Identification of a danger-associated peptide from apolipoprotein B100 (ApoBDS-1) that triggers innate proatherogenic responses

Circulation

Volumn 124, Issue 22, 2011, Pages 2433-2443

  Ketelhuth, Daniel F J ^a   Rios, Francisco J O ^b   Wang, Yajuan ^a,c   Liu, Huiqing ^a,d   Johansson, Maria E ^e   Fredrikson, Gunilla N ^f   Hedin, Ulf ^a,g   Gidlund, Magnus ^b   Nilsson, Jan ^f   Hansson, Göran K ^a   Yan, Zhong Qun ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c SHANDONG UNIVERSITY   (China)

^d SHANDONG UNIVERSITY   (China)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

^f LUND UNIVERSITY HOSPITAL   (Sweden)

^g KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

apolipoprotein B100; atherosclerosis; innate immunity; macrophage; oxidized LDL

Indexed keywords

APOLIPOPROTEIN B100; CUTANEOUS T CELL ATTRACTING CHEMOKINE; INTERLEUKIN 6; INTERLEUKIN 8; LOW DENSITY LIPOPROTEIN; PEPTIDE; PROSTAGLANDIN E2;

ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; EX VIVO STUDY; HUMAN; HUMAN CELL; IMMUNOASSAY; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; PRIORITY JOURNAL;

APOLIPOPROTEIN B-100; ATHEROSCLEROSIS; CALCIUM; CAROTID ARTERY DISEASES; CHEMOKINE CCL2; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-6; INTERLEUKIN-8; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PEPTIDES; PLAQUE, ATHEROSCLEROTIC; SIGNAL TRANSDUCTION;

EID: 82355175118     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.051599     Document Type: Article

References (41)

