Trends in Cardiovascular Medicine
Volume 17, Issue 2 , Pages 69-75 , February 2007

Selective Depletion of Macrophages in Atherosclerotic Plaques via Macrophage-Specific Initiation of Cell Death

  • Wim Martinet

      Affiliations

    • Division of Pharmacology, University of Antwerp, B-2610 Wilrijk, Belgium
    • Corresponding Author InformationAddress correspondence to: Dr. Wim Martinet, Division of Pharmacology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium. Tel.: (+32) 3-820-27-10; fax: (+32) 3-820-25-67.
  • ,
  • Stefan Verheye

      Affiliations

    • Antwerp Cardiovascular Institute Middelheim, B-2020 Antwerp, Belgium
  • ,
  • Guido R.Y. De Meyer

      Affiliations

    • Division of Pharmacology, University of Antwerp, B-2610 Wilrijk, Belgium

References 

  1. Abeliovich H. Regulation of autophagy by the target of rapamycin (Tor) proteins. In:  Klionsky DJ editors. Autophagy. Georgetown: Landes Bioscience; 2004;p. 60–69
  2. Aikawa M, Rabkin E, Okada Y, et al. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation. 1998;97:2433–2444
  3. Aikawa M, Sugiyama S, Hill CC. Lipid lowering reduces oxidative stress and endothelial cell activation in rabbit atheroma. Circulation. 2002;106:1390–1396
  4. Bjornheden T, Bondjers G. Oxygen consumption in aortic tissue from rabbits with diet-induced atherosclerosis. Arteriosclerosis. 1987;7:238–247
  5. Buiting AM, Van Rooijen N. Liposome mediated depletion of macrophages: an approach for fundamental studies. J Drug Target. 1994;2:357–362
  6. Clarke PGH. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol. 1990;181:195–213
  7. Croons V, Martinet W, Herman AG, et al. Selective clearance of macrophages in atherosclerotic plaques by the protein synthesis inhibitor cycloheximide. J Pharmacol Exp Ther. 2007;(in press)
  8. Danenberg HD, Fishbein I, Gao J, et al. Macrophage depletion by clodronate-containing liposomes reduces neointimal formation after balloon injury in rats and rabbits. Circulation. 2002;106:599–605
  9. De Meyer GRY, Kockx MM, Knaapen MWM, et al. Nitric oxide donor molsidomine favors features of atherosclerotic plaque stability during cholesterol lowering in rabbits. J Cardiovasc Pharmacol. 2003;41:970–978
  10. Demidova TN, Hamblin MR. Macrophage-targeted photodynamic therapy. Int J Immunopathol Pharmacol. 2004;17:117–126
  11. Duffield JS, Forbes SJ, Constandinou CM, et al. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest. 2005;115:56–65
  12. Festjens N, Vanden Berghe T, Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signaling cascades, important mediators and concomitant immune response. Biochim Biophys Acta. 2006;1757:1371–1387
  13. Gerrity RG. The role of the monocyte in atherogenesis: II. Migration of foam cells from atherosclerotic lesions. Am J Pathol. 1981;103:191–200
  14. Gotoh T, Mori M. Nitric oxide and endoplasmic reticulum stress. Arterioscler Thromb Vasc Biol. 2006;26:1439–1446
  15. Hansson GK. Inflammation, atherosclerosis and coronary artery disease. N Engl J Med. 2005;352:1685–1695
  16. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407:770–776
  17. Herman AG, Moncada S. Therapeutic potential of nitric oxide donors in the prevention and treatment of atherosclerosis. Eur Heart J. 2005;26:1945–1955
  18. Ho M-K, Springer TA. Preparation and use of monoclonal antimacrophage antibodies. Methods Enzymol. 1984;108:313–324
  19. Ishizaka S, Kuriyama S, Tsujii T. In vivo depletion of macrophages by desulfated iota-carrageenan in mice. J Immunol Methods. 1989;124:17–24
  20. Kagan E, Hartmann D-P. Elimination of macrophages with silica and asbestos. Methods Enzymol. 1984;108:325–335
  21. Kockx MM, De Meyer GRY, Buyssens N, et al. Cell composition, replication, and apoptosis in atherosclerotic plaques after 6 months of cholesterol withdrawal. Circ Res. 1998;83:378–387
