A Review on the Effects of New Anti-Diabetic Drugs on Platelet Function

Author(s): Habib Yaribeygi*, Stephen L. Atkin, Tannaz Jamialahmadi, Amirhossein Sahebkar*

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
(Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders)

Volume 20 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Cardiovascular complications account for the majority of deaths caused by diabetes mellitus. Platelet hyperactivity has been shown to increase the risk of thrombotic events and is a therapeutic target for their prevention in diabetes. Modulation of platelet function by diabetes agents in addition to their hypoglycemic effects would contribute to cardiovascular protection. Newly introduced antidiabetic drugs of sodium-glucose cotransporter 2 inhibitors (SGLT2i), glucagon like peptide-1 receptor agonists (GLP-1RA) and dipeptidyl peptidase-4 inhibitors may have anti-platelet effects, and in the case of SGLT2i and GLP-1RA may contribute to their proven cardiovascular benefit that has been shown clinically.

Objective: Here, we reviewed the potential effects of these agents on platelet function in diabetes.

Results and Conclusion: GLP-1RA and DPP-4i drugs have antiplatelet properties beyond their primary hypoglycemic effects. Whilst we have little direct evidence for the antiplatelet effects of SGLT2 inhibitors, some studies have shown that these agents may inhibit platelet aggregation and reduce the risk of thrombotic events in diabetes.

Keywords: Sodium-glucose cotransporter 2 inhibitors, glucagon like peptide-1 receptor agonists, dipeptidyl peptidase-4 inhibitors, diabetes mellitus, platelet, thrombosis, anti-diabetic drugs, cardiovascular.

[1]
Association, A.D. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care, 2013, 36(Suppl. 1), S67-S74.
[http://dx.doi.org/10.2337/dc13-S067] [PMID: 23264425]
[2]
Mayer-Davis, E.J.; Lawrence, J.M.; Dabelea, D.; Divers, J.; Isom, S.; Dolan, L.; Imperatore, G.; Linder, B.; Marcovina, S.; Pettitt, D.J.; Pihoker, C.; Saydah, S.; Wagenknecht, L. SEARCH for Diabetes in Youth Study. Incidence trends of type 1 and type 2 diabetes among youths, 2002–2012. N. Engl. J. Med., 2017, 376(15), 1419-1429.
[http://dx.doi.org/10.1056/NEJMoa1610187] [PMID: 28402773]
[3]
Yaribeygi, H.; Butler, A.E.; Sahebkar, A. Aerobic exercise can modulate the underlying mechanisms involved in the development of diabetic complications. J. Cell. Physiol., 2019, 234(8), 12508-12515.
[http://dx.doi.org/10.1002/jcp.28110] [PMID: 30623433]
[4]
Yaribeygi, H.; Atkin, S.L.; Pirro, M.; Sahebkar, A. A review of the anti‐inflammatory properties of antidiabetic agents providing protective effects against vascular complications in diabetes. J. Cell. Physiol., 2018.
[PMID: 30417367]
[5]
Yaribeygi, H.; Butler, A.E.; Barreto, G.E.; Sahebkar, A. Antioxidative potential of antidiabetic agents: A possible protective mechanism against vascular complications in diabetic patients. J. Cell. Physiol., 2019, 234(3), 2436-2446.
[http://dx.doi.org/10.1002/jcp.27278] [PMID: 30191997]
[6]
Bonadonna, R.C.; Borghi, C.; Consoli, A.; Volpe, M. Novel antidiabetic drugs and cardiovascular risk: Primum non nocere. Nutr. Metab. Cardiovasc. Dis., 2016, 26(9), 759-766.
[http://dx.doi.org/10.1016/j.numecd.2016.05.007] [PMID: 27373139]
[7]
Papazafiropoulou, A.; Papanas, N.; Pappas, S.; Maltezos, E.; Mikhailidis, D.P. Effects of oral hypoglycemic agents on platelet function. J. Diabetes Complications, 2015, 29(6), 846-851.
