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Oxidative Medicine and Cellular Longevity
Volume 2016 (2016), Article ID 2492858, 8 pages
http://dx.doi.org/10.1155/2016/2492858
Research Article

The Impact of Lipoprotein-Associated Oxidative Stress on Cell-Specific Microvesicle Release in Patients with Familial Hypercholesterolemia

1Danish PhD School of Molecular Metabolism, University of Southern Denmark, 5000 Odense, Denmark
2Department of Clinical Biochemistry, Aalborg University Hospital, 9000 Aalborg, Denmark
3Department of Medicine and Cardiology A, Aarhus University Hospital, 8000 Aarhus, Denmark
4Department of Radiology, Aarhus University Hospital, 8000 Aarhus, Denmark
5Department of Cardiology, Aalborg University Hospital, 9000 Aalborg, Denmark
6Department of Endocrinology M, University of Southern Denmark, 5000 Odense, Denmark
7Department of Clinical Medicine, Faculty of Medicine, Aalborg University, 9000 Aalborg, Denmark

Received 5 October 2015; Accepted 31 December 2015

Academic Editor: Domenico D’Arca

Copyright © 2016 M. H. Nielsen 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. D. J. Rader, J. Cohen, and H. H. Hobbs, “Monogenic hypercholesterolemia: new insights in pathogenesis and treatment,” The Journal of Clinical Investigation, vol. 111, no. 12, pp. 1795–1803, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. S. G. Tsouli, D. N. Kiortsis, M. I. Argyropoulou, D. P. Mikhailidis, and M. S. Elisaf, “Pathogenesis, detection and treatment of Achilles tendon xanthomas,” European Journal of Clinical Investigation, vol. 35, no. 4, pp. 236–244, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Civeira, S. Castillo, R. Alonso et al., “Tendon xanthomas in familial hypercholesterolemia are associated with cardiovascular risk independently of the low-density lipoprotein receptor gene mutation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 9, pp. 1960–1965, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. D. N. Kiortsis, M. I. Argyropoulou, V. Xydis, S. G. Tsouli, and M. S. Elisaf, “Correlation of achilles tendon thickness evaluated by ultrasonography with carotid intima-media thickness in patients with familial hypercholesterolemia,” Atherosclerosis, vol. 186, no. 1, pp. 228–229, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. S. G. Tsouli, D. N. Kiortsis, E. S. Lourida et al., “Autoantibody titers against OxLDL are correlated with Achilles tendon thickness in patients with familial hypercholesterolemia,” Journal of Lipid Research, vol. 47, no. 10, pp. 2208–2214, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Hjuler Nielsen, H. Irvine, S. Vedel et al., “Elevated atherosclerosis-related gene expression, monocyte activation and microparticle-release are related to increased lipoprotein-associated oxidative stress in familial hypercholesterolemia,” PLoS ONE, vol. 10, no. 4, Article ID e0121516, 2015. View at Publisher · View at Google Scholar
  7. E. Verhoye and M. R. Langlois, “Circulating oxidized low-density lipoprotein: a biomarker of atherosclerosis and cardiovascular risk?” Clinical Chemistry and Laboratory Medicine, vol. 47, no. 2, pp. 128–137, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Steinberg and J. L. Witztum, “Is the oxidative modification hypothesis relevant to human atherosclerosis? Do the antioxidant trials conducted to date refute the hypothesis?” Circulation, vol. 105, no. 17, pp. 2107–2111, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. M. Park, “CD36, a scavenger receptor implicated in atherosclerosis,” Experimental and Molecular Medicine, vol. 46, no. 6, article e99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. R. L. Silverstein, “Inflammation, atherosclerosis, and arterial thrombosis: role of the scavenger receptor CD36,” Cleveland Clinic Journal of Medicine, vol. 76, no. 2, pp. S27–S30, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Steinberg, “Low density lipoprotein oxidation and its pathobiological significance,” Journal of Biological Chemistry, vol. 272, no. 34, pp. 20963–20966, 1997. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Chen, M. Febbraio, W. Li, and R. L. Silverstein, “A specific cd36-dependent signaling pathway is required for platelet activation by oxidized low-density lipoprotein,” Circulation Research, vol. 102, no. 12, pp. 1512–1519, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Matsumoto, S. Nomura, H. Kamihata, Y. Kimura, and T. Iwasaka, “Increased level of oxidized LDL-dependent monocyte-derived microparticles in acute coronary syndrome,” Thrombosis and Haemostasis, vol. 91, no. 1, pp. 146–154, 2004. View at Google Scholar · View at Scopus
