Aβ-Induced Drp1 phosphorylation through Akt activation promotes excessive mitochondrial fission leading to neuronal apoptosis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1863, Issue 11, 2016, Pages 2820-2834

  Kim, Dah Ihm ^a   Lee, Ki Hoon ^a   Gabr, Amr Ahmed ^a   Choi, Gee Euhn ^a   Kim, Jun Sung ^a   Ko, So Hee ^a   Han, Ho Jae ^a  

^a Seoul National University   (South Korea)

Author keywords

Akt; Amyloid (A ); Autophagy; Drp1; Mitochondrial dynamics; ROS

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN; CASPASE 3; CASPASE 9; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; AMYLOID BETA-PROTEIN (1-42); DNM1L PROTEIN, HUMAN; DNM1L PROTEIN, MOUSE; DYNAMIN; GUANOSINE TRIPHOSPHATASE; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL PROTEIN; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; PEPTIDE FRAGMENT; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CALCIUM TRANSPORT; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HIPPOCAMPUS; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; OXIDATIVE STRESS; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR CELL LINE;

AMYLOID BETA-PEPTIDES; ANIMALS; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; DYNAMINS; GTP PHOSPHOHYDROLASES; HIPPOCAMPUS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; NEURONS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TOR SERINE-THREONINE KINASES; TRANSFECTION;

EID: 84986612733     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2016.09.003     Document Type: Article

References (81)

