Tamoxifen promotes superoxide production in platelets by activation of PI3-Kinase and NADPH oxidase pathways

Thrombosis Research

Volumn 129, Issue 1, 2012, Pages 36-42

  Shah, Vidhi P ^a   Chegini, Hesum A ^a   Vishneski, Susan R ^a   Weatherman, Ross V ^b   Blackmore, Peter F ^a   Dobrydneva, Yuliya ^a  

^a EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^b ROSE HULMAN INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Apocynin; Calcium influx; Phosphoinositide 3 kinase; Platelets; Reactive oxygen species; Tamoxifen

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 2,2,6,6 TETRAMETHYLPIPERIDINE 1 OXYL; ADENOSINE DIPHOSPHATE; AFIMOXIFENE; ANTIOXIDANT; APOCYNIN; CALCIUM ION; DIMER; ESTROGEN RECEPTOR; FURA 2; LUCIGENIN; PHOSPHATIDYLINOSITOL 3 KINASE; PIPERIDINE DERIVATIVE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TAMOXIFEN; TEMPOL; THROMBIN; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; THROMBOCYTE;

BLOOD PLATELETS; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; ENZYME INHIBITORS; ESTROGEN ANTAGONISTS; FEMALE; FREE RADICAL SCAVENGERS; HUMANS; MALE; NADPH OXIDASE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOLIPASE C GAMMA; SARCOPLASMIC RETICULUM; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SUPEROXIDES; TAMOXIFEN; TIME FACTORS; UP-REGULATION;

EID: 84855193225     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2011.08.010     Document Type: Article

References (66)

