Atherosclerosis
Volume 205, Issue 2 , Pages 369-375 , August 2009

Intracellular labile iron promotes firm adhesion of human monocytes to endothelium under flow and transendothelial migration: Iron and monocyte–endothelial cell interactions

  • Apriliana E.R. Kartikasari

      Affiliations

    • Eijkman-Winkler Centre for Microbiology, Infectious Diseases and Inflammation, Utrecht, The Netherlands
    • ,
  • Frank L.J. Visseren

      Affiliations

    • Department of Vascular Medicine, Utrecht, The Netherlands
    • ,
  • Joannes J.M. Marx

      Affiliations

    • Eijkman-Winkler Centre for Microbiology, Infectious Diseases and Inflammation, Utrecht, The Netherlands
    • ,
  • Sanne van Mullekom

      Affiliations

    • Eijkman-Winkler Centre for Microbiology, Infectious Diseases and Inflammation, Utrecht, The Netherlands
    • ,
  • J. Henny van Kats-Renaud

      Affiliations

    • Eijkman-Winkler Centre for Microbiology, Infectious Diseases and Inflammation, Utrecht, The Netherlands
    • ,
  • B. Sweder van Asbeck

      Affiliations

    • Department of Internal Medicine, University Medical Centre Utrecht, Utrecht, The Netherlands
    • ,
  • Laurien H. Ulfman

      Affiliations

    • Department of Pulmonary Diseases, Utrecht, The Netherlands
    • ,
  • Niki A. Georgiou

      Affiliations

    • Eijkman-Winkler Centre for Microbiology, Infectious Diseases and Inflammation, Utrecht, The Netherlands
    • Corresponding Author InformationCorresponding author. Current address: Danone Research-Centre for Specialised Nutrition, Immunology Platform P.O. Box 7005, 6700CA, Wageningen, The Netherlands. Tel.: +31 317467 885; fax: +31 317466 500.

Received 5 August 2008 ,Revised 15 December 2008 ,Accepted 18 December 2008.

