Atherosclerosis
Volume 197, Issue 2 , Pages 487-495 , April 2008

CXCL16/SR-PSOX—A friend or a foe in atherosclerosis?

  • Yuri Sheikine

      Affiliations

    • Noninvasive Cardiovascular Imaging Program, Division of Nuclear Medicine/PET, Departments of Medicine and Radiology, Brigham and Women's Hospital, Harvard Medical School, 75 Francis Street L1, Boston, MA 02115 USA
    • Alternative spelling of this author's name is Yury Sheykin.
    • Corresponding Author InformationCorresponding author.
  • ,
  • Allan Sirsjö

      Affiliations

    • Department of Clinical Medicine, Örebro University, Örebro, Sweden

Received 2 June 2007 ,Revised 15 November 2007 ,Accepted 18 November 2007.

References 

  1. Sheikine YA, Hansson GK. Chemokines as potential therapeutic targets in atherosclerosis. Curr Drug Targets. 2006;7:13–27
  2. Barlic J, Murphy PM. Chemokine regulation of atherosclerosis. J Leukoc Biol. 2007;82:226–236
  3. Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA. 1979;76:333–337
  4. van Berkel TJ, Out R, Hoekstra M, et al. Scavenger receptors: friend or foe in atherosclerosis?. Curr Opin Lipidol. 2005;16:525–535
  5. Moore KJ, Freeman MW. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol. 2006;26:1702–1711
  6. Shimaoka T, Kume N, Minami M, et al. Molecular cloning of a novel scavenger receptor for oxidized low density lipoprotein, SR-PSOX, on macrophages. J Biol Chem. 2000;275:40663–40666
  7. 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
  8. Wilbanks A, Zondlo SC, Murphy K, et al. Expression cloning of the STRL33/BONZO/TYMSTR ligand reveals elements of CC, CXC, and CX3C chemokines. J Immunol. 2001;166:5145–5154
  9. Shimaoka T, Nakayama T, Kume N, et al. Cutting edge: SR-PSOX/CXC chemokine ligand 16 mediates bacterial phagocytosis by APCs through its chemokine domain. J Immunol. 2003;171:1647–1651
  10. Shimaoka T, Nakayama T, Fukumoto N, et al. 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
  11. Abel S, Hundhausen C, Mentlein R, et al. The transmembrane CXC-chemokine ligand 16 is induced by IFN-gamma and TNF-alpha and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J Immunol. 2004;172:6362–6372
  12. Gough PJ, Garton KJ, Wille PT, et al. 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
  13. Schulte A, Schulz B, Andrzejewski MG, et al. Sequential processing of the transmembrane chemokines CX3CL1 and CXCL16 by alpha- and gamma-secretases. Biochem Biophys Res Commun. 2007;358:233–240
  14. Hundhausen C, Schulte A, Schulz B, et al. Regulated shedding of transmembrane chemokines by the disintegrin and metalloproteinase 10 facilitates detachment of adherent leukocytes. J Immunol. 2007;178:8064–8072
  15. Ludwig A, Hundhausen C, Lambert MH, et al. Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb Chem High Throughput Screen. 2005;8:161–171
  16. Ludwig A, Weber C. Transmembrane chemokines: versatile ‘special agents’ in vascular inflammation. Thromb Haemost. 2007;97:694–703
  17. Minami M, Kume N, Shimaoka T, et al. 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
  18. Tabata S, Kadowaki N, Kitawaki T, et al. Distribution and kinetics of SR-PSOX/CXCL16 and CXCR6 expression on human dendritic cell subsets and CD4+ T cells. J Leukoc Biol. 2005;77:777–786
  19. 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
  20. Wagsater D, Olofsson PS, Norgren L, Stenberg B, Sirsjo A. The chemokine and scavenger receptor CXCL16/SR-PSOX is expressed in human vascular smooth muscle cells and is induced by interferon-gamma. Biochem Biophys Res Commun. 2004;325:1187–1193
  21. Shashkin P, Simpson D, Mishin V, Chesnutt B, Ley K. Expression of CXCL16 in human T cells. Arterioscler Thromb Vasc Biol. 2003;23:148–149
  22. Sharron M, Pohlmann S, Price K, et al. Expression and coreceptor activity of STRL33/Bonzo on primary peripheral blood lymphocytes. Blood. 2000;96:41–49
