Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2013 (2013), Article ID 370212, 9 pages
http://dx.doi.org/10.1155/2013/370212
Research Article

Exacerbation of Glycoprotein VI-Dependent Platelet Responses in a Rhesus Monkey Model of Type 1 Diabetes

1Australian Centre for Blood Diseases, Alfred Medical Research & Education Precinct (AMREP), Monash University, Melbourne, VIC 3004, Australia
2Key Laboratory of Transplant Engineering and Immunology, West China Hospital, Ministry of Health, Sichuan University, Chengdu 610041, China

Received 19 December 2012; Accepted 7 May 2013

Academic Editor: Bernard Portha

Copyright © 2013 J. F. Arthur 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. Daneman, “Type 1 diabetes,” The Lancet, vol. 367, no. 9513, pp. 847–858, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Serebruany, I. Pokov, W. Kuliczkowski, J. Chesebro, and J. Badimon, “Baseline platelet activity and response after clopidogrel in 257 diabetics among 822 patients with coronary artery disease,” Thrombosis and Haemostasis, vol. 100, no. 1, pp. 76–82, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. J. L. Ferreiro, J. A. Gomez-Hospital, and D. J. Angiolillo, “Platelet abnormalities in diabetes mellitus,” Diabetes and Vascular Disease Research, vol. 7, no. 4, pp. 251–259, 2010. View at Publisher · View at Google Scholar
  4. M. E. Carr, “Diabetes mellitus: a hypercoagulable state,” Journal of Diabetes and Its Complications, vol. 15, no. 1, pp. 44–54, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. Antithrombotic Trialists' Collaboration, “Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients,” British Medical Journal, vol. 324, no. 7329, pp. 71–86, 2002. View at Google Scholar · View at Scopus
  6. L. Hansson, A. Zanchetti, S. G. Carruthers et al., “Effects of intensive blood-pressure lowering and low-dose aspirin in patients with hypertension: principal results of the Hypertension Optimal Treatment (HOT) randomised trial. HOT Study Group,” The Lancet, vol. 351, no. 9118, pp. 1755–1762, 1998. View at Publisher · View at Google Scholar
  7. G. Tocci, A. Ferrucci, P. Guida et al., “Impact of diabetes mellitus on the clinical management of global cardiovascular risk: analysis of the results of the Evaluation of Final Feasible Effect of Control Training and Ultra Sensitization (EFFECTUS) educational program,” Clinical Cardiology, vol. 34, no. 9, pp. 560–566, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. F. Arthur, Y. Shen, E. E. Gardiner et al., “TNF receptor-associated factor 4 (TRAF4) is a novel binding partner of glycoprotein Ib and glycoprotein VI in human platelets,” Journal of Thrombosis and Haemostasis, vol. 9, no. 1, pp. 163–172, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. J. F. Arthur, J. Qiao, Y. Shen et al., “ITAM receptor-mediated generation of reactive oxygen species in human platelets occurs via Syk-dependent and Syk-independent pathways,” Journal of Thrombosis and Haemostasis, vol. 10, no. 6, pp. 1133–1141, 2012. View at Publisher · View at Google Scholar
  10. J. L. Qiao, Y. Shen, E. E. Gardiner, and R. K. Andrews, “Proteolysis of platelet receptors in humans and other species,” Biological Chemistry, vol. 391, no. 8, pp. 893–900, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. E. E. Gardiner, D. Karunakaran, Y. Shen, J. F. Arthur, R. K. Andrews, and M. C. Berndt, “Controlled shedding of platelet glycoprotein (GP)VI and GPIb-IX-V by ADAM family metalloproteinases,” Journal of Thrombosis and Haemostasis, vol. 5, no. 7, pp. 1530–1537, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. E. E. Gardiner, J. F. Arthur, M. L. Kahn, M. C. Berndt, and R. K. Andrews, “Regulation of platelet membrane levels of glycoprotein VI by a platelet-derived metalloproteinase,” Blood, vol. 104, no. 12, pp. 3611–3617, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. X. Jin, L. Zeng, S. Rong et al., “Comparison of single high-dose STZ with partial pancreatectomy combined with low-dose STZ for diabetes induction in rhesus monkeys,” Experimental Biology and Medicine, vol. 235, pp. 877–885, 2010. View at Google Scholar
