Inhibition of chymotryptic-like standard proteasome activity exacerbates doxorubicin-induced cytotoxicity in primary cardiomyocytes

Toxicology

Volumn 353-354, Issue , 2016, Pages 34-47

  Spur, Eva Margarete ^a,b   Althof, Nadine ^a,b   Respondek, Dorota ^a,b   Klingel, Karin ^c   Heuser, Arnd ^d   Overkleeft, Hermen S ^e   Voigt, Antje ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Anthracycline cardiotoxicity; Proteasome; Proteostasis; Subunit specific proteasome inhibitors; Toxicology

Indexed keywords

BETA5 STANDARD PROTEASOME; CARFILZOMIB; DOXORUBICIN; PROTEASOME; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; LMP7 PROTEIN; OLIGOPEPTIDE; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CARDIAC MUSCLE CELL; CARDIOTOXICITY; CELL CULTURE; CELL DEATH; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAM; ENZYME ACTIVITY; ENZYME INHIBITION; IMMUNOBLOTTING; MALE; MOLECULAR WEIGHT; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; UBIQUITIN PROTEASOME SYSTEM; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; DOXORUBICIN; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE MYELOMA; MYOCYTES, CARDIAC; OLIGOPEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84967332894     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2016.04.010     Document Type: Article

References (55)