[http://dx.doi.org/10.1016/j.jdiacomp.2015.04.005] [PMID: 26026848]
[8]
Siegel-Axel, D.I.; Gawaz, M. Platelets and endothelial cellsed.^eds., Seminars in thrombosis and hemostasis; Copyright© 2007 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New, 2007, pp. 128-135.
[http://dx.doi.org/10.1055/s-2007-969025]
[9]
Yau, J.W.; Teoh, H.; Verma, S. Endothelial cell control of thrombosis. BMC Cardiovasc. Disord., 2015, 15, 130.
[http://dx.doi.org/10.1186/s12872-015-0124-z] [PMID: 26481314]
[10]
Association, A.D. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care, 2014, 37(Suppl. 1), S81-S90.
[http://dx.doi.org/10.2337/dc14-S081] [PMID: 24357215]
[11]
de Faria Maraschin, J. Classification of diabetes.ed.^eds., Diabetes; Springer 2013, 12-19.
[12]
O’Neal, K.S.; Johnson, J.L.; Panak, R.L. Recognizing and appropriately treating latent autoimmune diabetes in adults. Diabetes Spectr., 2016, 29(4), 249-252.
[http://dx.doi.org/10.2337/ds15-0047] [PMID: 27899877]
[13]
Paniccia, R.; Priora, R.; Liotta, A.A.; Abbate, R. Platelet function tests: a comparative review. Vasc. Health Risk Manag., 2015, 11, 133-148.
[http://dx.doi.org/10.2147/VHRM.S44469] [PMID: 25733843]
[14]
Gremmel, T.; Frelinger, A.L., III; Michelson, A.D. Platelet physiologyed.^eds., Seminars in thrombosis and hemostasis; Thieme Medical Publishers, 2016, pp. 191-204.
[15]
Schneider, W.; Gattermann, N. Megakaryocytes: origin of bleeding and thrombotic disorders. Eur. J. Clin. Invest., 1994, 24(Suppl. 1), 16-20.
[http://dx.doi.org/10.1111/j.1365-2362.1994.tb02420.x] [PMID: 8013527]
[16]
Lindsay, C.R.; Edelstein, L.C. MicroRNAs in platelet physiology and functioned.^eds., Seminars in thrombosis and hemostasis; Thieme Medical Publishers, 2016, pp. 215-222.
[http://dx.doi.org/10.1055/s-0035-1570077]
[17]
Badrnya, S.; Schrottmaier, W.C.; Kral, J.B.; Yaiw, K-C.; Volf, I.; Schabbauer, G.; Söderberg-Nauclér, C.; Assinger, A. Platelets mediate oxidized low-density lipoprotein-induced monocyte extravasation and foam cell formation. Arterioscler. Thromb. Vasc. Biol., 2014, 34(3), 571-580.
[http://dx.doi.org/10.1161/ATVBAHA.113.302919] [PMID: 24371083]
[18]
Engelmann, B.; Massberg, S. Thrombosis as an intravascular effector of innate immunity. Nat. Rev. Immunol., 2013, 13(1), 34-45.
[http://dx.doi.org/10.1038/nri3345] [PMID: 23222502]
[19]
Gay, L.J.; Felding-Habermann, B. Contribution of platelets to tumour metastasis. Nat. Rev. Cancer, 2011, 11(2), 123-134.
[http://dx.doi.org/10.1038/nrc3004] [PMID: 21258396]
[20]
Gresele, P. Subcommittee on Platelet Physiology of the International Society on Thrombosis and Hemostasis. Diagnosis of inherited platelet function disorders: guidance from the SSC of the ISTH. J. Thromb. Haemost., 2015, 13(2), 314-322.
[http://dx.doi.org/10.1111/jth.12792] [PMID: 25403439]
[21]
Jia, G.; Aroor, A.R.; Sowers, J.R. Glucagon-like peptide 1 receptor activation and platelet function: beyond glycemic control. Diabetes, 2016, 65(6), 1487-1489.
