Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 3087469, 11 pages
http://dx.doi.org/10.1155/2016/3087469
Research Article

Caspase-3 Deletion Promotes Necrosis in Atherosclerotic Plaques of ApoE Knockout Mice

1Laboratory of Physiopharmacology, University of Antwerp, 2610 Antwerp, Belgium
2Department of Clinical Chemistry, Antwerp University Hospital, 2610 Antwerp, Belgium

Received 2 June 2016; Revised 23 September 2016; Accepted 29 September 2016

Academic Editor: Chris Kevil

Copyright © 2016 Mandy O. J. Grootaert et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. M. Kockx, “Apoptosis in the atherosclerotic plaque: quantitative and qualitative aspects,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 18, no. 10, pp. 1519–1522, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. Z. Mallat and A. Tedgui, “Current perspective on the role of apoptosis in atherothrombotic disease,” Circulation Research, vol. 88, no. 10, pp. 998–1003, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. V. E. A. Stoneman and M. R. Bennett, “Role of apoptosis in atherosclerosis and its therapeutic implications,” Clinical Science, vol. 107, no. 4, pp. 343–354, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. F. D. Kolodgie, J. Narula, A. P. Burke et al., “Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death,” The American Journal of Pathology, vol. 157, no. 4, pp. 1259–1268, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. Y.-J. Geng and P. Libby, “Progression of atheroma: a struggle between death and procreation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 22, no. 9, pp. 1370–1380, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. D. W. Nicholson and N. A. Thornberry, “Caspases: killer proteases,” Trends in Biochemical Sciences, vol. 22, no. 8, pp. 299–306, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. J. F. Kerr, A. H. Wyllie, and A. R. Currie, “Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics,” British Journal of Cancer, vol. 26, no. 4, pp. 239–257, 1972. View at Publisher · View at Google Scholar · View at Scopus
  8. M. M. Kockx and A. G. Herman, “Apoptosis in atherosclerosis: beneficial or detrimental?” Cardiovascular Research, vol. 45, no. 3, pp. 736–746, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. Z. Mallat and A. Tedgui, “Apoptosis in the vasculature: mechanisms and functional importance,” British Journal of Pharmacology, vol. 130, no. 5, pp. 947–962, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. M. C. H. Clarke, N. Figg, J. J. Maguire et al., “Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis,” Nature Medicine, vol. 12, no. 9, pp. 1075–1080, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Arai, J. M. Shelton, M. Chen et al., “A role for the apoptosis inhibitory factor AIM/Spα/Api6 in atherosclerosis development,” Cell Metabolism, vol. 1, no. 3, pp. 201–213, 2005. View at Publisher · View at Google Scholar
  12. V. Stoneman, D. Braganza, N. Figg et al., “Monocyte/macrophage suppression in CD11b diphtheria toxin receptor transgenic mice differentially affects atherogenesis and established plaques,” Circulation Research, vol. 100, no. 6, pp. 884–893, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. E. L. Gautier, T. Huby, J. L. Witztum et al., “Macrophage apoptosis exerts divergent effects on atherogenesis as a function of lesion stage,” Circulation, vol. 119, no. 13, pp. 1795–1804, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. D. M. Schrijvers, G. R. Y. De Meyer, A. G. Herman, and W. Martinet, “Phagocytosis in atherosclerosis: molecular mechanisms and implications for plaque progression and stability,” Cardiovascular Research, vol. 73, no. 3, pp. 470–480, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Seimon and I. Tabas, “Mechanisms and consequences of macrophage apoptosis in atherosclerosis,” The Journal of Lipid Research, vol. 50, supplement, pp. S382–S387, 2009. View at Google Scholar