  14. C. F. Qiao, B. L. Tian, G. Mai et al., “Induction of diabetes in rhesus monkeys and establishment of insulin administration strategy,” Transplantation Proceedings, vol. 41, no. 1, pp. 413–417, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Bakdash and M. S. Williams, “Spatially distinct production of reactive oxygen species regulates platelet activation,” Free Radical Biology and Medicine, vol. 45, no. 2, pp. 158–166, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. A. J. Begonja, S. Gambaryan, J. R. Geiger et al., “Platelet NAD(P)H-oxidase-generated ROS production regulates αIIbβ3-integrin activation independent of the NO/cGMP pathway,” Blood, vol. 106, no. 8, pp. 2757–2760, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. P. C. Redondo, I. Jardin, J. M. Hernández-Cruz, J. A. Pariente, G. M. Salido, and J. A. Rosado, “Hydrogen peroxide and peroxynitrite enhance Ca2+ mobilization and aggregation in platelets from type 2 diabetic patients,” Biochemical and Biophysical Research Communications, vol. 333, no. 3, pp. 794–802, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. L. K. Jennings, M. E. Dockter, C. D. Wall, C. F. Fox, and D. M. Kennedy, “Calcium mobilization in human platelets using indo-1 and flow cytometry,” Blood, vol. 74, no. 8, pp. 2674–2680, 1989. View at Google Scholar · View at Scopus
  19. M. D. Monteiro, M. J. Goncalves, F. Sansonetty, and J. E. O'Connor, “Flow cytometric analysis of calcium mobilization in whole-blood platelets,” Current Protocols in Cytometry, chapter 9:unit 9.20, 2003. View at Publisher · View at Google Scholar
  20. M. Al-Tamimi, F. Mu, J. F. Arthur et al., “Anti-glycoprotein VI monoclonal antibodies directly aggregate platelets independently of FcγRIIa and induce GPVI ectodomain shedding,” Platelets, vol. 20, no. 2, pp. 75–82, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. E. E. Gardiner, D. Karunakaran, J. F. Arthur et al., “Dual ITAM-mediated proteolytic pathways for irreversible inactivation of platelet receptors: De-ITAM-izing FcγRIIa,” Blood, vol. 111, no. 1, pp. 165–174, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Shen, G. M. Romo, J. Dong et al., “Requirement of leucine-rich repeats of glycoprotein (GP) Ibα for shear- dependent and static binding of von willebrand factor to the platelet membrane GP Ib-IX-V complex,” Blood, vol. 95, no. 3, pp. 903–910, 2000. View at Google Scholar · View at Scopus
  23. S. J. Barsam, B. Psaila, M. Forestier et al., “Platelet production and platelet destruction: assessing mechanisms of treatment effect in immune thrombocytopenia,” Blood, vol. 117, no. 21, pp. 5723–5732, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Yamamoto, K. Takeshita, M. Shichijo et al., “The orally available spleen tyrosine kinase inhibitor 2-[7-(3,4-dimethoxyphenyl)-imidazo[1,2-c]pyrimidin-5-ylamino]-nicotinamide dihydrochloride (BAY 61-3606) blocks antigen-induced airway inflammation in rodents,” Journal of Pharmacology and Experimental Therapeutics, vol. 306, no. 3, pp. 1174–1181, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Best, Y. A. Senis, G. E. Jarvis et al., “GPVI levels in platelets: relationship to platelet function at high shear,” Blood, vol. 102, no. 8, pp. 2811–2818, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. H. Chen, D. Locke, Y. Liu, C. Liu, and M. L. Kahn, “The platelet receptor GPVI mediates both adhesion and signaling responses to collagen in a receptor density-dependent fashion,” Journal of Biological Chemistry, vol. 277, no. 4, pp. 3011–3019, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Leoncini, M. G. Signorello, A. Piana, M. Carrubba, and U. Armani, “Hyperactivity and increased hydrogen peroxide formation in platelets of NIDDM patients,” Thrombosis Research, vol. 86, no. 2, pp. 153–160, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. M. L. Lawson, H. C. Gerstein, E. Tsui, and B. Zinman, “Effect of intensive therapy on early macrovascular disease in young individuals with type 1 diabetes: a systematic review and meta-analysis,” Diabetes Care, vol. 22, no. 2, pp. B35–B39, 1999. View at Google Scholar · View at Scopus
