Mitochondrial Targeting of Doxorubicin Eliminates Nuclear Effects Associated with Cardiotoxicity

ACS Chemical Biology

Volumn 10, Issue 9, 2015, Pages 2007-2015

  Jean, Sae Rin ^a   Tulumello, David V ^b   Riganti, Chiara ^d   Liyanage, Sanduni U ^b,c   Schimmer, Aaron D ^b,c   Kelley, Shana O ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN;

ANALOGS AND DERIVATIVES; ANIMAL; CARDIAC MUSCLE CELL; CARDIOTOXICITY; CELL LINE; CELL NUCLEUS; CHEMISTRY; DNA DAMAGE; DRUG DELIVERY SYSTEM; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NEOPLASMS; RAT; TUMOR CELL LINE;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CARDIOTOXICITY; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; DNA DAMAGE; DOXORUBICIN; DRUG DELIVERY SYSTEMS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MYOCYTES, CARDIAC; NEOPLASMS; RATS;

EID: 84942041765     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00268     Document Type: Article

References (41)

1. Weiss, R. B. (1992) The anthracyclines: Will we ever find a better doxorubicin? Semin. Oncol. 19, 670-686
2. Nitiss, J. L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy Nat. Rev. Cancer. 9, 338-350
3. Pommier, Y. (2013) Drugging topoisomerases: lessons and challenges ACS Chem. Biol. 8, 82-95
4. Minotti, G., Menna, P., Salvatorelli, E., Cairo, G., and Gianni, L. (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity Pharmacol. Rev. 56, 185-229
5. Singal, P. K. and Iliskovic, N. (1998) Doxorubicin-induced cardiomyopathy N. Engl. J. Med. 339, 900-905
6. Berthiaume, J. M. and Wallace, K. B. (2007) Adriamycin-induced oxidative mitochondrial cardiotoxicity Cell. Biol. Toxicol. 23, 15-25
7. Low, R. L., Orton, S., and Friedman, D. B. (2003) A truncated form of DNA topoisomerase IIbeta associates with the mtDNA genome in mammalian mitochondria Eur. J. Biochem. 270, 4173-4186
8. Khiati, S., Dalla Rosa, I., Sourbier, C., Ma, X., Rao, V. A., Neckers, L. M., Zhang, H., and Pommier, Y. (2014) Mitochondrial topoisomerase I (Top1mt) is a novel limiting factor of doxorubicin cardiotoxicity Clin. Cancer Res. 20, 4873-4881
9. Zhang, S., Liu, X., Bawa-Khalfe, T., Lu, L. S., Lyu, Y. L., Liu, L. F., and Yeh, E. T. (2012) Identification of the molecular basis of doxorubicin-induced cardiotoxicity Nat. Med. 18, 1639-1642
10. Sawyer, D. B. (2013) Anthracyclines and heart failure N. Engl. J. Med. 368, 1154-1156
11. Suliman, H. B., Carraway, M. S., Ali, A. S., Reynolds, C. M., Welty-Wolf, K. E., and Piantadosi, C. A. (2007) The CO/HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy J. Clin. Invest. 117, 3730-3741
12. Ventura-Clapier, R., Garnier, A., and Veksler, V. (2008) Transcriptional control of mitochondrial biogenesis: The central role of PGC-1alpha Cardiovasc. Res. 79, 208-217
13. Jean, S. R., Tulumello, D. V., Wisnovsky, S. P., Lei, E. K., Pereira, M. P., and Kelley, S. O. (2014) Molecular vehicles for mitochondrial chemical biology and drug delivery ACS Chem. Biol. 9, 323-333
14. Kalafut, D., Anderson, T. N., and Chmielewski, J. (2012) Mitochondrial targeting of a cationic amphiphilic polyproline helix Bioorg. Med. Chem. Lett. 22, 561-563
15. Geisler, I. M. and Chmielewski, J. (2011) Dimeric cationic amphiphilic polyproline helices for mitochondrial targeting Pharm. Res. 28, 2797-2807
16. Li, L., Geisler, I., Chmielewski, J., and Cheng, J. X. (2010) Cationic amphiphilic polyproline helix P11LRR targets intracellular mitochondria J. Controlled Release 142, 259-266
17. Cullen, K. J., Yang, Z., Schumaker, L., and Guo, Z. (2007) Mitochondria as a critical target of the chemotheraputic agent cisplatin in head and neck cancer J. Bioenerg. Biomembr. 39, 43-50
18. Wisnovsky, S. P., Wilson, J. J., Radford, R. J., Pereira, M. P., Chan, M. R., Laposa, R. R., Lippard, S. J., and Kelley, S. O. (2013) Targeting mitochondrial DNA with a platinum-based anticancer agent Chem. Biol. 20, 1323-1328
19. Marrache, S., Pathak, R. K., and Dhar, S. (2014) Detouring of cisplatin to access mitochondrial genome for overcoming resistance Proc. Natl. Acad. Sci. U.S.A. 111, 10444-10449
20. Smith, R. A., Hartley, R. C., and Murphy, M. P. (2011) Mitochondria-targeted small molecule therapeutics and probes Antioxid. Redox Signaling 15, 3021-3038
21. Zhang, X., Fryknas, M., Hernlund, E., Fayad, W., De Milito, A., Olofsson, M. H., Gogvadze, V., Dang, L., Pahlman, S., Schughart, L. A., Rickardson, L., D'Arcy, P., Gullbo, J., Nygren, P., Larsson, R., and Linder, S. (2014) Induction of mitochondrial dysfunction as a strategy for targeting tumour cells in metabolically compromised microenvironments Nat. Commun. 5, 3295