  22. Kubota Y, Iwasaki Y, Harada H, et al. Depletion of alveolar macrophages by treatment with 2-chloroadenosine aerosol. Clin Diagn Lab Immunol. 1999;6:452–456
  23. Libby P, Aikawa M. Mechanisms of plaque stabilization with statins. Am J Cardiol. 2003;91:4B–8B
  24. Luoma JS, Stralin P, Marklund SL, et al. Expression of extracellular SOD and iNOS in macrophages and smooth muscle cells in human and rabbit atherosclerotic lesions. Colocalization with epitopes characteristic of oxidized LDL and peroxynitrite-modified proteins. Arterioscler Thromb Vasc Biol. 1998;18:157–167
  25. Martin KA, Rzucidlo EM, Merenick BL, et al. The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation. Am J Physiol Cell Physiol. 2004;286:C507–C517
  26. Martinet W, Kockx MM. Apoptosis in atherosclerosis: focus on oxidized lipids and inflammation. Curr Opin Lipidol. 2001;12:535–541
  27. Martinet W, De Meyer GRY, Timmermans J-P, et al. Macrophages but not smooth muscle cells undergo benzyloxycarbonyl-Val-Ala-DL-Asp(O-methyl)-fluoromethylketone-induced nonapoptotic cell death depending on receptor-interacting protein 1 expression: implications for the stabilization of macrophage-rich atherosclerotic plaques. J Pharmacol Exp Ther. 2006;317:1356–1364
  28. Mohr S, McCormick TS, Lapetina EG. Macrophages resistant to endogenously generated nitric oxide-mediated apoptosis are hypersensitive to exogenously added nitric oxide donors: dichotomous apoptotic response independent of caspase 3 and reversal by the mitogen-activated protein kinase (MEK) inhibitor PD 098059. Proc Natl Acad Sci U S A. 1998;95:5045–5050
  29. Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev. 2005;85:1–31
  30. Ross R. Atherosclerosis—an inflammatory disease. N Engl J Med. 1999;340:115–126
  31. Schrijvers DM, De Meyer GRY, Kockx MM, et al. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25:1256–1261
  32. Stoneman V, Braganza D, Figg N, et al. Selective macrophage apoptosis using CD11b diphtheria toxin receptor transgenic mice demonstrates a differential effect on atherogenesis and established plaques. J Vasc Res. 2005;42(Suppl. 2):160
  33. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol. 2005;25:2255–2264
  34. Vamvakopoulos JE, Green C. HMG-CoA reductase inhibition aborts functional differentiation and triggers apoptosis in cultured primary human monocytes: a potential mechanism of statin-mediated vasculoprotection. BMC Cardiovasc Dis. 2003;Retrieved from http://www.biomedcentral.com/1471-2261/3/6
  35. Van der Wal AC, Becker AE, Van der Loos CM, Das PK. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation. 1994;89:36–44
  36. Van Roon JAG, Bijlsma JWJ, Van de Winkel JGJ, Lafeber FPJG. Depletion of synovial macrophages in rheumatoid arthritis by an anti-FcγRI-calicheamicin immunoconjugate. Ann Rheum Dis. 2005;64:865–870
  37. Van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods. 1994;174:83–93
  38. Van Rooijen N, Sanders A, Van den Berg TK. Apoptosis of macrophages induced by liposome-mediated intracellular delivery of clodronate and propamidine. J Immunol Methods. 1996;193:93–99
  39. Verheye S, Martinet W, Kockx MM, et al. Selective clearance of macrophages in atherosclerotic plaques by autophagy. J Am Coll Cardiol. 2007;(in press)
  40. Wang Y, Mahajan D, Tay Y-C, et al. Partial depletion of macrophages by ED7 reduces renal injury in adriamycin nephropathy. Nephrology. 2005;10:470–477
  41. Wong DM, Varesio L. Depletion of macrophages from heterogeneous cell populations by the use of carbonyl iron. Methods Enzymol. 1984;108:307–313
  42. Yoshimori T. Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Comm. 2004;313:453–458

PII: S1050-1738(07)00005-9

doi: 10.1016/j.tcm.2006.12.004

Trends in Cardiovascular Medicine
Volume 17, Issue 2 , Pages 69-75 , February 2007