Platelet hemostasis in patients with metabolic syndrome and type 2 diabetes mellitus: cGMP- and NO-dependent mechanisms in the insulin-mediated platelet aggregation

Frontiers in Physiology

Volumn 6, Issue JAN, 2015, Pages

  Suslova, Tatiana E ^a,b   Sitozhevskii, Alexei V ^a   Ogurkova, Oksana N ^a   Kravchenko, Elena S ^a   Kologrivova, Irina V ^a   Anfinogenova, Yana ^a,c   Karpov, Rostislav S ^a  

^a CARDIOLOGY RESEARCH INSTITUTE   (Russian Federation)

^b TOMSK STATE UNIVERSITY   (Russian Federation)

^c NATIONAL RESEARCH TOMSK POLYTECHNIC UNIVERSITY   (Russian Federation)

Author keywords

Cyclic guanosine monophosphate; Metabolic syndrome; Nitric oxide; Nitric oxide synthase; Platelets; Type 2 diabetes mellitus

Indexed keywords

CYCLIC GMP; CYTOKINE; HOMOCYSTEINE; INSULIN; INSULIN RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

BLOOD CLOTTING; DYSLIPIDEMIA; ENZYME ACTIVITY; HEMOSTASIS; HUMAN; HYPERHOMOCYSTEINEMIA; INFLAMMATION; INSULIN RESISTANCE; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION;

EID: 84926432380     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00501     Document Type: Review

References (70)

