Mitophagy receptors sense stress signals and couple mitochondrial dynamic machinery for mitochondrial quality control

Free Radical Biology and Medicine

Volumn 100, Issue , 2016, Pages 199-209

  Wu, Hao ^a   Wei, Huifang ^b   Sehgal, Sheikh Arslan ^a,c   Liu, Lei ^a   Chen, Quan ^a,d  

^a INSTITUTE OF ZOOLOGY   (China)

^b CHINA US HENAN HORMEL CANCER INSTITUTE   (China)

^c COMSATS Institute of Information Technology ^*  (Pakistan)

^d NANKAI UNIVERSITY   (China)

Author keywords

Mitochondrial dynamics; Mitochondrial quality control; Mitochondrial stresses; Mitophagy receptor

Indexed keywords

AUTOPHAGY RELATED PROTEIN 32; PROTEIN; PROTEIN BCL 2; PROTEIN BNIP3; UNCLASSIFIED DRUG; AUTOPHAGY RELATED PROTEIN; CELL RECEPTOR; MITOCHONDRIAL PROTEIN;

ARTICLE; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MITOPHAGY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; QUALITY CONTROL; STRESS; ANIMAL; DEGENERATIVE DISEASE; HUMAN; METABOLISM; NEOPLASM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

ANIMALS; AUTOPHAGY-RELATED PROTEINS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; NEOPLASMS; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SACCHAROMYCES CEREVISIAE;

EID: 84962734183     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.03.030     Document Type: Review

References (191)