[http://dx.doi.org/10.2337/dbi16-0014] [PMID: 27222394]
[22]
Kashyap, S.R.; Roman, L.J.; Lamont, J.; Masters, B.S.S.; Bajaj, M.; Suraamornkul, S.; Belfort, R.; Berria, R.; Kellogg, D.L., Jr; Liu, Y.; DeFronzo, R.A. Insulin resistance is associated with impaired nitric oxide synthase activity in skeletal muscle of type 2 diabetic subjects. J. Clin. Endocrinol. Metab., 2005, 90(2), 1100-1105.
[http://dx.doi.org/10.1210/jc.2004-0745] [PMID: 15562034]
[23]
Gresele, P.; Marzotti, S.; Guglielmini, G.; Momi, S.; Giannini, S.; Minuz, P.; Lucidi, P.; Bolli, G.B. Hyperglycemia-induced platelet activation in type 2 diabetes is resistant to aspirin but not to a nitric oxide-donating agent. Diabetes Care, 2010, 33(6), 1262-1268.
[http://dx.doi.org/10.2337/dc09-2013] [PMID: 20299485]
[24]
Huskens, D.; Sang, Y.; Konings, J.; van der Vorm, L.; de Laat, B.; Kelchtermans, H.; Roest, M. Standardization and reference ranges for whole blood platelet function measurements using a flow cytometric platelet activation test. PLoS One, 2018, 13(2)e0192079
[http://dx.doi.org/10.1371/journal.pone.0192079] [PMID: 29389990]
[25]
Kamath, S.; Blann, A.D.; Lip, G.Y. Platelet activation: assessment and quantification. Eur. Heart J., 2001, 22(17), 1561-1571.
[http://dx.doi.org/10.1053/euhj.2000.2515] [PMID: 11492985]
[26]
Mutreja, D.; Sharma, R.K.; Purohit, A.; Aggarwal, M.; Saxena, R. Evaluation of platelet surface glycoproteins in patients with Glanzmann thrombasthenia: Association with bleeding symptoms. Indian J. Med. Res., 2017, 145(5), 629-634.
[PMID: 28948953]
[27]
Vinik, A.I.; Erbas, T.; Park, T.S.; Nolan, R.; Pittenger, G.L. Platelet dysfunction in type 2 diabetes. Diabetes Care, 2001, 24(8), 1476-1485.
[http://dx.doi.org/10.2337/diacare.24.8.1476] [PMID: 11473089]
[28]
Sowers, J.R.; Epstein, M.; Frohlich, E.D. Diabetes, hypertension, and cardiovascular disease: an update. Hypertension, 2001, 37(4), 1053-1059.
[http://dx.doi.org/10.1161/01.HYP.37.4.1053] [PMID: 11304502]
[29]
Santilli, F.; Simeone, P.; Liani, R.; Davì, G. Platelets and diabetes mellitus. Prostaglandins Other Lipid Mediat., 2015, 120, 28-39.
[http://dx.doi.org/10.1016/j.prostaglandins.2015.05.002] [PMID: 25986598]
[30]
Suslova, T.E.; Sitozhevskii, A.V.; Ogurkova, O.N.; Kravchenko, E.S.; Kologrivova, I.V.; Anfinogenova, Y.; Karpov, R.S. Platelet hemostasis in patients with metabolic syndrome and type 2 diabetes mellitus: cGMP- and NO-dependent mechanisms in the insulin-mediated platelet aggregation. Front. Physiol., 2015, 5, 501.
[http://dx.doi.org/10.3389/fphys.2014.00501] [PMID: 25601838]
[31]
Gkaliagkousi, E.; Corrigall, V.; Becker, S.; de Winter, P.; Shah, A.; Zamboulis, C.; Ritter, J.; Ferro, A. Decreased platelet nitric oxide contributes to increased circulating monocyte-platelet aggregates in hypertension. Eur. Heart J., 2009, 30(24), 3048-3054.
