Scavenger receptor BI and high-density lipoprotein regulate thymocyte apoptosis in sepsis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 5, 2014, Pages 966-975

  Guo, Ling ^a   Zheng, Zhong ^a   Ai, Junting ^a   Howatt, Deborah A ^a   Mittelstadt, Paul R ^b   Thacker, Seth ^c   Daugherty, Alan ^a   Ashwell, Jonathan D ^b   Remaley, Alan T ^c   Li, Xiang An ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

apolipoproteins; apoptosis; lipoproteins; scavenger receptors, class B; sepsis

Indexed keywords

CHOLESTEROL DERIVATIVE; GLUCOCORTICOID RECEPTOR; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; PROBUCOL; SCAVENGER RECEPTOR BI; UNCLASSIFIED DRUG; UNESTERIFIED CHOLESTEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELLULAR STRESS RESPONSE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SEPSIS; THYMOCYTE;

APOLIPOPROTEINS; APOPTOSIS; LIPOPROTEINS; SCAVENGER RECEPTORS, CLASS B; SEPSIS;

ANIMALS; APOPTOSIS; CECUM; CELLS, CULTURED; CHOLESTEROL, HDL; CORTICOSTERONE; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LIGATION; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHATIDYLCHOLINE-STEROL O-ACYLTRANSFERASE; PROBUCOL; PROTEIN TRANSPORT; PUNCTURES; RECEPTORS, GLUCOCORTICOID; SCAVENGER RECEPTORS, CLASS B; SEPSIS; SIGNAL TRANSDUCTION; THYMOCYTES;

EID: 84899630580     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.302484     Document Type: Article

References (52)

