Regulation of the transcription factor EB-PGC1α axis by beclin-1 controls mitochondrial quality and cardiomyocyte death under stress

Molecular and Cellular Biology

Volumn 35, Issue 6, 2015, Pages 956-976

  Ma, Xiucui ^a,b   Liu, Haiyan ^a,b   Murphy, John T ^a   Foyil, Sarah R ^a,b   Godar, Rebecca J ^a,b   Abuirqeba, Haedar ^a   Weinheimer, Carla J ^a   Barger, Philip M ^a   Diwan, Abhinav ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CATHEPSIN B; CATHEPSIN D; INITIATION FACTOR 4E BINDING PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MITOCHONDRIAL DNA; PROTEIN BNIP3; REACTIVE OXYGEN METABOLITE; S6 KINASE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EB PGC1ALPHA; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; BASE MISPAIRING; BIOGENESIS; CELL DEATH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPHOSPHORYLATION; DEPOLARIZATION; ENZYME PHOSPHORYLATION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HYPOXIA; IMMUNOHISTOCHEMISTRY; LYSOSOME; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MITOCHONDRION SWELLING; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; REOXYGENATION; REPERFUSION INJURY; STRESS; UPREGULATION; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE CELL; CELL CULTURE; GENETIC TRANSCRIPTION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DEATH; CELLS, CULTURED; HEK293 CELLS; HUMANS; LYSOSOMES; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84923147814     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01091-14     Document Type: Article

References (57)

