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Mediators of Inflammation
Volume 2014 (2014), Article ID 353614, 9 pages
http://dx.doi.org/10.1155/2014/353614
Research Article

Inhibiting C-Reactive Protein for the Treatment of Cardiovascular Disease: Promising Evidence from Rodent Models

1Division of Clinical Immunology and Rheumatology, Department of Medicine, The University of Alabama at Birmingham, 1825 University Boulevard, SHEL 214, Birmingham, Al 35294-2182, USA
2Division of Cardiovascular Disease, The University of Alabama at Birmingham, Birmingham, AL 35294-0006, USA
3Charles River Laboratories, Sparks, NV 89431, USA
4Isis Pharmaceuticals, 2855 Gazelle Court, Carlsbad, CA 92008, USA

Received 15 January 2014; Accepted 28 February 2014; Published 2 April 2014

Academic Editor: Jan Torzewski

Copyright © 2014 Alexander J. Szalai 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. E. T. H. Yeh, “A new perspective on the biology of C-reactive protein,” Circulation Research, vol. 97, no. 7, pp. 609–611, 2005. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Verma, P. E. Szmitko, and P. M. Ridker, “C-reactive protein comes of age,” Nature Clinical Practice Cardiovascular Medicine, vol. 2, no. 1, pp. 29–36, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Black, I. Kushner, and D. Samols, “C-reactive protein,” Journal of Biological Chemistry, vol. 279, no. 47, pp. 48487–48490, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. T. W. Du Clos, “Pentraxins: structure, function, and role in inflammation,” ISRN Inflammation, vol. 2013, Article ID 379040, 22 pages, 2013. View at Publisher · View at Google Scholar
  5. I. Kushner, S.-L. Jiang, D. Zhang, G. Lozanski, and D. Samols, “Do post-transcriptional mechanisms participate in induction of C-reactive protein and serum amyloid A by IL-6 and IL-1?” Annals of the New York Academy of Sciences, vol. 762, pp. 102–107, 1995. View at Google Scholar · View at Scopus
  6. I. Kushner, D. Rzewnicki, and D. Samols, “What does minor elevation of C-reactive protein signify?” American Journal of Medicine, vol. 119, no. 2, pp. 166.e17–166.e28, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. A. D. Pradhan, J. E. Manson, N. Rifai, J. E. Buring, and P. M. Ridker, “C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus,” Journal of the American Medical Association, vol. 286, no. 3, pp. 327–334, 2001. View at Google Scholar · View at Scopus
  8. D. E. Laaksonen, L. Niskanen, K. Nyyssönen et al., “C-reactive protein and the development of the metabolic syndrome and diabetes in middle-aged men,” Diabetologia, vol. 47, no. 8, pp. 1402–1410, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. S. M. Haffner, “The metabolic syndrome: inflammation, diabetes mellitus, and cardiovascular disease,” American Journal of Cardiology, vol. 97, no. 2, pp. 3A–11A, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. F. G. Hage and A. J. Szalai, “C-reactive protein gene polymorphisms, C-reactive protein nlood levels, and cardiovascular disease risk,” Journal of the American College of Cardiology, vol. 50, no. 12, pp. 1115–1122, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. S. E. Nissen, E. M. Tuzcu, P. Schoenhagen et al., “Statin therapy, LDL cholesterol, C-reactive protein, and coronary artery disease,” The New England Journal of Medicine, vol. 352, no. 1, pp. 29–38, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. P. M. Ridker, C. P. Cannon, D. Morrow et al., “C-reactive protein levels and outcomes after statin therapy,” The New England Journal of Medicine, vol. 352, no. 1, pp. 20–28, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. P. M. Ridker, E. Danielson, F. A. H. Fonseca et al., “Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein,” The New England Journal of Medicine, vol. 359, no. 21, pp. 2195–2207, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Puri, S. E. Nissen, P. Libby et al., “C-reactive protein, but not low-density lipoprotein cholesterol levels, associate with coronary atheroma regression and cardiovascular events after maximally intensive statin therapy,” Circulation, vol. 128, no. 22, pp. 2395–2403, 2013. View at Publisher · View at Google Scholar
  15. S. Verma, S. Devaraj, and I. Jialal, “C-reactive protein promotes atherothrombosis,” Circulation, vol. 113, no. 17, pp. 2135–2150, 2006. View at Google Scholar · View at Scopus