  16. E. A. Van Vré, H. Ait-Oufella, A. Tedgui, and Z. Mallat, “Apoptotic cell death and efferocytosis in atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 32, no. 4, pp. 887–893, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. S. A. Schreyer, J. J. Peschon, and R. C. LeBoeuf, “Accelerated atherosclerosis in mice lacking tumor necrosis factor receptor p55,” The Journal of Biological Chemistry, vol. 271, no. 42, pp. 26174–26178, 1996. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Aprahamian, I. Rifkin, R. Bonegio et al., “Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease,” The Journal of Experimental Medicine, vol. 199, no. 8, pp. 1121–1131, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Brånén, L. Hovgaard, M. Nitulescu, E. Bengtsson, J. Nilsson, and S. Jovinge, “Inhibition of tumor necrosis factor-α reduces atherosclerosis in apolipoprotein E knockout mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 11, pp. 2137–2142, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. X. Feng, H. Li, A. A. Rumbin et al., “ApoE−/−Fas−/− C57BL/6 mice: a novel murine model simultaneously exhibits lupus nephritis, atherosclerosis, and osteopenia,” Journal of Lipid Research, vol. 48, no. 4, pp. 794–805, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Liu, D. P. Thewke, Y. R. Su, M. F. Linton, S. Fazio, and M. S. Sinensky, “Reduced macrophage apoptosis is associated with accelerated atherosclerosis in low-density lipoprotein receptor-null mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 1, pp. 174–179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. N. V. Guevara, H.-S. Kim, E. I. Antonova, and L. Chan, “The absence of p53 accelerates atherosclerosis by increasing cell proliferation in vivo,” Nature Medicine, vol. 5, no. 3, pp. 335–339, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. B. J. M. van Vlijmen, G. Gerritsen, A. L. Franken et al., “Macrophage p53 deficiency leads to enhanced atherosclerosis in APOE3-Leiden transgenic mice,” Circulation Research, vol. 88, no. 8, pp. 780–786, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. A. J. Merched, E. Williams, and L. Chan, “Macrophage-specific p53 expression plays a crucial role in atherosclerosis development and plaque remodeling,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 23, no. 9, pp. 1608–1614, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Mercer, N. Figg, V. Stoneman, D. Braganza, and M. R. Bennett, “Endogenous p53 protects vascular smooth muscle cells from apoptosis and reduces atherosclerosis in ApoE knockout mice,” Circulation Research, vol. 96, no. 6, pp. 667–674, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. L. S. M. Boesten, A. S. M. Zadelaar, A. van Nieuwkoop et al., “Macrophage p53 controls macrophage death in atherosclerotic lesions of apolipoprotein E deficient mice,” Atherosclerosis, vol. 207, no. 2, pp. 399–404, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. H. González-Navarro, Y. N. Abu Nabah, Á. Vinué et al., “p19ARF deficiency reduces macrophage and vascular smooth muscle cell apoptosis and aggravates atherosclerosis,” Journal of the American College of Cardiology, vol. 55, no. 20, pp. 2258–2268, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. Z. Mallat, J. Ohan, G. Lesèche, and A. Tedgui, “Colocalization of CPP-32 with apoptotic cells in human atherosclerotic plaques,” Circulation, vol. 96, no. 2, pp. 424–428, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Q. Nhan, W. C. Liles, A. Chait, J. T. Fallon, and S. M. Schwartz, “The p17 cleaved form of caspase-3 is present within viable macrophages in vitro and in atherosclerotic plaque,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 23, no. 7, pp. 1276–1282, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Hutter, C. Valdiviezo, B. V. Sauter et al., “Caspase-3 and tissue factor expression in lipid-rich plaque macrophages: evidence for apoptosis as link between inflammation and atherothrombosis,” Circulation, vol. 109, no. 16, pp. 2001–2008, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. G. K. Owens, A. Loeb, D. Gordon, and M. M. Thompson, “Expression of smooth muscle-specific α-isoactin in cultured vascular smooth muscle cells: relationship between growth and cytodifferentiation,” Journal of Cell Biology, vol. 102, no. 2, pp. 343–352, 1986. View at Publisher · View at Google Scholar · View at Scopus
  32. A. A. T. Geisterfer and M. J. G. K. Peach Owens, “Angiotensin II induces hypertrophy, not hyperplasia, of cultured rat aortic smooth muscle cells,” Circulation Research, vol. 62, no. 4, pp. 749–756, 1988. View at Publisher · View at Google Scholar · View at Scopus
  33. M. O. Grootaert, P. A. da Costa Martins, N. Bitsch et al., “Defective autophagy in vascular smooth muscle cells accelerates senescence and promotes neointima formation and atherogenesis,” Autophagy, vol. 11, no. 11, pp. 2014–2032, 2015. View at Publisher · View at Google Scholar