References 

  1. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685–1695
  2. Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–116
  3. Han MK, McLaughlin VV, Criner GJ, Martinez FJ. Pulmonary diseases and the heart. Circulation. 2007;116:2992–3005
  4. Zlokovic BV. The blood–brain barrier in health and chronic neurodegenerative disorders. Neuron. 2008;57:178–201
  5. Liao F, Ali J, Greene T, Muller WA. Soluble domain 1 of platelet–endothelial cell adhesion molecule (PECAM) is sufficient to block transendothelial migration in vitro and in vivo. J Exp Med. 1997;185:1349–1357
  6. Gerszten RE, Garcia-Zepeda EA, Lim YC, et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature. 1999;398:718–723
  7. Shamri R, Grabovsky V, Gauguet JM, et al. Lymphocyte arrest requires instantaneous induction of an extended LFA-1 conformation mediated by endothelium-bound chemokines. Nat Immunol. 2005;6:497–506
  8. Gu L, Okada Y, Clinton SK, et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low-density lipoprotein receptor-deficient mice. Mol Cell. 1998;2:275–281
  9. Boring L, Gosling J, Cleary M, Charo IF. Decreased lesion formation in CCR2−/− mice reveals a role for chemokines in the initiation of atherosclerosis. Nature. 1998;394:894–897
  10. Boisvert WA, Santiago R, Curtiss LK, Terkeltaub RA. A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptor-deficient mice. J Clin Invest. 1998;101:353–363
  11. Kartikasari AE, Georgiou NA, Marx JJ. Iron intake and cardiovascular disease. In:  Arnoldi A editors. Functional foods, cardiovascular disease and diabetes. Boca Raton, FL, USA: Woodhead Publishing Ltd., Abington, Cambridge, UK and CRC Press LLC; 2004;p. 99–125
  12. Araujo JA, Romano EL, Brito BE, et al. Iron overload augments the development of atherosclerotic lesions in rabbits. Arterioscler Thromb Vasc Biol. 1995;15:1172–1180
  13. Lee TS, Shiao MS, Pan CC, Chau LY. Iron-deficient diet reduces atherosclerotic lesions in apoE-deficient mice. Circulation. 1999;99:1222–1229
  14. Matthews AJ, Vercellotti GM, Menchaca HJ, et al. Iron and atherosclerosis: inhibition by the iron chelator deferiprone (L1). J Surg Res. 1997;73:35–40
  15. Minqin R, Rajendran R, Pan N, et al. The iron chelator desferrioxamine inhibits atherosclerotic lesion development and decreases lesion iron concentrations in the cholesterol-fed rabbit. Free Radic Biol Med. 2005;38:1206–1211
  16. Stadler N, Lindner RA, Davies MJ. Direct detection and quantification of transition metal ions in human atherosclerotic plaques: evidence for the presence of elevated levels of iron and copper. Arterioscler Thromb Vasc Biol. 2004;24:949–954
  17. Roest M, van der Schouw YT, de Valk B, et al. Heterozygosity for a hereditary hemochromatosis gene is associated with cardiovascular death in women. Circulation. 1999;100:1268–1273
  18. Kartikasari AE, Georgiou NA, Visseren FL, et al. Endothelial activation and induction of monocyte adhesion by nontransferrin-bound iron present in human sera. FASEB J. 2006;20:353–355
  19. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest. 1973;52:2745–2756
  20. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63
  21. Grootveld M, Bell JD, Halliwell B, Aruoma OI, Bomford A, Sadler PJ. Non-transferrin-bound iron in plasma or serum from patients with idiopathic hemochromatosis. Characterization by high performance liquid chromatography and nuclear magnetic resonance spectroscopy. J Biol Chem. 1989;264:4417–4422
  22. Sakariassen KS, Aarts PA, de Groot PG, Houdijk WP, Sixma JJ. A perfusion chamber developed to investigate platelet interaction in flowing blood with human vessel wall cells, their extracellular matrix, and purified components. J Lab Clin Med. 1983;102:522–535
  23. van Zanten HG, Saelman EU, Schut-Hese KM, et al. Platelet adhesion to collagen type IV under flow conditions. Blood. 1996;88:3862–3871
  24. Kartikasari AE, Georgiou NA, de Geest M, et al. Iron enhances endothelial cell activation in response to Cytomegalovirus or Chlamydia pneumoniae infection. Eur J Clin Invest. 2006;36:743–752
  25. Saccani A, Saccani S, Orlando S, et al. Redox regulation of chemokine receptor expression. Proc Natl Acad Sci USA. 2000;97:2761–2766
  26. Kartikasari AE, Georgiou NA, Visseren FL, et al. Intracellular labile iron modulates adhesion of human monocytes to human endothelial cells. Arterioscler Thromb Vasc Biol. 2004;24:2257–2262
  27. Zhang WJ, Frei B. Intracellular metal ion chelators inhibit TNFalpha-induced SP-1 activation and adhesion molecule expression in human aortic endothelial cells. Free Radic Biol Med. 2003;34:674–682
  28. Weber KS, von Hundelshausen P, Clark-Lewis I, Weber PC, Weber C. Differential immobilization and hierarchical involvement of chemokines in monocyte arrest and transmigration on inflamed endothelium in shear flow. Eur J Immunol. 1999;29:700–712
  29. Ulfman LH, Alblas J, van Aalst CW, Zwaginga JJ, Koenderman L. Differences in potency of CXC chemokine ligand 8-, CC chemokine ligand 11-, and C5a-induced modulation of integrin function on human eosinophils. J Immunol. 2005;175:6092–6099
  30. Le Lan C, Loreal O, Cohen T, et al. Redox active plasma iron in C282Y/C282Y hemochromatosis. Blood. 2005;
  31. Ahmed NK, Hanna M, Wang W. Nontransferrin-bound serum iron in thalassemia and sickle cell patients. Int J Biochem. 1986;18:953–956
  32. Kooistra MP, Kersting S, Gosriwatana I, et al. Nontransferrin-bound iron in the plasma of haemodialysis patients after intravenous iron saccharate infusion. Eur J Clin Invest. 2002;32(Suppl 1):36–41
  33. Kohgo Y, Ikuta K, Ohtake T, Torimoto Y, Kato J. Iron overload and cofactors with special reference to alcohol, hepatitis C virus infection and steatosis/insulin resistance. World J Gastroenterol. 2007;13:4699–4706
  34. Chen XL, Zhang Q, Zhao R, Medford RM. Superoxide, H2O2, and iron are required for TNF-alpha-induced MCP-1 gene expression in endothelial cells: role of Rac1 and NADPH oxidase. Am J Physiol Heart Circ Physiol. 2004;286:H1001–H1007

PII: S0021-9150(08)00909-X

doi: 10.1016/j.atherosclerosis.2008.12.031

Atherosclerosis
Volume 205, Issue 2 , Pages 369-375 , August 2009

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