1. [1] Wallace, D.C., Mitochondria and cancer. Nat. Rev. Cancer 12 (2012), 685–698.
2. [2] Kroemer, G., Reed, J.C., Mitochondrial control of cell death. Nat. Med. 6 (2000), 513–519.
3. [3] Tait, S.W.G., Green, D.R., Mitochondria and cell death: outer membrane permeabilization and beyond. Nat. Rev. Mol. Cell Biol. 11 (2010), 621–632.
4. [4] Liochev, S.I., Reactive oxygen species and the free radical theory of aging. Free Radic. Biol. Med. 60 (2013), 1–4.
5. [5] Butow, R.A., Avadhani, N.G., Mitochondrial signaling: the retrograde response. Mol. Cell 14 (2004), 1–15.
6. [6] Liu, Z., Butow, R.A., Mitochondrial retrograde signaling. Annu. Rev. Genet. 40 (2006), 159–185.
7. [7] Boland, M.L., Chourasia, A.H., Macleod, K.F., Mitochondrial dysfunction in cancer. Front. Oncol., 3, 2013, 292.
8. [8] Lin, M.T., Beal, M.F., Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006), 787–795.
9. [9] Quiros, P.M., Langer, T., Lopez-Otin, C., New roles for mitochondrial proteases in health, ageing and disease. Nat Rev. Mol. Cell Biol. 16 (2015), 345–359.
10. [10] Rugarli, E.I., Langer, T., Mitochondrial quality control: a matter of life and death for neurons. EMBO J. 31 (2012), 1336–1349.
11. [11] Hemion, C., Flammer, J., Neutzner, A., Quality control of oxidatively damaged mitochondrial proteins is mediated by p97 and the proteasome. Free Radic. Biol. Med. 75 (2014), 121–128.
12. [12] Taylor, E.B., Rutter, J., Mitochondrial quality control by the ubiquitin–proteasome system. Biochem. Soc. Trans. 39 (2011), 1509–1513.
13. [13] McLelland, G.L., Soubannier, V., Chen, C.X., McBride, H.M., Fon, E.A., Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J. 33 (2014), 282–295.
14. [14] Sugiura, A., McLelland, G.L., Fon, E.A., McBride, H.M., A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J. 33 (2014), 2142–2156.
15. [15] Ni, H.M., Williams, J.A., Ding, W.X., Mitochondrial dynamics and mitochondrial quality control. Redox Biol. 4 (2015), 6–13.
16. [16] Kim, I., Rodriguez-Enriquez, S., Lemasters, J.J., Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 462 (2007), 245–253.
17. [17] Rodriguez-Enriquez, S., Kim, I., Currin, R.T., Lemasters, J.J., Tracker dyes to probe mitochondrial autophagy (mitophagy) in rat hepatocytes. Autophagy 2 (2006), 39–46.
18. [18] Ashrafi, G., Schwarz, T.L., The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 20 (2013), 31–42.
19. [19] Twig, G., Elorza, A., Molina, A.J., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G., Alroy, J., Wu, M., Py, B.F., Yuan, J., Deeney, J.T., Corkey, B.E., Shirihai, O.S., Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27 (2008), 433–446.
20. [20] Sheng, Z.H., Cai, Q., Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 13 (2012), 77–93.
21. [21] Chan, D.C., Mitochondria: dynamic organelles in disease, aging, and development. Cell 125 (2006), 1241–1252.
22. [22] Okamoto, K., Shaw, J.M., Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 39 (2005), 503–536.
23. [23] Chan, D.C., Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 22 (2006), 79–99.
24. [24] Friedman, J.R., Lackner, L.L., West, M., DiBenedetto, J.R., Nunnari, J., Voeltz, G.K., ER tubules mark sites of mitochondrial division. Science 334 (2011), 358–362.
25. [25] Yoon, Y., Krueger, E.W., Oswald, B.J., McNiven, M.A., The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol. Cell. Biol. 23 (2003), 5409–5420.
26. [26] Otera, H., Wang, C.X., Cleland, M.M., Setoguchi, K., Yokota, S., Youle, R.J., Mihara, K., Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J. Cell Biol. 191 (2010), 1141–1158.
27. [27] Loson, O.C., Song, Z., Chen, H., Chan, D.C., Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24 (2013), 659–667.
28. [28] van der Bliek, A.M., Shen, Q., Kawajiri, S., Mechanisms of mitochondrial fission and fusion. Cold Spring Harbor Perspect. Biol., 5, 2013.
29. [29] 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.
30. [30] Cereghetti, G.M., Stangherlin, A., Martins de Brito, O., Chang, C.R., Blackstone, C., Bernardi, P., Scorrano, L., Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. USA 105 (2008), 15803–15808.
31. [31] Dickey, A.S., Strack, S., PKA/AKAP1 and PP2A/Bbeta2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. J. Neurosci. 31 (2011), 15716–15726.