  14. H. Wang, Z.-H. Wang, J. Kong et al., “Oxidized low-density lipoprotein-dependent platelet- derived microvesicles trigger procoagulant effects and amplify oxidative stress,” Molecular Medicine, vol. 18, no. 2, pp. 159–166, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Combes, A.-C. Simon, G.-E. Grau et al., “In vitro generation of endothelial microparticles and possible prothrombotic activity in patients with lupus anticoagulant,” The Journal of Clinical Investigation, vol. 104, no. 1, pp. 93–102, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. M.-L. Liu, M. P. Reilly, P. Casasanto, S. E. McKenzie, and K. J. Williams, “Cholesterol enrichment of human monocyte/macrophages induces surface exposure of phosphatidylserine and the release of biologically-active tissue factor-positive microvesicles,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 2, pp. 430–435, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Théry, M. Ostrowski, and E. Segura, “Membrane vesicles as conveyors of immune responses,” Nature Reviews Immunology, vol. 9, no. 8, pp. 581–593, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. P.-E. Rautou, A.-C. Vion, N. Amabile et al., “Microparticles, vascular function, and atherothrombosis,” Circulation Research, vol. 109, no. 5, pp. 593–606, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. A. S. Leroyer, A. Tedgui, and C. M. Boulanger, “Microparticles and type 2 diabetes,” Diabetes and Metabolism, vol. 34, supplement 1, pp. S27–S32, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. S. Leroyer, A. Tedgui, and C. M. Boulanger, “Role of microparticles in atherothrombosis,” Journal of Internal Medicine, vol. 263, no. 5, pp. 528–537, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. C. M. Boulanger, N. Amabile, and A. Tedgui, “Circulating microparticles: a potential prognostic marker for atherosclerotic vascular disease,” Hypertension, vol. 48, no. 2, pp. 180–186, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. J. VanWijk, E. VanBavel, A. Sturk, and R. Nieuwland, “Microparticles in cardiovascular diseases,” Cardiovascular Research, vol. 59, no. 2, pp. 277–287, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Angelillo-Scherrer, “Leukocyte-derived microparticles in vascular homeostasis,” Circulation Research, vol. 110, no. 2, pp. 356–369, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. C. M. Boulanger, A. Scoazec, T. Ebrahimian et al., “Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction,” Circulation, vol. 104, no. 22, pp. 2649–2652, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. G. N. Chironi, A. Simon, C. M. Boulanger et al., “Circulating microparticles may influence early carotid artery remodeling,” Journal of Hypertension, vol. 28, no. 4, pp. 789–796, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. S. Nomura, M. Suzuki, K. Katsura et al., “Platelet-derived microparticles may influence the development of atherosclerosis in diabetes mellitus,” Atherosclerosis, vol. 116, no. 2, pp. 235–240, 1995. View at Publisher · View at Google Scholar · View at Scopus
  27. W. T. Friedewald, R. I. Levy, and D. S. Fredrickson, “Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge,” Clinical Chemistry, vol. 18, no. 6, pp. 499–502, 1972. View at Google Scholar · View at Scopus
  28. M. H. Nielsen, H. Beck-Nielsen, and M. N. Andersen, “A flow cytometric method for characterization of circulating cell-derived microparticles in plasma,” Journal of Extracellular Vesicles, vol. 3, Article ID 20795, 2014. View at Publisher · View at Google Scholar
  29. J. Shi, C. W. Heegaard, J. T. Rasmussen, and G. E. Gilbert, “Lactadherin binds selectively to membranes containing phosphatidyl-L-serine and increased curvature,” Biochimica et Biophysica Acta—Biomembranes, vol. 1667, no. 1, pp. 82–90, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Shi, Y. Shi, L. N. Waehrens, J. T. Rasmussen, C. W. Heegaard, and G. E. Gilbert, “Lactadherin detects early phosphatidylserine exposure on immortalized leukemia cells undergoing programmed cell death,” Cytometry A, vol. 69, no. 12, pp. 1193–1201, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. R. A. Preston, W. Jy, J. J. Jimenez et al., “Effects of severe hypertension on endothelial and platelet microparticles,” Hypertension, vol. 41, no. 2, pp. 211–217, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. M. E. Tushuizen, M. Diamant, A. Sturk, and R. Nieuwland, “Cell-derived microparticles in the pathogenesis of cardiovascular disease: friend or foe?” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 1, pp. 4–9, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. C. N. França, M. C. Izar, J. B. Amaral, D. M. Tegani, and F. A. Fonseca, “Microparticles as potential biomarkers of cardiovascular disease,” Arquivos Brasileiros de Cardiologia, vol. 104, no. 2, pp. 169–174, 2015. View at Publisher · View at Google Scholar
  34. A. C. Goldberg, P. N. Hopkins, P. P. Toth et al., “Familial hypercholesterolemia: screening, diagnosis and management of pediatric and adult patients: clinical guidance from the National Lipid Association Expert Panel on Familial Hypercholesterolemia,” Journal of Clinical Lipidology, vol. 5, no. 3, pp. 133–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Suades, T. Padró, R. Alonso, P. Mata, and L. Badimon, “Lipid-lowering therapy with statins reduces microparticle shedding from endothelium, platelets and inflammatory cells,” Thrombosis and Haemostasis, vol. 110, no. 2, pp. 366–377, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Suades, T. Padró, R. Alonso, J. López-Miranda, P. Mata, and L. Badimon, “Circulating CD45+/CD3+ lymphocyte-derived microparticles map lipid-rich atherosclerotic plaques in familial hypercholesterolaemia patients,” Thrombosis and Haemostasis, vol. 111, no. 1, pp. 111–121, 2014. View at Publisher · View at Google Scholar