1. Martin GS, Mannino DM, Eaton S, Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med. 2003;348:1546-1554.
2. Hotchkiss RS, Swanson PE, Cobb JP, Jacobson A, Buchman TG, Karl IE. Apoptosis in lymphoid and parenchymal cells during sepsis: findings in normal and T- and B-cell-deficient mice. Crit Care Med. 1997;25:1298-1307.
3. Ayala A, Herdon CD, Lehman DL, DeMaso CM, Ayala CA, Chaudry IH. The induction of accelerated thymic programmed cell death during polymicrobial sepsis: control by corticosteroids but not tumor necrosis factor. Shock. 1995;3:259-267.
4. SchmidtS, Rainer J, Ploner C, Presul E, Riml S, Kofler R. Glucocorticoid-induced apoptosis and glucocorticoid resistance: molecular mechanisms and clinical relevance. Cell Death Differ. 2004;11(suppl 1):S45-S55.
5. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs HH. 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;98:984-995.
6. Calvo D, Vega MA. Identification, primary structure, and distribution of CLA-1, a novel member of the CD36/LIMPII gene family. J Biol Chem. 1993;268:18929-18935.
7. Acton SL, Scherer PE, Lodish HF, Krieger M. Expression cloning of SR-BI, a CD36-related class B scavenger receptor. J Biol Chem. 1994;269:21003-21009.
8. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996;271:518-520.
9. Holmes RS, LA C. Comparative studies of vertebrate scavenger receptor class b type 1: a high-density lipoprotein binding protein. Res Rep Biochem. 2012;2:9-24.
10. Mineo C, Shaul PW. Functions of scavenger receptor class B, type I in atherosclerosis. Curr Opin Lipidol. 2012;23:487-493.
11. Krieger M. Charting the fate of the "good cholesterol": identification and characterization of the high-density lipoprotein receptor SR-BI. Annu Rev Biochem. 1999;68:523-558.
12. Arai T, Rinninger F, Varban L, Fairchild-Huntress V, Liang CP, Chen W, Seo T, Deckelbaum R, Huszar D, Tall AR. Decreased selective uptake of high density lipoprotein cholesteryl esters in apolipoprotein E knock-out mice. Proc Natl Acad Sci U S A. 1999;96:12050-12055.
13. Braun A, Trigatti BL, Post MJ, Sato K, Simons M, Edelberg JM, Rosenberg RD, Schrenzel M, Krieger M. 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.
14. Kozarsky KF, Donahee MH, Glick JM, Krieger M, Rader DJ. 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. 2000;20:721-727.
15. Yu H, Zhang W, Yancey PG, Koury MJ, Zhang Y, Fazio S, Linton MF. Macrophage apolipoprotein E reduces atherosclerosis and prevents premature death in apolipoprotein E and scavenger receptor-class BI double-knockout mice. Arterioscler Thromb Vasc Biol. 2006;26:150-156.
16. Van Eck M, Twisk J, Hoekstra M, Van Rij BT, Van der Lans CA, Bos IS, Kruijt JK, Kuipers F, Van Berkel TJ. 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.
17. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, Krieger M. 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.
18. Brundert M, Ewert A, Heeren J, Behrendt B, Ramakrishnan R, Greten H, Merkel M, Rinninger F. 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.
19. Brundert M, Heeren J, Bahar-Bayansar M, Ewert A, Moore KJ, Rinninger F. Selective uptake of HDL cholesteryl esters and cholesterol efflux from mouse peritoneal macrophages independent of SR-BI. J Lipid Res. 2006;47:2408-2421.
20. Ma K, Forte T, Otvos JD, Chan L. Differential additive effects of endothelial lipase and scavenger receptor-class B type I on high-density lipoprotein metabolism in knockout mouse models. Arterioscler Thromb Vasc Biol. 2005;25:149-154.
21. Miettinen HE, Rayburn H, Krieger M. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J Clin Invest. 2001;108:1717-1722.
22. Braun A, Zhang S, Miettinen HE, Ebrahim S, Holm TM, Vasile E, Post MJ, Yoerger DM, Picard MH, Krieger JL, Andrews NC, Simons M, Krieger M. 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.
23. Holm TM, Braun A, Trigatti BL, Brugnara C, Sakamoto M, Krieger M, Andrews NC. Failure of red blood cell maturation in mice with defects in the high-density lipoprotein receptor SR-BI. Blood. 2002;99:1817-1824.
24. Meurs I, Hoekstra M, van Wanrooij EJ, Hildebrand RB, Kuiper J, Kuipers F, Hardeman MR, Van Berkel TJ, Van Eck M. HDL cholesterol levels are an important factor for determining the lifespan of erythrocytes. Exp Hematol. 2005;33:1309-1319.
25. Feng H, Guo L, Wang D, Gao H, Hou G, Zheng Z, Ai J, Foreman O, Daugherty A, Li XA. Deficiency of scavenger receptor BI leads to impaired lymphocyte homeostasis and autoimmune disorders in mice. Arterioscler Thromb Vasc Biol. 2011;31:2543-2551.
26. Guo L, Song Z, Li M, Wu Q, Wang D, Feng H, Bernard P, Daugherty A, Huang B, Li XA. Scavenger receptor BI protects against septic death through its role in modulating inflammatory response. J Biol Chem. 2009;284:19826-19834.
27. Hoekstra M, Meurs I, Koenders M, Out R, Hildebrand RB, Kruijt JK, Van Eck M, Van Berkel TJ. Absence of HDL cholesteryl ester uptake in mice via SR-BI impairs an adequate adrenal glucocorticoid-mediated stress response to fasting. J Lipid Res. 2008;49:738-745.