1. Leone TC, Kelly DP. 2011. Transcriptional control of cardiac fuel metabolism and mitochondrial function. Cold Spring Harb Symp Quant Biol 76:175-182. http://dx.doi.org/10.1101/sqb.2011.76.011965.
2. Hausenloy DJ, Duchen MR, Yellon DM. 2003. Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury. Cardiovasc Res 60:617-625. http://dx.doi.org/10.1016/j.cardiores.2003.09.025.
3. Carreira RS, Lee Y, Ghochani M, Gustafsson AB, Gottlieb RA. 2010. Cyclophilin D is required for mitochondrial removal by autophagy in cardiac cells. Autophagy 6:462-472. http://dx.doi.org/10.4161/auto.6.4.11553.
4. Kubli DA, Zhang X, Lee Y, Hanna RA, Quinsay MN, Nguyen CK, Jimenez R, Petrosyan S, Murphy AN, Gustafsson AB. 2013. Parkin protein deficiency exacerbates cardiac injury and reduces survival following myocardial infarction. J Biol Chem 288:915-926. http://dx.doi.org/10.1074/jbc.M112.411363.
5. 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 AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 100:914-922. http://dx.doi.org/10.1161/01.RES.0000261924.76669.36.
6. Ma X, Liu H, Foyil SR, Godar RJ, Weinheimer CJ, Hill JA, Diwan A. 2012. Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation 125:3170-3181. http://dx.doi.org/10.1161/CIRCULATIONAHA.111.041814.
7. Bruick RK. 2000. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci U S A 97:9082-9087. http://dx.doi.org/10.1073/pnas.97.16.9082.
8. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. 2002. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci U S A 99:12825-12830. http://dx.doi.org/10.1073/pnas.202474099.
9. Chen G, Ray R, Dubik D, Shi L, Cizeau J, Bleackley RC, Saxena S, Gietz RD, Greenberg AH. 1997. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J Exp Med 186:1975-1983. http://dx.doi.org/10.1084/jem.186.12.1975.
10. Kubli DA, Ycaza JE, Gustafsson AB. 2007. Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak. Biochem J 405:407-415. http://dx.doi.org/10.1042/BJ20070319.
11. Regula KM, Ens K, Kirshenbaum LA. 2002. Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ Res 91:226-231. http://dx.doi.org/10.1161/01.RES.0000029232.42227.16.
12. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, Gustafsson AB. 2007. Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14:146-157. http://dx.doi.org/10.1038/sj.cdd.4401936.
13. Hamacher-Brady A, Brady NR, Gottlieb RA, Gustafsson AB. 2006. Autophagy as a protective response to Bnip3-mediated apoptotic signaling in the heart. Autophagy 2:307-309. http://dx.doi.org/10.4161/auto.2947.
14. Zhang H, Bosch-Marce M, Shimoda LA, Tan YS, Baek JH, Wesley JB, Gonzalez FJ, Semenza GL. 2008. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem 283:10892-10903. http://dx.doi.org/10.1074/jbc.M800102200.
15. Ma X, Godar RJ, Liu H, Diwan A. 2012. Enhancing lysosome biogenesis attenuates BNIP3-induced cardiomyocyte death. Autophagy 8:297-309. http://dx.doi.org/10.4161/auto.18658.
16. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ. 2011. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331:456-461. http://dx.doi.org/10.1126/science.1196371.
17. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. 2007. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 13:619-624. http://dx.doi.org/10.1038/nm1574.
18. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, Mi N, Zhao Y, Liu Z, Wan F, Hailey DW, Oorschot V, Klumperman J, Baehrecke EH, Lenardo MJ. 2010. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465:942-946. http://dx.doi.org/10.1038/nature09076.
19. Rong Y, McPhee CK, Deng S, Huang L, Chen L, Liu M, Tracy K, Baehrecke EH, Yu L, Lenardo MJ. 2011. Spinster is required for autophagic lysosome reformation and mTOR reactivation following starvation. Proc Natl Acad Sci U S A 108:7826-7831. http://dx.doi.org/10.1073/pnas.1013800108.
20. Sridhar S, Patel B, Aphkhazava D, Macian F, Santambrogio L, Shields D, Cuervo AM. 2013. The lipid kinase PI4KIIIbeta preserves lysosomal identity. EMBOJ 32:324-339. http://dx.doi.org/10.1038/emboj.2012.341.
21. Martina JA, Chen Y, Gucek M, Puertollano R. 2012. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 8:903-914. http://dx.doi.org/10.4161/auto.19653.
22. Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J, Angarola B, Walther TC, Ferguson SM. 2012. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 5:ra42. http://dx.doi.org/10.1126/scisignal.2002790.
23. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A. 2011. TFEB links autophagy to lysosomal biogenesis. Science 332:1429-1433. http://dx.doi.org/10.1126/science.1204592.
24. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V, Sabatini D, Ballabio A. 2012. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 31:1095-1108. http://dx.doi.org/10.1038/emboj.2012.32.
25. Settembre C, De Cegli R, Mansueto G, Saha PK, Vetrini F, Visvikis O, Huynh T, Carissimo A, Palmer D, Klisch TJ, Wollenberg AC, Di Bernardo D, Chan L, Irazoqui JE, Ballabio A. 2013. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat Cell Biol 15:647-658. http://dx.doi.org/10.1038/ncb2718.
26. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B. 2003. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112:1809-1820. http://dx.doi.org/10.1172/JCI20039.
27. 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. http://dx.doi.org/10.4161/auto.5603.
28. Rikka S, Quinsay MN, Thomas RL, Kubli DA, Zhang X, Murphy AN, Gustafsson AB. 2011. Bnip3 impairs mitochondrial bioenergetics and stimulates mitochondrial turnover. Cell Death Differ 18:721-731. http://dx.doi.org/10.1038/cdd.2010.146.
29. Pagel-Langenickel I, Bao J, Joseph JJ, Schwartz DR, Mantell BS, Xu X, Raghavachari N, Sack MN. 2008. PGC-1alpha integrates insulin signaling, mitochondrial regulation, and bioenergetic function in skeletal muscle. J Biol Chem 283:22464-22472. http://dx.doi.org/10.1074/jbc.M800842200.
30. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J, Deeney JT, Corkey BE, Shirihai OS. 2008. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 27:433-446. http://dx.doi.org/10.1038/sj.emboj.7601963.