1. Aki M., Shimbara N., Takashina M., Akiyama K., Kagawa S., Tamura T., Tanahashi N., Yoshimura T., Tanaka K., Ichihara A. Interferon-gamma induces different subunit organizations and functional diversity of proteasomes. J. Biol. Chem. 1994, 115(2):257-269.
2. Chau V., Tobias J.W., Bachmair A., Marriott D., Ecker D.J., Gonda D.K., Varshavsky A. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 1989, 243(4898):1576-1583.
3. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat. Rev. Mol. Cell Biol. 2005, 6(1):79-86.
4. Dantuma N.P., Lindsten K., Glas R., Jellne M., Masucci M.G. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat. Biotechnol. 2000, 18(5):538-543.
5. Dantuma N.P., Groothuis T.A., Salomons F.A., Neefjes J. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 2006, 173(1):19-26.
6. de Bruin G., Xin B.T., Kraus M., van der Stelt M., van der Marel G.A., Kisselev A.F., Driessen C., Florea B.I., Overkleeft H.S. A set of activity-based probes to visualize human (immuno)proteasome activities. Angew. Chem. 2015, 10.1002/anie.201509092.
7. Dick T.P., Nussbaum A.K., Deeg M., Heinemeyer W., Groll M., Schirle M., Keilholz W., Stevanovic S., Wolf D.H., Huber R., Rammensee H.G., Schild H. Contribution of proteasomal beta-subunits to the cleavage of peptide substrates analyzed with yeast mutants. J. Biol. Chem. 1998, 273(40):25637-25646.
8. Dimitrakis P., Romay-Ogando M.I., Timolati F., Suter T.M., Zuppinger C. Effects of doxorubicin cancer therapy on autophagy and the ubiquitin-proteasome system in long-term cultured adult rat cardiomyocytes. Cell Tissue Res. 2012, 350(2):361-372.
9. Drews O., Tsukamoto O., Liem D., Streicher J., Wang Y.B., Ping P.P. Differential regulation of proteasome function in isoproterenol-Induced cardiac hypertrophy. Circul. Res. 2010, 107(9):1094-1101.
10. Ebstein F., Voigt A., Lange N., Warnatsch A., Schroter F., Prozorovski T., Kuckelkorn U., Aktas O., Seifert U., Kloetzel P.M., Kruger E. Immunoproteasomes are important for proteostasis in immune responses. Cell 2013, 152(5):935-937.
11. Fehling H.J., Swat W., Laplace C., Kuhn R., Rajewsky K., Muller U., Vonboehmer H. Mhc class-I expression in mice lacking the proteasome subunit Lmp-7. Science 1994, 265(5176):1234-1237.
12. Fekete M.R., McBride W.H., Pajonk F. Anthracyclines, proteasome activity and multi-drug-resistance. BMC Cancer 2005, 5:114.
13. Gomes A.V., Zong C., Edmondson R.D., Li X., Stefani E., Zhang J., Jones R.C., Thyparambil S., Wang G.W., Qiao X., Bardag-Gorce F., Ping P.P. Mapping the murine cardiac 26S proteasome complexes. Circul. Res. 2006, 99(4):362-371.
14. Groopman J.E., Itri L.M. Chemotherapy-induced anemia in adults: incidence and treatment. J. Natl. Cancer Inst. 1999, 91:1616-1634.
15. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144(5):646-674.
16. Jakel S., Kuckelkorn U., Szalay G., Plotz M., Textoris-Taube K., Opitz E., Klingel K., Stevanovic S., Kandolf R., Kotsch K., Stangl K., Kloetzel P.M., Voigt A. Differential interferon responses enhance viral epitope generation by myocardial immunoproteasomes in murine enterovirus myocarditis. Am. J. Pathol. 2009, 175(2):510-518.
17. Kiyomiya K., Matsuo S., Kurebe M. Proteasome is a carrier to translocate doxorubicin from cytoplasm into nucleus. Life Sci. 1998, 62(20):1853-1860.
18. Kloetzel P.M. Antigen processing by the proteasome. Nat. Rev. Mol. Cell Biol. 2001, 2(3):179-187.
19. Kruger E., Kloetzel P.M. Immunoproteasomes at the interface of innate and adaptive immune responses: two faces of one enzyme. Curr. Opin. Immunol. 2012, 24(1):77-83.
20. Kuhn D.J., Hunsucker S.A., Chen Q., Voorhees P.M., Orlowski M., Orlowski R.Z. Targeted inhibition of the immunoproteasome is a potent strategy against models of multiple myeloma that overcomes resistance to conventional drugs and nonspecific proteasome inhibitors. Blood 2009, 113(19):4667-4676.
21. Kumarapeli A.R., Horak K.M., Glasford J.W., Li J., Chen Q., Liu J., Zheng H., Wang X. A novel transgenic mouse model reveals deregulation of the ubiquitin-proteasome system in the heart by doxorubicin. FASEB J. 2005, 19(14):2051-2053.
22. Lang F., Lang E., Foller M. Physiology and pathophysiology of eryptosis. Transfus. Med. Hemother. 2012, 39:308-314.