28. Cai L, Ji A, de Beer FC, Tannock LR, van der Westhuyzen DR. SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance. J Clin Invest. 2008;118:364-375.
29. Li XA, Guo L, Dressman JL, Asmis R, Smart EJ. A novel ligand-independent apoptotic pathway induced by scavenger receptor class B, type I and suppressed by endothelial nitric-oxide synthase and high density lipoprotein. J Biol Chem. 2005;280:19087-19096.
30. Ravichandran KS, Lorenz U. Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol. 2007;7:964-974.
31. Swan R, Chung CS, Albina J, Cioffi W, Perl M, Ayala A. Polymicrobial sepsis enhances clearance of apoptotic immune cells by splenic macrophages. Surgery. 2007;142:253-261.
32. Pariante CM, Pearce BD, Pisell TL, Su C, Miller AH. The steroid receptor antagonists RU40555 and RU486 activate glucocorticoid receptor translocation and are not excreted by the steroid hormones transporter in L929 cells. J Endocrinol. 2001;169:309-320.
33. Williamson R, Lee D, Hagaman J, Maeda N. Marked reduction of high density lipoprotein cholesterol in mice genetically modified to lack apolipoprotein A-I. Proc Natl Acad Sci U S A. 1992;89:7134-7138.
34. Suzuki M, Pritchard DK, Becker L, Hoofnagle AN, Tanimura N, Bammler TK, Beyer RP, Bumgarner R, Vaisar T, de Beer MC, de Beer FC, Miyake K, Oram JF, Heinecke JW. High-density lipoprotein suppresses the type I interferon response, a family of potent antiviral immunoregulators, in macrophages challenged with lipopolysaccharide. Circulation. 2010;122:1919-1927.
35. Sorci-Thomas MG, Zabalawi M, Bharadwaj MS, Wilhelm AJ, Owen JS, Asztalos BF, Bhat S, Thomas MJ. Dysfunctional HDL containing L159R ApoA-I leads to exacerbation of atherosclerosis in hyperlipidemic mice. Biochim Biophys Acta. 2012;1821:502-512.
36. Wilhelm AJ, Zabalawi M, Grayson JM, Weant AE, Major AS, Owen J, Bharadwaj M, Walzem R, Chan L, Oka K, Thomas MJ, Sorci-Thomas MG. Apolipoprotein A-I and its role in lymphocyte cholesterol homeostasis and autoimmunity. Arterioscler Thromb Vasc Biol. 2009;29:843-849.
37. Plump AS, Erickson SK, Weng W, Partin JS, Breslow JL, Williams DL. Apolipoprotein A-I is required for cholesteryl ester accumulation in steroidogenic cells and for normal adrenal steroid production. J Clin Invest. 1996;97:2660-2671.
38. Cooper RA, Arner EC, Wiley JS, Shattil SJ. Modification of red cell membrane structure by cholesterol-rich lipid dispersions. A model for the primary spur cell defect. J Clin Invest. 1975;55:115-126.
39. Bhattacharyya S, Brown DE, Brewer JA, Vogt SK, Muglia LJ. Macrophage glucocorticoid receptors regulate Toll-like receptor 4-mediated inflammatory responses by selective inhibition of p38 MAP kinase. Blood. 2007;109:4313-4319.
40. Kleiman A, Hübner S, Rodriguez Parkitna JM, Neumann A, Hofer S, Weigand MA, Bauer M, Schmid W, Schütz G, Libert C, Reichardt HM, Tuckermann JP. Glucocorticoid receptor dimerization is required for survival in septic shock via suppression of interleukin-1 in macrophages. FASEB J. 2012;26:722-729.
41. Goodwin JE, Feng Y, Velazquez H, Sessa WC. Endothelial glucocorticoid receptor is required for protection against sepsis. Proc Natl Acad Sci U S A. 2013;110:306-311.
42. Kraemer FB. Adrenal cholesterol utilization. Mol Cell Endocrinol. 2007;265-266:42-45.
43. Allen JM, Thompson GR, Myant NB. Normal adrenocortical response to adrenocorticotrophic hormone in patients with homozygous familial hypercholesterolaemia. Clin Sci (Lond). 1983;65:99-101.
44. Illingworth DR, Alam NA, Lindsey S. Adrenocortical response to adrenocorticotropin in heterozygous familial hypercholesterolemia. J Clin Endocrinol Metab. 1984;58:206-211.
45. Vergeer M, Korporaal SJ, Franssen R, Meurs I, Out R, Hovingh GK, Hoekstra M, Sierts JA, Dallinga-Thie GM, Motazacker MM, Holleboom AG, Van Berkel TJ, Kastelein JJ, Van Eck M, Kuivenhoven JA. Genetic variant of the scavenger receptor BI in humans. N Engl J Med. 2011;364:136-145.
46. Barter PJ, Nicholls S, Rye KA, Anantharamaiah GM, Navab M, Fogelman AM. Antiinflammatory properties of HDL. Circ Res. 2004;95:764-772.
47. Lewis GF, Rader DJ. New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ Res. 2005;96:1221-1232.
48. Feng H, Li XA. Dysfunctional high-density lipoprotein. Curr Opin Endocrinol Diabetes Obes. 2009;16:156-162.
49. Smith JD. Dysfunctional HDL as a diagnostic and therapeutic target. Arterioscler Thromb Vasc Biol. 2010;30:151-155.
50. Otocka-Kmiecik A, Mikhailidis DP, Nicholls SJ, Davidson M, Rysz J, Banach M. Dysfunctional HDL: a novel important diagnostic and therapeutic target in cardiovascular disease? Prog Lipid Res. 2012;51:314-324.
51. Hewing B, Moore KJ, Fisher EA. HDL and cardiovascular risk. Circ Res. 2012;111:1117-1120.
52. Mittelstadt PR, Monteiro JP, Ashwell JD. Thymocyte responsiveness to endogenous glucocorticoids is required for immunological fitness. J Clin Invest. 2012;122:2384-2394.