  16. G. J. Wolbink, M. C. Brouwer, S. Buysmann, I. J. M. T. Berge, and C. E. Hack, “CRP-mediated activation of complement in vivo: assessment by measuring circulating complement-C-reactive protein complexes,” Journal of Immunology, vol. 157, no. 1, pp. 473–479, 1996. View at Google Scholar · View at Scopus
  17. H. Sun, T. Koike, T. Ichikawa et al., “C-reactive protein in atherosclerotic lesions: its origin and pathophysiological significance,” American Journal of Pathology, vol. 167, no. 4, pp. 1139–1148, 2005. View at Google Scholar · View at Scopus
  18. J. Torzewski, M. Torzewski, D. E. Bowyer et al., “C-reactive protein frequently colocalizes with the terminal complement complex in the intima of early atherosclerotic lesions of human coronary arteries,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 18, no. 9, pp. 1386–1392, 1998. View at Google Scholar · View at Scopus
  19. M. Meuwissen, A. C. van der Wal, H. W. M. Niessen et al., “Colocalisation of intraplaque C reactive protein, complement, oxidised low density lipoprotein, and macrophages in stable and unstable angina and acute myocardial infarction,” Journal of Clinical Pathology, vol. 59, no. 2, pp. 196–201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. S.-R. Ji, Y. Wu, L. A. Potempa, Y.-H. Liang, and J. Zhao, “Effect of modified C-reactive protein on complement activation: a possible complement regulatory role of modified or monomeric C-reactive protein in atherosclerotic lesions,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, no. 4, pp. 934–941, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Bhakdi, M. Torzewski, M. Klouche, and M. Hemmes, “Complement and atherogenesis: binding of CRP to degraded, nonoxidized LDL enhances complement activation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 19, no. 10, pp. 2348–2354, 1999. View at Google Scholar · View at Scopus
  22. H. D. Danenberg, A. J. Szalai, R. V. Swaminathan et al., “Increased thrombosis after arterial injury in human C-reactive protein-transgenic mice,” Circulation, vol. 108, no. 5, pp. 512–515, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Paul, K. W. S. Ko, L. Li et al., “C-reactive protein accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice,” Circulation, vol. 109, no. 5, pp. 647–655, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Wang, S. Oparil, Y.-F. Chen et al., “Estrogen treatment abrogates neointima formation in human C-reactive protein transgenic mice,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 10, pp. 2094–2099, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Xing, F. G. Hage, Y.-F. Chen et al., “Exaggerated neointima formation in human C-reactive protein transgenic mice is IgG Fc receptor type I (FcγRI)-dependent,” American Journal of Pathology, vol. 172, no. 1, pp. 22–30, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. A. D. Hingorani, T. Shah, and J. P. Casas, “Linking observational and genetic approaches to determine the role of C-reactive protein in heart disease risk,” European Heart Journal, vol. 27, no. 11, pp. 1261–1263, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. M. B. Pepys, G. M. Hirschfield, G. A. Tennent et al., “Targeting C-reactive protein for the treatment of cardiovascular disease,” Nature, vol. 440, no. 7088, pp. 1217–1221, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. S. T. Crooke, “Progress in antisense technology,” Annual Review of Medicine, vol. 55, pp. 61–95, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. A. J. Szalai and M. A. McCrory, “Varied biologic functions of C-reactive protein: lessons learned from transgenic mice,” Immunologic Research, vol. 26, no. 1–3, pp. 279–287, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Murphy, J. Beckers, and U. Ruther, “Regulation of the human C-reactive protein gene in transgenic mice,” Journal of Biological Chemistry, vol. 270, no. 2, pp. 704–708, 1995. View at Publisher · View at Google Scholar · View at Scopus
  31. N. R. Jones, M. A. Pegues, M. A. McCrory et al., “A selective inhibitor of human C-reactive protein translation is efficacious in vitro and in C-reactive protein transgenic mice and humans,” Molecular therapy: Nucleic acids, vol. 1, article e52, 2012. View at Google Scholar