23. Li N., Kuo C.L., Paniagua G., van den Elst H., Verdoes M., Willems L.I., van der Linden W.A., Ruben M., van G.E., Gubbens J., van Wezel G.P., Overkleeft H.S., Florea B.I. Relative quantification of proteasome activity by activity-based protein profiling and LC-MS/MS. Nat. Protoc. 2013, 8(6):1155-1168.
24. Liu J., Zheng H., Tang M., Ryu Y.C., Wang X. A therapeutic dose of doxorubicin activates ubiquitin-proteasome system-mediated proteolysis by acting on both the ubiquitination apparatus and proteasome. Am. J. Physiol. Heart Circ. Physiol. 2008, 295(6):H2541-50.
25. Lyu Y.L., Kerrigan J.E., Lin C.P., Azarova A.M., Tsai Y.C., Ban Y., Liu L.F. Topoisomerase IIbeta mediated DNA double-strand breaks: implications in doxorubicin cardiotoxicity and prevention by dexrazoxane. Cancer Res. 2007, 67(18):8839-8846.
26. Mandili G., Khadjavi A., Gallo V., Minero V.G., Bessone L., Carta F., Giribaldi G., Turrini F. Characterization of the protein ubiquitination response induced by Doxorubicin. FEBS J. 2012, 279(12):2182-2191.
27. Mishto M., Liepe J., Textoris-Taube K., Keller C., Henklein P., Weberruss M., Dahlmann B., Enenkel C., Voigt A., Kuckelkorn U., Stumpf M.P., Kloetzel P.M. Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur. J. Immunol. 2014, 44(12):3508-3521.
28. Muchamuel T., Basler M., Aujay M.A., Suzuki E., Kalim K.W., Lauer C., Sylvain C., Ring E.R., Shields J., Jiang J., Shwonek P., Parlati F., Demo S.D., Bennett M.K., Kirk C.J., Groettrup M. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat. Med. 2009, 15(7):781-787.
29. Opitz E., Koch A., Klingel K., Schmidt F., Prokop S., Rahnefeld A., Sauter M., Heppner F.L., Volker U., Kandolf R., Kuckelkorn U., Stangl K., Kruger E., Kloetzel P.M., Voigt A. Impairment of immunoproteasome function by beta5i/LMP7 subunit deficiency results in severe enterovirus myocarditis. PLoS Pathog. 2011, 7(9):1-13.
30. Orlowski M., Wilk S. Catalytic activities of the 20S proteasome, a multicatalytic proteinase complex. Arch. Biochem. Biophys. 2000, 383(1):1-16.
31. Paeschke A., Possehl A., Klingel K., Voss M., Voss K., Kesphol M., Sauter M., Overkleeft H.S., Althof N., Garlanda C., Voigt A. The immunoproteasome controls the availability of the cardio-protective pattern recognition molecule Pentraxin3. Eur. J. Immunol. 2015, 10.1002/eji.201545892.
32. Parlati F., Lee S.J., Aujay M., Suzuki E., Levitsky K., Lorens J.B., Micklem D.R., Ruurs P., Sylvain C., Lu Y., Shenk K.D., Bennett M.K. Carfilzomib can induce tumor cell death through selective inhibition of the chymotrypsin-like activity of the proteasome. Blood 2009, 114(16):3439-3447.
33. Pickering A.M., Koop A.L., Teoh C.Y., Ermak G., Grune T., Davies K.J.A. The immunoproteasome, the 20S proteasome and the PA28 alpha beta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem. J. 2010, 432:585-594.
34. Pickering A.M., Linder R.A., Zhang H., Forman H.J., Davies K.J. Nrf2-dependent induction of proteasome and Pa28alphabeta regulator are required for adaptation to oxidative stress. J. Biol. Chem. 2012, 287(13):10021-10031.
35. Rahnefeld A., Klingel K., Schuermann A., Diny N.L., Althof N., Lindner A., Bleienheuft P., Savvatis K., Respondek D., Opitz E., Ketscher L., Sauter M., Seifert U., Tschope C., Poller W., Knobeloch K.P., Voigt A. Ubiquitin-like protein ISG15 (interferon-stimulated gene of 15 kDa) in host defense against heart failure in a mouse model of virus-induced cardiomyopathy. Circulation 2014, 130(18):1589-1600.
36. Ranek M.J., Wang X. Activation of the ubiquitin-proteasome system in doxorubicin cardiomyopathy. Curr. Hypertens. Rep. 2009, 11(6):389-395.
37. Richardson P.G., Barlogie B., Berenson J., Singhal S., Jagannath S., Irwin D., Rajkumar S.V., Srkalovic G., Alsina M., Alexanian R., Siegel D., Orlowski R.Z., Kuter D., Limentani S.A., Lee S., Hideshima T., Esseltine D.L., Kauffman M., Adams J., Schenkein D.P., Anderson K.C. A phase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 2003, 348(26):2609-2617.
38. Richardson P.G., Sonneveld P., Schuster M.W., Irwin D., Stadtmauer E.A., Facon T., Harousseau J.L., Ben-Yehuda D., Lonial S., Goldschmidt H., Reece D., San-Miguel J.F., Blade J., Boccadoro M., Cavenagh J., Dalton W.S., Boral A.L., Esseltine D.L., Porter J.B., Schenkein D., Anderson K.C. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N. Engl. J. Med. 2005, 352(24):2487-2498.
