Plant food anthocyanins inhibit platelet granule secretion in hypercholesterolaemia: Involving the signalling pathway of PI3K–Akt

Thrombosis and Haemostasis

Volumn 112, Issue 5, 2014, Pages 981-991

  Song, Fenglin ^a   Zhu, Yanna ^a   Shi, Zhenyin ^b   Tian, Jinju ^a   Deng, Xiujuan ^a   Ren, Jing ^a   Andrews, Marc C ^c,d,e   Ni, Heyu ^c,d,e,f   Ling, Wenhua ^a   Yang, Yan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b Gansu Province Center for Disease Control and Prevention   (China)

^c Toronto Platelet Immunobiology Group   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

^f CANADIAN BLOOD SERVICES   (Canada)

Author keywords

Anthocyanins; Hypercholesterolaemia; PI3K; Platelet granule

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADENOSINE TRIPHOSPHATE; ANTHOCYANIN; BETA THROMBOGLOBULIN; CALCIUM ION; CD63 ANTIGEN; CYANIDIN 3 GLUCOSIDE; CYCLIC GMP; DELPHINIDIN 3 GLUCOSIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PADGEM PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PLACEBO; PROTEIN KINASE B; RANTES; SEROTONIN; STRESS ACTIVATED PROTEIN KINASE; THROMBOCYTE FACTOR 4; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; AKT1 PROTEIN, HUMAN; CARDIOTONIC AGENT; CYANIDIN 3-O-GLUCOSIDE; DELPHINIDIN 3-O-GLUCOPYRANOSIDE; GLUCOSIDE; PLASMA PROTEIN; SIGNAL PEPTIDE;

ARTICLE; BIOASSAY; BLOOD SAMPLING; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOUBLE BLIND PROCEDURE; ENZYME ACTIVITY; FLOW CYTOMETRY; FOOD CROP; HUMAN; HYPERCHOLESTEROLEMIA; INTRACELLULAR SIGNALING; LYSOSOME; MAJOR CLINICAL STUDY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RANDOMIZED CONTROLLED TRIAL; SECRETION (PROCESS); THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE RELEASE REACTION; WESTERN BLOTTING; ADULT; BLOOD; CELL GRANULE; CLINICAL TRIAL; COMPARATIVE STUDY; DRUG EFFECTS; FEMALE; MALE; MIDDLE AGED; MULTICENTER STUDY; PHOSPHORYLATION; PHYSIOLOGY; PHYTOTHERAPY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ADULT; ANTHOCYANINS; BLOOD PLATELETS; BLOOD PROTEINS; CARDIOTONIC AGENTS; CYTOPLASMIC GRANULES; DOUBLE-BLIND METHOD; FEMALE; GLUCOSIDES; HUMANS; HYPERCHOLESTEROLEMIA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; MALE; MAP KINASE SIGNALING SYSTEM; MIDDLE AGED; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PHYTOTHERAPY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84908540569     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH13-12-1002     Document Type: Article

References (49)