  32. R. M. Crooke, M. J. Graham, K. M. Lemonidis, C. P. Whipple, S. Koo, and R. J. Perera, “An apolipoprotein B antisense oligonucleotide lowers LDL cholesterol in hyperlipidemic mice without causing hepatic steatosis,” Journal of Lipid Research, vol. 46, no. 5, pp. 872–884, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. X. Zhao, W. Zhang, D. Xing et al., “Endothelial cells overexpressing IL-8 receptor reduce cardiac remodeling and dysfunction following myocardial infarction,” American Journal of Physiology: Heart and Circulatory Physiology, vol. 305, no. 4, pp. H590–H598, 2013. View at Publisher · View at Google Scholar
  34. J. V. Castell, T. Andus, D. Kunz, and P. C. Heinrich, “Interleukin-6: the major regulator of acute-phase protein synthesis in man and rat,” Annals of the New York Academy of Sciences, vol. 557, pp. 87–101, 1989. View at Google Scholar · View at Scopus
  35. B. M. Scirica, D. A. Morrow, S. Verma, and I. Jialal, “The verdict is still out,” Circulation, vol. 113, no. 17, pp. 2128–2134, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. H. C. Ablij and A. E. Meinders, “C-reactive protein: history and revival,” European Journal of Internal Medicine, vol. 13, no. 7, pp. 412–422, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. I. Jialal, S. Devaraj, and S. K. Venugopal, “C-reactive protein: risk marker or mediator in atherothrombosis?” Hypertension, vol. 44, no. 1, pp. 6–11, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. S.-O. Olofsson and J. Boren, “Apolipoprotein B: a clinically important apolipoprotein which assembles atherogenic lipoproteins and promotes the development of atherosclerosis,” Journal of Internal Medicine, vol. 258, no. 5, pp. 395–410, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. J. J. P. Kastelein, M. K. Wedel, B. F. Baker et al., “Potent reduction of apolipoprotein B and low-density lipoprotein cholesterol by short-term administration of an antisense inhibitor of apolipoprotein B,” Circulation, vol. 114, no. 16, pp. 1729–1735, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. F. Akdim, E. S. G. Stroes, and J. J. P. Kastelein, “Antisense apolipoprotein B therapy: where do we stand?” Current Opinion in Lipidology, vol. 18, no. 4, pp. 397–400, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. T. J. Kwoh, “An overview of the clinical safety experience of first- and second- generation antisense oligonucleotides,” in Antisense Drug Technology: Principles, Strategies and Applications, S. T. Crooke, Ed., pp. 299–365, CRC Press, Boca Raton, Fla, USA, 2nd edition, 2008. View at Google Scholar
  42. R. S. Geary, R. Z. Yu, A. Siwkowski, and A. A. Levin, “Pharmacokinetic properties of phosphorothioate 2′-O-(2-methoxyethyl)-modified antisense oligonucleotides in animals and man,” in Antisense Drug Technology: Principles, Strategies and Applications, S. T. Crooke, Ed., pp. 305–326, CRC Press, Boca Raton, Fla, USA, 2nd edition, 2008. View at Google Scholar
  43. R. Z. Yu, T.-W. Kim, A. Hong, T. A. Watanabe, H. J. Gaus, and R. S. Geary, “Cross-species pharmacokinetic comparison from mouse to man of a second-generation antisense oligonucleotide, ISIS 301012, targeting human apolipoprotein B-100,” Drug Metabolism and Disposition, vol. 35, no. 3, pp. 460–468, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. M. J. Graham, S. T. Crooke, K. M. Lemonidis, H. J. Gaus, M. V. Templin, and R. M. Crooke, “Hepatic distribution of a phosphorothioate oligodeoxynucleotide within rodents following intravenous administration,” Biochemical Pharmacology, vol. 62, no. 3, pp. 297–306, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. F. G. Hage, S. Oparil, D. Xing, Y.-F. Chen, M. A. McCrory, and A. J. Szalai, “C-reactive protein-mediated vascular injury requires complement,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 6, pp. 1189–1195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. A. M. Wilson, M. C. Ryan, and A. J. Boyle, “The novel role of C-reactive protein in cardiovascular disease: risk marker or pathogen,” International Journal of Cardiology, vol. 106, no. 3, pp. 291–297, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. S. D. de Ferranti and N. Rifai, “C-reactive protein: a nontraditional serum marker of cardiovascular risk,” Cardiovascular Pathology, vol. 16, no. 1, pp. 14–21, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. L. M. Biasucci, “CDC/AHA Workshop on Markers of Inflammation and Cardiovascular Disease: Application to Clinical and Public Health Practice: clinical use of inflammatory markers in patients with cardiovascular diseases: a background paper,” Circulation, vol. 110, no. 25, pp. e560–e567, 2004. View at Google Scholar · View at Scopus