[http://dx.doi.org/10.1093/eurheartj/ehp330] [PMID: 19687162]
[32]
Wang, G-R.; Zhu, Y.; Halushka, P.V.; Lincoln, T.M.; Mendelsohn, M.E. Mechanism of platelet inhibition by nitric oxide: in vivo phosphorylation of thromboxane receptor by cyclic GMP-dependent protein kinase. Proc. Natl. Acad. Sci. USA, 1998, 95(9), 4888-4893.
[http://dx.doi.org/10.1073/pnas.95.9.4888] [PMID: 9560198]
[33]
Yaribeygi, H.; Atkin, S.L.; Butler, A.E.; Sahebkar, A. Sodium–glucose cotransporter inhibitors and oxidative stress: An update. J. Cell. Physiol., 2018.
[PMID: 30443936]
[34]
Davidson, J.A.; Kuritzky, L. Sodium glucose co-transporter 2 inhibitors and their mechanism for improving glycemia in patients with type 2 diabetes. Postgrad. Med., 2014, 126(6), 33-48.
[http://dx.doi.org/10.3810/pgm.2014.10.2819] [PMID: 25414933]
[35]
Yaribeygi, H.; Katsiki, N.; Butler, A.E.; Atkin, S.L.; Sahebkar, A. A response to “In response to ‘Sodium-glucose cotransporter 2 inhibitors and inflammation in chronic kidney disease: Possible molecular pathways’”. J. Cell. Physiol., 2019, 234(7), 9908-9909.
[http://dx.doi.org/10.1002/jcp.28041] [PMID: 30710347]
[36]
Chao, E.C. SGLT-2 inhibitors: a new mechanism for glycemic control. Clin. Diabetes, 2014, 32(1), 4-11.
[http://dx.doi.org/10.2337/diaclin.32.1.4] [PMID: 26246672]
[37]
Makarova, E.; Górnaś, P.; Konrade, I.; Tirzite, D.; Cirule, H.; Gulbe, A.; Pugajeva, I.; Seglina, D.; Dambrova, M. Acute anti-hyperglycaemic effects of an unripe apple preparation containing phlorizin in healthy volunteers: a preliminary study. J. Sci. Food Agric., 2015, 95(3), 560-568.
[http://dx.doi.org/10.1002/jsfa.6779] [PMID: 24917557]
[38]
Chao, E.C.; Henry, R.R. SGLT2 inhibition--a novel strategy for diabetes treatment. Nat. Rev. Drug Discov., 2010, 9(7), 551-559.
[http://dx.doi.org/10.1038/nrd3180] [PMID: 20508640]
[39]
Clar, C.; Gill, J.A.; Court, R.; Waugh, N. Systematic review of SGLT2 receptor inhibitors in dual or triple therapy in type 2 diabetes. BMJ Open, 2012, 2(5)e001007
[http://dx.doi.org/10.1136/bmjopen-2012-001007] [PMID: 23087012]
[40]
Kern, M.; Klöting, N.; Mark, M.; Mayoux, E.; Klein, T.; Blüher, M. The SGLT2 inhibitor empagliflozin improves insulin sensitivity in db/db mice both as monotherapy and in combination with linagliptin. Metabolism, 2016, 65(2), 114-123.
[http://dx.doi.org/10.1016/j.metabol.2015.10.010] [PMID: 26773934]
[41]
Han, S.; Hagan, D.L.; Taylor, J.R.; Xin, L.; Meng, W.; Biller, S.A.; Wetterau, J.R.; Washburn, W.N.; Whaley, J.M. Dapagliflozin, a selective SGLT2 inhibitor, improves glucose homeostasis in normal and diabetic rats. Diabetes, 2008, 57(6), 1723-1729.
[http://dx.doi.org/10.2337/db07-1472] [PMID: 18356408]
[42]
Wilding, J.P.; Woo, V.; Rohwedder, K.; Sugg, J.; Parikh, S. Dapagliflozin 006 Study Group. Dapagliflozin in patients with type 2 diabetes receiving high doses of insulin: efficacy and safety over 2 years. Diabetes Obes. Metab., 2014, 16(2), 124-136.