39. Segref A., Kevei E., Pokrzywa W., Schmeisser K., Mansfeld J., Livnat-Levanon N., Ensenauer R., Glickman M.H., Ristow M., Hoppe T. Pathogenesis of human mitochondrial diseases is modulated by reduced activity of the ubiquitin/proteasome system. Cell Metab. 2014, 19(4):642-652.
40. Seifert U., Bialy L.P., Ebstein F., Bech-Otschir D., Voigt A., Schroter F., Prozorovski T., Lange N., Steffen J., Rieger M., Kuckelkorn U., Aktas O., Kloetzel P.M., Kruger E. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 2010, 142(4):613-624.
41. Siegel D., Martin T., Nooka A., Harvey R.D., Vij R., Niesvizky R., Badros A.Z., Jagannath S., McCulloch L., Rajangam K., Lonial S. Integrated safety profile of single-agent carfilzomib: experience from 526 patients enrolled in 4 phase II clinical studies. Haematologica 2013, 98(11):1753-1761.
42. Singh A.V., Bandi M., Aujay M.A., Kirk C.J., Hark D.E., Raje N., Chauhan D., Anderson K.C. PR-924, a selective inhibitor of the immunoproteasome subunit LMP-7, blocks multiple myeloma cell growth both in vitro and in vivo. Br. J. Haematol. 2011, 152(2):155-163.
43. Singh P., Sharma R., McElhanon K., Allen C.D., Megyesi J.K., Benes H., Singh S.P. Sulforaphane protects the heart from doxorubicin-induced toxicity. Free Radic. Biol. Med. 2015, 86:90-101.
44. Sishi B.J., Loos B., van Rooyen J., Engelbrecht A.M. Doxorubicin induces protein ubiquitination and inhibits proteasome activity during cardiotoxicity. Toxicology 2013, 309:23-29.
45. Sophia D., Martin S., Leo R., Susanne S., Hermann E., Stefan K. Real life experience of pre-approval carfilzomib-based therapy in myeloma-analysis of cardiac toxicity and predisposing factors. Eur. J. Haematol. 2015, 10.1111/ejh.12677.
46. Sterba M., Popelova O., Vavrova A., Jirkovsky E., Kovarikova P., Gersl V., Simunek T. Oxidative stress, redox signaling, and metal chelation in anthracycline cardiotoxicity and pharmacological cardioprotection. Antioxid. Redox Signal. 2013, 18(8):899-929.
47. Stewart A.K., Rajkumar S.V., Dimopoulos M.A., Masszi T., Spicka I., Oriol A., Hajek R., Rosinol L., Siegel D.S., Mihaylov G.G., Goranova-Marinova V., Rajnics P., Suvorov A., Niesvizky R., Jakubowiak A.J., San-Miguel J.F., Ludwig H., Wang M., Maisnar V., Minarik J., Bensinger W.I., Mateos M.V., Ben-Yehuda D., Kukreti V., Zojwalla N., Tonda M.E., Yang X., Xing B., Moreau P., Palumbo A. Carfilzomib, lenalidomide, and dexamethasone for relapsed multiple myeloma. N. Engl. J. Med. 2015, 372(2):142-152.
48. Strehl B., Textoris-Taube K., Jakel S., Voigt A., Henklein P., Steinhoff U., Kloetzel P.M., Kuckelkorn U. Antitopes define preferential proteasomal cleavage site usage. J. Biol. Chem. 2008, 283(26):17891-17897.
49. Szalay G., Meiners S., Voigt A., Lauber J., Spieth C., Speer N., Sauter M., Kuckelkorn U., Zell A., Klingel K., Stangl K., Kandolf R. Ongoing coxsackievirus myocarditis is associated with increased formation and activity of myocardial immunoproteasomes. Am. J. Pathol. 2006, 168(5):1542-1552.
50. Voigt A., Bartel K., Egerer K., Trimpert C., Feist E., Gericke C., Kandolf R., Klingel K., Kuckelkorn U., Stangl K., Felix S.B., Baumann G., Kloetzel P.M., Staudt A. Humoral anti-proteasomal autoimmunity in dilated cardiomyopathy. Basic Res. Cardiol. 2010, 105(1):9-18.
51. Voigt A., Jakel S., Textoris-Taube K., Keller C., Drung I., Szalay G., Klingel K., Henklein P., Stangl K., Kloetzel P.M., Kuckelkorn U. Generation of in silico predicted coxsackievirus B3-derived MHC class I epitopes by proteasomes. Amino Acids 2010, 39(1):243-255.
52. Yamamoto Y., Hoshino Y., Ito T., Nariai T., Mohri T., Obana M., Hayata N., Uozumi Y., Maeda M., Fujio Y., Azuma J. Atrogin-1 ubiquitin ligase is upregulated by doxorubicin via p38-MAP kinase in cardiac myocytes. Cardiovasc. Res. 2008, 79(1):89-96.
53. Zhang S., Liu X., Bawa-Khalfe T., Lu L.S., Lyu Y.L., Liu L.F., Yeh E.T. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat. Med. 2012, 18(11):1639-1642.
54. Zhao W.J., Wei S.N., Zeng X.J., Xia Y.L., Du J., Li H.H. Gene expression profiling identifies the novel role of immunoproteasome in doxorubicin-induced cardiotoxicity. Toxicology 2015, 333:76-88.
55. Zhu W., Soonpaa M.H., Chen H., Shen W., Payne R.M., Liechty E.A., Caldwell R.L., Shou W., Field L.J. Acute doxorubicin cardiotoxicity is associated with p53-induced inhibition of the mammalian target of rapamycin pathway. Circulation 2009, 119(1):99-106.