  23. Kim CH, Kunkel EJ, Boisvert J, et al. Bonzo/CXCR6 expression defines type 1-polarized T-cell subsets with extralymphoid tissue homing potential. J Clin Invest. 2001;107:595–601
  24. Sato T, Thorlacius H, Johnston B, et al. Role for CXCR6 in recruitment of activated CD8+ lymphocytes to inflamed liver. J Immunol. 2005;174:277–283
  25. Chandrasekar B, Bysani S, Mummidi S. CXCL16 signals via Gi, phosphatidylinositol 3-kinase, Akt, I kappa B kinase, and nuclear factor-kappa B and induces cell–cell adhesion and aortic smooth muscle cell proliferation. J Biol Chem. 2004;279:3188–3196
  26. Ignatius R, Wei Y, Beaulieu S, et al. The immunodeficiency virus coreceptor, Bonzo/STRL33/TYMSTR, is expressed by macaque and human skin- and blood-derived dendritic cells. AIDS Res Hum Retroviruses. 2000;16:1055–1059
  27. Nakayama T, Hieshima K, Izawa D, et al. Cutting edge: profile of chemokine receptor expression on human plasma cells accounts for their efficient recruitment to target tissues. J Immunol. 2003;170:1136–1140
  28. Galkina E, Harry BL, Ludwig A, et al. CXCR6 promotes atherosclerosis by supporting T-cell homing, interferon-gamma production, and macrophage accumulation in the aortic wall. Circulation. 2007;116:1801–1811
  29. Kim CH, Johnston B, Butcher EC. Trafficking machinery of NKT cells: shared and differential chemokine receptor expression among V alpha 24(+)V beta 11(+) NKT cell subsets with distinct cytokine-producing capacity. Blood. 2002;100:11–16
  30. Motsinger A, Haas DW, Stanic AK, et al. CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J Exp Med. 2002;195:869–879
  31. Thomas SY, Hou R, Boyson JE, et al. CD1d-restricted NKT cells express a chemokine receptor profile indicative of Th1-type inflammatory homing cells. J Immunol. 2003;171:2571–2580
  32. Johnston B, Kim CH, Soler D, Emoto M, Butcher EC. Differential chemokine responses and homing patterns of murine TCRalphabeta NKT cell subsets. J Immunol. 2003;171:2960–2969
  33. Hara T, Katakai T, Lee JH, et al. A transmembrane chemokine, CXC chemokine ligand 16, expressed by lymph node fibroblastic reticular cells has the potential to regulate T cell migration and adhesion. Int Immunol. 2006;18:301–311
  34. Hase K, Murakami T, Takatsu H, et al. The membrane-bound chemokine CXCL16 expressed on follicle-associated epithelium and M cells mediates lympho-epithelial interaction in GALT. J Immunol. 2006;176:43–51
  35. van der Voort R, van Lieshout AW, Toonen LW, et al. Elevated CXCL16 expression by synovial macrophages recruits memory T cells into rheumatoid joints. Arthritis Rheum. 2005;52:1381–1391
  36. Boisvert J, Kunkel EJ, Campbell JJ, et al. Liver-infiltrating lymphocytes in end-stage hepatitis C virus: subsets, activation status, and chemokine receptor phenotypes. J Hepatol. 2003;38:67–75
  37. Heydtmann M, Lalor PF, Eksteen JA, Hubscher SG, Briskin M, Adams DH. CXC chemokine ligand 16 promotes integrin-mediated adhesion of liver-infiltrating lymphocytes to cholangiocytes and hepatocytes within the inflamed human liver. J Immunol. 2005;174:1055–1062
  38. Wuttge DM, Zhou X, Sheikine Y, et al. CXCL16/SR-PSOX is an interferon-gamma-regulated chemokine and scavenger receptor expressed in atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2004;24:750–755
  39. Aslanian AM, Charo IF. Targeted disruption of the scavenger receptor and chemokine CXCL16 accelerates atherosclerosis. Circulation. 2006;114:583–590
  40. Tenger C, Sundborger A, Jawien J, Zhou X. IL-18 accelerates atherosclerosis accompanied by elevation of IFN-gamma and CXCL16 expression independently of T cells. Arterioscler Thromb Vasc Biol. 2005;25:791–796
  41. Okamura H, Tsutsi H, Komatsu T, et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature. 1995;378:88–91