1. V.C. Jordan Tamoxifen: a most unlikely pioneering medicine Nat Rev Drug Discov 2 2003 205 213 (Pubitemid 37361665)
2. B. Fisher, J.P. Costantino, D.L. Wickerham, C.K. Redmon, M. Kavanah, and W.M. Cronin Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study J Natl Cancer Inst 90 1998 1371 1388 (Pubitemid 28439961)
3. M. Cushman, J.P. Costantino, E.G. Bovill, D.L. Wickerham, L. Buckley, and J.D. Roberts Effect of tamoxifen on venous thrombosis risk factors in women without cancer: the Breast Cancer Prevention Trial Br J Haematol 120 2003 109 116 (Pubitemid 36056917)
4. I.C. Weitz, V.K. Israel, and H.A. Liebman Tamoxifen-associated venous thrombosis and activated protein C resistance due to factor V Leiden Cancer 79 1997 2024 2027 (Pubitemid 27200388)
5. J.E. Garber, S. Halabi, S.M. Tolaney, E. Kaplan, L. Archer, and J.N. Atkins Factor V Leiden and thromboembolism risk in women receiving adjuvant tamoxifen for breast cancer J Natl Cancer Inst 102 2010 942 949
6. C. Duggan, K. Marriott, R. Edwards, and J. Cuzick Inherited and acquired risk factors for venous thromboembolic disease among women taking tamoxifen to prevent breast cancer J Clin Oncol 21 2003 3588 3593 (Pubitemid 46594050)
7. N. Abramson, J.P. Costantino, J.E. Garber, N. Berliner, D.L. Wickerham, and N. Wolmark Effect of Factor V Leiden and prothrombin G20210 → A mutations on thromboembolic risk in the national surgical adjuvant breast and bowel project breast cancer prevention trial J Natl Cancer Inst 98 2006 904 910 (Pubitemid 44018920)
8. P.A. Kyrle, G. Hron, S. Eichinger, and O. Wagner Circulating P-selectin and the risk of recurrent venous thromboembolism Thromb Haemost 97 2007 880 883 (Pubitemid 46939199)
9. J. Polgar, J. Matuskova, and D.D. Wagner The P-selectin, tissue factor, coagulation triad J Thromb Haemost 3 2005 1590 1596 (Pubitemid 41716543)
10. J.A. Chirinos, G.A. Heresi, H. Velasquez, W. Jy, J.J. Jimenez, and E. Ahn Elevation of endothelial microparticles, platelets, and leukocyte activation in patients with venous thromboembolism J Am Coll Cardiol 45 2005 1467 1471 (Pubitemid 40615620)
11. S.O. Sage The Wellcome Prize Lecture. Calcium entry mechanisms in human platelets Exp Physiol 82 1997 807 823 (Pubitemid 127469191)
12. S.M. Hourani, and N.J. Cusack Pharmacological receptors on blood platelets Pharmacol Rev 43 1991 243 298
13. D. Varga-Szabo, A. Braun, and B. Nieswandt Calcium signaling in platelets J Thromb Haemost 7 2009 1057 1066
14. F. Krötz, H.Y. Sohn, and U. Pohl Reactive oxygen species: players in the platelet game Arterioscler Thromb Vasc Biol 24 2004 1988 1996 (Pubitemid 39482420)
15. S. Chlopicki, R. Olszanecki, M. Janiszewski, F.R. Laurindo, T. Panz, and J. Miedzobrodzki Functional role of NADPH oxidase in activation of platelets Antioxid Redox Signal 6 2004 691 698 (Pubitemid 38890785)
16. T. Seno, N. Inoue, D. Gao, M. Okuda, Y. Sumi, and K. Matsui Involvement of NADH/NADPH oxidase in human platelet ROS production Thromb Res 103 2001 399 409 (Pubitemid 32831474)
17. F. Krötz, H.Y. Sohn, T. Gloe, S. Zahler, T. Riexinger, and T.M. Schiele NAD(P)H oxidase-dependent platelet superoxide anion release increases platelet recruitment Blood 100 2002 917 924 (Pubitemid 34832618)
18. T.K. Sato, M. Overduin, and S.D. Emr Location, location, location: membrane targeting directed by PX domains Science 294 2007 1881 1885
19. P.T. Hawkins, K. Davidson, and L.R. Stephens The role of PI3ks in the regulation of the neutrophil NADPH oxidase Biochem Soc Symp 74 2007 59 67
20. A.J. Begonja, S. Gambaryan, J. Geiger, B. Aktas, M. Pozgajova, and B. Nieswandt Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbbeta3-integrin activation independent of the NO/cGMP pathway Blood 106 2005 2757 2760 (Pubitemid 41510751)
21. J.I. Kourie Interaction of reactive oxygen species with ion transport mechanisms Am J Physiol 275 1998 C1 C24
22. P. Waring Redox active calcium ion channels and cell death Arch Biochem Biophys 434 2005 33 42 (Pubitemid 40040468)