1. Abu-Amara, M., Yang, S. Y., Seifalian, A., Davidson, B., and Fuller, B. (2012). The nitric oxide pathway-evidence and mechanisms for protection against liver ischaemia reperfusion injury. Liver Int. 32, 531-543. doi: 10.1111/j.1478-3231.2012.02755.x
2. Anfossi, G., Mularoni, E. M., Burzacca, S., Ponziani, M. C., Massucco, P., Mattiello, L., et al. (1998). Platelet resistance to nitrates in obesity and obese NIDDM, and normal platelet sensitivity to both insulin and nitrates in lean NIDDM. Diabetes Care 21, 121-126. doi: 10.2337/diacare.21.1.121
3. Anfossi, G., Russo, I., Doronzo, G., Pomero, A., and Trovati, M. (2010). Adipocytokines in atherothrombosis: focus on platelets and vascular smooth muscle cells. Mediators Inflamm. 2010:174341. doi: 10.1155/2010/174341
4. Anwaar, I., Gottsäter, A., Eriksson, K., Jacobsson, L., Lindgärde, F., and Mattiasson, I. (2000). Increased plasma endothelin-1 and intraplatelet cyclic guanosine monophosphate in men with disturbed glucose metabolism. Diabetes Res. Clin. Pract. 50, 127-136. doi: 10.1016/S0168-8227(00)00190-X
5. Beaulieu, L. M., Lin, E., Mick, E., Koupenova, M., Weinberg, E. O., Kramer, C. D., et al. (2014). Interleukin 1ß receptor 1 and interleukin 1ß regulate megakaryocyte maturation, platelet activation, and transcript profile during inflammation in mice and humans. Arterioscler. Thromb. Vasc. Biol. 34, 552-564. doi: 10.1161/ATVBAHA.113.302700
6. Berezova, T. T., and Korovkin, M. (ed.). (1998). Biologic Chemistry. Moscow: Medistina.
7. Berkovskaya, M. A., and Butrova, S. A. (2009). Metabolic syndrome as prothrombogenic condition. Obes. Metab. 3, 3-9.
8. Bode-Böger, S. M., Böger, R. H., Galland, A., and Frölich, J. C. (1998). Differential inhibition of human platelet aggregation and thromboxane A2 formation by L-arginine in vivo and in vitro. Naunyn Schmiedebergs Arch. Pharmacol. 357, 143-150. doi: 10.1007/PL00005148
9. Bondarenko, O. N., Galstyan, G. R., Antsiferov, M. B., Kuznetsova, T. V., and Kobylyansky, A. G. (2002). Biological role of nitric oxide in diabetes mellitus. Sakharny Diabet 2, 56-63.
10. Boushey, C. J., Beresford, S. A., Omenn, G. S., and Motulsky, A. G. (1995). A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. JAMA 274, 1049-1057. doi: 10.1001/jama.1995.03530130055028
11. Busse, R., and Mülsch, A. (1990). Induction of nitric oxide synthase by cytokines in vascular smooth muscle cells. FEBS Lett. 275, 87-90. doi: 10.1016/0014-5793(90)81445-T
12. Buvaltsev, V. I. (2011). Endothalial dysfunction as new concept of prevention and treatment of cardiovascular diseases. Int. Med. J. 51, 260-267.
13. Cambien, B., Bergmeier, W., Saffaripour, S., Mitchell, H. A., and Wagner, D. D. (2003). Antithrombotic activity of TNF-alpha. J. Clin. Invest. 112, 1589-1596. doi: 10.1172/JCI19284
14. Dandona, P., and Aljada, A. (2004). Advances in diabetes for the millennium: diabetes and the endothelium. MedGenMed 6, 6.
15. Das, M., and Das, D. K. (2008). Molecular mechanism of preconditioning. IUBMB Life 60, 199-203. doi: 10.1002/iub.31
16. De La Cruz, J. P., Moreno, A., Guerrero, A., Ortega, G., González-Correa, J. A., and Sánchez de la Cuesta, F. (2002). Nitric oxide-cGMP and prostacyclin-cAMP pathways in patients with type II diabetes and different types of retinopathy. Pathophysiol. Haemost. Thromb. 32, 25-32. doi: 10.1159/000057285
17. Esmon, C. T. (1999). Possible involvement of cytokines in diffuse intravascular coagulation and thrombosis. Baillieres Best Pract. Res. Clin. Haematol. 12, 343-359. doi: 10.1053/beha.1999.0029
18. Esmon, C. T. (2004). The impact of the inflammatory response on coagulation. Thromb. Res. 114, 321-327. doi: 10.1016/j.thromres.2004.06.028
19. Gkaliagkousi, E., Ritter, J., and Ferro, A. (2007). Platelet-derived nitric oxide signaling and regulation. Circ. Res. 101, 654-662. doi: 10.1161/CIRCRESAHA.107.158410