1. Ruggeri ZM. Platelets in atherothrombosis. Nat Med 2002; 8: 1227-1234.
2. Ni H, Freedman J. Platelets in haemostasis and thrombosis: role of integrins and their ligands. Transfus Apher Sci 2003; 28: 257-264.
3. Li C, Li J, Li Y, et al. Crosstalk between Platelets and the Immune System: Old Systems with New Discoveries. Adv Hematol 2012; 2012: 384685.
4. Murphy AJ, Bijl N, Yvan-Charvet L, et al. Cholesterol efflux in megakaryocyte progenitors suppresses platelet production and thrombocytosis. Nat Med 2013; 19: 586-594.
5. Blair P, Flaumenhaft R. Platelet alpha-granules: basic biology and clinical correlates. Blood Rev 2009; 23: 177-189.
6. McNicol A, Israels SJ. Platelet dense granules: structure, function and implications for haemostasis. Thromb Res 1999; 95: 1-18.
7. Li J, Callum JL, Lin Y, et al. Severe platelet desialylation in a patient with glycoprotein Ib/IX antibody-mediated immune thrombocytopenia and fatal pulmonary haemorrhage. Haematologica 2014; 99: e61-63.
8. Rendu F, Brohard-Bohn B. The platelet release reaction: granules' constituents, secretion and functions. Platelets 2001; 12: 261-273.
9. 2+-induced alpha-granule secretion in platelets. J Biol Chem 2000; 275: 33844-33849.
10. Cipollone F, Mezzetti A, Porreca E, et al. Association between enhanced soluble CD40L and prothrombotic state in hypercholesterolaemia: effects of statin therapy. Circulation 2002; 106: 399-402.
11. Prisco D, Rogasi PG, Paniccia R, et al. Altered lipid composition and thromboxane A2 formation in platelets from patients affected by IIa hyperlipoproteinemia. Thromb Res 1988; 50: 593-604.
12. King SM, McNamee RA, Houng AK, et al. Platelet dense-granule secretion plays a critical role in thrombosis and subsequent vascular remodeling in atherosclerotic mice. Circulation 2009; 120: 785-791.
13. Paigen B, Holmes PA, Novak EK, et al. Analysis of atherosclerosis susceptibility in mice with genetic defects in platelet function. Arteriosclerosis 1990; 10: 648-652.
14. Kennedy SG, Wagner AJ, Conzen SD, et al. The PI3-kinase/Akt signalling pathway delivers an anti-apoptotic signal. Genes Dev 1997; 11: 701-713.
15. Morello F, Perino A, Hirsch E. Phosphoinositide 3-kinase signalling in the vascular system. Cardiovasc Res 2009; 82: 261-271.
16. Li Z, Delaney MK, O'Brien KA, et al. Signalling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010; 30: 2341-2349.
17. Wallace TC. Anthocyanins in cardiovascular disease. Adv Nutr 2011; 2: 1-7.
18. Karlsen A, Retterstol L, Laake P, et al. Anthocyanins inhibit nuclear factor-kappaB activation in monocytes and reduce plasma concentrations of pro-inflammatory mediators in healthy adults. J Nutr 2007; 137: 1951-1954.
19. Yang Y, Shi Z, Reheman A, et al. Plant food delphinidin-3-glucoside significantly inhibits platelet activation and thrombosis: novel protective roles against cardiovascular diseases. PLoS One 2012; 7: e37323.
20. Rechner AR, Kroner C. Anthocyanins and colonic metabolites of dietary polyphenols inhibit platelet function. Thromb Res 2005; 116: 327-334.
21. Yang Y, Andrews MC, Hu Y, et al. Anthocyanin extract from black rice significantly ameliorates platelet hyperactivity and hypertriglyceridemia in dyslipidaemc rats induced by high fat diets. J Agric Food Chem 2011; 59: 6759-6764.
22. Zhu Y, Xia M, Yang Y, et al. Purified anthocyanin supplementation improves endothelial function via NO-cGMP activation in hypercholesterolaemic individuals. Clin Chem 2011; 57: 1524-1533.
23. Zhu Y, Ling W, Guo H, et al. Anti-inflammatory effect of purified dietary anthocyanin in adults with hypercholesterolaemia: a randomized controlled trial. Nutr Metab Cardiovasc Dis 2013; 23: 843-849.
24. Yang H, Reheman A, Chen P, et al. Fibrinogen and von Willebrand factor-independent platelet aggregation in vitro and in vivo. J Thromb Haemost 2006; 4: 2230-2237.
25. Li Z, Zhang G, Le Breton GC, et al. Two waves of platelet secretion induced by thromboxane A2 receptor and a critical role for phosphoinositide 3-kinases. J Biol Chem 2003; 278: 30725-30731.