1. [1] Saxena, S., Caroni, P., Selective neuronal vulnerability in neurodegenerative diseases: from stressor thresholds to degeneration. Neuron 71 (2011), 35–48.
2. [2] Marr, R.A., Hafez, D.M., Amyloid-β and Alzheimer's disease: the role of neprilysin-2 in amyloid-β clearance. Front. Aging Neurosci., 6, 2014, 187.
3. [3] Tu, S., Okamoto, S.-i., Lipton, S.A., Xu, H., Oligomeric Aβ-induced synaptic dysfunction in Alzheimer's disease. Mol. Neurodegener. 9 (2014), 1–12.
4. [4] Silva, D.F., Esteves, A.R., Oliveira, C.R., Cardoso, S.M., Mitochondria: the common upstream driver of amyloid-β and tau pathology in Alzheimer's disease. Current Alzheimer research 8 (2011), 563–572.
5. [5] Klein, W.L., Synaptotoxic amyloid-β oligomers: a molecular basis for the cause, diagnosis, and treatment of Alzheimer's disease?. Journal of Alzheimer's disease: JAD 33:Suppl. 1 (2013), S49–S65.
6. [6] Verri, M., Pastoris, O., Dossena, M., Aquilani, R., Guerriero, F., Cuzzoni, G., Venturini, L., Ricevuti, G., Bongiorno, A.I., Mitochondrial alterations, oxidative stress and neuroinflammation in Alzheimer's disease. Int. J. Immunopathol. Pharmacol. 25 (2012), 345–353.
7. [7] Moreira, P.I., Carvalho, C., Zhu, X., Smith, M.A., Perry, G., Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology. Biochim. Biophys. Acta 1802 (2010), 2–10.
8. [8] Suliman, H.B., Piantadosi, C.A., Mitochondrial quality control as a therapeutic target. Pharmacol. Rev. 68 (2016), 20–48.
9. [9] Eckert, G.P., Renner, K., Eckert, S.H., Eckmann, J., Hagl, S., Abdel-Kader, R.M., Kurz, C., Leuner, K., Muller, W.E., Mitochondrial dysfunction—a pharmacological target in Alzheimer's disease. Mol. Neurobiol. 46 (2012), 136–150.
10. [10] DuBoff, B., Feany, M., Gotz, J., Why size matters - balancing mitochondrial dynamics in Alzheimer's disease. Trends Neurosci. 36 (2013), 325–335.
11. [11] Reddy, P.H., Tripathi, R., Troung, Q., Tirumala, K., Reddy, T.P., Anekonda, V., Shirendeb, U.P., Calkins, M.J., Reddy, A.P., Mao, P., Manczak, M., Abnormal mitochondrial dynamics and synaptic degeneration as early events in Alzheimer's disease: implications to mitochondria-targeted antioxidant therapeutics. Biochim. Biophys. Acta 1822 (2012), 639–649.
12. [12] Seo, A.Y., Joseph, A.M., Dutta, D., Hwang, J.C., Aris, J.P., Leeuwenburgh, C., New insights into the role of mitochondria in aging: mitochondrial dynamics and more. J. Cell Sci. 123 (2010), 2533–2542.
13. [13] Palmer, C.S., Osellame, L.D., Stojanovski, D., Ryan, M.T., The regulation of mitochondrial morphology: intricate mechanisms and dynamic machinery. Cell. Signal. 23 (2011), 1534–1545.
14. [14] Han, X.J., Tomizawa, K., Fujimura, A., Ohmori, I., Nishiki, T., Matsushita, M., Matsui, H., Regulation of mitochondrial dynamics and neurodegenerative diseases. Acta Med. Okayama 65 (2011), 1–10.
15. [15] Cho, B., Choi, S.Y., Cho, H.M., Kim, H.J., Sun, W., Physiological and pathological significance of dynamin-related protein 1 (drp1)-dependent mitochondrial fission in the nervous system. Exp Neurobiol 22 (2013), 149–157.
16. [16] Zaja, I., Bai, X., Liu, Y., Kikuchi, C., Dosenovic, S., Yan, Y., Canfield, S.G., Bosnjak, Z.J., Cdk1, PKCδ and calcineurin-mediated Drp1 pathway contributes to mitochondrial fission-induced cardiomyocyte death. Biochem. Biophys. Res. Commun. 453 (2014), 710–721.
17. [17] Kashatus, J.A., Nascimento, A., Myers, L.J., Sher, A., Byrne, F.L., Hoehn, K.L., Counter, C.M., Kashatus, D.F., Erk2 phosphorylation of Drp1 promotes mitochondrial fission and MAPK-driven tumor growth. Mol. Cell 57 (2015), 537–551.
18. [18] Prieto, J., Leon, M., Ponsoda, X., Sendra, R., Bort, R., Ferrer-Lorente, R., Raya, A., Lopez-Garcia, C., Torres, J., Early ERK1/2 activation promotes DRP1-dependent mitochondrial fission necessary for cell reprogramming. Nat. Commun., 7, 2016, 11124.
19. [19] Cho, B., Cho, H.M., Kim, H.J., Jeong, J., Park, S.K., Hwang, E.M., Park, J.Y., Kim, W.R., Kim, H., Sun, W., CDK5-dependent inhibitory phosphorylation of Drp1 during neuronal maturation. Exp. Mol. Med., 46, 2014, e105.
20. [20] Cribbs, J.T., Strack, S., Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8 (2007), 939–944.
