Doxorubicin-induced platelet procoagulant activities: An important clue for chemotherapy-associated thrombosis

Toxicological Sciences

Volumn 124, Issue 1, 2011, Pages 215-224

  Kim, Se Hwan ^a   Lim, Kyung Min ^a,b   Noh, Ji Yoon ^a   Kim, Keunyoung ^a   Kang, Seojin ^a   Chang, Youn Kyeong ^a   Shin, Sue ^c   Chung, Jin Ho ^a  

^a Seoul National University   (South Korea)

^b AmorePacific Corporation   (South Korea)

^c Seoul National University Boramae Hospital   (South Korea)

Author keywords

Doxorubicin; Platelets; PS exposure; Thrombosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA TUBULIN; ASCORBIC ACID; BIOLOGICAL MARKER; CALCIUM; CASPASE 3; CASPASE INHIBITOR; CYTOCHROME C; DOXORUBICIN; EGTAZIC ACID; ENZYME; FLIPPASE; PHOSPHATIDYLSERINE; PROCOAGULANT; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; SCRAMBLASE; TROLOX C; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; NORMAL HUMAN; PROTEIN LOCALIZATION; RAT; THROMBOCYTE; THROMBOGENESIS; THROMBOSIS; VEIN THROMBOSIS;

ADOLESCENT; ADULT; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BCL-2-ASSOCIATED X PROTEIN; BLOOD PLATELETS; CASPASE 3; CELLS, CULTURED; CYTOCHROMES C; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; HUMANS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, CONFOCAL; PLATELET ACTIVATION; PLATELET AGGREGATION; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; THROMBOSIS; TIME FACTORS; YOUNG ADULT;

EID: 84155175860     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr222     Document Type: Article

References (54)