  37. F. Dignat-George and C. M. Boulanger, “The many faces of endothelial microparticles,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 31, no. 1, pp. 27–33, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. E. J. van Beers, M. C. L. Schaap, R. J. Berckmans et al., “Circulating erythrocyte-derived microparticles are associated with coagulation activation in sickle cell disease,” Haematologica, vol. 94, no. 11, pp. 1513–1519, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. R. L. Koshiar, S. Somajo, E. Norström, B. Dahlbäck, and T. Miyata, “Erythrocyte-derived microparticles supporting activated protein c-mediated regulation of blood coagulation,” PLoS ONE, vol. 9, no. 8, Article ID e104200, 2014. View at Publisher · View at Google Scholar
  40. A. S. Shet, O. Aras, K. Gupta et al., “Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes,” Blood, vol. 102, no. 7, pp. 2678–2683, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. É. Biró, K. N. Sturk-Maquelin, G. M. T. Vogel et al., “Human cell-derived microparticles promote thrombus formation in vivo in a tissue factor-dependent manner,” Journal of Thrombosis and Haemostasis, vol. 1, no. 12, pp. 2561–2568, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. A. P. Owens III and N. MacKman, “Microparticles in hemostasis and thrombosis,” Circulation Research, vol. 108, no. 10, pp. 1284–1297, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. J.-G. Wang, J. C. Williams, B. K. Davis et al., “Monocytic microparticles activate endothelial cells in an IL-1β-dependent manner,” Blood, vol. 118, no. 8, pp. 2366–2374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. A. P. Owens III and N. MacKman, “Sources of tissue factor that contribute to thrombosis after rupture of an atherosclerotic plaque,” Thrombosis Research, vol. 129, supplement 2, pp. S30–S33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. A. P. Owens III, F. H. Passam, S. Antoniak et al., “Monocyte tissue factor–dependent activation of coagulation in hypercholesterolemic mice and monkeys is inhibited by simvastatin,” The Journal of Clinical Investigation, vol. 122, no. 2, pp. 558–568, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. M. B. Fessler, K. Rose, Y. Zhang, R. Jaramillo, and D. C. Zeldin, “Relationship between serum cholesterol and indices of erythrocytes and platelets in the US population,” Journal of Lipid Research, vol. 54, no. 11, pp. 3177–3188, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. P. M. Moriarty and C. A. Gibson, “Association between hematological parameters and high-density lipoprotein cholesterol,” Current Opinion in Cardiology, vol. 20, no. 4, pp. 318–323, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Blum, “The possible role of red blood cell microvesicles in atherosclerosis,” European Journal of Internal Medicine, vol. 20, no. 2, pp. 101–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Nomura, A. Shouzu, S. Omoto, M. Nishikawa, T. Iwasaka, and S. Fukuhara, “Activated platelet and oxidized LDL induce endothelial membrane vesiculation: clinical significance of endothelial cell-derived microparticles in patients with type 2 diabetes,” Clinical and Applied Thrombosis/Hemostasis, vol. 10, no. 3, pp. 205–215, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Nagahama, S. Nomura, S. Kanazawa, Y. Ozaki, H. Kagawa, and S. Fukuhara, “Significance of anti-oxidized LDL antibody and monocyte-derived microparticles in anti-phospholipid antibody syndrome,” Autoimmunity, vol. 36, no. 3, pp. 125–131, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Nergiz-Unal, T. Rademakers, J. M. M. Cosemans, and J. W. M. Heemskerk, “Cd36 as a multiple-ligand signaling receptor in atherothrombosis,” Cardiovascular and Hematological Agents in Medicinal Chemistry, vol. 9, no. 1, pp. 42–55, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. R. Nergiz-Unal, M. M. E. Lamers, R. Van Kruchten et al., “Signaling role of CD36 in platelet activation and thrombus formation on immobilized thrombospondin or oxidized low-density lipoprotein,” Journal of Thrombosis and Haemostasis, vol. 9, no. 9, pp. 1835–1846, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Lacroix, S. Robert, P. Poncelet, R. S. Kasthuri, N. S. Key, and F. Dignat-George, “Standardization of platelet-derived microparticle enumeration by flow cytometry with calibrated beads: results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop,” Journal of Thrombosis and Haemostasis, vol. 8, no. 11, pp. 2571–2574, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Lacroix, S. Robert, P. Poncelet, and F. Dignat-George, “Overcoming limitations of microparticle measurement by flow cytometry,” Seminars in Thrombosis and Hemostasis, vol. 36, no. 8, pp. 807–818, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. E. van der Pol, M. J. C. van Gemert, A. Sturk, R. Nieuwland, and T. G. van Leeuwen, “Single vs. swarm detection of microparticles and exosomes by flow cytometry,” Journal of Thrombosis and Haemostasis, vol. 10, no. 5, pp. 919–930, 2012. View at Publisher · View at Google Scholar · View at Scopus