20. Granik, V. G., Ryabova, S. Y., and Grigoriev, N. B. (1997). Exogenic nitric-oxide donors and inhibitors of its formation (the chemical aspects). Uspekhi Khimii 66, 792-807. doi: 10.1070/RC1997v066n08ABEH000317
21. Gresele, P., Marzotti, S., Guglielmini, G., Momi, S., Giannini, S., and Minuz, P. (2010). Hyperglycemia-induced platelet activation in type 2 diabetes is resistant to aspirin but not to a nitric oxide-donating agent. Diabetes Care 33, 1262-1268. doi: 10.2337/dc09-2013
22. Gruzdeva, O. V., Kremeno, S. V., Suslova, T. E., and Levashkina, E. A. (2008). Platelet-mediated hemostasis and parameters of carbohydrate metabolism in patients with combination of type 2 diabetes mellitus and arterial hypertension. Siberian Med. J. 4-2, 28-30.
23. Idrisova, E. M., Bushkova, E. A., Krasnova, N. M., Mananko, E. I., Kalashnikova, T. P., Vorobyova, E. V., et al. (2007). Hemostatic parameters and their relationships with main components of metabolic syndrome. Siberian Med. J. 4, 106-112.
24. Inada, H., Shindo, H., Tawata, M., and Onaya, T. (2008). cAMP regulates nitric oxide production and ouabain sensitive Na+, K+-ATPase activity in SH-SY5Y human neuroblastoma cells. Diabetologia 41, 1451-1458. doi: 10.1007/s001250051091
25. Jarazo-Dietrich, S., Jacobo, P., Pérez, C. V., Guazzone, V. A., Lustig, L., and Theas, M. S. (2012). Up regulation of nitric oxide synthase-nitric oxide system in the testis of rats undergoing autoimmune orchitis. Immunobiology 217, 778-787. doi: 10.1016/j.imbio.2012.04.007
26. Joannides, R., Haefeli, W. E., Linder, L., Richard, V., Bakkali, E. H., Thuillez, C., et al. (1995). Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 91, 1314-1319. doi: 10.1161/01.CIR.91.5.1314
27. Kawamato, E. M., Glezer, I., Munhoz, C. D., Bernardes, C., Scavone, C., and Marcourakis, T. (2002). Human platelet nitric oxide synthase activity: an optimized method. Braz. J. Pharm. Sci. 38, 305-313. doi: 10.1590/S1516-93322002000300006
28. Kotani, K., Sakane, N., Saiga, K., Mu, H., and Kurozawa, Y. (2007). Clustered components of the metabolic syndrome and platelet counts in Japanese females. Clin. Chem. Lab. Med. 45, 376-379. doi: 10.1515/CCLM.2007.063
29. Kutti, J., Wadenvik, H., Henestam, B., and Stenström, G. (1986). Evaluation of platelet reactivity in diabetes mellitus. Acta Med. Scand. 219, 195-199. doi: 10.1111/j.0954-6820.1986.tb03298.x
30. Lindenblatt, N., Braun, B., Menger, M. D., Klar, E., and Vollmar, B. (2006). C-peptide exerts antithrombotic effects that are repressed by insulin in normal and diabetic mice. Diabetologia 49, 792-800. doi: 10.1007/s00125-006-0152-4
31. Malakhov, V. A., Zavgorodnaya, A. N., Lychko, V. S., Dzhanelidze, T. T., and Volokh, F. A. (2009). The Problem of Nitric Oxide in Neurology. Kharkov: SumDPU n.a. Makarenka. Available online at: http://mognovse.ru/ivl-malahov-v-a-zavgorodnyaya-a-n-lichko-v-s.html
32. Matsakaria, A. D., Peredervyaeva, E. B., and Pshenichnikova, T. B. (2006). Metabolic syndrome and low molecular weight heparins. Consilium Medicum 6, 35-41.
33. Medvedev, I. N., Gromnatsky, N. I., Naumov, M. M., and Bespartochny, B. D. (2004). Intravascular platelet activity in patients with arterial hypertension and metabolic syndrome and its correction by siofor and non-pharmacological methods. Farmateka 5, 58-62.
34. Muratova, A. Y. (2004). Status of Platelet-Mediated Hemostasis in Patients with Vascular Complications of Type 2 Diabetes Mellitus in Development of Anemia Syndrome. Saratov: Author's abstract of dissertation thesis for Ph.D.
35. Mutus, B., Rabini, R. A., Staffolani, R., Ricciotti, R., Fumelli, P., Moretti, N., et al. (2001). Homocysteine-induced inhibition of nitric oxide production in platelets: a study on healthy and diabetic subjects. Diabetologia 44, 979-982. doi: 10.1007/s001250100581
36. Naseem, K. M., and Riba, R. J. (2008). Unresolved roles of platelet nitric oxide synthase. Thromb. Haemost. 6, 10-19. doi: 10.1111/j.1538-7836.2007.02802.x
