Targeted disruption of the scavenger receptor and chemokine CXCL16 accelerates atherosclerosis

Circulation

Volumn 114, Issue 6, 2006, Pages 583-590

  Aslanian, Ara M ^a   Charo, Israel F ^a,b  

^a GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atherosclerosis; Chemokines; Leukocytes; Lipids

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCL 16; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LOW DENSITY LIPOPROTEIN RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLSERINE; SCAVENGER RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DNA LIBRARY; FEMALE; FOAM CELL; GENE DISRUPTION; GENE TARGETING; HELPER CELL; LEUKOCYTE ACTIVATION; LIPID BLOOD LEVEL; MACROPHAGE ACTIVATION; MALE; MEMBRANE BINDING; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; AORTA, THORACIC; CHEMOKINE CCL2; CHEMOKINES, CXC; CORONARY ARTERIOSCLEROSIS; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; LIPOPROTEINS, LDL; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; RECEPTORS, CHEMOKINE; RECEPTORS, LDL; RECEPTORS, SCAVENGER; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33746918723     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.105.540583     Document Type: Article

References (44)

1. Parthasarathy S, Steinberg D, Witztum JL. The role of oxidized low-density lipoproteins in the pathogenesis of atherosclerosis. Annu Rev Med. 1992;43:219-225.
2. Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem. 1997;272:20963-20966.
3. Lougheed M, Lum CM, Ling W, Suzuki H, Kodama T, Steinbrecher U. High affinity saturable uptake of oxidized low density lipoprotein by macrophages from mice lacking the scavenger receptor class A type I/II. J Biol Chem. 1997;272:12938-12944.
4. Podrez EA, Febbraio M, Sheibani N, Schmitt D, Silverstein RL, Hajjar DP, Cohen PA, Frazier WA, Hoff HF, Hazen SL. Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J Clin Invest. 2000;105:1095-1108.
5. Febbraio M, Podrez EA, Smith JD, Hajjar DP, Hazen SL, Hoff HF, Sharma K, Silverstein RL. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest. 2000;105:1049-1056.
6. Moriwaki H, Kume N, Sawamura T, Aoyama T, Hoshikawa H, Ochi H, Nishi E, Masaki T, Kita T. Ligand specificity of LOX-1, a novel endothelial receptor for oxidized low density lipoprotein. Arterioscler Thromb Vasc Biol. 1998;18:1541-1547.
7. Ramprasad MP, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotein. Proc Natl Acad Sci U S A. 1996;93:14833-14838.
8. Ramprasad MP, Fischer W, Witztum JL, Sambrano GR, Quehenberger O, Steinberg D. The 94- to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc Natl Acad Sci U S A. 1995;92:9580-9584.
9. Shimaoka T, Kume N, Minami M, Hayashida K, Kataoka H, Kita T, Yonehara S. Molecular cloning of a novel scavenger receptor for oxidized low density lipoprotein, SR-PSOX, on macrophages. J Biol Chem. 2000;275:40663-40666.
10. Wilbanks A, Zondlo SC, Murphy K, Mak S, Soler D, Langdon P, Andrew DP, Wu L, Briskin M. Expression cloning of the STRL33/BONZO/TYMSTR ligand reveals elements of CC, CXC, and CX3C chemokines. J Immunol. 2001;166:5145-5154.
11. Matloubian M, David A, Engel S, Ryan JE, Cyster JG. A transmembrane CXC chemokine is a ligand for HIV-coreceptor Bonzo. Nat Immunol. 2000;1:298-304.
12. Hofnagel O, Luechtenborg B, Plenz G, Robenek H. Expression of the novel scavenger receptor SR-PSOX in cultured aortic smooth muscle cells and umbilical endothelial cells. Arterioscler Thromb Vasc Biol. 2002;22:710-711.