  34. T. A. Seimon, Y. Wang, S. Han et al., “Macrophage deficiency of p38α MAPK promotes apoptosis and plaque necrosis in advanced atherosclerotic lesions in mice,” Journal of Clinical Investigation, vol. 119, no. 4, pp. 886–898, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Croons, W. Martinet, A. G. Herman, J.-P. Timmermans, and G. R. Y. De Meyer, “Selective clearance of macrophages in atherosclerotic plaques by the protein synthesis inhibitor cycloheximide,” Journal of Pharmacology and Experimental Therapeutics, vol. 320, no. 3, pp. 986–993, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Croons, W. Martinet, A. G. Herman, and G. R. Y. De Meyer, “Differential effect of the protein synthesis inhibitors puromycin and cycloheximide on vascular smooth muscle cell viability,” Journal of Pharmacology and Experimental Therapeutics, vol. 325, no. 3, pp. 824–832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. C. Scheller, J. Knöferle, A. Ullrich et al., “Caspase inhibition in apoptotic T cells triggers necrotic cell death depending on the cell type and the proapoptotic stimulus,” Journal of Cellular Biochemistry, vol. 97, no. 6, pp. 1350–1361, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Lemaire, K. Andréau, V. Souvannavong, and A. Adam, “Inhibition of caspase activity induces a switch from apoptosis to necrosis,” FEBS Letters, vol. 425, no. 2, pp. 266–270, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. O. Meilhac, I. Escargueil-Blanc, J.-C. Thiers, R. Salvayre, and A. Nègre-Salvayre, “Bcl-2 alters the balance between apoptosis and necrosis, but does not prevent cell death induced by oxidized low density lipoproteins,” FASEB Journal, vol. 13, no. 3, pp. 485–494, 1999. View at Google Scholar · View at Scopus
  40. N. Auge, M.-T. Pieraggi, J.-C. Thiers, A. Negre-Salvayre, and R. Salvayre, “Proliferative and cytotoxic effects of mildly oxidized low-density lipoproteins on vascular smooth-muscle cells,” Biochemical Journal, vol. 309, no. 3, pp. 1015–1020, 1995. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Björkerud and S. Björkerud, “Contrary effects of lightly and strongly oxidized LDL with potent promotion of growth versus apoptosis on arterial smooth muscle cells, macrophages, and fibroblasts,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 16, no. 3, pp. 416–424, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. J. A. Dubland and G. A. Francis, “So Much Cholesterol: the unrecognized importance of smooth muscle cells in atherosclerotic foam cell formation,” Current Opinion in Lipidology, vol. 27, no. 2, pp. 155–161, 2016. View at Publisher · View at Google Scholar
  43. N. Vanlangenakker, M. J. M. Bertrand, P. Bogaert, P. Vandenabeele, and T. Vanden Berghe, “TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex i and II members,” Cell Death and Disease, vol. 2, article e230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Yang, D. Ye, and Y. Wang, “Caspase-3 as a therapeutic target for heart failure,” Expert Opinion on Therapeutic Targets, vol. 17, no. 3, pp. 255–263, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. U. Fischer and K. Schulze-Osthoff, “Apoptosis-based therapies and drug targets,” Cell Death and Differentiation, vol. 12, no. 1, pp. 942–961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Yaoita, K. Ogawa, K. Maehara, and Y. Maruyama, “Attenuation of ischemia/reperfusion injury in rats by a caspase inhibitor,” Circulation, vol. 97, no. 3, pp. 276–281, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. T. A. Holly, A. Drincic, Y. Byun et al., “Caspase inhibition reduces myocyte cell death induced by myocardial ischemia and reperfusion in vivo,” Journal of Molecular and Cellular Cardiology, vol. 31, no. 9, pp. 1709–1715, 1999. View at Publisher · View at Google Scholar · View at Scopus
  48. J.-Q. Huang, S. Radinovic, P. Rezaiefar, and S. C. Black, “In vivo myocardial infarct size reduction by a caspase inhibitor administered after the onset of ischemia,” European Journal of Pharmacology, vol. 402, no. 1-2, pp. 139–142, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Condorelli, R. Roncarati, J. Ross Jr. et al., “Heart-targeted overexpression of caspase3 in mice increases infarct size and depresses cardiac function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 17, pp. 9977–9982, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. W. Martinet, D. M. Schrijvers, and G. R. Y. De Meyer, “Necrotic cell death in atherosclerosis,” Basic Research in Cardiology, vol. 106, no. 5, pp. 749–760, 2011. View at Publisher · View at Google Scholar · View at Scopus