32. [32] 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.
33. [33] Meuer, K., Suppanz, I.E., Lingor, P., Planchamp, V., Goricke, B., Fichtner, L., Braus, G.H., Dietz, G.P.H., Jakobs, S., Bahr, M., Weishaupt, J.H., Cyclin-dependent kinase 5 is an upstream regulator of mitochondrial fission during neuronal apoptosis. Cell Death Differ. 14 (2007), 651–661.
34. [34] Barsoum, M.J., Yuan, H., Gerencser, A.A., Liot, G., Kushnareva, Y.E., Graber, S., Kovacs, I., Lee, W.D., Waggoner, J., Cui, J.K., 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.
35. [35] Yonashiro, R., Ishido, S., Kyo, S., Fukuda, T., Goto, E., Matsuki, Y., Ohmura-Hoshino, M., Sada, K., Hotta, H., Yamamura, H., Inatome, R., Yanagi, S., A novel mitochondrial ubiquitin ligase plays a critical role in mitochondrial dynamics. Embo J. 25 (2006), 3618–3626.
36. [36] Wang, H.X., Song, P.P., Du, L., Tian, W.L., Yue, W., Liu, M., Li, D.W., Wang, B., Zhu, Y.S., Cao, C., Zhou, J., Chen, Q.A., Parkin ubiquitinates Drp1 for proteasome-dependent degradation implication of dysregulated mitochondrial dynamics in parkinson disease. J. Biol. Chem. 286 (2011), 11649–11658.
37. [37] Pyakurel, A., Savoia, C., Hess, D., Scorrano, L., Extracellular regulated kinase phosphorylates mitofusin 1 to control mitochondrial morphology and apoptosis. Mol. Cell 58 (2015), 244–254.
38. [38] Glauser, L., Sonnay, S., Stafa, K., Moore, D.J., Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J. Neurochem. 118 (2011), 636–645.
39. [39] Park, Y.Y., Cho, H., Mitofusin 1 is degraded at G2/M phase through ubiquitylation by MARCH5. Mol. Biol. Cell, 23, 2012.
40. [40] Sugiura, A., Nagashima, S., Tokuyama, T., Amo, T., Matsuki, Y., Ishido, S., Kudo, Y., McBride, H.M., Fukuda, T., Matsushita, N., Inatome, R., Yanagi, S., MITOL regulates endoplasmic reticulum–mitochondria contacts via mitofusin2. Mol. Cell 51 (2013), 20–34.
41. [41] Yue, W., Chen, Z.H., Liu, H.Y., Yan, C., Chen, M., Feng, D., Yan, C.J., Wu, H., Du, L., Wang, Y.Y., Liu, J.H., Huang, X.H., Xia, L.X., Liu, L., Wang, X.H., Jin, H.J., Wang, J., Song, Z.Y., Hao, X.J., Chen, Q., A small natural molecule promotes mitochondrial fusion through inhibition of the deubiquitinase USP30. Cell Res. 24 (2014), 482–496.
42. [42] Leboucher, G.P., Tsai, Y.C., Yang, M., Shaw, K.C., Zhou, M., Veenstra, T.D., Glickman, M.H., Weissman, A.M., Stress-induced phosphorylation and proteasomal degradation of mitofusin 2 facilitates mitochondrial fragmentation and apoptosis. Mol. Cell 47 (2012), 547–557.
43. [43] Chan, N.C., Salazar, A.M., Pham, A.H., Sweredoski, M.J., Kolawa, N.J., Graham, R.L.J., Hess, S., Chan, D.C., Broad activation of the ubiquitin–proteasome system by Parkin is critical for mitophagy. Hum. Mol. Genet. 20 (2011), 1726–1737.
44. [44] Song, Z.Y., Chen, H.C., Fiket, M., Alexander, C., Chan, D.C., OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J. Cell Biol. 178 (2007), 749–755.
45. [45] Ehses, S., Raschke, I., Mancuso, G., Bernacchia, A., Geimer, S., Tondera, D., Martinou, J.C., Westermann, B., Rugarli, E.I., Langer, T., Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 187 (2009), 1023–1036.
46. [46] Chen, H., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E., Chan, D.C., Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160 (2003), 189–200.
47. [47] Labrousse, A.M., Zappaterra, M.D., Rube, D.A., van der Bliek, A.M., C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell 4 (1999), 815–826.
48. [48] Ishihara, N., Nomura, M., Jofuku, A., Kato, H., Suzuki, S.O., Masuda, K., Otera, H., Nakanishi, Y., Nonaka, I., Goto, Y.I., Taguchi, N., Morinaga, H., Maeda, M., Takayanagi, R., Yokota, S., Mihara, K., Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol., 11, 2009 (958-U114).
49. [49] Zuchner, S., Mersiyanova, I.V., Muglia, M., Bissar-Tadmouri, N., Rochelle, J., Dadali, E.L., Zappia, M., Nelis, E., Patitucci, A., Senderek, J., Parman, Y., Evgrafov, O., De Jonghe, P., Takahashi, Y., Tsuji, S., Pericak-Vance, M.A., Quattrone, A., Battologlu, E., Polyakov, A.V., Timmerman, V., Schroder, J.M., Vance, J.M., Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A (vol. 36, pp. 327, 2004). Nat. Genet., 36, 2004, 660.
