Loss of MCL-1 leads to impaired autophagy and rapid development of heart failure

Genes and Development

Volumn 27, Issue 12, 2013, Pages 1365-1377

  Thomas, Robert L ^a   Roberts, David J ^b   Kubli, Dieter A ^a   Lee, Youngil ^a   Quinsay, Melissa N ^a   Owens, Jarvis B ^a   Fischer, Kimberlee M ^c   Sussman, Mark A ^c   Miyamoto, Shigeki ^a,b   Gustafsson, Åsa B ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

Autophagy; BCL 2; Heart failure; MCL 1; Mitochondria; Necrosis

Indexed keywords

CALCIUM ION; CYCLOPHILIN D; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PROTEIN MCL 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CARDITIS; CELL RESPIRATION; CONTROLLED STUDY; DEATH; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENOTYPE; HEART CONTRACTION; HEART FAILURE; HEART HYPERTROPHY; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART STRESS; HEART VENTRICLE HYPERTROPHY; KNOCKOUT MOUSE; MORTALITY; MOUSE; NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SARCOMERE; SURVIVAL TIME; ULTRASTRUCTURE ANALYSIS AND ELECTRON MICROSCOPY;

AUTOPHAGY; BCL-2; HEART FAILURE; MCL-1; MITOCHONDRIA; NECROSIS;

ANIMALS; AUTOPHAGY; CARDIOMEGALY; CELL RESPIRATION; CYCLOPHILINS; HEART FAILURE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; NECROSIS; PROTO-ONCOGENE PROTEINS C-BCL-2; SURVIVAL ANALYSIS;

MUS;

EID: 84879138938     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.215871.113     Document Type: Article

References (51)

