Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 276457, 17 pages
http://dx.doi.org/10.1155/2014/276457
Research Article

Relationship of MMP-14 and TIMP-3 Expression with Macrophage Activation and Human Atherosclerotic Plaque Vulnerability

1Laboratory of Cardiovascular Pathology, School of Clinical Sciences, Level 7, Bristol Royal Infirmary, Bristol BS2 8HW, UK
2School of Clinical Sciences, University of Bristol, Bristol BS2 8HW, UK
3University Medical Centre, 3584 Utrecht, The Netherlands

Received 31 March 2014; Revised 9 July 2014; Accepted 21 July 2014; Published 24 August 2014

Academic Editor: Beatriz De las Heras

Copyright © 2014 Jason L. Johnson 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. R. Virmani, A. P. Burke, A. Farb, and F. D. Kolodgie, “Pathology of the vulnerable plaque,” Journal of the American College of Cardiology, vol. 47, no. 8, pp. C13–C18, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. A. C. Newby, “Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture,” Physiological Reviews, vol. 85, no. 1, pp. 1–31, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. C. M. Dollery and P. Libby, “Atherosclerosis and proteinase activation,” Cardiovascular Research, vol. 69, no. 3, pp. 625–635, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. A. C. Newby, “Matrix metalloproteinase inhibition therapy for vascular diseases.,” Vascular pharmacology, vol. 56, no. 5-6, pp. 232–244, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Schneider, G. K. Sukhova, M. Aikawa et al., “Matrix metalloproteinase-14 deficiency in bone marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques,” Circulation, vol. 117, no. 7, pp. 931–939, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. V. Casagrande, R. Menghini, S. Menini et al., “Overexpression of tissue inhibitor of metalloproteinase 3 in macrophages reduces atherosclerosis in low-density lipoprotein receptor knockout mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 32, no. 1, pp. 74–81, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. J. L. Johnson, G. B. Sala-Newby, Y. Ismail, C. M. Aguilera, and A. C. Newby, “Low tissue inhibitor of metalloproteinases 3 and high matrix metalloproteinase 14 levels defines a subpopulation of highly invasive foam-cell macrophages,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 9, pp. 1647–1653, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. F. O. Martinez, L. Helming, and S. Gordon, “Alternative activation of macrophages: an immunologic functional perspective,” Annual Review of Immunology, vol. 27, pp. 451–483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Monaco, S. M. Gregan, T. J. Navin, B. M. J. Foxwell, A. H. Davies, and M. Feldmann, “Toll-like receptor-2 mediates inflammation and matrix degradation in human atherosclerosis,” Circulation, vol. 120, no. 24, pp. 2462–2469, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. A. C. Newby, S. J. George, Y. Ismail, J. L. Johnson, G. B. Sala-Newby, and A. C. Thomas, “Vulnerable atherosclerotic plaque metalloproteinases and foam cell phenotypes,” Thrombosis and Haemostasis, vol. 101, no. 6, pp. 1006–1011, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. M. A. Bouhlel, B. Derudas, E. Rigamonti et al., “PPARγ activation primes human monocytes into alternative m2 macrophages with anti-inflammatory properties,” Cell Metabolism, vol. 6, no. 2, pp. 137–143, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Chinetti-Gbaguidi, M. Baron, M. A. Bouhlel et al., “Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARγ and LXRα pathways,” Circulation Research, vol. 108, no. 8, pp. 985–995, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. J. L. Stöger, M. J. J. Gijbels, S. van der Velden et al., “Distribution of macrophage polarization markers in human atherosclerosis,” Atherosclerosis, vol. 225, no. 2, pp. 461–468, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. A. V. Finn, O. Saeed, and R. Virmani, “Macrophage subsets in human atherosclerosis,” Circulation Research, vol. 110, article e64, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Kadl, A. K. Meher, P. R. Sharma et al., “Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2,” Circulation Research, vol. 107, no. 6, pp. 737–746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. J. J. Boyle, H. A. Harrington, E. Piper et al., “Coronary intraplaque hemorrhage evokes a novel atheroprotective macrophage phenotype,” The American Journal of Pathology, vol. 174, no. 3, pp. 1097–1108, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. J. Boyle, M. Johns, T. Kampfer et al., “Activating transcription factor 1 directs Mhem atheroprotective macrophages through coordinated iron handling and foam cell protection,” Circulation Research, vol. 110, no. 1, pp. 20–33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. A. V. Finn, M. Nakano, R. Polavarapu et al., “Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques,” Journal of the American College of Cardiology, vol. 59, no. 2, pp. 166–177, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. B. A. N. Verhoeven, E. Velema, A. H. Schoneveld et al., “Athero-express: differential atherosclerotic plaque expression of mRNA and protein in relation to cardiovascular events and patient characteristics. Rationale and design,” European Journal of Epidemiology, vol. 19, no. 12, pp. 