Cardiotoxicity of the anticancer therapeutic agent bortezomib

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2658-2668

  Nowis, Dominika ^a   Ma̧czewski, Michał ^b   Mackiewicz, Urszula ^b   Kujawa, Marek ^a   Ratajska, Anna ^a   Wieckowski, Mariusz R ^c   Wilczyński, Grzegorz M ^c   Malinowska, Monika ^c   Bil, Jacek ^a   Salwa, Paweł ^a   Bugajski, Marek ^a   Wójcik, Cezary ^d   Siński, Maciej ^b   Abramczyk, Piotr ^b   Winiarska, Magdalena ^a   Da̧browska Iwanicka, Anna ^e   Duszyński, Jerzy ^c   Jakóbisiak, Marek ^a   Golab, Jakub ^a,f  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b MEDICAL UNIVERSITY OF WARSAW   (Poland)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^d Indiana University School of Medicine Evansville   (United States)

^e INSTITUTE OF ONCOLOGY   (Poland)

^f INSTITUTE OF PHYSICAL CHEMISTRY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; CARBOBENZOXYL ISOLEUCYLGLUTAMIC ACID (O TERT BUTYL)ALANINE LEUCINAL; DASATINIB; EPOXOMYCIN; IMATINIB; PROTEASOME INHIBITOR; SORAFENIB; SUNITINIB; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BORONIC ACID DERIVATIVE; PROTEINASE INHIBITOR; PYRAZINE DERIVATIVE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BREATHING; CALCIUM TRANSPORT; CANCER CHEMOTHERAPY; CARDIOTOXICITY; CELL SURVIVAL; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DRUG EFFECT; ECHOCARDIOGRAPHY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM STRESS; FEMALE; HEART FUNCTION; HEART LEFT VENTRICLE CONTRACTILITY; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE FUNCTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; POLAROGRAPHY; PRIORITY JOURNAL; RAT; ANIMAL; C57BL MOUSE; CELL LINE; CELL RESPIRATION; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; HEART; HEART DISEASE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXICITY; WISTAR RAT;

ANIMALS; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; CELL LINE; CELL RESPIRATION; ECHOCARDIOGRAPHY; FEMALE; HEART; HEART DISEASES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; PROTEASE INHIBITORS; PYRAZINES; RATS; RATS, WISTAR; VENTRICULAR DYSFUNCTION, LEFT;

EID: 77953217057     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090690     Document Type: Article

References (42)

1. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M, Baselga J, Norton L: Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001, 344:783-792
2. Kerkela R, Grazette L, Yacobi R, Iliescu C, Patten R, Beahm C, Walters B, Shevtsov S, Pesant S, Clubb FJ, Rosenzweig A, Salomon RN, Van Etten RA, Alroy J, Durand JB, Force T: Cardiotoxicity of the cancer therapeutic agent imatinib mesylate. Nat Med 2006, 12:908-916
3. Mego M, Reckova M, Obertova J, Sycova-Mila Z, Brozmanova K, Mardiak J: Increased cardiotoxicity of sorafenib in sunitinib-pretreated patients with metastatic renal cell carcinoma. Ann Oncol 2007, 18:1906-1907
4. Schmidinger M, Zielinski CC, Vogl UM, Bojic A, Bojic M, Schukro C, Ruhsam M, Hejna M, Schmidinger H: Cardiac toxicity of sunitinib and sorafenib in patients with metastatic renal cell carcinoma. J Clin Oncol 2008, 26:5204-5212
5. Aghajanian C, Soignet S, Dizon DS, Pien CS, Adams J, Elliott PJ, Sabbatini P, Miller V, Hensley ML, Pezzulli S, Canales C, Daud A, Spriggs DR: A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin Cancer Res 2002, 8:2505-2511 (Pubitemid 34856332)
6. Argyriou AA, Iconomou G, Kalofonos HP: Bortezomib-induced peripheral neuropathy in multiple myeloma: a comprehensive review of the literature. Blood 2008, 112:1593-1599
7. Voortman J, Giaccone G: Severe reversible cardiac failure after bortezomib treatment combined with chemotherapy in a non-small cell lung cancer patient: a case report. BMC Cancer 2006, 6:129
8. Orciuolo E, Buda G, Cecconi N, Galimberti S, Versari D, Cervetti G, Salvetti A, Petrini M: Unexpected cardiotoxicity in haematological bortezomib-treated patients. Br J Haematol 2007, 138:396-397
9. Hacihanefioglu A, Tarkun P, Gonullu E: Acute severe cardiac failure in a myeloma patient due to proteasome inhibitor bortezomib. Int J Hematol 2008, 88:219-222
10. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728
11. Schaller H, Letko G, Kunz W: Influence of Mg2+-ions on the properties of rat heart mitochondria in dependence on the preparation. Acta Biol Med Ger 1978, 37:31-38 (Pubitemid 9102466)
12. Nowis D, Legat M, Grzela T, Niderla J, Wilczek E, Wilczynski GM, Glodkowska E, Mrowka P, Issat T, Dulak J, Jozkowicz A, Was H, Adamek M, Wrzosek A, Nazarewski S, Makowski M, Stoklosa T, Jakobisiak M, Golab J: Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity. Oncogene 2006, 25:3365-3374
13. Mackiewicz U, Emanuel K, Lewartowski B: Voltage dependent activation of tonic contraction in cardiac myocytes. J Physiol Pharmacol 2003, 54:409-421 (Pubitemid 37169005)
14. Spurgeon HA, Stern MD, Baartz G, Raffaeli S, Hansford RG, Talo A, Lakatta EG, Capogrossi MC: Simultaneous measurement of Ca2+, contraction, and potential in cardiac myocytes. Am J Physiol 1990, 258:H574-586
15. Choi HS, Eisner DA: The role of sarcolemmal Ca2+-ATPase in the regulation of resting calcium concentration in rat ventricular myocytes. J Physiol 1999, 515 (Pt 1):109-118
16. Leveque D, Carvalho MC, Maloisel F: Review. Clinical pharmacokinetics of bortezomib. In Vivo 2007, 21:273-278
17. Fribley A, Zeng Q, Wang CY: Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol Cell Biol 2004, 24:9695-9704
18. Tannous P, Zhu H, Nemchenko A, Berry JM, Johnstone JL, Shelton JM, Miller FJ, Jr., Rothermel BA, Hill JA: Intracellular protein aggregation is a proximal trigger of cardiomyocyte autophagy. Circulation 2008, 117:3070-3078
19. Will Y, Dykens JA, Nadanaciva S, Hirakawa B, Jamieson J, Marroquin LD, Hynes J, Patyna S, Jessen BA: Effect of the multitargeted tyrosine kinase inhibitors imatinib, dasatinib, sunitinib, and sorafenib on mitochondrial function in isolated rat heart mitochondria and H9c2 cells. Toxicol Sci 2008, 106:153-161
20. Hemeryck A, Geerts R, Monbaliu J, Hassler S, Verhaeghe T, Diels L, Verluyten W, van Beijsterveldt L, Mamidi RN, Janssen C, De Coster R: Tissue distribution and depletion kinetics of bortezomib and bortezomib-related radioactivity in male rats after single and repeated intravenous injection of 14 C-bortezomib. Cancer Chemother Pharmacol 2007, 60:777-787
21. Drexler HC, Risau W, Konerding MA: Inhibition of proteasome function induces programmed cell death in proliferating endothelial cells. FASEB J 2000, 14:65-77 (Pubitemid 30051524)