1. Azmi AS, Wang Z, Philip PA, Mohammad RM, Sarkar FH. 2011. Emerging Bcl-2 inhibitors for the treatment of cancer. Expert Opin Emerg Drugs 16: 59-70.
2. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, et al. 2005. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434: 658-662.
3. Bandyopadhyay U, Sridhar S, Kaushik S, Kiffin R, Cuervo AM. 2010. Identification of regulators of chaperone-mediated autophagy. Mol Cell 39: 535-547.
4. Bensinger SJ, Christofk HR. 2012. New aspects of the Warburg effect in cancer cell biology. Semin Cell Dev Biol 23: 352-361.
5. Berman SB, Chen YB, Qi B, McCaffery JM, Rucker EB 3rd, Goebbels S, Nave KA, Arnold BA, Jonas EA, Pineda FJ, et al. 2009. Bcl-xL increases mitochondrial fission, fusion, and biomass in neurons. J Cell Biol 184: 707-719.
6. Dash R, Azab B, Quinn BA, Shen X, Wang XY, Das SK, Rahmani M, Wei J, Hedvat M, Dent P, et al. 2011. Apogossypol derivative BI-97C1 (Sabutoclax) targeting Mcl-1 sensitizes prostate cancer cells to mda-7/IL-24-mediated toxicity. Proc Natl Acad Sci 108: 8785-8790.
7. Diwan A, Krenz M, Syed FM, Wansapura J, Ren X, Koesters AG, Li H, Kirshenbaum LA, Hahn HS, Robbins J, et al. 2007. Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. J Clin Invest 117: 2825-2833.
8. Dorn GW 2nd. 2010. Mitochondrial pruning by Nix and BNip3: An essential function for cardiac-expressed death factors. J Cardiovasc Transl Res 3: 374-383.
9. Frangogiannis NG. 2012. Regulation of the inflammatory response in cardiac repair. Circ Res 110: 159-173.
10. Frazier AE, Thorburn DR. 2012. Biochemical analyses of the electron transport chain by spectrophotometry. Methods Mol Biol 837: 49-62.
11. Germain M, Nguyen AP, Le Grand JN, Arbour N, Vanderluit JL, Park DS, Opferman JT, Slack RS. 2011. MCL-1 is a stress sensor that regulates autophagy in a developmentally regulated manner. EMBO J 30: 395-407.
12. Gustafsson AB, Gottlieb RA. 2007. Bcl-2 family members and apoptosis, taken to heart. Am J Physiol Cell Physiol 292: C45-C51.
13. Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, Gustafsson Å B. 2012. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem 287: 19094-19104.
14. He C, Bassik MC, Moresi V, Sun K, Wei Y, Zou Z, An Z, Loh J, Fisher J, Sun Q, et al. 2012. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 481: 511-515.
15. Huang J, Ito Y, Morikawa M, Uchida H, Kobune M, Sasaki K, Abe T, Hamada H. 2003. Bcl-xL gene transfer protects the heart against ischemia/reperfusion injury. Biochem Biophys Res Commun 311: 64-70.
16. Imahashi K, Schneider MD, Steenbergen C, Murphy E. 2004. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ Res 95: 734-741.
17. Iwai-Kanai E, Yuan H, Huang C, Sayen MR, Perry-Garza CN, Kim L, Gottlieb RA. 2008. A method to measure cardiac autophagic flux in vivo. Autophagy 4: 322-329.
18. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728.
19. Kang MH, Reynolds CP. 2009. Bcl-2 inhibitors: Targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15: 1126-1132.
20. Kirshenbaum LA, de Moissac D. 1997. The bcl-2 gene product prevents programmed cell death of ventricular myocytes. Circulation 96: 1580-1585.
21. Koitabashi N, Bedja D, Zaiman AL, Pinto YM, Zhang M, Gabrielson KL, Takimoto E, Kass DA. 2009. Avoidance of transient cardiomyopathy in cardiomyocyte-targeted tamoxifen-induced MerCreMer gene deletion models. Circ Res 105: 12-15.
22. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S, et al. 2007. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131: 1149-1163.
23. Krajewski S, Bodrug S, Krajewska M, Shabaik A, Gascoyne R, Berean K, Reed JC. 1995. Immunohistochemical analysis of Mcl-1 protein in human tissues. Differential regulation of Mcl-1 and Bcl-2 protein production suggests a unique role for Mcl-1 in control of programmed cell death in vivo. Am J Pathol 146: 1309-1319.
24. Kubli DA, Gustafsson Å B. 2012. Mitochondria and mitophagy: The yin and yang of cell death control. Circ Res 111: 1208-1221.
25. Kubli DA, Ycaza JE, Gustafsson AB. 2007. Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak. Biochem J 405: 407-415.
26. Kubli DA, Zhang X, Lee Y, Hanna RA, Quinsay MN, Nguyen CK, Jimenez R, Petrosyan S, Murphy AN, Gustafsson AB. 2013. Parkin deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem 288: 915-926.
27. Levine B, Kroemer G. 2008. Autophagy in the pathogenesis of disease. Cell 132: 27-42.
28. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, et al. 2007. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J 26: 2527-2539.
29. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J. 2007. Distinct roles of autophagy in the heart during ischemia and reperfusion: Roles of AMPactivated protein kinase and Beclin 1 in mediating autophagy. Circ Res 100: 914-922.
30. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S, et al. 1995. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267: 1506-1510.
31. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, AsahiM, et al. 2007. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 13: 619-624.
32. Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T, Mora M, Riggs JE, Oh SJ, Koga Y, et al. 2000. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 406: 906-910.
33. Opferman JT, Letai A, Beard C, SorcinelliMD, Ong CC, Korsmeyer SJ. 2003. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426: 671-676.
34. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939.
35. Perciavalle RM, Stewart DP, Koss B, Lynch J, Milasta S, Bathina M, Temirov J, Cleland MM, Pelletier S, Schuetz JD, et al. 2012. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat Cell Biol 14: 575-583.
36. Quinsay MN, Lee Y, Rikka S, Sayen MR, Molkentin JD, Gottlieb RA, Gustafsson AB. 2010a. Bnip3 mediates permeabilization of mitochondria and release of cytochrome c via a novel mechanism. J Mol Cell Cardiol 48: 1146-1156.
37. Quinsay MN, Thomas RL, Lee Y, Gustafsson AB. 2010b. Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6: 855-862.
38. Rinkenberger JL, Horning S, Klocke B, Roth K, Korsmeyer SJ. 2000. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev 14: 23-27.
39. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
40. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM, Penninger JM, Molkentin JD. 2001. Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res 89: 20-25.
41. Susin SA, Lorenzo HK, Zmzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Constantini P, Loeffler M, et al. 1999. Molecular characterization of mitochondrial apoptosisinducing factor. Nature 397: 441-446.
42. Thomas LW, Lam C, Edwards SW. 2010. Mcl-1; the molecular regulation of protein function. FEBS Lett 584: 2981-2989.
43. Veis DJ, Sorenson CM, Shutter JR, Korsmeyer SJ. 1993. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75: 229-240.
44. Wang X, Bathina M, Lynch J, Koss B, Calabrese C, Frase S, Schuetz JD, Rehg JE, Opferman JT. 2013. Deletion of MCL-1 causes lethal cardiac failure and mitochondrial dysfunction. Genes Dev (this issue) doi: 10.1101/gad.215855.113.
45. Wencker D, Chandra M, Nguyen K, Miao W, Garantziotis S, Factor SM, Shirani J, Armstrong RC, Kitsis RN. 2003. A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest 111: 1497-1594.
46. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S, Yang Y, Calvert JW, Lindsten T, Thompson CB, et al. 2012. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci 109: 6566-6571.
47. Wu CF, Bishopric NH, Pratt RE. 1997. Atrial natriuretic peptide induces apoptosis in neonatal rat cardiac myocytes. J Biol Chem 272: 14860-14866.
48. Xiang SY, Vanhoutte D, Del Re DP, Purcell NH, Ling H, Banerjee I, Bossuyt J, Lang RA, Zheng Y, Matkovich SJ, et al. 2011. RhoA protects the mouse heart against ischemia/reperfusion injury. J Clin Invest 121: 3269-3276.
49. Zhou P, Qian L, Kozopas KM, Craig RW. 1997. Mcl-1, a Bcl-2 family member, delays the death of hematopoietic cells under a variety of apoptosis-inducing conditions. Blood 89: 630-643.
50. Zhu L, Yu Y, Chua BH, Ho YS, Kuo TH. 2001. Regulation of sodium-calcium exchange and mitochondrial energetics by Bcl-2 in the heart of transgenic mice. J Mol Cell Cardiol 33: 2135-2144.
51. Zhu H, Tannous P, Johnstone JL, Kong Y, Shelton JM, Richardson JA, Le V, Levine B, Rothermel BA, Hill JA. 2007. Cardiac autophagy is a maldaptive response to hemodynamic stress. J Clin Invest 177: 1782-1793.