21. [21] Han, X.J., Lu, Y.F., Li, S.A., Kaitsuka, T., Sato, Y., Tomizawa, K., Nairn, A.C., Takei, K., Matsui, H., Matsushita, M., CaM kinase I α-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell Biol. 182 (2008), 573–585.
22. [22] Wang, W., Wang, Y., Long, J., Wang, J., Haudek, S.B., Overbeek, P., Chang, B.H., Schumacker, P.T., Danesh, F.R., Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab. 15 (2012), 186–200.
23. [23] Shinde, R., Shukla, A., Large-scale first principles configuration interaction calculations of optical absorption in aluminum clusters. Physical chemistry chemical physics: PCCP 16 (2014), 20714–20723.
24. [24] Chou, C.H., Lin, C.C., Yang, M.C., Wei, C.C., Liao, H.D., Lin, R.C., Tu, W.Y., Kao, T.C., Hsu, C.M., Cheng, J.T., Chou, A.K., Lee, C.I., Loh, J.K., Howng, S.L., Hong, Y.R., GSK3β-mediated Drp1 phosphorylation induced elongated mitochondrial morphology against oxidative stress. PLoS One, 7, 2012, e49112.
25. [25] Kandimalla, R., Reddy, P.H., Multiple faces of dynamin-related protein 1 and its role in Alzheimer's disease pathogenesis. Biochim. Biophys. Acta 1862 (2016), 814–828.
26. [26] Bertholet, A.M., Delerue, T., Millet, A.M., Moulis, M.F., David, C., Daloyau, M., Arnaune-Pelloquin, L., Davezac, N., Mils, V., Miquel, M.C., Rojo, M., Belenguer, P., Mitochondrial fusion/fission dynamics in neurodegeneration and neuronal plasticity. Neurobiol. Dis. 90 (2016), 3–19.
27. [27] Yamano, K., Youle, R.J., Coupling mitochondrial and cell division. Nat. Cell Biol. 13 (2011), 1026–1027.
28. [28] Taguchi, N., Ishihara, N., Jofuku, A., Oka, T., Mihara, K., Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282 (2007), 11521–11529.
29. [29] Park, J., Choi, H., Min, J.S., Kim, B., Lee, S.R., Yun, J.W., Choi, M.S., Chang, K.T., Lee, D.S., Loss of mitofusin 2 links β-amyloid-mediated mitochondrial fragmentation and Cdk5-induced oxidative stress in neuron cells. J. Neurochem. 132 (2015), 687–702.
30. [30] Jahani-Asl, A., Huang, E., Irrcher, I., Rashidian, J., Ishihara, N., Lagace, D.C., Slack, R.S., Park, D.S., CDK5 phosphorylates DRP1 and drives mitochondrial defects in NMDA-induced neuronal death. Hum. Mol. Genet. 24 (2015), 4573–4583.
31. [31] Bradshaw, T.Y., Romano, L.E., Duncan, E.J., Nethisinghe, S., Abeti, R., Michael, G.J., Giunti, P., Vermeer, S., Chapple, J.P., A Reduction in Drp1-mediated Fission Compromises Mitochondrial Health in Autosomal Recessive Spastic Ataxia of Charlevoix Saguenay. Human molecular genetics, 2016.
32. [32] Biedler, J.L., Helson, L., Spengler, B.A., Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res. 33 (1973), 2643–2652.
33. [33] Rettig, W.J., Spengler, B.A., Chesa, P.G., Old, L.J., Biedler, J.L., Coordinate changes in neuronal phenotype and surface antigen expression in human neuroblastoma cell variants. Cancer Res. 47 (1987), 1383–1389.
34. [34] Acosta, S., Lavarino, C., Paris, R., Garcia, I., de Torres, C., Rodriguez, E., Beleta, H., Mora, J., Comprehensive characterization of neuroblastoma cell line subtypes reveals bilineage potential similar to neural crest stem cells. BMC Dev. Biol., 9, 2009, 12.
35. [35] Encinas, M., Iglesias, M., Liu, Y., Wang, H., Muhaisen, A., Cena, V., Gallego, C., Comella, J.X., Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J. Neurochem. 75 (2000), 991–1003.
36. [36] Seibenhener, M.L., Wooten, M.W., Isolation and Culture of Hippocampal Neurons from Prenatal Mice. 2012, J. Vis. Exp.
37. [37] Lee, I.S., Jung, K., Kim, I.S., Park, K.I., Amyloid-β oligomers regulate the properties of human neural stem cells through GSK-3β signaling. Exp. Mol. Med., 45, 2013, e60.
38. [38] Song, E.J., Lee, S.J., Lim, H.S., Kim, J.S., Jang, K.K., Choi, S.H., Han, H.J., Vibrio vulnificus VvhA induces autophagy-related cell death through the lipid raft-dependent c-Src/NOX signaling pathway. Sci Rep, 6, 2016, 27080.
39. [39] Lee, S.J., Jung, Y.H., Ryu, J.M., Jang, K.K., Choi, S.H., Han, H.J., VvpE mediates the intestinal colonization of Vibrio vulnificus by the disruption of tight junctions. International journal of medical microbiology: IJMM 306 (2016), 10–19.