22. Curran MP, McKeage K: Bortezomib: a review of its use in patients with multiple myeloma. Drugs 2009, 69:859-888
23. Orlowski RZ, Nagler A, Sonneveld P, Blade J, Hajek R, Spencer A, San Miguel J, Robak T, Dmoszynska A, Horvath N, Spicka I, Sutherland HJ, Suvorov AN, Zhuang SH, Parekh T, Xiu L, Yuan Z, Rackoff W, Harousseau JL: Randomized phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J Clin Oncol 2007, 25:3892-3901
24. Grazette LP, Boecker W, Matsui T, Semigran M, Force TL, Hajjar RJ, Rosenzweig A: Inhibition of ErbB2 causes mitochondrial dysfunction in cardiomyocytes: implications for herceptin-induced cardiomyopathy. J Am Coll Cardiol 2004, 44:2231-2238
25. Berthiaume JM, Wallace KB: Adriamycin-induced oxidative mitochondrial cardiotoxicity. Cell Biol Toxicol 2007, 23:15-25
26. Neutzner A, Youle RJ, Karbowski M: Outer mitochondrial membrane protein degradation by the proteasome. Novartis Found Symp 2007, 287:4-14; discussion 14-20
27. Giorgio M, Trinei M, Migliaccio E, Pelicci PG: Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nature Rev Mol Cell Biol 2007, 8:722-728
28. Kawamura K, Kashii C, Imamura K: Ultrastructural changes in hypertrophied myocardium of spontaneously hypertensive rats. Jpn Circ J 1976, 40:1119-1145 (Pubitemid 8010999)
29. Kobayashi M, Kawamura K, Honma M, Masuda H, Suzuki Y, Hasegawa H: Tunnel capillaries of cardiac myocyte in pressure-overloaded rat heart-an ultrastructural three-dimensional study. Microvasc Res 1999, 57:258-272
30. Henninger N, Sicard KM, Bouley J, Fisher M, Stagliano NE: The proteasome inhibitor VELCADE reduces infarction in rat models of focal cerebral ischemia. Neurosci Lett 2006, 398:300-305
31. Sunwoo JB, Chen Z, Dong G, Yeh N, Crowl Bancroft C, Sausville E, Adams J, Elliott P, Van Waes C: Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 2001, 7:1419-1428 (Pubitemid 32708698)
32. Olson H, Betton G, Robinson D, Thomas K, Monro A, Kolaja G, Lilly P, Sanders J, Sipes G, Bracken W, Dorato M, Van Deun K, Smith P, Berger B, Heller A: Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 2000, 32:56-67
33. Meiners S, Dreger H, Fechner M, Bieler S, Rother W, Gunther C, Baumann G, Stangl V, Stangl K: Suppression of cardiomyocyte hypertrophy by inhibition of the ubiquitin-proteasome system. Hypertension 2008, 51:302-308
34. Luss H, Schmitz W, Neumann J: A proteasome inhibitor confers cardioprotection. Cardiovasc Res 2002, 54:140-151
35. Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, Polyakova V, Bauer EP, Klovekorn WP, Schaper J: Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 2003, 107:984-991
36. Birks EJ, Latif N, Enesa K, Folkvang T, Luong le A, Sarathchandra P, Khan M, Ovaa H, Terracciano CM, Barton PJ, Yacoub MH, Evans PC: Elevated p53 expression is associated with dysregulation of the ubiquitin-proteasome system in dilated cardiomyopathy. Cardiovasc Res 2008, 79:472-480
37. Tsukamoto O, Minamino T, Okada K, Shintani Y, Takashima S, Kato H, Liao Y, Okazaki H, Asai M, Hirata A, Fujita M, Asano Y, Yamazaki S, Asanuma H, Hori M, Kitakaze M: Depression of proteasome activities during the progression of cardiac dysfunction in pressure-overloaded heart of mice. Biochem Biophys Res Commun 2006, 340:1125-1133
38. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsukamoto O, Takashima S, Hirata A, Fujita M, Nagamachi Y, Nakatani T, Yutani C, Ozawa K, Ogawa S, Tomoike H, Hori M, Kitakaze M: Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 2004, 110:705-712
39. Bulteau AL, Lundberg KC, Humphries KM, Sadek HA, Szweda PA, Friguet B, Szweda LI: Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem 2001, 276:30057-30063
40. Divald A, Powell SR: Proteasome mediates removal of proteins oxidized during myocardial ischemia. Free Radic Biol Med 2006, 40:156-164
41. Fu HY, Minamino T, Tsukamoto O, Sawada T, Asai M, Kato H, Asano Y, Fujita M, Takashima S, Hori M, Kitakaze M: Overexpression of endoplasmic reticulum-resident chaperone attenuates cardiomyocyte death induced by proteasome inhibition. Cardiovasc Res 2008, 79:600-610
42. Palumbo A, Gay F, Bringhen S, Falcone A, Pescosta N, Callea V, Caravita T, Morabito F, Magarotto V, Ruggeri M, Avonto I, Musto P, Cascavilla N, Bruno B, Boccadoro M: Bortezomib, doxorubicin and dexamethasone in advanced multiple myeloma. Ann Oncol 2008, 19:1160-1165