[http://dx.doi.org/10.1111/dom.12187] [PMID: 23911013]
[43]
Ferrannini, E.; Muscelli, E.; Frascerra, S.; Baldi, S.; Mari, A.; Heise, T.; Broedl, U.C.; Woerle, H-J. Metabolic response to sodium-glucose cotransporter 2 inhibition in type 2 diabetic patients. J. Clin. Invest., 2014, 124(2), 499-508.
[http://dx.doi.org/10.1172/JCI72227] [PMID: 24463454]
[44]
Drucker, D.J.; Nauck, M.A. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet, 2006, 368(9548), 1696-1705.
[http://dx.doi.org/10.1016/S0140-6736(06)69705-5] [PMID: 17098089]
[45]
Islam, M. Insulinotropic Effect of Herbal Drugs for Management of Diabetes Mellitus: A Congregational Approach. Biosens J, 2016, 5, 2.
[46]
Meier, J.J. GLP-1 receptor agonists for individualized treatment of type 2 diabetes mellitus. Nat. Rev. Endocrinol., 2012, 8(12), 728-742.
[http://dx.doi.org/10.1038/nrendo.2012.140] [PMID: 22945360]
[47]
Baggio, L.L.; Drucker, D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology, 2007, 132(6), 2131-2157.
[http://dx.doi.org/10.1053/j.gastro.2007.03.054] [PMID: 17498508]
[48]
Scott, K.A.; Moran, T.H. The GLP-1 agonist exendin-4 reduces food intake in nonhuman primates through changes in meal size. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2007, 293(3), R983-R987.
[http://dx.doi.org/10.1152/ajpregu.00323.2007] [PMID: 17581835]
[49]
Ding, X.; Saxena, N.K.; Lin, S.; Gupta, N.A.; Anania, F.A. Exendin-4, a glucagon-like protein-1 (GLP-1) receptor agonist, reverses hepatic steatosis in ob/ob mice. Hepatology, 2006, 43(1), 173-181.
[http://dx.doi.org/10.1002/hep.21006] [PMID: 16374859]
[50]
Wootten, D.; Simms, J.; Koole, C.; Woodman, O.L.; Summers, R.J.; Christopoulos, A.; Sexton, P.M. Modulation of the glucagon-like peptide-1 receptor signaling by naturally occurring and synthetic flavonoids. J. Pharmacol. Exp. Ther., 2011, 336(2), 540-550.
[http://dx.doi.org/10.1124/jpet.110.176362] [PMID: 21075839]
[51]
Association, A.D. American Diabetes Association. 2. Classification and diagnosis of diabetes: standards of medical care in diabetes—2018. Diabetes Care, 2018, 41(Suppl. 1), S13-S27.
[http://dx.doi.org/10.2337/dc18-S002] [PMID: 29222373]
[52]
Ahrén, B. DPP-4 inhibitors. Best Pract. Res. Clin. Endocrinol. Metab., 2007, 21(4), 517-533.
[http://dx.doi.org/10.1016/j.beem.2007.07.005] [PMID: 18054733]
[53]
Brubaker, P.L. The glucagon-like peptides: pleiotropic regulators of nutrient homeostasis. Ann. N. Y. Acad. Sci., 2006, 1070, 10-26.
[http://dx.doi.org/10.1196/annals.1317.006] [PMID: 16888147]
[54]
Steven, S.; Oelze, M.; Hanf, A.; Kröller-Schön, S.; Kashani, F.; Roohani, S.; Welschof, P.; Kopp, M.; Gödtel-Armbrust, U.; Xia, N.; Li, H.; Schulz, E.; Lackner, K.J.; Wojnowski, L.; Bottari, S.P.; Wenzel, P.; Mayoux, E.; Münzel, T.; Daiber, A. The SGLT2 inhibitor empagliflozin improves the primary diabetic complications in ZDF rats. Redox Biol., 2017, 13, 370-385.