40. [40] Lee, S.J., Jung, Y.H., Oh, S.Y., Yong, M.S., Ryu, J.M., Han, H.J., Netrin-1 induces MMP-12-dependent E-cadherin degradation via the distinct activation of PKCα and FAK/Fyn in promoting mesenchymal stem cell motility. Stem Cells Dev. 23 (2014), 1870–1882.
41. [41] Yu, T., Robotham, J.L., Yoon, Y., Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 2653–2658.
42. [42] Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
43. [43] Ostrom, R.S., Gregorian, C., Insel, P.A., Cellular release of and response to ATP as key determinants of the set-point of signal transduction pathways. J. Biol. Chem. 275 (2000), 11735–11739.
44. [44] Moon, J.Y., Roh, D.H., Yoon, S.Y., Choi, S.R., Kwon, S.G., Choi, H.S., Kang, S.Y., Han, H.J., Beitz, A.J., Oh, S.B., Lee, J.H., Sigma1 receptors activate astrocytes via p38 MAPK phosphorylation leading to the development of mechanical allodynia in a mouse model of neuropathic pain. Br. J. Pharmacol. 171 (2014), 5881–5897.
45. [45] Suh, H.N., Han, H.J., Sonic hedgehog increases the skin wound-healing ability of mouse embryonic stem cells through the microRNA 200 family. Br. J. Pharmacol. 172 (2015), 815–828.
46. [46] Franken, N.A., Rodermond, H.M., Stap, J., Haveman, J., van Bree, C., Clonogenic assay of cells in vitro. Nat. Protoc. 1 (2006), 2315–2319.
47. [47] Villalonga-Planells, R., Coll-Mulet, L., Martinez-Soler, F., Castano, E., Acebes, J.J., Gimenez-Bonafe, P., Gil, J., Tortosa, A., Activation of p53 by nutlin-3a induces apoptosis and cellular senescence in human glioblastoma multiforme. PLoS One, 6, 2011, e18588.
48. [48] Dikalov, S., Cross talk between mitochondria and NADPH oxidases. Free Radic. Biol. Med. 51 (2011), 1289–1301.
49. [49] Sun, S.Y., N-acetylcysteine, reactive oxygen species and beyond. Cancer biology & therapy 9 (2010), 109–110.
50. [50] Burte, F., Carelli, V., Chinnery, P.F., Yu-Wai-Man, P., Disturbed mitochondrial dynamics and neurodegenerative disorders. Nat. Rev. Neurol. 11 (2015), 11–24.
51. [51] Calkins, M.J., Manczak, M., Mao, P., Shirendeb, U., Reddy, P.H., Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease. Hum. Mol. Genet. 20 (2011), 4515–4529.
52. [52] Manczak, M., Calkins, M.J., Reddy, P.H., Impaired mitochondrial dynamics and abnormal interaction of amyloid β with mitochondrial protein Drp1 in neurons from patients with Alzheimer's disease: implications for neuronal damage. Hum. Mol. Genet. 20 (2011), 2495–2509.
53. [53] Godoy, J.A., Arrazola, M.S., Ordenes, D., Silva-Alvarez, C., Braidy, N., Inestrosa, N.C., Wnt-5a ligand modulates mitochondrial fission-fusion in rat hippocampal neurons. J. Biol. Chem. 289 (2014), 36179–36193.
54. [54] Barsoum, M.J., Yuan, H., Gerencser, A.A., Liot, G., Kushnareva, Y., Graber, S., Kovacs, I., Lee, W.D., Waggoner, J., Cui, J., White, A.D., Bossy, B., Martinou, J.C., Youle, R.J., Lipton, S.A., Ellisman, M.H., Perkins, G.A., Bossy-Wetzel, E., Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J. 25 (2006), 3900–3911.
55. [55] Cho, D.H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., Lipton, S.A., S-nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury. Science 324 (2009), 102–105.
56. [56] Toyama, E.Q., Herzig, S., Courchet, J., Lewis, T.L. Jr., Loson, O.C., Hellberg, K., Young, N.P., Chen, H., Polleux, F., Chan, D.C., Shaw, R.J., Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress. Science 351 (2016), 275–281.
57. [57] Blackstone, C., Chang, C.R., Mitochondria unite to survive. Nat. Cell Biol. 13 (2011), 521–522.
58. [58] Otera, H., Ishihara, N., Mihara, K., New insights into the function and regulation of mitochondrial fission. Biochim. Biophys. Acta 1833 (2013), 1256–1268.
59. [59] Picone, P., Nuzzo, D., Caruana, L., Scafidi, V., Di Carlo, M., Mitochondrial dysfunction: different routes to Alzheimer's disease therapy. Oxidative Med. Cell. Longev., 2014, 2014, 780179.
60. [60] Youle, R.J., Karbowski, M., Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6 (2005), 657–663.
61. [61] Otera, H., Mihara, K., Mitochondrial dynamics: functional link with apoptosis. Int J Cell Biol, 2012, 2012, 821676.
