Korean Journal of Veterinary Research (대한수의학회지)

The Korean Society of Veterinary Science (대한수의학회)
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Water soluble tomato concentrate regulates platelet function via the mitogen-activated protein kinase pathway

  • Jeong, Dahye (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Irfan, Muhammad (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Saba, Evelyn (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University) ;
  • Kim, Sung-Dae (Research Center, Dongnam Institute of Radiological and Medical Sciences) ;
  • Kim, Seung-Hyung (Institute of Traditional Medicine & Bioscience, Daejeon University) ;
  • Rhee, Man Hee (Department of Veterinary Medicine, College of Veterinary Medicine, Kyungpook National University)
  • Received : 2016.03.10
  • Accepted : 2016.04.05
  • Published : 2016.06.30
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Abstract

Tomato extract has been shown to exert antiplatelet activity in vitro and to change platelet function ex vivo, but with limitations. In this study, antiplatelet activity of water soluble tomato concentrate (Fruitflow I) and dry water soluble tomato concentrate (Fruitflow II) was investigated using rat platelets. Aggregation was induced by collagen and adenosine diphosphate and granule-secretion, $[Ca^{2+}]_i$, thromboxane B2, cyclic adenosine monophosphate (cAMP) and cyclic guanosine monophosphate (cGMP) levels were examined. The activation of integrin ${\alpha}_{IIb}{\beta}_3$ and phosphorylation of signaling molecules, including mitogen-activated protein kinase (MAPK) and PI3K/Akt, were investigated by flow cytometry and immunoblotting, respectively. Prothrombin time (PT) and activated partial thromboplastin time (aPTT) were examined. Moreover, in vivo thrombus weight was tested by an arteriovenous shunt model. Fruitflow I and Fruitflow II significantly inhibited agonist induced platelet aggregation, adenosine triphosphate and serotonin release, $[Ca^{2+}]_i$, and thromboxane B2 concentration, while having no effect on cAMP and cGMP levels. Integrin ${\alpha}_{IIb}{\beta}_3$ activation was also significantly decreased. Moreover, both concentrates reduced phosphorylation of MAPK pathway factors such as ERK, JNK, P38, and PI3K/Akt. In vivo thrombus formation was also inhibited. Taken together, these concentrates have the potential for ethnomedicinal applications to prevent cardiovascular ailments and can be used as functional foods.