37. Nieto-Vazquez, I., Fernández-Veledo, S., Krämer, D. K., Vila-Bedmar, R., Garcia-Guerra, L., and Lorenzo, M. (2008). Insulin resistance associated to obesity: the link TNF-alpha. Arch. Physiol. Biochem. 114, 183-194. doi: 10.1080/13813450802181047
38. Oemar, B. S., Tschudi, M. R., Godoy, N., Brovkovich, V., Malinski, T., and Lüscher, T. F. (1998). Reduced endothelial nitric oxide synthase expression and production in human atherosclerosis. Circulation 97, 2494-2498. doi: 10.1161/01.CIR.97.25.2494
39. Ogurkova, O. N., Sitozhevskii, A. V., Koshelskaya, O. A., and Fedorova, T. S. (2007). Nitric oxide production by platelets in patients with metabolic syndrome. Siberian Med. J. 2, 15-18.
40. Ogurkova, O. N., Suslova, T. Y. E., Sitoshevsky, A. V., and Koshelskaya, O. A. (2012). cGMP- and cAMP-dependent intracellular signaling systems in the insulin-mediated regulation of platelet aggregation activity in patients with heart failure and metabolic disturbances. Bull. Exp. Biol. Med. 6, 76-81.
41. Padfield, G. J., Din, J. N., Koushiappi, E., Mills, N. L., Robinson, S. D., Cruden, N., et al. (2013). Cardiovascular effects of tumour necrosis factor a antagonism in patients with acute myocardial infarction: a first in human study. Heart 99, 1330-1335. doi: 10.1136/heartjnl-2013-303648
42. Paneni, F., Beckman, J. A., Creager, M. A., and Cosentino, F. (2013). Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur. Heart J. 34, 2436-2443. doi: 10.1093/eurheartj/eht149
43. Paolocci, N., Biondi, R., Bettini, M., Lee, C. I., Berlowitz, C. O., Rossi, R., et al. (2001). Oxygen radical-mediated reduction in basal and agonist-evoked NO release in isolated rat heart. J. Mol. Cell. Cardiol. 33, 671-679. doi: 10.1006/jmcc.2000.1334
44. Pavlishchuk, S. A., Petrik, G. G., and Katushkina Yu, A. (2007). Parameters of metabolism and platelet-mediated hemostasis in type 2 diabetes mellitus. Kubanskiy Nauchny Meditsinsky Vestnik 1-2, 132-135.
45. Petrik, G. G., and Pavlishchuk, S. A. (2008). Relationships between parameters of metabolism and hemostasis in type 2 diabetes mellitus. Kubanskiy Nauchny Meditsinsky Vestnik 6, 51-54.
46. Pignatelli, P., De Biase, L., Lenti, L., Tocci, G., Brunelli, A., Cangemi, R., et al. (2005). Tumor necrosis factor-alpha as trigger of platelet activation in patients with heart failure. Blood 106, 1992-1994. doi: 10.1182/blood-2005-03-1247
47. Pircher, J., Merkle, M., Wörnle, M., Ribeiro, A., Czermak, T., Stampnik, Y., et al. (2012). Prothrombotic effects of tumor necrosis factor alpha in vivo are amplified by the absence of TNF-alpha receptor subtype 1 and require TNF-alpha receptor subtype 2. Arthritis. Res. Ther. 14, R225. doi: 10.1186/ar4064
48. Rabini, R. A., Staffolani, R., Fumelli, P., Mutus, B., Curatola, G., and Mazzanti, L. (1998). Decreased nitric oxide synthase activity in platelets from IDDM and NIDDM patients. Diabetologia 41, 101-104. doi: 10.1007/s001250050873
49. Randriamboavonjy, V., and Fleming, I. (2005). Endothelial nitric oxide synthase (eNOS) in platelets: how is it regulated and what is it doing there? Pharmacol. Rep. 57(Suppl.), 59-65.
50. Randriamboavonjy, V., and Fleming, I. (2009). Insulin, insulin resistance, and platelet signaling in diabetes. Diabetes Care 32, 528-530. doi: 10.2337/dc08-1942
51. Schaeffer, G., Wascher, T. C., Kostner, G. M., and Graier, W. F. (1999). Alterations in platelet Ca2+ signalling in diabetic patients is due to increased formation of superoxide anions and reduced nitric oxide production. Diabetologia 42, 167-176. doi: 10.1007/s001250051135
52. Scherrer, U., and Sartori, C. (1997). Insulin as a vascular and sympathoexcitatory hormone: implications for blood pressure regulation, insulin sensitivity, and cardiovascular morbidity. Circulation 96, 4104-4113. doi: 10.1161/01.CIR.96.11.4104