31. Chambers KT, Leone TC, Sambandam N, Kovacs A, Wagg CS, Lopaschuk GD, Finck BN, Kelly DP. 2011. Chronic inhibition of pyruvate dehydrogenase in heart triggers an adaptive metabolic response. J Biol Chem 286:11155-11162. http://dx.doi.org/10.1074/jbc.M110.217349.
32. Hu J, Zacharek S, He YJ, Lee H, Shumway S, Duronio RJ, Xiong Y. 2008. WD40 protein FBW5 promotes ubiquitination of tumor suppressor TSC2 by DDB1-CUL4-ROC1 ligase. Genes Dev 22:866-871. http://dx.doi.org/10.1101/gad.1624008.
33. Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, Ballabio A. 2011. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 20:3852-3866. http://dx.doi.org/10.1093/hmg/ddr306.
34. Xiao Q, Yan P, Ma X, Liu H, Perez R, Zhu A, Gonzales E, Burchett JM, Schuler DR, Cirrito JR, Diwan A, Lee JM. 2014. Enhancing astrocytic lysosome biogenesis facilitates Aß clearance and attenuates amyloid plaque pathogenesis. J Neurosci 34:9607-9620. http://dx.doi.org/10.1523/JNEUROSCI.3788-13.2014.
35. Sardiello M, Palmieri M, di Ronza A, Medina DL, Valenza M, Gennarino VA, Di Malta C, Donaudy F, Embrione V, Polishchuk RS, Banfi S, Parenti G, Cattaneo E, Ballabio A. 2009. A gene network regulating lysosomal biogenesis and function. Science 325:473-477. http://dx.doi.org/10.1126/science.1174447.
36. Kiffin R, Christian C, Knecht E, Cuervo AM. 2004. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 15:4829-4840. http://dx.doi.org/10.1091/mbc.E04-06-0477.
37. Wang L, Gout I, Proud CG. 2001. Cross-talk between the ERK and p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J Biol Chem 276:32670-32677. http://dx.doi.org/10.1074/jbc.M102776200.
38. Martina JA, Puertollano R. 2013. Rag GTPases mediate amino aciddependent recruitment of TFEB and MITF to lysosomes. J Cell Biol 200:475-491. http://dx.doi.org/10.1083/jcb.201209135.
39. Behrends C, Sowa ME, Gygi SP, Harper JW. 2010. Network organization of the human autophagy system. Nature 466:68-76. http://dx.doi.org/10.1038/nature09204.
40. Menon S, Dibble CC, Talbott G, Hoxhaj G, Valvezan AJ, Takahashi H, Cantley LC, Manning BD. 2014. Spatial control of the TSC complex integrates insulin and nutrient regulation of mTORC1 at the lysosome. Cell 156:771-785. http://dx.doi.org/10.1016/j.cell.2013.11.049.
41. Dibble CC, Elis W, Menon S, Qin W, Klekota J, Asara JM, Finan PM, Kwiatkowski DJ, Murphy LO, Manning BD. 2012. TBC1D7 is a third subunit of the TSC1-TSC2 complex upstream of mTORC1. Mol Cell 47:535-546. http://dx.doi.org/10.1016/j.molcel.2012.06.009.
42. Scott I, Webster BR, Chan CK, Okonkwo JU, Han K, Sack MN. 2014. GCN5-like protein 1 (GCN5L1) controls mitochondrial content through coordinated regulation of mitochondrial biogenesis and mitophagy. J Biol Chem 289:2864-2872. http://dx.doi.org/10.1074/jbc.M113.521641.
43. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, Flanagan DP, Medeiros DM, Kovacs A, Kelly DP. 2008. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev 22:1948-1961. http://dx.doi.org/10.1101/gad.1661708.
44. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413:179-183. http://dx.doi.org/10.1038/35093131.
45. Wu Z, Huang X, Feng Y, Handschin C, Feng Y, Gullicksen PS, Bare O, Labow M, Spiegelman B, Stevenson SC. 2006. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc Natl Acad Sci U S A 103:14379-14384. http://dx.doi.org/10.1073/pnas.0606714103.
46. Tan CY, Hagen T. 2013. Post-translational regulation of mTOR complex 1 in hypoxia and reoxygenation. Cell Signal 25:1235-1244. http://dx.doi.org/10.1016/j.cellsig.2013.02.012.
47. O'Rourke EJ, Ruvkun G. 2013. MXL-3 and HLH-30 transcriptionally link lipolysis and autophagy to nutrient availability. Nat Cell Biol 15:668-676. http://dx.doi.org/10.1038/ncb2741.
48. Kloner RA, Hale SL, Dai W, Gorman RC, Shuto T, Koomalsingh KJ, Gorman JH, III, Sloan RC, Frasier CR, Watson CA, Bostian PA, Kypson AP, Brown DA. 2012. Reduction of ischemia/reperfusion injury with bendavia, a mitochondria-targeting cytoprotective peptide. J Am Heart Assoc 1:e001644. http://dx.doi.org/10.1161/JAHA.112.001644.
49. Hughes AL, Gottschling DE. 2012. An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492:261-265. http://dx.doi.org/10.1038/nature11654.
50. Kurihara Y, Kanki T, Aoki Y, Hirota Y, Saigusa T, Uchiumi T, Kang D. 2012. Mitophagy plays an essential role in reducing mitochondrial production of reactive oxygen species and mutation of mitochondrial DNA by maintaining mitochondrial quantity and quality in yeast. J Biol Chem 287:3265-3272. http://dx.doi.org/10.1074/jbc.M111.280156.
51. Rafelski SM, Viana MP, Zhang Y, Chan YH, Thorn KS, Yam P, Fung JC, Li H, Costa LF, Marshall WF. 2012. Mitochondrial network size scaling in budding yeast. Science 338:822-824. http://dx.doi.org/10.1126/science.1225720.
52. Wu JJ, Quijano C, Chen E, Liu H, Cao L, Fergusson MM, Rovira II, Gutkind S, Daniels MP, Komatsu M, Finkel T. 2009. Mitochondrial dysfunction and oxidative stress mediate the physiological impairment induced by the disruption of autophagy. Aging (Albany, NY) 1:425-437.
53. Chauhan S, Goodwin JG, Chauhan S, Manyam G, Wang J, Kamat AM, Boyd DD. 2013. ZKSCAN3 is a master transcriptional repressor of autophagy. Mol Cell 50:16-28. http://dx.doi.org/10.1016/j.molcel.2013.01.024.
54. Pan W, Zhong Y, Cheng C, Liu B, Wang L, Li A, Xiong L, Liu S. 2013. MiR-30-regulated autophagy mediates angiotensin II-induced myocardial hypertrophy. PLoS One 8:e53950. http://dx.doi.org/10.1371/journal.pone.0053950.
55. Liang XH, Yu J, Brown K, Levine B. 2001. Beclin 1 contains a leucinerich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res 61:3443-3449.
56. Kuiper RP, Schepens M, Thijssen J, van Asseldonk M, van den Berg E, Bridge J, Schuuring E, Schoenmakers EF, van Kessel AG. 2003. Upregulation of the transcription factor TFEB in t(6;11)(p21;q13)-positive renal cell carcinomas due to promoter substitution. Hum Mol Genet 12:1661-1669. http://dx.doi.org/10.1093/hmg/ddg178.
57. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 100:15077-15082. http://dx.doi.org/10.1073/pnas.2436255100.