1. Hevonoja T, Pentikainen MO, Hyvonen MT, Kovanen PT, Ala-Korpela M. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim Biophys Acta. 2000;1488:189-210.
2. Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation. 2007;116:1832-1844. (Pubitemid 350287108)
3. Oorni K, Kovanen PT. Lipoprotein modification by secretory phospholipase A(2) enzymes contributes to the initiation and progression of atherosclerosis. Curr Opin Lipidol. 2009;20:421-427.
4. Esterbauer H, Gebicki J, Puhl H, Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med. 1992;13:341-390.
5. Chen K, Thomas SR, Keaney JF Jr. Beyond LDL oxidation: ROS in vascular signal transduction. Free Radic Biol Med. 2003;35:117-132. (Pubitemid 36835912)
6. Libby P, Ridker PM, Hansson GK. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol. 2009;54:2129-2138.
7. Watson AD, Leitinger N, Navab M, Faull KF, Horkko S, Witztum JL, Palinski W, Schwenke D, Salomon RG, Sha W, Subbanagounder G, Fogelman AM, Berliner JA. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem. 1997;272:13597-13607. (Pubitemid 27224791)
8. Gharavi NM, Alva JA, Mouillesseaux KP, Lai C, Yeh M, Yeung W, Johnson J, Szeto WL, Hong L, Fishbein M, Wei L, Pfeffer LM, Berliner JA. Role of the Jak/STAT pathway in the regulation of interleukin-8 transcription by oxidized phospholipids in vitro and in atherosclerosis in vivo. J Biol Chem. 2007;282:31460-31468. (Pubitemid 350044874)
9. Seimon TA, Nadolski MJ, Liao X, Magallon J, Nguyen M, Feric NT, Koschinsky ML, Harkewicz R, Witztum JL, Tsimikas S, Golenbock D, Moore KJ, Tabas I. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metabol. 2010;12:467-482.
10. Miller YI, Viriyakosol S, Worrall DS, Boullier A, Butler S, Witztum JL. Toll-like receptor 4-dependent and-independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler Thromb Vasc Biol. 2005;25:1213-1219. (Pubitemid 40776611)
11. Stewart CR, Stuart LM, Wilkinson K, van Gils JM, Deng J, Halle A, Rayner KJ, Boyer L, Zhong R, Frazier WA, Lacy-Hulbert A, El Khoury J, Golenbock DT, Moore KJ. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol. 2010;11:155-161.
12. Hermansson A, Ketelhuth DF, Strodthoff D, Wurm M, Hansson EM, Nicoletti A, Paulsson-Berne G, Hansson GK. Inhibition of T cell response to native low-density lipoprotein reduces atherosclerosis. J Exp Med. 2010;207:1081-1093.
13. Ketelhuth DF, Tonini GC, Carvalho MD, Ramos RF, Boschcov P, Gidlund M. Autoantibody response to chromatographic fractions from oxidized LDL in unstable angina patients and healthy controls. Scand J Immunol. 2008;68:456-462.
14. Svensjo E, Boschcov P, Ketelhuth DF, Jancar S, Gidlund M. Increased microvascular permeability in the hamster cheek pouch induced by oxidized low density lipoprotein (oxLDL) and some fragmented apolipoprotein B proteins. Inflamm Res. 2003;52:215-220. (Pubitemid 36712966)
15. Fredrikson GN, Hedblad B, Berglund G, Alm R, Ares M, Cercek B, Chyu KY, Shah PK, Nilsson J. Identification of immune responses against aldehyde-modified peptide sequences in apoB associated with cardiovascular disease. Arterioscler Thromb Vasc Biol. 2003;23:872-878. (Pubitemid 36566180)
16. Goncalves I, Nitulescu M, Ares MP, Fredrikson GN, Jansson B, Li ZC, Nilsson J. Identification of the target for therapeutic recombinant antiapoB-100 peptide antibodies in human atherosclerotic lesions. Atherosclerosis. 2009;205:96-100.
17. Otsu N. A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern. 1979;9:62-66. (Pubitemid 9413341)
18. Rozengurt E. Mitogenic signaling pathways induced by G proteincoupled receptors. J Cell Physiol. 2007;213:589-602. (Pubitemid 350058250)
19. Quinn MT, Parthasarathy S, Fong LG, Steinberg D. Oxidatively modified low density lipoproteins: a potential role in recruitment and retention of monocyte/macrophages during atherogenesis. Proc Natl Acad Sci USA. 1987;84:2995-2998. (Pubitemid 17064764)
20. Quinn MT, Parthasarathy S, Steinberg D. Lysophosphatidylcholine: a chemotactic factor for human monocytes and its potential role in atherogenesis. Proc Natl Acad Sci USA. 1988;85:2805-2809.
21. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010;464:1357-1361.
22. Park YS, Kim J, Misonou Y, Takamiya R, Takahashi M, Freeman MR, Taniguchi N. Acrolein induces cyclooxygenase-2 and prostaglandin production in human umbilical vein endothelial cells: roles of p38 MAP kinase. Arterioscler Thromb Vasc Biol. 2007;27:1319-1325. (Pubitemid 46809420)