62. [62] Clinton, R.W., Francy, C.A., Ramachandran, R., Qi, X., Mears, J.A., Dynamin-related protein 1 oligomerization in solution impairs functional interactions with membrane-anchored mitochondrial fission factor. J. Biol. Chem. 291 (2016), 478–492.
63. [63] Song, G., Ouyang, G., Bao, S., The activation of Akt/PKB signaling pathway and cell survival. J. Cell. Mol. Med. 9 (2005), 59–71.
64. [64] Kitagishi, Y., Nakanishi, A., Ogura, Y., Matsuda, S., Dietary regulation of PI3K/AKT/GSK-3β pathway in Alzheimer's disease. Alzheimers Res. Ther., 6, 2014, 35.
65. [65] O.N. C, PI3-kinase/Akt/mTOR signaling: impaired on/off switches in aging, cognitive decline and Alzheimer's disease. Exp. Gerontol., 48, 2013, 647–653.
66. [66] Tramutola, A., Triplett, J.C., Di Domenico, F., Niedowicz, D.M., Murphy, M.P., Coccia, R., Perluigi, M., Butterfield, D.A., Alteration of mTOR signaling occurs early in the progression of Alzheimer disease (AD): analysis of brain from subjects with pre-clinical AD, amnestic mild cognitive impairment and late-stage AD. J. Neurochem. 133 (2015), 739–749.
67. [67] Liu, Q., Qiu, J., Liang, M., Golinski, J., van Leyen, K., Jung, J.E., You, Z., Lo, E.H., Degterev, A., Whalen, M.J., Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis., 5, 2014, e1084.
68. [68] Stratton, M., Lee, I.H., Bhattacharyya, M., Christensen, S.M., Chao, L.H., Schulman, H., Groves, J.T., Kuriyan, J., Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity. eLife, 3, 2014, e01610.
69. [69] Ghosh, A., Giese, K.P., Calcium/calmodulin-dependent kinase II and Alzheimer's disease. Molecular brain, 8, 2015, 78.
70. 2 +/calmodulin/CaMKII/CaV1.2 signaling in experimental models of Alzheimer's disease and vascular dementia. Neurosci. Lett. 538 (2013), 60–65.
71. [71] Fan, C.D., Lum, M.A., Xu, C., Black, J.D., Wang, X., Ubiquitin-dependent regulation of phospho-AKT dynamics by the ubiquitin E3 ligase, NEDD4-1, in the insulin-like growth factor-1 response. J. Biol. Chem. 288 (2013), 1674–1684.
72. [72] Ban-Ishihara, R., Ishihara, T., Sasaki, N., Mihara, K., Ishihara, N., Dynamics of nucleoid structure regulated by mitochondrial fission contributes to cristae reformation and release of cytochrome c. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 11863–11868.
73. [73] Estaquier, J., Arnoult, D., Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ. 14 (2007), 1086–1094.
74. [74] Holzerova, E., Prokisch, H., Mitochondria: much ado about nothing? How dangerous is reactive oxygen species production?. Int. J. Biochem. Cell Biol. 63 (2015), 16–20.
75. [75] Hua, Y., Zhang, Y., Ceylan-Isik, A.F., Wold, L.E., Nunn, J.M., Ren, J., Chronic Akt activation accentuates aging-induced cardiac hypertrophy and myocardial contractile dysfunction: role of autophagy. Basic Res. Cardiol. 106 (2011), 1173–1191.
76. [76] Akopova, O.V., Kolchinskaya, L.I., Nosar, V.I., Bouryi, V.A., Mankovska, I.N., Sagach, V.F., Cytochrome C as an amplifier of ROS release in mitochondria. Fiziol. Zh. 58 (2012), 3–12.
77. [77] Zuo, W., Zhang, S., Xia, C.Y., Guo, X.F., He, W.B., Chen, N.H., Mitochondria autophagy is induced after hypoxic/ischemic stress in a Drp1 dependent manner: the role of inhibition of Drp1 in ischemic brain damage. Neuropharmacology 86 (2014), 103–115.
78. [78] Twig, G., Shirihai, O.S., The interplay between mitochondrial dynamics and mitophagy. Antioxid. Redox Signal. 14 (2011), 1939–1951.
79. [79] Kageyama, Y., Hoshijima, M., Seo, K., Bedja, D., Sysa-Shah, P., Andrabi, S.A., Chen, W., Hoke, A., Dawson, V.L., Dawson, T.M., Gabrielson, K., Kass, D.A., Iijima, M., Sesaki, H., Parkin-independent mitophagy requires Drp1 and maintains the integrity of mammalian heart and brain. EMBO J. 33 (2014), 2798–2813.
80. [80] Gomes, L.C., Scorrano, L., Mitochondrial morphology in mitophagy and macroautophagy. Biochim. Biophys. Acta 1833 (2013), 205–212.
81. [81] Moreira, P.I., Siedlak, S.L., Wang, X., Santos, M.S., Oliveira, C.R., Tabaton, M., Nunomura, A., Szweda, L.I., Aliev, G., Smith, M.A., Zhu, X., Perry, G., Increased autophagic degradation of mitochondria in Alzheimer disease. Autophagy 3 (2007), 614–615.