23. 2+ mobilization and aggregation in platelets from type 2 diabetic patients Biochem Biophys Res Commun 333 2005 794 802 (Pubitemid 40854229)
24. J. Stefanska, and R. Pawliczak Apocynin: Molecular Aptitudes Mediators Inflamm 106507 2008 1 10
25. V.F. Ximenes, M.P. Kanegae, S.R. Rissato, and M.S. Galhiane The oxidation of apocynin catalyzed by myeloperoxidase: proposal for NADPH oxidase inhibition Arch Biochem Biophys 457 2007 134 141 (Pubitemid 46048700)
26. Y.S. Lee, Y.S. Kang, S.H. Lee, and J.A. Kim Role of NAD(P)H oxidase in the tamoxifen-induced generation of reactive oxygen species and apoptosis in HepG2 human hepatoblastoma cells Cell Death Differ 7 2000 925 932
27. A. Kallio, A. Zheng, J. Dahllund, K.M. Heiskanen, and P. Härkönen Role of mitochondria in tamoxifen-induced rapid death of MCF-7 breast cancer cells Apoptosis 10 2005 1395 1410 (Pubitemid 43117684)
28. O. Vitseva, D.A. Flockhart, Y. Jin, S. Varghese, and J.E. Freedman The effects of tamoxifen and its metabolites on platelet function and release of reactive oxygen intermediates J Pharmacol Exp Ther 312 2005 1144 1150 (Pubitemid 40293775)
29. Y. Dobrydneva, R.V. Weatherman, J.P. Trebley, M.M. Morrell, M.C. Fitzgerald, and C.E. Fichandler Tamoxifen stimulates calcium entry into human platelets J Cardiovasc Pharmacol 50 2007 380 390 (Pubitemid 350303815)
30. A. Pedram, M. Razandi, M. Aitkenhead, C.C. Hughes, and E.R. Levin Integration of the non-genomic and genomic actions of estrogen. Membrane-initiated signaling by steroid to transcription and cell biology J Biol Chem 277 2002 50768 50775 (Pubitemid 36042240)
31. 2+ channels Eur J Pharmacol 445 2002 257 266 (Pubitemid 34655683)
32. G.M. Dick, C.F. Rossow, S. Smirnov, B. Horowitz, and K.M. Sanders Tamoxifen activates smooth muscle BK channels through the regulatory beta 1 subunit J Biol Chem 276 2001 34594 34599
33. M.L. Dodds, M.E. Kargacin, and G.J. Kargacin Effects of anti-oestrogens and beta-estradiol on calcium uptake by cardiac sarcoplasmic reticulum Br J Pharmacol 132 2001 1374 1382 (Pubitemid 32281024)
34. 2+ influx in the mechanism of tamoxifen-induced apoptosis in HepG2 human hepatoblastoma cells Cancer Lett 147 1999 115 123
35. P. Lehenkari, V. Parikka, T.J. Rautiala, M. Weckström, J. Dahllund, and P.L. Härkönen The effects of tamoxifen and toremifene on bone cells involve changes in plasma membrane ion conductance J Bone Miner Res 18 2002 473 481 (Pubitemid 36241064)
36. Y.Y. Chao, C.R. Jan, Y.C. Ko, J.J. Chen, B.P. Jiann, and Y.C. Lu Effect of lignans isolated from Hernandia nymphaeifolia on estrogenic compounds-induced calcium mobilization in human neutrophils Life Sci 70 2002 3109 3121 (Pubitemid 34467002)
37. 2+ levels in human breast cancer cells Breast Cancer Res Treat 71 2002 125 131
38. G. Delogu, M.A. Dettori, A. Patti, S. Pedotti, A. Forni, and G. Casalone Stereoselective oxazaborolidine-borane reduction of biphenyl alkyl diketones-lignin models: enantiopure dehydrodiapocynol derivatives Tetrahedron-Asymmetry 14 2003 2467 2474 (Pubitemid 36959917)
39. Y. Dobrydneva, and P.F. Blackmore 2-Aminoethoxydiphenyl borate directly inhibits store-operated calcium entry channels in human platelets Mol Pharm 60 2001 541 552 (Pubitemid 32781562)
40. Y. Dobrydneva, C.J. Abelt, B. Dovel, C.M. Thadigiri, R.L. Williams, and P.F. Blackmore 2-Aminoethoxydiphenyl borate as a prototype drug for a group of structurally related calcium channel blockers in human platelets Mol Pharm 69 2006 247 256 (Pubitemid 43048911)
41. A. Howell, C.K. Osborne, C. Morris, and A.E. Wakeling ICI 182,780 (Faslodex): development of a novel, "pure" antiestrogen Cancer 89 2000 817 825 (Pubitemid 30658581)
42. B.J. Furr, and V.C. Jordan The pharmacology and clinical uses of tamoxifen Pharmacol Ther 25 1984 127 205 (Pubitemid 14015738)
43. S. Heumüller, S. Wind, E. Barbosa-Sicard, H.H. Schmidt, R. Busse, and K. Schröder Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant Hypertension 51 2008 211 217 (Pubitemid 351159930)