26. Kroner C, Eybrechts K, Akkerman JW. Dual regulation of platelet protein kinase B. J Biol Chem 2000; 275: 27790-27798.
27. Stojanovic A, Marjanovic JA, Brovkovych VM, et al. A phosphoinositide 3-kinase-AKT-nitric oxide-cGMP signalling pathway in stimulating platelet secretion and aggregation. J Biol Chem 2006; 281: 16333-16339.
28. Li Z, Xi X, Du X. A mitogen-activated protein kinase-dependent signalling pathway in the activation of platelet integrin alpha IIbbeta3. J Biol Chem 2001; 276: 42226-42232.
29. Flevaris P, Li Z, Zhang G, et al. Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signalling pathway. Blood 2009; 113: 893-901.
30. Kramer RM, Roberts EF, Strifler BA, et al. Thrombin induces activation of p38 MAP kinase in human platelets. J Biol Chem 1995; 270: 27395-27398.
31. Bugaud F, Nadal-Wollbold F, Levy-Toledano S, et al. Regulation of c-jun-NH2 terminal kinase and extracellular-signal regulated kinase in human platelets. Blood 1999; 94: 3800-3805.
32. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest 2005; 115: 3378-3384.
33. King SM, Reed GL. Development of platelet secretory granules. Semin Cell Dev Biol 2002; 13: 293-302.
34. Yang H, Lang S, Zhai Z, et al. Fibrinogen is required for maintenance of platelet intracellular and cell-surface P-selectin expression. Blood 2009; 114: 425-436.
35. Kaplan KL, Owen J. Plasma levels of beta-thromboglobulin and platelet factor 4 as indices of platelet activation in vivo. Blood 1981; 57: 199-202.
36. Lane DA, Ireland H, Wolff S, et al. Detection of enhanced in vivo platelet alphagranule release in different patient groups-comparison of beta-thromboglobulin, platelet factor 4 and thrombospondin assays. Thromb Haemost 1984; 52: 183-187.
37. Assoian RK, Komoriya A, Meyers CA, et al. Transforming growth factor-beta in human platelets. Identification of a major storage site, purification, and characterization. J Biol Chem 1983; 258: 7155-7160.
38. Ferroni P, Martini F, Riondino S, et al. Soluble P-selectin as a marker of in vivo platelet activation. Clin Chim Acta 2009; 399: 88-91.
39. Podrez EA, Byzova TV, Febbraio M, et al. Platelet CD36 links hyperlipidaema, oxidant stress and a prothrombotic phenotype. Nat Med 2007; 13: 1086-1095.
40. Friend M, Vucenik I, Miller M. Research pointers: Platelet responsiveness to aspirin in patients with hyperlipidaemia. BMJ 2003; 326: 82-83.
41. Hohlfeld T, Scharnowski F, Braun M, et al. Antiplatelet effects of ticlopidine are reduced in experimental hypercholesterolaemia. Thromb Haemost 1994; 71: 112-118.
42. McGhie TK, Walton MC. The bioavailability and absorption of anthocyanins: towards a better understanding. Mol Nutr Food Res 2007; 51: 702-713.
43. Kay CD. Aspects of anthocyanin absorption, metabolism and pharmacokinetics in humans. Nutr Res Rev 2006; 19: 137-146.
44. Garcia-Alonso M, Minihane AM, Rimbach G, et al. Red wine anthocyanins are rapidly absorbed in humans and affect monocyte chaemoattractant protein 1 levels and antioxidant capacity of plasma. J Nutr Biochem 2009; 20: 521-529.
45. Kim K, Bae ON, Lim KM, et al. Novel antiplatelet activity of protocatechuic acid through the inhibition of high shear stress-induced platelet aggregation. J Pharmacol Exp Ther 2012; 343: 704-711.
46. Voss B, McLaughlin JN, Holinstat M, et al. PAR1, but not PAR4, activates human platelets through a Gi/o/phosphoinositide-3 kinase signalling axis. Mol Pharmacol 2007; 71: 1399-1406.
47. Radomski MW, Palmer RM, Moncada S. The role of nitric oxide and cGMP in platelet adhesion to vascular endothelium. Biochem Biophys Res Commun 1987; 148: 1482-1489.
48. Radomski MW, Palmer RM, Moncada S. An L-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc Natl Acad Sci USA 1990; 87: 5193-5197.
49. Marjanovic JA, Li Z, Stojanovic A, et al. Stimulatory roles of nitric-oxide synthase 3 and guanylyl cyclase in platelet activation. J Biol Chem 2005; 280: 37430-37438.