  29. B. Roshan, G. H. Tofler, L. A. Weinrauch et al., “Improved glycemic control and platelet function abnormalities in diabetic patients with microvascular disease,” Metabolism, vol. 49, no. 1, pp. 88–91, 2000. View at Google Scholar · View at Scopus
  30. G. Davi, M. Averna, I. Catalano et al., “Platelet function in patients with type 2 diabetes mellitus: the effect of glycaemic control,” Diabetes Research, vol. 10, no. 1, pp. 7–12, 1989. View at Google Scholar · View at Scopus
  31. P. A. Rowe, K. Kavanagh, L. Zhang, H. J. Harwood Jr., and J. D. Wagner, “Short-term hyperglycemia increases arterial superoxide production and iron dysregulation in atherosclerotic monkeys,” Metabolism, vol. 60, no. 8, pp. 1070–1080, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Westerbacka, H. Yki-Järvinen, A. Turpeinen et al., “Inhibition of platelet-collagen interaction: an in vivo action of insulin abolished by insulin resistance in obesity,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 22, no. 1, pp. 167–172, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Rauchfuss, J. Geiger, U. Walter, T. Renne, and S. Gambaryan, “Insulin inhibition of platelet-endothelial interaction is mediated by insulin effects on endothelial cells without direct effects on platelets,” Journal of Thrombosis and Haemostasis, vol. 6, no. 5, pp. 856–864, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. J. W. Akkerman, A. J. Gerrits, I. A. Ferreira, and J. W. M. Heemskerk, “Insulin inhibition of platelet-endothelial interaction is mediated by insulin effects on endothelial cells without direct effects on platelets: a rebuttal,” Journal of Thrombosis and Haemostasis, vol. 7, no. 2, pp. 369–371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Jindal, S. Gupta, R. Gupta et al., “Platelet indices in diabetes mellitus: indicators of diabetic microvascular complications,” Hematology, vol. 16, no. 2, pp. 86–89, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Watala, M. Boncler, T. Pietrucha, and Z. Trojanowski, “Possible mechanisms of the altered platelet volume distribution in type 2 diabetes: does increased platelet activation contribute to platelet size heterogeneity?” Platelets, vol. 10, no. 1, pp. 52–60, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. N. Cabeza, Z. Li, C. Schulz et al., “Surface expression of collagen receptor Fc receptor-γ/glycoprotein VI is enhanced on platelets in type 2 diabetes and mediates release of CD40 ligand and activation of endothelial cells,” Diabetes, vol. 53, no. 8, pp. 2117–2121, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Takaya, Y. Iwamoto, H. Higashino, R. Ishihara, and Y. Kobayashi, “Increased intracellular calcium and altered phorbol dibutyrate binding to intact platelets in young subjects with insulin-dependent and non-insulin- dependent diabetes mellitus,” Metabolism, vol. 46, no. 8, pp. 949–953, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. I. Jardín, P. C. Redondo, G. M. Salido, J. A. Pariente, and J. A. Rosado, “Endogenously generated reactive oxygen species reduce PMCA activity in platelets from patients with non-insulin-dependent diabetes mellitus,” Platelets, vol. 17, no. 5, pp. 283–288, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Andre, T. Morooka, D. Sim et al., “Critical role for Syk in responses to vascular injury,” Blood, vol. 118, no. 18, pp. 5000–5010, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Colonna, G. Catalano, C. Chew et al., “Therapeutic targeting of Syk in autoimmune diabetes,” Journal of Immunology, vol. 185, no. 3, pp. 1532–1543, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Schulz, N. V. Leuschen, T. Fröhlich et al., “Identification of novel downstream targets of platelet glycoprotein VI activation by differential proteome analysis: implications for thrombus formation,” Blood, vol. 115, no. 20, pp. 4102–4110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. W. H. Tang, J. Stitham, S. Gleim et al., “Glucose and collagen regulate human platelet activity through aldose reductase induction of thromboxane,” Journal of Clinical Investigation, vol. 121, no. 11, pp. 4462–4476, 2011. View at Publisher · View at Google Scholar · View at Scopus