmidt, A. J. Borburgh, J. F. van de Calseyde, and B. J. Wolthers. 1989. Steroid profile for urine: reference values. Clin. Chem. 35: 2281-2284. (Pubitemid 20017681)
24. Coolens, J. L., van Baelen, H., and W. Heyns. 1987. Clinical use of unbound plasma cortisol as calculated from total cortisol and corticosteroid-binding globulin. J. Steroid Biochem. 26: 197-202. (Pubitemid 17040122)
25. Doi, S. A., I. Lasheen, K. Al-Humood, and K. A. Al-Shoumer. 2006. Relationship between cortisol increment and basal cortisol: implications for the low-dose short adrenocorticotropic hormone stimulation test. Clin. Chem. 52: 746-749.
26. Thaler, L. M., and L. S. Blevins, Jr. 1998. The low dose (1-microg) adrenocorticotropin stimulation test in the evaluation of patients with suspected central adrenal insufficiency. J. Clin. Endocrinol. Metab. 83: 2726-2729. (Pubitemid 28493767)
27. Vahouny, G. V., R. Chanderbhan, R. Hinds, V. A. Hodges, and C. R. Treadwell. 1978. ACTH-induced hydrolysis of cholesteryl esters in rat adrenal cells. J. Lipid Res. 19: 570-577. (Pubitemid 8395753)
28. Azhar, S., Y. D. Chen, and G. M. Reaven. 1983. Stimulation of lipoprotein receptors and role of lipoprotein and cellular cholesterol during gonadotropin-induced desensitization of steroidogenic response in luteinized rat ovary. J. Biol. Chem. 258:3735-3740. (Pubitemid 13055787)
29. Schumacher, M., M. Schwarz, and F. Leidenberger. 1985. Desensitization of mouse Leydig cells in vivo: evidence for the depletion of cellular cholesterol. Biol. Reprod. 33: 335-345. (Pubitemid 15020629)
30. Snow, K., N. S. Jiang, P. C. Kao, and B. W. Scheithauer. 1992. Biochemical evaluation of adrenal dysfunction: the laboratory perspective. Mayo Clin. Proc. 67: 1055-1065.
31. Streeten, D. H., G. H. Anderson, Jr., T. G. Dalakos, D. Seeley, J. S. Mallov, R. Eusebio, F. S. Sunderlin, S. Z. Badawy, and R. B. King. 1984. Normal and abnormal function of the hypothalamic-pituitary-adrenocortical system in man. Endocr. Rev. 5: 371-394.
32. Wellington, C. L., E. K. Walker, A. Suarez, A. Kwok, N. Bissada, R. Singaraja, Y. Z. Yang, L. H. Zhang, E. James, J. E. Wilson, et al. 2002. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab. Invest. 82: 273-283. (Pubitemid 34242521)
33. Brunham, L. R., J. K. Kruit, T. D. Pape, J. M. Timmins, A. Q. Reuwer, Z. Vasanji, B. J. Marsh, B. Rodrigues, J. D. Johnson, J. S. Parks, et al. 2007. Beta-cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat. Med.13: 340-347. (Pubitemid 46376682)
34. Vergeer, M., L. R. Brunham, J. Koetsveld, J. K. Kruit, C. B. Verchere, J. J. Kastelein, M. R. Hayden, and E. S. Stroes. 2010. Carriers of loss-of-function mutations in ABCA1 display pancreatic beta-cell dysfunction. Diabetes Care. 33: 869-874.