1127–1133, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. J. P. G. Sluijter, W. P. C. Pulskens, A. H. Schoneveld et al., “Matrix metalloproteinase 2 is associated with stable and matrix metalloproteinases 8 and 9 with vulnerable carotid atherosclerotic lesions—a study in human endarterectomy specimen pointing to a role for different extracellular matrix metalloproteinase inducer glycosylation forms,” Stroke, vol. 37, no. 1, pp. 235–239, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. D. P. V. de Kleijn, F. L. Moll, W. E. Hellings et al., “Local atherosclerotic plaques are a source of prognostic biomarkers for adverse cardiovascular events,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 3, pp. 612–619, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. W. E. Hellings, G. Pasterkamp, A. Vollebregt et al., “Intraobserver and interobserver variability and spatial differences in histologic examination of carotid endarterectomy specimens,” Journal of Vascular Surgery, vol. 46, no. 6, pp. 1147–1154, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. V. P. W. Scholtes, J. L. Johnson, N. Jenkins et al., “Carotid atherosclerotic plaque matrix metalloproteinase-12-positive macrophage subpopulation predicts adverse outcome after endarterectomy,” Journal of the American Heart Association, vol. 1, no. 6, Article ID e001040, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Monsalve, A. Ruiz-García, V. Baladrón et al., “Notch1 upregulates LPS-induced macrophage activation by increasing NF-κB activity,” European Journal of Immunology, vol. 39, no. 9, pp. 2556–2570, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. F. O. Martinez, S. Gordon, M. Locati, and A. Mantovani, “Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression,” Journal of Immunology, vol. 177, no. 10, pp. 7303–7311, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. D. Shiffman, T. Mikita, J. T. N. Tai et al., “Large scale gene expression analysis of cholesterol-loaded macrophages,” The Journal of Biological Chemistry, vol. 275, no. 48, pp. 37324–37332, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. S.-C. Sun, P. A. Ganchi, D. W. Ballard, and W. C. Greene, “NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway,” Science, vol. 259, no. 5103, pp. 1912–1915, 1993. View at Publisher · View at Google Scholar · View at Scopus
  29. K. di Gregoli, N. Jenkins, R. Salter, S. White, A. C.. Newby, and J. L. Johnson, “Microrna-24 regulates macrophage behavior and retards atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, 2014. View at Publisher · View at Google Scholar
  30. A. Mantovani, C. Garlanda, and M. Locati, “Macrophage diversity and polarization in atherosclerosis: a question of balance,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 10, pp. 1419–1423, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. C. Thomas, G. B. Sala-Newby, Y. Ismail, J. L. Johnson, G. Pasterkamp, and A. C. Newby, “Genomics of foam cells and nonfoamy macrophages from rabbits identifies arginase-I as a differential regulator of nitric oxide production,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 3, pp. 571–577, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Peeters, W. E. Hellings, D. P. V. de Kleijn et al., “Carotid atherosclerotic plaques stabilize after stroke: insights into the natural process of atherosclerotic plaque stabilization,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 29, no. 1, pp. 128–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Chinetti-Gbaguidi and B. Staels, “Macrophage polarization in metabolic disorders: functions and regulation,” Current Opinion in Lipidology, vol. 22, no. 5, pp. 365–372, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. J. L. Johnson and A. C. Newby, “Macrophage heterogeneity in atherosclerotic plaques,” Current Opinion in Lipidology, vol. 20, no. 5, pp. 370–378, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. W.-C. Huang, G. B. Sala-Newby, A. Susana, J. L. Johnson, and A. C. Newby, “Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-κB,” PLoS ONE, vol. 7, no. 8, Article ID e42507, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Reel, G. B. Sala-Newby, W. Huang, and A. C. Newby, “Diverse patterns of cyclooxygenase-independent metalloproteinase gene regulation in human monocytes,” British Journal of Pharmacology, vol. 163, no. 8, pp. 1679–1690, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Spann Nathanael, X. Garmire Lana, G. McDonald Jeffrey et al., “Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses,” Cell, vol. 151, pp. 138–152, 2012. View at Google Scholar
  38. R. P. Fabunmi, G. K. Sukhova, S. Sugiyama, and P. Libby, “Expression of tissue inhibitor of metalloproteinases-3 in human atheroma and regulation in lesion-associated cells: a potential protective mechanism in plaque stability,” Circulation Research, vol. 83, no. 3, pp. 270–278, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Wick, R. Haronen, D. Mumberg et al., “Structure of the human TIMP-3 gene and its cell cycle-regulated promoter,” Biochemical Journal, vol. 311, no. 2, pp. 549–554, 1995. View at Google Scholar · View at Scopus
  40. G. A. R. Doyle, U. K. Saarialho-Kere, and W. C. Parks, “Distinct mechanisms regulate TIMP-1 expression at different stages of phorbol ester-mediated differentiation of U937 cells,” Biochemistry, vol. 36, no. 9, pp. 2492–2500, 1997. View at Publisher · View at Google Scholar · View at Scopus