Doxorubicin impairs cardiomyocyte viability by suppressing transcription factor EB expression and disrupting autophagy

Biochemical Journal

Volumn 473, Issue 21, 2016, Pages 3769-3789

  Bartlett, Jordan J ^a   Trivedi, Purvi C ^a   Yeung, Pollen ^a   Kienesberger, Petra C ^a   Pulinilkunnil, Thomas ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CATHEPSIN B; DOXORUBICIN; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; TFEB PROTEIN, RAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CARDIAC MUSCLE CELL; CARDIOTOXICITY; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME REPRESSION; EX VIVO STUDY; FEMALE; IN VIVO STUDY; INTRACELLULAR SIGNALING; LYSOSOME; MACROAUTOPHAGY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; GENETICS; IMMUNOBLOTTING; METABOLISM; MOUSE; NEWBORN; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TUNEL ASSAY;

ANIMALS; ANIMALS, NEWBORN; AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; DOXORUBICIN; IMMUNOBLOTTING; IN SITU NICK-END LABELING; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; MYOCYTES, CARDIAC; POLYMERASE CHAIN REACTION; PROTEOLYSIS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84988549384     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160385     Document Type: Article

References (66)

1. Chatterjee, K., Zhang, J., Honbo, N. and Karliner, J.S. (2010) Doxorubicin cardiomyopathy. Cardiology 115, 155-162 doi:10.1159/000265166.
2. Volkova, M. and Russell, R. (2011) Anthracycline cardiotoxicity: prevalence, pathogenesis and treatment. Curr. Cardiol. Rev. 7, 214-220 doi:10.2174/157340311799960645.
3. Fu, H.Y., Sanada, S., Matsuzaki, T., Liao, Y., Okuda, K., Yamato, M. et al. (2016) Chemical endoplasmic reticulum chaperone alleviates doxorubicin-induced cardiac dysfunction. Circ. Res. 118, 798-809 doi:10.1161/CIRCRESAHA.115.307604.
4. Green, P.S. and Leeuwenburgh, C. (2002) Mitochondrial dysfunction is an early indicator of doxorubicin-induced apoptosis. Biochim. Biophys. Acta, Mol. Basis Dis. 1588, 94-101 doi:10.1016/S0925-4439(02)00144-8.
5. Sardão, V.A., Oliveira, P.J., Holy, J., Oliveira, C.R. and Wallace, K.B. (2009) Morphological alterations induced by doxorubicin on H9c2 myoblasts: nuclear, mitochondrial, and cytoskeletal targets. Cell Biol. Toxicol. 25, 227-243 doi:10.1007/s10565-008-9070-1.
6. Wang, Z.V. and Hill, J.A. (2015) Protein quality control and metabolism: bidirectional control in the heart. Cell Metab. 21, 215-226 doi:10.1016/j.cmet.2015.01.016.
7. Senft, D. and Ronai, Z.A. (2015) UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem. Sci. 40, 141-148 doi:10.1016/j.tibs.2015.01.002.
8. Sishi, B.J.N., Loos, B., van Rooyen, J. and Engelbrecht, A.-M. (2013) Autophagy upregulation promotes survival and attenuates doxorubicin-induced cardiotoxicity. Biochem. Pharmacol. 85, 124-134 doi:10.1016/j.bcp.2012.10.005.
9. Zhao, D., Yuan, H., Yi, F., Meng, C. and Zhu, Q. (2014) Autophagy prevents doxorubicin-induced apoptosis in osteosarcoma. Mol. Med. Rep. 9, 1975-1981 PMID: 24639013.
10. Li, D.L., Wang, Z.V., Ding, G., Tan, W., Luo, X., Criollo, A. et al. (2016) Doxorubicin blocks cardiomyocyte autophagic flux by inhibiting lysosome acidification. Circulation 133, 1668-1687. doi:10.1161/CIRCULATIONAHA.115.017443.
11. Cuervo, A.M. (2004) Autophagy: in sickness and in health. Trends Cell Biol. 14, 70-77 doi:10.1016/j.tcb.2003.12.002.
12. Cuervo, A.M. (2011) Autophagy's top chef. Science 332, 1392-1393 doi:10.1126/science.1208607.
13. Kitsis, R.N., Peng, C.-F. and Cuervo, A.M. (2007) Eat your heart out. Nat. Med. 13, 539-541 doi:10.1038/nm0507-539.
14. Kaushik, S., Singh, R. and Cuervo, A.M. (2010) Autophagic pathways and metabolic stress. Diabetes Obes. Metab. 12 (Suppl. 2), 4-14 doi:10.1111/j.1463-1326.2010.01263.x.