53. Serebruany, V. L., McKenzie, M. E., Meister, A. F., Fuzaylov, S. Y., Gurbel, P. A., Atar, D., et al. (2002). Failure of platelet parameters and biomarkers to correlate platelet function to severity and etiology of heart failure in patients enrolled in the EPCOT trial. With special reference to the hemodyne hemostatic analyzer. Whole blood impedance aggregometry for the assessment of platelet function in patients with congestive heart failure. Pathophysiol. Haemost. Thromb. 32, 8-15. doi: 10.1159/000057283
54. Shaturny, V. I., Shakhidzhanov, S. S., Sveshnikova, A. N., and Panteleev, M. A. (2014). Activators, receptors, and signal transduction pathways in blood platelets. Biomeditsinskaya Khimiya 60, 182-200.
55. Shitikova, A. S. (2000). Platelet Hemostasis. St. Petersburg: St. Petersburg State Medical University.
56. Singer, G., Stokes, K. Y., and Neil Granger, D. (2013). Reactive oxygen and nitrogen species in sepsis-induced hepatic microvascular dysfunction. Inflamm. Res. 62, 155-164. doi: 10.1007/s00011-012-0562-3
57. Smolenski, A. (2012). Novel roles of cAMP/cGMP-dependent signaling in platelets. J. Thromb. Haemost. 10, 167-176. doi: 10.1111/j.1538-7836.2011.04576.x
58. Soslau, G., Morgan, D. A., Jaffe, J. S., Brodsky, I., and Wang, Y. (1997). Cytokine mRNA expression in human platelets and a megakaryocytic cell line and cytokine modulation of platelet function. Cytokine 9, 405-411. doi: 10.1006/cyto.1996.0182
59. Stalker, T. J., Newman, D. K., Ma Cruz, P., Wannemacher, K. M., and Lawrence, F. (2012). Platelet Signaling. Berlin; Heidelberg: Brass Springer-Verlag.
60. Suslova, T. E., Grusdeva, O. V., Kremeno, S. V., Koshlskaya, O. A., Levashkina, E. A., Zheltonogova, N. M., et al. (2007). Platelet aggregation activity and biochemical markers of metabolic syndrome. Siberian Med. J. 3, 30-34.
61. Suslova, T. E., Sitozhevskii, A. V., Ogurkova, O. N., Gruzdeva, O. V., Fedorova, T. S., and Karpov, R. S. (2005). Effect of insulin on NO production by monocytes from patients with metabolic cardiovascular syndrome. Bull. Exp. Biol. Med. 139, 391-393. doi: 10.1007/s10517-005-0302-6
62. Tokuda, H., Kato, K., Kasahara, S., Matsushima-Nishiwaki, R., Mizuno, T., Sakakibara, S., et al. (2012). Significant correlation between the acceleration of platelet aggregation and phosphorylation of HSP27 at Ser-78 in diabetic patients. Int. J. Mol. Med. 30, 1387-1395. doi: 10.3892/ijmm.2012.1146
63. Trovati, M., Anfossi, G., Cavalot, F., Massucco, P., Mularoni, E., and Emanuelli, G. (1998). Insulin directly reduces platelet sensitivity to aggregating agents. Studies in vitro and in vivo. Diabetes 37, 780-786. doi: 10.2337/diab.37.6.780
64. Trovati, M., Mularoni, E. M., Burzacca, S., Ponziani, M. C., Massucco, P., Mattiello, L., et al. (1995). Impaired insulin-induced platelet antiaggregating effect in obesity and in obese NIDDM patients. Diabetes 44, 1318-1322. doi: 10.2337/diab.44.11.1318
65. Udvardy, M., Pfliegler, G., and Rak, K. (1985). Platelet insulin receptor determination in non-insulin dependent diabetes mellitus. Experientia 41, 422-423. doi: 10.1007/BF02004539
66. Vinik, A. I., and Erbas, T. (2013). Diabetic autonomic neuropathy. Handb. Clin. Neurol. 117, 279-294. doi: 10.1016/B978-0-444-53491-0.00022-5
67. Wahl, S. M., McCartney-Francis, N., Chan, J., Dionne, R., Ta, L., and Orenstein, J. M. (2003). Nitric oxide in experimental joint inflammation. Benefit or detriment? Cells Tissues Organs 174, 26-33. doi: 10.1159/000070572
68. Welch, G. N., and Loscalzo, J. (1998). Homocysteine and atherothrombosis. N. Engl. J. Med. 338, 1042-1050. doi: 10.1056/NEJM199804093381507
69. Westerbacka, J., Yki-Järvinen, H., Turpeinen, A., Rissanen, A., Vehkavaara, S., Syrjälä, M., et al. (2002). Inhibition of platelet-collagen interaction: an in vivo action of insulin abolished by insulin resistance in obesity. Arterioscler. Thromb. Vasc. Biol. 22, 167-172. doi: 10.1161/hq0102.101546
70. Ye, Y., Perez-Polo, J. R., and Birnbaum, Y. (2010). Protecting against ischemia-reperfusion injury: antiplatelet drugs, statins, and their potential interactions. Ann. N.Y. Acad. Sci. 1207, 76-82. doi: 10.1111/j.1749-6632.2010.05725.x