[http://dx.doi.org/10.1016/j.redox.2017.06.009] [PMID: 28667906]
[55]
van der Zee, P.M.; Biró, E.; Ko, Y.; de Winter, R.J.; Hack, C.E.; Sturk, A.; Nieuwland, R. P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin. Chem., 2006, 52(4), 657-664.
[http://dx.doi.org/10.1373/clinchem.2005.057414] [PMID: 16439610]
[56]
Théorêt, J-F.; Yacoub, D.; Hachem, A.; Gillis, M-A.; Merhi, Y. P-selectin ligation induces platelet activation and enhances microaggregate and thrombus formation. Thromb. Res., 2011, 128(3), 243-250.
[http://dx.doi.org/10.1016/j.thromres.2011.04.018] [PMID: 21600632]
[57]
Perrone-Filardi, P.; Avogaro, A.; Bonora, E.; Colivicchi, F.; Fioretto, P.; Maggioni, A.P.; Sesti, G.; Ferrannini, E. Mechanisms linking empagliflozin to cardiovascular and renal protection. Int. J. Cardiol., 2017, 241, 450-456.
[http://dx.doi.org/10.1016/j.ijcard.2017.03.089] [PMID: 28395981]
[58]
Heerspink, H.J.; Perkins, B.A.; Fitchett, D.H.; Husain, M.; Cherney, D.Z. Sodium glucose cotransporter 2 inhibitors in the treatment of diabetes mellitus: cardiovascular and kidney effects, potential mechanisms, and clinical applications. Circulation, 2016, 134(10), 752-772.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.116.021887] [PMID: 27470878]
[59]
Santos-Gallego, C.G.; Zafar, M.; San Antonio, R.; Ibanez, J.A.R.; Botija, M.B.P.; Ishikawa, K.; Watanabe, S.; Hajjar, R.; Fuster, V.; Badimon, J. The SGLT2 inhibitor empagliflozin does not exhibit pro thrombotic effects. J. Am. Coll. Cardiol., 2018, 71, A1852.
[http://dx.doi.org/10.1016/S0735-1097(18)32393-3]
[60]
Ueda, P; Svanström, H; Melbye, M; Eliasson, B; Svensson, A-M; Franzén, S; Gudbjörnsdottir, S; Hveem, K; Jonasson, C Pasternak, B Sodium glucose cotransporter 2 inhibitors and risk of serious adverse events: nationwide register based cohort study. bmj, 2018, 363, k4365.
[61]
Tessari, P.; Cecchet, D.; Cosma, A.; Vettore, M.; Coracina, A.; Millioni, R.; Iori, E.; Puricelli, L.; Avogaro, A.; Vedovato, M. Nitric oxide synthesis is reduced in subjects with type 2 diabetes and nephropathy. Diabetes, 2010, 59(9), 2152-2159.
[http://dx.doi.org/10.2337/db09-1772] [PMID: 20484137]
[62]
Smyth, E.; Solomon, A.; Birrell, M.A.; Smallwood, M.J.; Winyard, P.G.; Tetley, T.D.; Emerson, M. Influence of inflammation and nitric oxide upon platelet aggregation following deposition of diesel exhaust particles in the airways. Br. J. Pharmacol., 2017, 174(13), 2130-2139.
[http://dx.doi.org/10.1111/bph.13831] [PMID: 28437857]
[63]
Aroor, A.R.; Das, N.A.; Carpenter, A.J.; Habibi, J.; Jia, G.; Ramirez-Perez, F.I.; Martinez-Lemus, L.; Manrique-Acevedo, C.M.; Hayden, M.R.; Duta, C.; Nistala, R.; Mayoux, E.; Padilla, J.; Chandrasekar, B.; DeMarco, V.G. Glycemic control by the SGLT2 inhibitor empagliflozin decreases aortic stiffness, renal resistivity index and kidney injury. Cardiovasc. Diabetol., 2018, 17(1), 108.
[http://dx.doi.org/10.1186/s12933-018-0750-8] [PMID: 30060748]
[64]
Ghalayini, I.F. Nitric oxide-cyclic GMP pathway with some emphasis on cavernosal contractility. Int. J. Impot. Res., 2004, 16(6), 459-469.