15. Kaushik, S. and Cuervo, A.M. (2012) Chaperone-mediated autophagy: A unique way to enter the lysosome world. Trends Cell Biol. 22, 407-417 doi:10.1016/j.tcb.2012.05.006.
16. Arias, E. and Cuervo, A.M. (2011) Chaperone-mediated autophagy in protein quality control. Curr. Opin. Cell Biol. 23, 184-189 doi:10.1016/j.ceb.2010.10.009.
17. Mizushima, N., Yoshimori, T. and Ohsumi, Y. (2011) The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132 doi:10.1146/annurev-cellbio-092910-154005.
18. Tanida, I. (2011) Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox Signal. 14, 2201-2214 doi:10.1089/ars.2010.3482.
19. Lippai, M. and Low, P. (2014) The role of the selective adaptor p62 and ubiquitin-like proteins in autophagy. Biomed. Res. Int. 2014, 832704 doi:10.1155/2014/832704.
20. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21, 2861-2873 doi:10.1101/gad.1599207.
21. Xie, Y., Kang, R., Sun, X., Zhong, M., Huang, J., Klionsky, D.J. et al. (2015) Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy 11, 28-45 doi:10.4161/15548627.2014.984267.
22. Nishida, K., Taneike, M. and Otsu, K. (2015) The role of autophagic degradation in the heart. J. Mol. Cell. Cardiol. 78, 73-79 doi:10.1016/j.yjmcc.2014.09.029.
23. Settembre, C., Fraldi, A., Medina, D.L. and Ballabio, A. (2013) Signals from the lysosome: A control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14, 283-296 doi:10.1038/nrm3565.
24. Shen, H.-M. and Mizushima, N. (2014) At the end of the autophagic road: An emerging understanding of lysosomal functions in autophagy. Trends Biochem. Sci. 39, 61-71 doi:10.1016/j.tibs.2013.12.001.
25. Kaushik, S. and Cuervo, A.M. (2012) Chaperones in autophagy. Pharmacol. Res. 66, 484-493 doi:10.1016/j.phrs.2012.10.002.
26. Settembre, C., Di Malta, C., Polito, V.A., Garcia Arencibia, M., Vetrini, F., Erdin, S. et al. (2011) TFEB links autophagy to lysosomal biogenesis. Science 332, 1429-1433 doi:10.1126/science.1204592.
27. Settembre, C. and Ballabio, A. (2011) TFEB regulates autophagy: An integrated coordination of cellular degradation and recycling processes. Autophagy 7, 1379-1381 doi:10.4161/auto.7.11.17166.
28. Sardiello, M., Palmieri, M., di Ronza, A., Medina, D.L., Valenza, M., Gennarino, V.A. et al. (2009) A gene network regulating lysosomal biogenesis and function. Science 325, 473-477.
29. Song, W., Wang, F., Savini, M., Ake, A., di Ronza, A., Sardiello, M. et al. (2013) TFEB regulates lysosomal proteostasis. Hum. Mol. Genet. 22, 1994-2009 doi:10.1093/hmg/ddt052.
30. Kobayashi, S., Volden, P., Timm, D., Mao, K., Xu, X. and Liang, Q. (2010) Transcription factor GATA4 inhibits doxorubicin-induced autophagy and cardiomyocyte death. J. Biol. Chem. 285, 793-804 doi:10.1074/jbc.M109.070037.
31. Sishi, B.J.N., Loos, B., van Rooyen, J. and Engelbrecht, A.-M. (2013) Doxorubicin induces protein ubiquitination and inhibits proteasome activity during cardiotoxicity. Toxicology 309, 23-29 doi:10.1016/j.tox.2013.04.016.
32. Wang, X., Wang, X.-L., Chen, H.-L., Wu, D., Chen, J.-X., Wang, X.-X. et al. (2014) Ghrelin inhibits doxorubicin cardiotoxicity by inhibiting excessive autophagy through AMPK and p38-MAPK. Biochem. Pharmacol. 88, 334-350 doi:10.1016/j.bcp.2014.01.040.
33. Xu, X., Chen, K., Kobayashi, S., Timm, D. and Liang, Q. (2012) Resveratrol attenuates doxorubicin-induced cardiomyocyte death via inhibition of p70 S6 kinase 1-mediated autophagy. J. Pharmacol. Exp. Ther. 341, 183-195 doi:10.1124/jpet.111.189589.