22. Skrtic, M., Sriskanthadevan, S., Jhas, B., Gebbia, M., Wang, X., Wang, Z., Hurren, R., Jitkova, Y., Gronda, M., Maclean, N., Lai, C. K., Eberhard, Y., Bartoszko, J., Spagnuolo, P., Rutledge, A. C., Datti, A., Ketela, T., Moffat, J., Robinson, B. H., Cameron, J. H., Wrana, J., Eaves, C. J., Minden, M. D., Wang, J. C., Dick, J. E., Humphries, K., Nislow, C., Giaever, G., and Schimmer, A. D. (2011) Inhibition of mitochondrial translation as a therapeutic strategy for human acute myeloid leukemia Cancer Cell 20, 674-688
23. Fonseca, S. B., Pereira, M. P., Mourtada, R., Gronda, M., Horton, K. L., Hurren, R., Minden, M. D., Schimmer, A. D., and Kelley, S. O. (2011) Rerouting chlorambucil to mitochondria combats drug deactivation and resistance in cancer cells Chem. Biol. 18, 445-453
24. Jean, S. R., Pereira, M. P., and Kelley, S. O. (2014) Structural modifications of mitochondria-targeted chlorambucil alter cell death mechanism but preserve MDR evasion Mol. Pharmaceutics 11, 2675-2682
25. Fulda, S., Galluzzi, L., and Kroemer, G. (2010) Targeting mitochondria for cancer therapy Nat. Rev. Drug Discovery 9, 447-464
26. Jung, K. and Reszka, R. (2001) Mitochondria as subcellular targets for clinically useful anthracyclines Adv. Drug Delivery Rev. 49, 87-105
27. Malhi, S. S., Budhiraja, A., Arora, S., Chaudhari, K. R., Nepali, K., Kumar, R., Sohi, H., and Murthy, R. S. (2012) Intracellular delivery of redox cycler-doxorubicin to the mitochondria of cancer cell by folate receptor targeted mitocancerotropic liposomes Int. J. Pharm. 432, 63-74
28. Chamberlain, G. R., Tulumello, D. V., and Kelley, S. O. (2013) Targeted delivery of doxorubicin to mitochondria ACS Chem. Biol. 8, 1389-1395
29. Han, M., Vakili, M. R., Soleymani Abyaneh, H., Molavi, O., Lai, R., and Lavasanifar, A. (2014) Mitochondrial delivery of doxorubicin via triphenylphosphine modification for overcoming drug resistance in MDA-MB-435/DOX cells Mol. Pharmaceutics 11, 2640-2649
30. Riganti, C., Rolando, B., Kopecka, J., Campia, I., Chegaev, K., Lazzarato, L., Federico, A., Fruttero, R., and Ghigo, D. (2013) Mitochondrial-targeting nitrooxy-doxorubicin: A new approach to overcome drug resistance Mol. Pharmaceutics 10, 161-174
31. Theodossiou, T. A., Sideratou, Z., Katsarou, M. E., and Tsiourvas, D. (2013) Mitochondrial delivery of doxorubicin by triphenylphosphonium-functionalized hyperbranched nanocarriers results in rapid and severe cytotoxicity Pharm. Res. 30, 2832-2842
32. Horton, K. L., Stewart, K. M., Fonseca, S. B., Guo, Q., and Kelley, S. O. (2008) Mitochondria-penetrating peptides Chem. Biol. 15, 375-382
33. Riganti, C., Aldieri, E., Bergandi, L., Fenoglio, I., Costamagna, C., Fubini, B., Bosia, A., and Ghigo, D. (2002) Crocidolite asbestos inhibits pentose phosphate oxidative pathway and glucose 6-phosphate dehydrogenase activity in human lung epithelial cells Free Radical Biol. Med. 32, 938-949
34. Wibom, R., Hagenfeldt, L., and von Dobeln, U. (2002) Measurement of ATP production and respiratory chain enzyme activities in mitochondria isolated from small muscle biopsy samples Anal. Biochem. 311, 139-151
35. Santos, J. H., Meyer, J. N., Mandavilli, B. S., and Van Houten, B. (2006) Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells Methods Mol. Biol. 314, 183-199
36. Modica-Napolitano, J. S. and Aprille, J. R. (2001) Delocalized lipophilic cations selectively target the mitochondria of carcinoma cells Adv. Drug Delivery Rev. 49, 63-70
37. Marcillat, O., Zhang, Y., and Davies, K. J. (1989) Oxidative and non-oxidative mechanisms in the inactivation of cardiac mitochondrial electron transport chain components by doxorubicin Biochem. J. 259, 181-189
38. Strigun, A., Wahrheit, J., Niklas, J., Heinzle, E., and Noor, F. (2012) Doxorubicin increases oxidative metabolism in HL-1 cardiomyocytes as shown by 13C metabolic flux analysis Toxicol. Sci. 125, 595-606
39. Chouchani, E. T., Methner, C., Nadtochiy, S. M., Logan, A., Pell, V. R., Ding, S., James, A. M., Cocheme, H. M., Reinhold, J., Lilley, K. S., Partridge, L., Fearnley, I. M., Robinson, A. J., Hartley, R. C., Smith, R. A., Krieg, T., Brookes, P. S., and Murphy, M. P. (2013) Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I Nat. Med. 19, 753-759
40. Chouchani, E. T., Methner, C., Buonincontri, G., Hu, C. H., Logan, A., Sawiak, S. J., Murphy, M. P., and Krieg, T. (2014) Complex I deficiency due to selective loss of Ndufs4 in the mouse heart results in severe hypertrophic cardiomyopathy PLoS One 9, e94157
41. Deblois, G., St-Pierre, J., and Giguere, V. (2013) The PGC-1/ERR signaling axis in cancer Oncogene 32, 3483-3490