1. Bae, O. N., Lim, K. M., Noh, J. Y., Chung, S. M., Kim, H., Lee, C. R., Park, J. D., and Chung, J. H. (2007). Arsenite-enhanced procoagulant activity through phosphatidylserine exposure in platelets. Chem. Res. Toxicol. 20, 1760-1768.
2. Barber, L. A., Palascak, M. B., Joiner, C. H., and Franco, R. S. (2009). Aminophospholipid translocase and phospholipid scramblase activities in sickle erythrocyte subpopulations. Br. J. Haematol. 146, 447-455.
3. Begonja, A. J., Gambaryan, S., Geiger, J., Aktas, B., Pozgajova, M., Nieswandt, B., and Walter, U. (2005). Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbbeta3-integrin activation independent of the NO/cGMP pathway. Blood 106, 2757-2760.
4. Bernat, A., and Herbert, J. M. (1994). Effect of various drugs on adriamycinenhanced venous thrombosis in the rat: importance of PAF. Thromb. Res. 75, 91-97.
5. Berthiaume, J. M., and Wallace, K. B. (2007). Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol. Toxicol. 23, 15-25.
6. Bidot, L., Jy, W., Bidot, C., Jr, Jimenez, J. J., Fontana, V., Horstman, L. L., and Ahn, Y. S. (2008). Microparticle-mediated thrombin generation assay: increased activity in patients with recurrent thrombosis. J. Thromb. Haemost. 6, 913-919.
7. Bonomini, M., Dottori, S., Amoroso, L., Arduini, A., and Sirolli, V. (2004). Increased platelet phosphatidylserine exposure and caspase activation in chronic uremia. J. Thromb. Haemost. 2, 1275-1281.
8. Cantwell, B. M., Mannix, K. A., Roberts, J. T., Ghani, S. E., and Harris, A. L. (1988). Thromboembolic events during combination chemotherapy for germ cell-malignancy. Lancet 2, 1086-1087.
9. Childs, A. C., Phaneuf, S. L., Dirks, A. J., Phillips, T., and Leeuwenburgh, C. (2002). Doxorubicin treatment in vivo causes cytochrome C release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2:Bax ratio. Cancer Res. 62, 4592-4598.
10. Cwikiel, M., Eskilsson, J., Albertsson, M., and Stavenow, L. (1996). The influence of 5-fluorouracil and methotrexate on vascular endothelium. An experimental study using endothelial cells in the culture. Ann. Oncol. 7, 731-737.
11. Forsberg, A. J., Kagan, V. E., and Schroit, A. J. (2004). Thiol oxidation enforces phosphatidylserine externalization in apoptosis-sensitive and -resistant cells through a deltapsim/cytochrome C release-dependent mechanism. Antioxid. Redox Signal. 6, 203-208.
12. Fulda, S., Galluzzi, L., and Kroemer, G. (2010). Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discov. 9, 447-464.
13. Gawaz, M. (2004). Role of platelets in coronary thrombosis and reperfusion of ischemic myocardium. Cardiovasc. Res. 61, 498-511.
14. Gewirtz, D. A. (1999). A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 57, 727-741.
15. Goodnough, L. T., Saito, H., Manni, A., Jones, P. K., and Pearson, O. H. (1984). Increased incidence of thromboembolism in stage IV breast cancer patients treated with a five-drug chemotherapy regimen. A study of 159 patients. Cancer 54, 1264-1268.
16. Greene, R. F., Collins, J. M., Jenkins, J. F., Speyer, J. L., and Myers, C. E. (1983). Plasma pharmacokinetics of adriamycin and adriamycinol: implications for the design of in vitro experiments and treatment protocols. Cancer Res. 43, 3417-3421.
17. Heemskerk, J. W., Bevers, E. M., and Lindhout, T. O. (2002). Platelet activation and blood coagulation. Thromb. Haemost. 88, 186-193.
18. Heemskerk, J. W., Willems, G. M., Rook, M. B., and Sage, S. O. (2001). Ragged spiking of free calcium in ADP-stimulated human platelets: regulation of puff-like calcium signals in vitro and ex vivo. J. Physiol. 535, 625-635.
19. Hilarius, P. M., Ebbing, I. G., Dekkers, D. W., Lagerberg, J. W., de Korte, D., and Verhoeven, A. J. (2004). Generation of singlet oxygen induces phospholipid scrambling in human erythrocytes. Biochemistry 43, 4012-4019.
20. Hugel, B., Martínez, M. C., Kunzelmann, C., and Freyssinet, J. M. (2005). Membrane microparticles: two sides of the coin. Physiology (Bethesda) 20, 22-27.
21. Kotamraju, S., Chitambar, C. R., Kalivendi, S. V., Joseph, J., and Kalyanaraman, B. (2002). Transferrin receptor-dependent iron uptake is responsible for doxorubicin-mediated apoptosis in endothelial cells: role of oxidant-induced iron signaling in apoptosis. J. Biol. Chem. 277, 17179-17187.
22. Kumar, R., Beguin, S., and Hemker, C. (1994). The influence of fibrinogen and fibrin on thrombin generation-evidence for feedback activation of the clotting system by clot bound thrombin. Thromb. Haemost. 72, 713-721.
23. Lee, J. Y., Lee, M. Y., Chung, S. M., and Chung, J. H. (1998). Chemically induced platelet lysis causes vasoconstriction by release of serotonin. Toxicol. Appl. Pharmacol. 149, 235-242.
24. Lee, M. Y., Bae, O. N., Chung, S. M., Kang, K. T., Lee, J. Y., and Chung, J. H. (2002). Enhancement of platelet aggregation and thrombus formation by arsenic in drinking water: a contributing factor to cardiovascular disease. Toxicol. Appl. Pharmacol. 179, 83-88.
25. Lentz, B. R. (2003). Exposure of platelet membrane phosphatidylserine regulates blood coagulation. Prog. Lipid. Res. 42, 423-438.
26. Levine, M. N., Gent, M., Hirsh, J., Arnold, A., Goodyear, M. D., Hryniuk, W., and De Pauw, S. (1988). The thrombogenic effect of anticancer drug therapy in women with stage II breast cancer. N. Engl. J. Med. 318, 404-407.