34. Ma, X., Liu, H., Murphy, J.T., Foyil, S.R., Godar, R.J., Abuirqeba, H. et al. (2015) Regulation of the transcription factor EB-PGC1α axis by beclin-1 controls mitochondrial quality and cardiomyocyte death under stress. Mol. Cell. Biol. 35, 956-976 doi:10.1128/MCB.01091-14.
35. Godar, R.J., Ma, X., Liu, H., Murphy, J.T., Weinheimer, C.J., Kovacs, A. et al. (2015) Repetitive stimulation of autophagy-lysosome machinery by intermittent fasting preconditions the myocardium to ischemia-reperfusion injury. Autophagy 11, 1537-1560 doi:10.1080/15548627.2015.1063768.
36. Schneider, J.L., Suh, Y. and Cuervo, A.M. (2014) Deficient chaperone-mediated autophagy in liver leads to metabolic dysregulation. Cell Metab. 20, 417-432 doi:10.1016/j.cmet.2014.06.009.
37. Guan, J., Mishra, S., Qiu, Y., Shi, J., Trudeau, K., Las, G. et al. (2014) Lysosomal dysfunction and impaired autophagy underlie the pathogenesis of amyloidogenic light chain-mediated cardiotoxicity. EMBO Mol. Med. 6, 1493-1507 doi:10.15252/emmm.201404190.
38. Pulinilkunnil, T., Puthanveetil, P., Kim, M.S., Wang, F., Schmitt, V. and Rodrigues, B. (2010) Ischemia-reperfusion alters cardiac lipoprotein lipase. Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 1801, 171-175 doi:10.1016/j.bbalip.2009.10.008.
39. Kienesberger, P.C., Pulinilkunnil, T., Nagendran, J., Young, M.E., Bogner-Strauss, J.G., Hackl, H. et al. (2013) Early structural and metabolic cardiac remodelling in response to inducible adipose triglyceride lipase ablation. Cardiovasc. Res. 99, 442-451 doi:10.1093/cvr/cvt124.
40. Kimura, S., Noda, T. and Yoshimori, T. (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-Tagged LC3. Autophagy 3, 452-460 doi:10.4161/auto.4451.
41. Martina, J.A., Diab, H.I., Li, H. and Puertollano, R. (2014) Novel roles for the MiTF/TFE family of transcription factors in organelle biogenesis, nutrient sensing, and energy homeostasis. Cell. Mol. Life Sci. 71, 2483-2497 doi:10.1007/s00018-014-1565-8.
42. Roczniak-Ferguson, A., Petit, C.S., Froehlich, F., Qian, S., Ky, J., Angarola, B. et al. (2012) The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 5, ra 42 doi:10.1126/scisignal.2002790.
43. Settembre, C., Zoncu, R., Medina, D.L., Vetrini, F., Erdin, S., Erdin, S. et al. (2012) A lysosome-To-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31, 1095-1108 doi:10.1038/emboj.2012.32.
44. Crowley, M.A. and Connors, D.D. (1985) Critique of "The use of animals in nursing research". Adv. Nurs. Sci. 7, 23-32 doi:10.1097/00012272-198507000-00005.
45. Tanida, I., Ueno, T. and Kominami, E. (2008) LC3 and autophagy. Methods Mol. Biol. 445, 77-88 doi:10.1007/978-1-59745-157-4-4.
46. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T. et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728 doi:10.1093/emboj/19.21.5720.
47. Yang, J., Carra, S., Zhu, W.-G. and Kampinga, H.H. (2013) The regulation of the autophagic network and its implications for human disease. Int. J. Biol. Sci. 9, 1121-1133 doi:10.7150/ijbs.6666.
48. Zhang, X., Cheng, X., Yu, L., Yang, J., Calvo, R., Patnaik, S. et al. (2016) MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nat. Commun. 7, 12109 doi:10.1038/ncomms12109.
49. Cheung, K.G., Cole, L.K., Xiang, B., Chen, K., Ma, X., Myal, Y. et al. (2015) Sirtuin-3 (SIRT3) protein attenuates doxorubicin-induced oxidative stress and improves mitochondrial respiration in H9c2 cardiomyocytes. J. Biol. Chem. 290, 10981-10993 doi:10.1074/jbc.M114.607960.
50. Pillai, V.B., Bindu, S., Sharp, W., Fang, Y.H., Kim, G., Gupta, M. et al. (2016) Sirt3 protects mitochondrial DNA damage and blocks the development of doxorubicin-induced cardiomyopathy in mice. Am. J. Physiol. Heart Circ. Physiol. 310, H962-H972 PMID: 26873966.