44. B. Wachowicz, B. Olas, H.M. Zbikowska, and A. Buczynski Generation of reactive oxygen species in blood platelets Platelets 13 2002 175 182 (Pubitemid 34638923)
45. P. Clutton, A. Miermont, and J.E. Freedman Regulation of endogenous reactive oxygen species in platelets can reverse aggregation Arterioscler Thromb Vasc Biol 24 2004 167 192
46. S. Reineri, A. Bertoni, E. Sanna, S. Baldassarri, C. Sarasso, and M. Zanfa Membrane lipid rafts coordinate estrogen-dependent signaling in human platelets Biochem Biophys Acta 1773 2007 273 278 (Pubitemid 46123621)
47. Watson CS, Gametchu B. Proteins of multiple classes may participate in nongenomic steroid action. Exp Biol Med (Maywood) 2003;228:1272-81. (Pubitemid 37549232)
48. E.R. Levin Rapid signaling by steroid receptors Am J Physiol Regul Integr Comp Physiol 295 2008 R1425 R1430
49. M. Wehling, and R. Lösel Non-genomic steroid hormone effects: membrane or intracellular receptors? J Steroid Biochem Mol Biol 102 2006 180 183 (Pubitemid 44781186)
50. Y. Dobrydneva, R.L. Williams, and P.F. Blackmore Diethylstilbestrol and other nonsteroidal estrogens; novel class of store-operated calcium channel modulators J Cardiovasc Pharmacol 55 2010 522 530
51. Y. Dobrydneva, R.L. Williams, J.A. Katzenellenbogen, P.H. Ratz, and P.F. Blackmore Diethylstilbestrol and tetrahydrochrysenes are calcium channel blockers in human platelets: relationship to the stilbene pharmacophore Thromb Res 110 2003 23 31 (Pubitemid 36859851)
52. 2+ influx Mol Pharmacol 66 2004 702 707 (Pubitemid 39329270)
53. K.R. Gibson, I.L. Neilson, F. Barrett, T.J. Winterburn, S. Sharma, and S.M. MacRury Evaluation of the antioxidant properties of N-acetylcysteine in human platelets: prerequisite for bioconversion to glutathione for antioxidant and antiplatelet activity J Cardiovasc Pharmacol 54 2009 319 326
54. 2+ mobilization in human platelets through sulfhydryl oxidation dependent and independent mechanisms Biochem Pharmacol 67 2004 491 502 (Pubitemid 38232889)
55. Y. Yan, C. Wei, W. Zhang, H. Cheng, and J. Liu Cross-talk between calcium and reactive oxygen species signaling Acta Pharmacol Sin 27 2006 821 826 (Pubitemid 44366014)
56. J.A. Rosado, P.C. Redondo, G.M. Salido, E. Gomez-Arteta, and S.O. Sage Hydrogen peroxide generation induces pp 60src activation in human platelets: evidence for the involvement of this pathway in store-mediated calcium entry J Biol Chem 279 2004 1665 1675 (Pubitemid 38084433)
57. W.M. Nauseef How human neutrophils kill and degrade microbes: an integrated view Immunol Rev 219 2007 88 102 (Pubitemid 47390004)
58. S.P. Watson, J.M. Auger, O.J.T. McCarty, and A.C. Pearce GPVI and integrin αIIbβ3 signaling in platelets J Thromb Haemost 3 2005 1752 1762 (Pubitemid 41716562)
59. I. Canobbio, C. Balduini, and M. Torti Signalling through the platelet glycoprotein Ib-V-IX complex Cell Signal 16 2004 1329 1344 (Pubitemid 39277499)
60. Y.I. Chang, J.J. Lee, W.F. Chen, D.S. Chou, S.Y. Huang, and J.R. Sheu A novel role for tamoxifen in the inhibition of human platelets Transl Res 157 2011 81 91
61. J. Hirsh, S.S. Anand, J.L. Halperin, and V. Fuster Guide to anticoagulant therapy: heparin. A statement for healthcare professionals from the American heart association Circulation 103 2001 2994 3018 (Pubitemid 32578141)
62. M.C. Trappenburg, M. van Schilgaarde, E.O. Bredewold, M. van Aalderen, H.M.H. Spronk, ten Cate Hugo, A. Leyte, and W.E. Terpstra Elevated numbers and altered subsets of procoagulant microparticles in breast cancer patients using endocrine therapy Thromb Res 127 2011 363 369
63. O. Morel, L. Jesel, J.-M. Freyssinet, and F. Toti Cellular mechanisms underylying the formation of circulating microparticles Arterioscler Thromb Vasc Biol 31 2011 15 26
64. 2+ entry Nat Cell Biol 11 2009 669 677
65. CRAC by hydrogen peroxide Cell Calcium 48 2010 1 9
66. M. Trebak, R. Ginnan, H.A. Singer, and D. Jourd'heuil Interplay between calcium and reactive oxygen/nitrogen species: an essential paradigm for vascular smooth muscle signaling Antioxid Redox Signal 12 2010 657 674