27. Libourel, E. J., Sonneveld, P., van der Holt, B., de Maat, M. P., and Leebeek, F. W. (2010). High incidence of arterial thrombosis in young patients treated for multiple myeloma: results of a prospective cohort study. Blood 116, 22-26.
28. Lin, K. H., Hsiao, G., Shih, C. M., Chou, D. S., and Sheu, J. R. (2009). Mechanisms of resveratrol-induced platelet apoptosis. Cardiovasc. Res. 83, 575-585.
29. Lokich, J. J., Zipoli, T. E., Moore, C., Sonneborn, H., Paul, S., and Greene, R. (1986). Doxorubicin/vinblastine and doxorubicin/cyclophosphamide combination chemotherapy by continuous infusion. Cancer 58, 1020-1023.
30. Mallat, Z., Benamer, H., Hugel, B., Benessiano, J., Steg, P. G., Freyssinet, J. M., and Tedgui, A. (2000). Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation 101, 841-843.
31. Orrenius, S., Nicotera, P., and Zhivotovsky, B. (2011). Cell death mechanisms and their implications in toxicology. Toxicol. Sci. 19, 3-19.
32. Pai, V. B., and Nahata, M. C. (2000). Cardiotoxicity of chemotherapeutic agents: incidence, treatment and prevention. Drug Saf. 22, 263-302.
33. Paredes, N., Xu, L., Berry, L. R., and Chan, A. K. (2003). The effects of chemotherapeutic agents on the regulation of thrombin on cell surfaces. Br. J. Haematol. 120, 315-324.
34. Prandoni, P., Falanga, A., and Piccioli, A. (2005). Cancer and venous thromboembolism. Lancet Oncol. 6, 401-410.
35. Robert, J., Vrignaud, P., Nguyen-Ngoc, T., Iliadis, A., Mauriac, L., and Hurteloup, P. (1985). Comparative pharmacokinetics and metabolism of doxorubicin and epirubicin in patients with metastatic breast cancer. Cancer Treat. Rep. 69, 633-640.
36. Rogers, J. S., II, Murgo, A. J., Fontana, J. A., and Raich, P. C. (1988). Chemotherapy for breast cancer decreases plasma protein C and protein S. J. Clin. Oncol. 6, 276-281.
37. Ruggeri, Z. M. (2002). Platelets in atherothrombosis. Nat. Med. 8, 1227-1234.
38. Santos, D. L., Moreno, A. J., Leino, R. L., Froberg, M. K., and Wallace, K. B. (2002). Carvedilol protects against doxorubicin-induced mitochondrial cardiomyopathy. Toxicol. Appl. Pharmacol. 185, 218-227.
39. Schoenwaelder, S. M., Yuan, Y., Josefsson, E. C., White, M. J., Yao, Y., Mason, K. D., O'Reilly, L. A., Henley, K. J., Ono, A., Hsiao, S., et al. (2009). Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 114, 663-666.
40. Siljander, P., Farndale, R. W., Feijge, M. A., Comfurius, P., Kos, S., Bevers, E. M., and Heemskerk, J. W. (2001). Platelet adhesion enhances the glycoprotein VI-dependent procoagulant response: involvement of p38 MAP kinase and calpain. Arterioscler. Thromb. Vasc. Biol. 21, 618-627.
41. Singal, P. K., and Iliskovic, N. (1998). Doxorubicin-induced cardiomyopathy. N. Engl. J. Med. 339, 900-905.
42. Sousou, T., and Khorana, A. A. (2009). New insights into cancer-associated thrombosis. Arterioscler. Thromb. Vasc. Biol. 29, 316-320.
43. Strumberg, D., Brugge, S., Korn, M. W., Koeppen, S., Ranft, J., Scheiber, G., Reiners, C., Mockel, C., Seeber, S., and Scheulen, M. E. (2002). Evaluation of long-term toxicity in patients after cisplatin-based chemotherapy for nonseminomatous testicular cancer. Ann. Oncol. 13, 229-236.
44. Swystun, L. L., Shin, L. Y., Beaudin, S., and Liaw, P. C. (2009). Chemotherapeutic agents doxorubicin and epirubicin induce a procoagulant phenotype on endothelial cells and blood monocytes. J. Thromb. Haemost. 7, 619-626.
45. Takemura, G., and Fujiwara, H. (2007). Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog. Cardiovasc. Dis. 49, 330-352.
46. Togna, G. I., Togna, A. R., Franconi, M., and Caprino, L. (2000). Cisplatin triggers platelet activation. Thromb. Res. 99, 503-509.
47. Vidal, C., Spaulding, C., Picard, F., Schaison, F., Melle, J., Weber, S., and Fontenay-Roupie, M. (2001). Flow cytometry detection of platelet procoagulation activity and microparticles in patients with unstable angina treated by percutaneous coronary angioplasty and stent implantation. Thromb. Haemost. 86, 784-790.
48. Walsh, J., Wheeler, H. R., and Geczy, C. L. (1992). Modulation of tissue factor on human monocytes by cisplatin and adriamycin. Br. J. Haematol. 81, 480-488.
49. Wang, X., Smith, P. L., Hsu, M. Y., Ogletree, M. L., and Schumacher, W. A. (2006). Murine model of ferric chloride-induced vena cava thrombosis: evidence for effect of potato carboxypeptidase inhibitor. J. Thromb. Haemost. 4, 403-410.
50. Weijl, N. I., Rutten, M. F., Zwinderman, A. H., Keizer, H. J., Nooy, M. A., Rosendaal, F. R., Cleton, F. J., and Osanto, S. (2000). Thromboembolic events during chemotherapy for germ cell cancer: a cohort study and review of the literature. J. Clin. Oncol. 18, 2169-2178.
51. Zangari, M., Siegel, E., Barlogie, B., Anaissie, E., Saghafifar, F., Fassas, A., Morris, C., Fink, L., and Tricot, G. (2002). Thrombogenic activity of doxorubicin in myeloma patients receiving thalidomide: implications for therapy. Blood 100, 1168-1171.
52. Zhou, S., Heller, L. J., and Wallace, K. B. (2001a). Interference with calciumdependent mitochondrial bioenergetics in cardiac myocytes isolated from doxorubicin-treated rats. Toxicol. Appl. Pharmacol. 175, 60-67.
53. Zhou, S., Starkov, A., Froberg, M. K., Leino, R. L., and Wallace, K. B. (2001b). Cumulative and irreversible cardiac mitochondrial dysfunction induced by doxorubicin. Cancer Res. 61, 771-777.
54. Zwaal, R. F., Comfurius, P., and Bevers, E. M. (2005). Surface exposure of phosphatidylserine in pathological cells. Cell. Mol. Life Sci. 62, 971-988.