13. Minami M, Kume N, Shimaoka T, Kataoka H, Hayashida K, Akiyama Y, Nagata I, Ando K, Nobuyoshi M, Hanyuu M, Komeda M, Yonehara S, Kita T. Expression of SR-PSOX, a novel cell-surface scavenger receptor for phosphatidylserine and oxidized LDL in human atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2001;21:1796-1800.
14. Wuttge DM, Zhou X, Sheikine Y, Wågsäter D, Stemme V, Hedin U, Stemme S, Hansson GK, Sirsjö A. CXCL16/SR-PSOX is an interferon-γ- regulated chemokine and scavenger receptor expressed in atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2004;24:750-755.
15. Shimaoka T, Nakayama T, Fukumoto N, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O, Yonehara S. Cell surface-anchored SR-PSOX/CXC chemokine ligand 16 mediates firm adhesion of CXC chemokine receptor 6-expressing cells. J Leukoc Biol. 2004;75:267-274.
16. Shimaoka T, Nakayama T, Kume N, Takahashi S, Yamaguchi J, Minami M, Hayashida K, Kita T, Ohsumi J, Yoshie O, Yonehara S. Cutting edge: SR-PSOX/CXC chemokine ligand 16 mediates bacterial phagocytosis by APCs through its chemokine domain. J Immunol. 2003;171:1647-1651.
17. Gough PJ, Garton KJ, Wille PT, Rychlewski M, Dempsey PJ, Raines EW. A disintegrin and metalloproteinase 10-mediated cleavage and shedding regulates the cell surface expression of CXC chemokine ligand 16. J Immunol. 2004;172:3678-3685.
18. Abel S, Hundhausen C, Mentlein R, Schulte A, Berkhout TA, Broadway N, Hartmann D, Sedlacek R, Dietrich S, Muetze B, Schuster B, Kallen K-J, Saftig P, Rose-John S, Ludwig A. The transmembrane CXC-chemokine ligand 16 is induced by IFN-γ and TNF-α and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J Immunol. 2004;172:6362-6372.
19. Unutmaz D, Xiang W, Sunshine MJ, Campbell J, Butcher E, Littman DR. The primate lentiviral receptor Bonzo/STRL33 is coordinately regulated with CCR5 and its expression pattern is conserved between human and mouse. J Immunol. 2000;165:3284-3292.
20. Kim CH, Kunkel EJ, Boisvert J, Johnston B, Campbell JJ, Genovese MC, Greenberg HB, Butcher EC. Bonzo/CXCR6 expression defines type 1-polarized T-cell subsets with extralymphoid tissue homing potential. J Clin Invest. 2001;107:595-601.
21. Moore KJ, Kunjathoor VV, Koehn SL, Manning JJ, Tseng AA, Silver JM, McKee M, Freeman MW. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest. 2005;115:2192-2201.
22. 3CR1 reveals a role for fractalkine in cardiac allograft rejection. J Clin Invest. 2001;108:679-688.
23. Meiner VL, Cases S, Myers HM, Sande ER, Bellosta S, Schambelan M, Pitas RE, McGuire J, Herz J, Farese RV Jr. 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;93:14041-14046.
24. -/- mice reveals a role for fractalkine in atherogenesis. J Clin Invest. 2003;111:333-340.
25. Aslanian AM, Chapman HA, Charo IF. Transient role for CD1d-restricted natural killer T cells in the formation of atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2005;25:628-632.
26. Trogan E, Choudhury RP, Dansky HM, Rong JX, Breslow JL, Fisher EA. Laser capture microdissection analysis of gene expression in macrophages from atherosclerotic lesions of apolipoprotein E-deficient mice. Proc Natl Acad Sci U S A. 2002;99:2234-2239.
27. Overbergh L, Giulietti A, Valckx D, Decallonne R, Bouillon R, Mathieu C. The use of real-time reverse transcriptase PCR for the quantification of cytokine gene expression. J Biomol Tech. 2003;14:33-43.
28. Teupser D, Thiery J, Walli AK, Seidel D. Determination of LDL- and scavenger-receptor activity in adherent and non-adherent cultured cells with a new single-step fluorometric assay. Biochim Biophys Acta. 1996;1303:193-198.