51. Wang, X.-Y., Yang, C.-T., Zheng, D.-D., Mo, L.-Q., Lan, A.-P., Yang, Z.-L. et al. (2012) Hydrogen sulfide protects H9c2 cells against doxorubicin-induced cardiotoxicity through inhibition of endoplasmic reticulum stress. Mol. Cell. Biochem. 363, 419-426 doi:10.1007/s11010-011-1194-6.
52. Konorev, E.A., Vanamala, S. and Kalyanaraman, B. (2008) Differences in doxorubicin-induced apoptotic signaling in adult and immature cardiomyocytes. Free Radic. Biol. Med. 45, 1723-1728 doi:10.1016/j.freeradbiomed.2008.09.006.
53. Pereira, S.L., Ramalho-Santos, J., Branco, A.F., Sardão, V.A., Oliveira, P.J. and Carvalho, R.A. (2011) Metabolic remodeling during H9c2 myoblast differentiation: Relevance for in vitro toxicity studies. Cardiovasc. Toxicol. 11, 180-190 doi:10.1007/s12012-011-9112-4.
54. Im-Aram, A., Farrand, L., Bae, S.-M., Song, G., Song, Y.S., Han, J.Y. et al. (2013) The mTORC2 component rictor contributes to cisplatin resistance in human ovarian cancer cells. PLoS ONE 8, e75455 doi:10.1371/journal.pone.0075455.
55. Seok, S., Fu, T., Choi, S.E., Li, Y., Zhu, R., Kumar, S. et al. (2014) Transcriptional regulation of autophagy by an FXR-CREB axis. Nature 516, 108-111 PMID: 25383523.
56. Tiribuzi, R., Crispoltoni, L., Porcellati, S., Di Lullo, M., Florenzano, F., Pirro, M. et al. (2014) miR128 up-regulation correlates with impaired amyloid β (1-42) degradation in monocytes from patients with sporadic Alzheimer's disease. Neurobiol. Aging 35, 345-356 doi:10.1016/j.neurobiolaging.2013.08.003.
57. Lu, L., Wu, W., Yan, J., Li, X., Yu, H. and Yu, X. (2009) Adriamycin-induced autophagic cardiomyocyte death plays a pathogenic role in a rat model of heart failure. Int. J. Cardiol. 134, 82-90 doi:10.1016/j.ijcard.2008.01.043.
58. Kawaguchi, T., Takemura, G., Kanamori, H., Takeyama, T., Watanabe, T., Morishita, K. et al. (2012) Prior starvation mitigates acute doxorubicin cardiotoxicity through restoration of autophagy in affected cardiomyocytes. Cardiovasc. Res. 96, 456-465 doi:10.1093/cvr/cvs282.
59. Itakura, E. and Mizushima, N. (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6, 764-776 doi:10.4161/auto.6.6.12709.
60. Xu, X., Bucala, R. and Ren, J. (2013) Macrophage migration inhibitory factor deficiency augments doxorubicin-induced cardiomyopathy. J. Am. Heart Assoc. 2, e000439 doi:10.1161/JAHA.113.000439.
61. Medina, D.L., Fraldi, A., Bouche, V., Annunziata, F., Mansueto, G., Spampanato, C. et al. (2011) Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev. Cell 21, 421-430 doi:10.1016/j.devcel.2011.07.016.
62. Demers-Lamarche, J., Guillebaud, G., Tlili, M., Todkar, K., Bélanger, N., Grondin, M. et al. (2016) Loss of mitochondrial function impairs lysosomes. J. Biol. Chem. 291, 10263-10276 doi:10.1074/jbc.M115.695825.
63. Martina, J.A., Chen, Y., Gucek, M. and Puertollano, R. (2012) MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 8, 903-914 doi:10.4161/auto.19653.
64. Kuo, T.H., Giacomelli, F. and Wiener, J. (1984) Lysosomal and nonlysosomal proteolytic activities in experimental diabetic cardiomyopathy. Exp. Mol. Pathol. 40, 280-287 doi:10.1016/0014-4800(84)90045-5.
65. Spira, D., Stypmann, J., Tobin, D.J., Petermann, I., Mayer, C., Hagemann, S. et al. (2007) Cell type-specific functions of the lysosomal protease cathepsin L in the heart. J. Biol. Chem. 282, 37045-37052 doi:10.1074/jbc.M703447200.
66. Orenstein, S.J. and Cuervo, A.M. (2010) Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin. Cell Dev. Biol. 21, 719-726 doi:10.1016/j.semcdb.2010.02.005.