  42. Chandrasekar B, Mummidi S, Valente AJ, et al. The pro-atherogenic cytokine interleukin-18 induces CXCL16 expression in rat aortic smooth muscle cells via MyD88, interleukin-1 receptor-associated kinase, tumor necrosis factor receptor-associated factor 6, c-Src, phosphatidylinositol 3-kinase, Akt, c-Jun N-terminal kinase, and activator protein-1 signaling. J Biol Chem. 2005;280:26263–26277
  43. Gupta S, Pablo AM, Jiang X, et al. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest. 1997;99:2752–2761
  44. Whitman SC, Ravisankar P, Elam H, Daugherty A. Exogenous interferon-gamma enhances atherosclerosis in apolipoprotein E−/− mice. Am J Pathol. 2000;157:1819–1824
  45. Moore KJ, Kunjathoor VV, Koehn SL, et al. 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
  46. Aitman TJ, Glazier AM, Wallace CA, et al. Identification of Cd36 (Fat) as an insulin-resistance gene causing defective fatty acid and glucose metabolism in hypertensive rats. Nat Genet. 1999;21:76–83
  47. Gotoda T, Iizuka Y, Yamada N. Complex connection between CD36 and atherosclerosis, lipid metabolism, and insulin resistance syndromes. Curr Atheroscler Rep. 2000;2:453–454
  48. Miyaoka K, Kuwasako T, Hirano K, et al. CD36 deficiency associated with insulin resistance. Lancet. 2001;357:686–687
  49. Cybulsky MI, Won D, Haidari M. Leukocyte recruitment to atherosclerotic lesions. Can J Cardiol. 2004;20(Suppl. B):24B–28B
  50. Stoneman VE, Bennett MR. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin Sci (Lond). 2004;107:343–354
  51. Robertson AK, Hansson GK. T cells in atherogenesis: for better or for worse?. Arterioscler Thromb Vasc Biol. 2006;26:2421–2432
  52. Yamauchi R, Tanaka M, Kume N, et al. Upregulation of SR-PSOX/CXCL16 and recruitment of CD8+ T cells in cardiac valves during inflammatory valvular heart disease. Arterioscler Thromb Vasc Biol. 2004;24:282–287
  53. Wetzker R, Rommel C. Phosphoinositide 3-kinases as targets for therapeutic intervention. Curr Pharm Des. 2004;10:1915–1922
  54. Zhuge X, Murayama T, Arai H, et al. CXCL16 is a novel angiogenic factor for human umbilical vein endothelial cells. Biochem Biophys Res Commun. 2005;331:1295–1300
  55. Lundberg GA, Kellin A, Samnegard A, et al. Severity of coronary artery stenosis is associated with a polymorphism in the CXCL16/SR-PSOX gene. J Intern Med. 2005;257:415–422
  56. Sheikine Y, Bang CS, Nilsson L, et al. Decreased plasma CXCL16/SR-PSOX concentration is associated with coronary artery disease. Atherosclerosis. 2006;188:462–466
  57. Mitsuoka H, Kume N, Hayashida K, Tanaka M, Kita T. Serum soluble SR-PSOX/CXCL16 is an independent biomarker for acute coronary syndrome. Atheroscler Suppl. 2006;7:85–86
  58. Lehrke M, Millington SC, Lefterova M, et al. CXCL16 is a marker of inflammation, atherosclerosis, and acute coronary syndromes in humans. J Am Coll Cardiol. 2007;49:442–449
  59. van Lieshout AW, Popa C, Meyer-Wentrup F, et al. Circulating CXCL16 is not related to circulating oxLDL in patients with rheumatoid arthritis. Biochem Biophys Res Commun. 2007;355:392–397
  60. van Lieshout AW, Fransen J, Flendrie M, et al. Circulating levels of the chemokine CCL18, but not CXCL16 are elevated and correlate with disease activity in rheumatoid arthritis. Ann Rheum Dis. 2007;Epub March 9
  61. Shimaoka T, Nakayama T, Hieshima K, et al. Chemokines generally exhibit scavenger receptor activity through their receptor-binding domain. J Biol Chem. 2004;279:26807–26810
  62. Nanki T, Shimaoka T, Hayashida K, et al. Pathogenic role of the CXCL16-CXCR6 pathway in rheumatoid arthritis. Arthritis Rheum. 2005;52:3004–3014

PII: S0021-9150(07)00756-3

doi: 10.1016/j.atherosclerosis.2007.11.034

Atherosclerosis
Volume 197, Issue 2 , Pages 487-495 , April 2008