29. Harada K, Chen Z, Ishibashi S, Osuga J-I, Yagyu H, Ohashi K, Yahagi N, Shionoiri F, Sun L, Yazaki Y, Yamada N. Apoptotic cell death in atherosclerotic plaques of hyperlipidemic knockout mice. Atherosclerosis. 1997;135:235-239.
30. Mach F, Sauty A, Iarossi AS, Sukhova GK, Neote K, Libby P, Luster AD. Differential expression of three T lymphocyte-activating CXC chemokines by human atheroma-associated cells. J Clin Invest. 1999;104:1041-1050.
31. Takahashi T, Tanaka M, Brannan CI, Jenkins NA, Copeland NG, Suda T, Nagata S. Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell. 1994;76:969-976.
32. Aprahamian T, Rifkin I, Bonegio R, Hugel B, Freyssinet J-M, Sato K, Castellot JJ Jr, Walsh K. Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease. J Exp Med. 2004;199:1121-1131.
33. Braun A, Trigatti BL, Post MJ, Sato K, Simons M, Edelberg JM, Rosenberg RD, Schrenzel M, Krieger M. Loss of SR-B1 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.
34. Trigatti BL, Krieger M, Rigotti A. Influence of the HDL receptor SR-BI on lipoprotein metabolism and atherosclerosis. Arterioscler Thromb Vasc Biol. 2003;23:1732-1738.
35. Kunjathoor VV, Febbraio M, Podrez EA, Moore KJ, Andersson L, Koehn S, Rhee JS, Silverstein R, Hoff HF, Freeman MW. Scavenger receptors class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J Biol Chem. 2002;277:49982-49988.
36. Suzuki H, Kurihara Y, Takeya M, Kamada N, Kataoka M, Jishage K, Ueda O, Sakaguchi H, Higashi T, Suzuki T, Takashima Y, Kawabe Y, Cynshi O, Wada Y, Honda M, Kurihara H, Aburatani H, Doi T, Matsumoto A, Azuma S, Noda T, Toyoda Y, Itakura H, Yazaki Y, Horiuchi S, Takahashi K, Kruijt JK, van Berkel TJC, Steinbrecher UP, Ishibashi S, Maeda N, Gordon S, Kodama T. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature. 1997;386:292-296.
37. Sakaguchi H, Takeya M, Suzuki H, Hakamata H, Kodama T, Horiuchi S, Gordon S, van der Laan LJW, Kraal G, Ishibashi S, Kitamura N, Takahashi K. Role of macrophage scavenger receptors in diet-induced atherosclerosis in mice. Lab Invest. 1998;78:423-434.
38. Febbraio M, Guy E, Silverstein RL. Stem cell transplantation reveals that absence of macrophage CD36 is protective against atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:2333-2338.
39. Witztum JL. You are right too! J Clin Invest. 2005;115:2072-2075.
40. Khoo JC, Miller E, McLoughlin P, Steinberg D. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis. 1988;8:348-358.
41. Kruth HS, Jones NL, Huang W, Zhao B, Ishii I, Chang J, Combs CA, Malide D, Zhang WY. Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein. J Biol Chem. 2005;280:2352-2360.
42. Reddy S, Hama S, Grijalva V, Hassan K, Mottahedeh R, Hough G, Wadleigh DJ, Navab M, Fogelman AM. Mitogen-activated protein kinase phosphatase 1 activity is necessary for oxidized phospholipids to induce monocyte chemotactic activity in human aortic endothelial cells. J Biol Chem. 2001;276:17030-17035.
43. Lundberg GA, Kellin A, Samnegård A, Lundman P, Tornvall P, Dimmeler S, Zeiher AM, Hamsten A, Hansson GK, Eriksson P. Severity of coronary artery stenosis is associated with a polymorphism in the CXCL16/SR-PSOX gene. J Intern Med. 2005;257:415-422.
44. Sheikine Y, Bang CS, Nilsson L, Samnegard A, Hamsten A, Jonasson L, Eriksson P, Sirsjo A. Decreased plasma CXCL16/SR-PSOX concentration is associated with coronary artery disease. Atherosclerosis. Published online before print, December 2005.