[http://dx.doi.org/10.1038/sj.ijir.3901256] [PMID: 15229623]
[65]
Bryan, N.S.; Bian, K.; Murad, F. Discovery of the nitric oxide signaling pathway and targets for drug development. Front. Biosci., 2009, 14, 1-18.
[http://dx.doi.org/10.2741/3228] [PMID: 19273051]
[66]
Knowles, R.G.; Moncada, S. Nitric oxide as a signal in blood vessels. Trends Biochem. Sci., 1992, 17(10), 399-402.
[http://dx.doi.org/10.1016/0968-0004(92)90008-W] [PMID: 1280869]
[67]
Riddell, D.R.; Owen, J.S. Nitric oxide and platelet aggregation. ed.^eds., Vitamins & Hormone; Elsevier, 1997, pp. 25-48.
[http://dx.doi.org/10.1016/S0083-6729(08)60639-1]
[68]
Cameron-Vendrig, A.; Reheman, A.; Siraj, M.A.; Xu, X.R.; Wang, Y.; Lei, X.; Afroze, T.; Shikatani, E.; El-Mounayri, O.; Noyan, H.; Weissleder, R.; Ni, H.; Husain, M. Glucagon-like peptide 1 receptor activation attenuates platelet aggregation and thrombosis. Diabetes, 2016, 65(6), 1714-1723.
[http://dx.doi.org/10.2337/db15-1141] [PMID: 26936963]
[69]
Modrego, J.; Azcona, L.; Martín-Palacios, N.; Zamorano-León, J.J.; Segura, A.; Rodríguez, P.; Guerra, R.; Tamargo, J.; Macaya, C.; López-Farré, A.J. Platelet content of nitric oxide synthase 3 phosphorylated at Serine 1177 is associated with the functional response of platelets to aspirin. PLoS One, 2013, 8(12)e82574
[http://dx.doi.org/10.1371/journal.pone.0082574] [PMID: 24376548]
[70]
Gambaryan, S.; Tsikas, D. A review and discussion of platelet nitric oxide and nitric oxide synthase: do blood platelets produce nitric oxide from L-arginine or nitrite? Amino Acids, 2015, 47(9), 1779-1793.
[http://dx.doi.org/10.1007/s00726-015-1986-1] [PMID: 25929585]
[71]
Russo, I.; Barale, C.; Mattiello, L.; Cavalot, F.; Trovati, M. GLP-1 and liraglutide increase the platelet inhibitory effects of nitric oxide. Diabetologia, 2013, 56, 397-398.
[72]
Barale, C.; Frascaroli, C.; Cavalot, F.; Guerrasio, A.; Russo, I. In Type 2 Diabetes mellitus the GLP-1 effects on platelets are impaired. Atherosclerosis, 2016, 252, e257-e258.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.07.081]
[73]
Ding, L.; Zhang, J. Glucagon-like peptide-1 activates endothelial nitric oxide synthase in human umbilical vein endothelial cells. Acta Pharmacol. Sin., 2012, 33(1), 75-81.
[http://dx.doi.org/10.1038/aps.2011.149] [PMID: 22120969]
[74]
Hattori, Y.; Jojima, T.; Tomizawa, A.; Satoh, H.; Hattori, S.; Kasai, K.; Hayashi, T. A glucagon-like peptide-1 (GLP-1) analogue, liraglutide, upregulates nitric oxide production and exerts anti-inflammatory action in endothelial cells. Diabetologia, 2010, 53(10), 2256-2263.
[http://dx.doi.org/10.1007/s00125-010-1831-8] [PMID: 20593161]
[75]
Dong, Z.; Chai, W.; Wang, W.; Zhao, L.; Fu, Z.; Cao, W.; Liu, Z. Protein kinase A mediates glucagon-like peptide 1-induced nitric oxide production and muscle microvascular recruitment. Am. J. Physiol. Heart Circ. Physiol., 2012.