23. Gross S, Tilly P, Hentsch D, Vonesch JL, Fabre JE. Vascular wallproduced prostaglandin E2 exacerbates arterial thrombosis and atherothrombosis through platelet EP3 receptors. J Exp Med. 2007;204: 311-320. (Pubitemid 46294547)
24. Wang M, Zukas AM, Hui Y, Ricciotti E, Pure E, FitzGerald GA. Deletion of microsomal prostaglandin E synthase-1 augments prostacyclin and retards atherogenesis. Proc Natl Acad Sci USA. 2006;103:14507-14512. (Pubitemid 44484780)
25. Samuelsson B, Morgenstern R, Jakobsson PJ. Membrane prostaglandin E synthase-1: a novel therapeutic target. Pharmacol Rev. 2007;59:207-224. (Pubitemid 47481434)
26. Schieffer B, Selle T, Hilfiker A, Hilfiker-Kleiner D, Grote K, Tietge UJ, Trautwein C, Luchtefeld M, Schmittkamp C, Heeneman S, Daemen MJ, Drexler H. Impact of interleukin-6 on plaque development and morphology in experimental atherosclerosis. Circulation. 2004;110: 3493-3500. (Pubitemid 39602229)
27. Luchtefeld M, Schunkert H, Stoll M, Selle T, Lorier R, Grote K, Sagebiel C, Jagavelu K, Tietge UJ, Assmus U, Streetz K, Hengstenberg C, Fischer M, Mayer B, Maresso K, El Mokhtari NE, Schreiber S, Muller W, Bavendiek U, Grothusen C, Drexler H, Trautwein C, Broeckel U, Schieffer B. Signal transducer of inflammation gp130 modulates atherosclerosis in mice and man. J Exp Med. 2007;204:1935-1944. (Pubitemid 47236328)
28. Kumar S, Boehm J, Lee JC. p38 MAP kinases: key signalling molecules as therapeutic targets for inflammatory diseases. Nat Rev Drug Discov. 2003;2:717-726. (Pubitemid 37361787)
29. Jing Q, Xin SM, Cheng ZJ, Zhang WB, Zhang R, Qin YW, Pei G. Activation of p38 mitogen-activated protein kinase by oxidized LDL in vascular smooth muscle cells: mediation via pertussis toxin-sensitive G proteins and association with oxidized LDL-induced cytotoxicity. Circ Res. 1999;84:831-839. (Pubitemid 29181490)
30. Kusuhara M, Chait A, Cader A, Berk BC. Oxidized LDL stimulates mitogen-activated protein kinases in smooth muscle cells and macrophages. Arterioscler Thromb Vasc Biol. 1997;17:141-148. (Pubitemid 27057336)
31. Fredrikson GN, Andersson L, Soderberg I, Dimayuga P, Chyu KY, Shah PK, Nilsson J. Atheroprotective immunization with MDA-modified apo B-100 peptide sequences is associated with activation of Th2 specific antibody expression. Autoimmunity. 2005;38:171-179. (Pubitemid 40872742)
32. Fredrikson GN, Bjorkbacka H, Soderberg I, Ljungcrantz I, Nilsson J. Treatment with apo B peptide vaccines inhibits atherosclerosis in human apo B-100 transgenic mice without inducing an increase in peptidespecific antibodies. J Intern Med. 2008;264:563-570.
33. Fredrikson GN, Soderberg I, Lindholm M, Dimayuga P, Chyu KY, Shah PK, Nilsson J. Inhibition of atherosclerosis in apoE-null mice by immunization with apoB-100 peptide sequences. Arterioscler Thromb Vasc Biol. 2003;23:879-884. (Pubitemid 36566181)
34. Segrest JP, Jones MK, De Loof H, Dashti N. Structure of apolipoprotein B-100 in low density lipoproteins. J Lipid Res. 2001;42:1346-1367. (Pubitemid 34007665)
35. Forgez P, Gregory H, Young JA, Knott T, Scott J, Chapman MJ. Identification of surface-exposed segments of apolipoprotein B-100 in the LDL particle. Biochem Biophys Res Commun. 1986;140:250-257. (Pubitemid 17190020)
36. Hakala JK, Oksjoki R, Laine P, Du H, Grabowski GA, Kovanen PT, Pentikainen MO. Lysosomal enzymes are released from cultured human macrophages, hydrolyze LDL in vitro, and are present extracellularly in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2003;23: 1430-1436. (Pubitemid 37006376)
37. Oorni K, Sneck M, Bromme D, Pentikainen MO, Lindstedt KA, Mayranpaa M, Aitio H, Kovanen PT. Cysteine protease cathepsin F is expressed in human atherosclerotic lesions, is secreted by cultured macrophages, and modifies low density lipoprotein particles in vitro. J Biol Chem. 2004;279:34776-34784. (Pubitemid 39318110)
38. Jaffer FA, Kim DE, Quinti L, Tung CH, Aikawa E, Pande AN, Kohler RH, Shi GP, Libby P, Weissleder R. Optical visualization of cathepsin K activity in atherosclerosis with a novel, protease-activatable fluorescence sensor. Circulation. 2007;115:2292-2298. (Pubitemid 46685897)
39. Pepin JM, O'Neil JA, Hoff HF. Quantification of apo[a] and apoB in human atherosclerotic lesions. J Lipid Res. 1991;32: 317-327.
40. Kruth HS, Shekhonin B. Evidence for loss of apo B from LDL in human atherosclerotic lesions: extracellular cholesteryl ester lipid particles lacking apo B. Atherosclerosis. 1994;105:227-234. (Pubitemid 24086513)
41. Matzinger P. The danger model: a renewed sense of self. Science. 2002; 296:301-305. (Pubitemid 34303674)