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References

  1. Canene-Adams K, Campbell JK, Zaripheh S, Jeffery EH, Erdman JW Jr. The tomato as a functional food. J Nutr 2005, 135, 1226-1230. https://doi.org/10.1093/jn/135.5.1226
  2. Dutta-Roy AK, Crosbie L, Gordon MJ. Effects of tomato extract on human platelet aggregation in vitro. Platelets 2001, 12, 218-227. https://doi.org/10.1080/09537100120058757
  3. Endale M, Lee WM, Kamruzzaman SM, Kim SD, Park JY, Park MH, Park TY, Park HJ, Cho JY, Rhee MH. Ginsenoside-Rp1 inhibits platelet activation and thrombus formation via impaired glycoprotein VI signalling pathway, tyrosine phosphorylation and MAPK activation. Br J Pharmacol 2012, 167, 109-127. https://doi.org/10.1111/j.1476-5381.2012.01967.x
  4. Furman MI, Benoit SE, Barnard MR, Valeri CR, Borbone ML, Becker RC, Hechtman HB, Michelson AD. Increased platelet reactivity and circulating monocyte-platelet aggregates in patients with stable coronary artery disease. J Am Coll Cardiol 1998, 31, 352-358. https://doi.org/10.1016/S0735-1097(98)82170-0
  5. Giovannucci E. Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J Natl Cancer Inst 1999, 91, 317-331. https://doi.org/10.1093/jnci/91.4.317
  6. Hu FB, Rimm EB, Stampfer MJ, Ascherio A, Spiegelman D, Willett WC. Prospective study of major dietary patterns and risk of coronary heart disease in men. Am J Clin Nutr 2000, 72, 912-921. https://doi.org/10.1093/ajcn/72.4.912
  7. Jackson SP. Arterial thrombosis-insidious, unpredictable and deadly. Nat Med 2011, 17, 1423-1436. https://doi.org/10.1038/nm.2515
  8. Jeon BR, Kim SJ, Hong SB, Park HJ, Cho JY, Rhee MH. The inhibitory mechanism of crude saponin fraction from Korean Red Ginseng in collagen-induced platelet aggregation. J Ginseng Res 2015, 39, 279-285. https://doi.org/10.1016/j.jgr.2015.02.001
  9. Kamruzzaman SM, Endale M, Oh WJ, Park SC, Kim KS, Hong JH, Kwak YS, Yun BS, Rhee MH. Inhibitory effects of Bulnesia sarmienti aqueous extract on agonist-induced platelet activation and thrombus formation involves mitogen-activated protein kinases. J Ethnopharmacol 2010, 130, 614-620. https://doi.org/10.1016/j.jep.2010.05.049
  10. Kerver JM, Yang EJ, Bianchi L, Song WO. Dietary patterns associated with risk factors for cardiovascular disease in healthy US adults. Am J Clin Nutr 2003, 78, 1103-1110. https://doi.org/10.1093/ajcn/78.6.1103
  11. Lee HS, Kim SD, Lee WM, Endale M, Kamruzzaman SM, Oh WJ, Cho JY, Kim SK, Cho HJ, Park HJ, Rhee MH. A noble function of BAY 11-7082: inhibition of platelet aggregation mediated by an elevated cAMP-induced VASP, and decreased ERK2/JNK1 phosphorylations. Eur J Pharmacol 2010, 627, 85-91. https://doi.org/10.1016/j.ejphar.2009.11.005
  12. Lhermusier T, Severin S, Van Rothem J, Garcia C, Bertrand-Michel J, Le Faouder P, Hechler B, Broccardo C, Couvert P, Chimini G, Sie P, Payrastre B. ATP-binding cassette transporter 1 (ABCA1) deficiency decreases platelet reactivity and reduces thromboxane A2 production independently of hematopoietic ABCA1. J Thromb Haemost 2016, 14, 585-595. https://doi.org/10.1111/jth.13247
  13. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010, 30, 2341-2349. https://doi.org/10.1161/ATVBAHA.110.207522
  14. Libby P. Coronary artery injury and the biology of atherosclerosis: inflammation, thrombosis, and stabilization. Am J Cardiol 2000, 86 (Suppl 2), 3J-9J.
  15. Mehta SR, Yusuf S; Clopidogrel in Unstable angina to prevent Recurrent Events (CURE) Study Investigators. The Clopidogrel in Unstable angina to prevent Recurrent Events (CURE) trial programme. Rationale, design and baseline characteristics including a meta-analysis of the effects of thienopyridines in vascular disease. Eur Heart J 2000, 21, 2033-2041. https://doi.org/10.1053/euhj.2000.2474
  16. O'Kennedy N, Crosbie L, Whelan S, Luther V, Horgan G, Broom JI, Webb DJ, Duttaroy AK. Effects of tomato extract on platelet function: a double-blinded crossover study in healthy humans. Am J Clin Nutr 2006, 84, 561-569. https://doi.org/10.1093/ajcn/84.3.561
  17. Oh WJ, Endale M, Park SC, Cho JY, Rhee MH. Dual roles of quercetin in platelets: phosphoinositide-3-kinase and MAP kinases inhibition, and cAMP-dependent vasodilatorstimulated phosphoprotein stimulation. Evid Based Complement Alternat Med 2012, 2012, 485262.
  18. Park JY, Ji HD, Jeon BR, Im EJ, Son YM, Lee JY, Lee DH, Lee YC, Hyun E, Jia Q, Hong M, Park HJ, Rhee MH. Chlorin e6 prevents ADP-induced platelet aggregation by decreasing PI3K-Akt phosphorylation and promoting cAMP production. Evid Based Complement Alternat Med 2013, 2013, 569160.
  19. Pearson TA, Blair SN, Daniels SR, Eckel RH, Fair JM, Fortmann SP, Franklin BA, Goldstein LB, Greenland P, Grundy SM, Hong Y, Miller NH, Lauer RM, Ockene IS, Sacco RL, Sallis JF Jr, Smith SC Jr, Stone NJ, Taubert KA. AHA guidelines for primary prevention of cardiovascular disease and stroke: 2002 update. Consensus panel guide to comprehensive risk reduction for adult patients without coronary or other atherosclerotic vascular diseases. Circulation 2002, 106, 388-391. https://doi.org/10.1161/01.CIR.0000020190.45892.75
  20. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 2008, 22, 659-661. https://doi.org/10.1096/fj.07-9574LSF
  21. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circ Res 2007, 100, 1673-1685. https://doi.org/10.1161/01.RES.0000267878.97021.ab
  22. Schaeffer J, Blaustein MP. Platelet free calcium concentrations measured with fura-2 are influenced by the transmembrane sodium gradient. Cell Calcium 1989, 10, 101-113. https://doi.org/10.1016/0143-4160(89)90050-X
  23. Sesso HD, Liu S, Gaziano JM, Buring JE. Dietary lycopene, tomato-based food products and cardiovascular disease in women. J Nutr 2003, 133, 2336-2341. https://doi.org/10.1093/jn/133.7.2336
  24. Shattil SJ, Newman PJ. Integrins: dynamic scaffolds for adhesion and signaling in platelets. Blood 2004, 104, 1606-1615. https://doi.org/10.1182/blood-2004-04-1257
  25. Trip MD, Cats VM, van Capelle FJL, Vreeken J. Platelet hyperreactivity and prognosis in survivors of myocardial infarction. N Engl J Med 1990, 322, 1549-1554. https://doi.org/10.1056/NEJM199005313222201
  26. Umetsu T, Sanai K. Effect of 1-methyl-2-mercapto-5-(3-pyridyl)-imidazole (KC-6141), an anti-aggregating compound, on experimental thrombosis in rats. Thromb Haemost 1978, 39, 74-83. https://doi.org/10.1055/s-0038-1646657
  27. Varga-Szabo D, Pleines I, Nieswandt B. Cell adhesion mechanisms in platelets. Arterioscler Thromb Vasc Biol 2008, 28, 403-412. https://doi.org/10.1161/ATVBAHA.107.150474
  28. Willcox JK, Catignani GL, Lazarus S. Tomatoes and cardiovascular health. Crit Rev Food Sci Nutr 2003, 43, 1-18. https://doi.org/10.1080/10408690390826437
  29. Xu XL, Huang YJ, Chen XF, Lin DY, Zhang W. 2,3,4,5-tetrahydroxystilbene-2-O-$\beta$-D-glucoside inhibits proliferation of vascular smooth muscle cells: involvement of NO/cGMP/PKG pathway. Phytother Res 2012, 26, 1068-1074. https://doi.org/10.1002/ptr.3691

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