[PMID: 23193054]
[76]
Aroor, A.R.; Sowers, J.R.; Bender, S.B.; Nistala, R.; Garro, M.; Mugerfeld, I.; Hayden, M.R.; Johnson, M.S.; Salam, M.; Whaley-Connell, A.; Demarco, V.G. Dipeptidylpeptidase inhibition is associated with improvement in blood pressure and diastolic function in insulin-resistant male Zucker obese rats. Endocrinology, 2013, 154(7), 2501-2513.
[http://dx.doi.org/10.1210/en.2013-1096] [PMID: 23653460]
[77]
Chien, C-T.; Fan, S-C.; Lin, S-C.; Kuo, C-C.; Yang, C-H.; Yu, T-Y.; Lee, S-P.; Cheng, D-Y.; Li, P-C. Glucagon-like peptide-1 receptor agonist activation ameliorates venous thrombosis-induced arteriovenous fistula failure in chronic kidney disease. Thromb. Haemost., 2014, 112(5), 1051-1064.
[http://dx.doi.org/10.1160/th14-03-0258] [PMID: 25030617]
[78]
Kahal, H. GLP-1R, a novel receptor in platelets, and the use of liraglutide in the treatment of obesity in women with PCOS In: ed.^eds. University of Hull and University of York; , 2013.
[79]
Steven, S.; Jurk, K.; Kopp, M.; Kroeller-Schoen, S.; Mikhed, Y.; Schwierczek, K.; Roohani, S.; Kashani, F.; Tokalov, S.; Danckwardt, S. Glucagon-like peptide-1 (GLP-1) reduces microvascular thrombosis, systemic inflammation and platelet activation in endotoxemic mice. In: ed.^eds., European heart journal; Oxford univ press great clarendon st, oxford ox2 6dp, England,, 2016; pp. 111-112.
[80]
Gupta, A.K.; Verma, A.K.; Kailashiya, J.; Singh, S.K.; Kumar, N. Sitagliptin: anti-platelet effect in diabetes and healthy volunteers. Platelets, 2012, 23(8), 565-570.
[http://dx.doi.org/10.3109/09537104.2012.721907] [PMID: 22950787]
[81]
Fadini, G.P.; Avogaro, A.; Degli Esposti, L.; Russo, P.; Saragoni, S.; Buda, S.; Rosano, G.; Pecorelli, S.; Pani, L. OsMed Health-DB Network. Risk of hospitalization for heart failure in patients with type 2 diabetes newly treated with DPP-4 inhibitors or other oral glucose-lowering medications: a retrospective registry study on 127,555 patients from the Nationwide OsMed Health-DB Database. Eur. Heart J., 2015, 36(36), 2454-2462.
[http://dx.doi.org/10.1093/eurheartj/ehv301] [PMID: 26112890]
[82]
Omoto, S.; Taniura, T.; Nishizawa, T.; Tamaki, T.; Shouzu, A.; Nomura, S. Anti-atherosclerotic effects of sitagliptin in patients with type 2 diabetes mellitus. Diabetes Metab. Syndr. Obes., 2015, 8, 339-345.
[PMID: 26251624]
[83]
Davidson, M.H. Potential impact of dipeptidyl peptidase-4 inhibitors on cardiovascular pathophysiology in type 2 diabetes mellitus. Postgrad. Med., 2014, 126(3), 56-65.
[http://dx.doi.org/10.3810/pgm.2014.05.2756] [PMID: 24918792]
[84]
Scheen, A.J. Cardiovascular effects of dipeptidyl peptidase-4 inhibitors: from risk factors to clinical outcomes. Postgrad. Med., 2013, 125(3), 7-20.
[http://dx.doi.org/10.3810/pgm.2013.05.2659] [PMID: 23748503]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 20
ISSUE: 3
Year: 2020
Page: [328 - 334]
Pages: 7
DOI: 10.2174/1871530319666191014110414
Price: $65

Article Metrics

PDF: 25
HTML: 3
EPUB: 1
PRC: 3