50. [50] Alexander, C., Votruba, M., Pesch, U.E.A., Thiselton, D.L., Mayer, S., Moore, A., Rodriguez, M., Kellner, U., Leo-Kottler, B., Auburger, G., Bhattacharya, S.S., Wissinger, B., OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26 (2000), 211–215.
51. [51] Delettre, C., Lenaers, G., Griffoin, J.M., Gigarel, N., Lorenzo, C., Belenguer, P., Pelloquin, L., Grosgeorge, J., Turc-Carel, C., Perret, E., Astarie-Dequeker, C., Lasquellec, L., Arnaud, B., Ducommun, B., Kaplan, J., Hamel, C.P., Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26 (2000), 207–210.
52. [52] Chen, H.C., Detmer, S.A., Ewald, A.J., Griffin, E.E., Fraser, S.E., Chan, D.C., Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 160 (2003), 189–200.
53. [53] Chen, H.C., McCaffery, J.M., Chan, D.C., Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130 (2007), 548–562.
54. [54] van der Bliek, A.M., Shen, Q.F., Kawajiri, S., Mechanisms of mitochondrial fission and fusion. Cold Spring Harbor Perspect. Biol., 5, 2013.
55. [55] Chen, H.C., Chomyn, A., Chan, D.C., Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280 (2005), 26185–26192.
56. [56] Wakabayashi, J., Zhang, Z.Y., Wakabayashi, N., Tamura, Y., Fukaya, M., Kensler, T.W., Iijima, M., Sesaki, H., The dynamin-related GTPase Drp1 is required for embryonic and brain development in mice. J. Cell Biol. 186 (2009), 805–816.
57. [57] Ikeda, Y., Shirakabe, A., Maejima, Y., Zhai, P.Y., Sciarretta, S., Toli, J., Nomura, M., Mihara, K., Egashira, K., Ohishi, M., Abdellatif, M., Sadoshima, J., Endogenous Drp1 mediates mitochondrial autophagy and protects the heart against energy stress. Circ. Res., 116, 2015 (264-U177).
58. [58] Mizushima, N., Autophagy: process and function. Gene Dev. 21 (2007), 2861–2873.
59. [59] Kraft, C., Peter, M., Hofmann, K., Selective autophagy: ubiquitin-mediated recognition and beyond. Nat. Cell Biol. 12 (2010), 836–841.
60. [60] Johansen, T., Lamark, T., Selective autophagy mediated by autophagic adapter proteins. Autophagy 7 (2011), 279–296.
61. [61] Birgisdottir, A.B., Lamark, T., Johansen, T., The LIR motif – crucial for selective autophagy. J. Cell Sci. 126 (2013), 3237–3247.
62. [62] Rogov, V., Dotsch, V., Johansen, T., Kirkin, V., Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol. Cell 53 (2014), 167–178.
63. [63] Liu, L., Sakakibara, K., Chen, Q., Okamoto, K., Receptor-mediated mitophagy in yeast and mammalian systems. Cell Res. 24 (2014), 787–795.
64. [64] Mizushima, N., Levine, B., Autophagy in mammalian development and differentiation. Nat. Cell Biol. 12 (2010), 823–830.
65. [65] Doria, A., Gatto, M., Punzi, L., Autophagy in human health and disease. N. Engl. J. Med., 368, 2013, 1845.
66. [66] Kim, I., Rodriguez-Enriquez, S., Lemasters, J.J., Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 462 (2007), 245–253.
67. [67] Lemasters, J.J., Perspective – selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 8 (2005), 3–5.
68. [68] Narendra, D., Tanaka, A., Suen, D.F., Youle, R.J., Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183 (2008), 795–803.
69. [69] Narendra, D.P., Jin, S.M., Tanaka, A., Suen, D.F., Gautier, C.A., Shen, J., Cookson, M.R., Youle, R.J., PINK1 is selectively stabilized on impaired mitochondria to activate parkin. PLoS Biol., 8, 2010.
70. [70] Iguchi, M., Kujuro, Y., Okatsu, K., Koyano, F., Kosako, H., Kimura, M., Suzuki, N., Uchiyama, S., Tanaka, K., Matsuda, N., Parkin-catalyzed ubiquitin-ester transfer is triggered by PINK1-dependent phosphorylation. J. Biol. Chem., 288, 2013.
71. [71] Kondapalli, C., Kazlauskaite, A., Zhang, N., Woodroof, H.I., Campbell, D.G., Gourlay, R., Burchell, L., Walden, H., Macartney, T.J., Deak, M., Knebel, A., Alessi, D.R., Muqit, M.M.K., PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol., 2, 2012.
72. [72] Kane, L.A., Lazarou, M., Fogel, A.I., Li, Y., Yamano, K., Sarraf, S.A., Banerjee, S., Youle, R.J., PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell Biol. 205 (2014), 143–153.
73. [73] Koyano, F., Okatsu, K., Kosako, H., Tamura, Y., Go, E., Kimura, M., Kimura, Y., Tsuchiya, H., Yoshihara, H., Hirokawa, T., Endo, T., Fon, E.A., Trempe, J.F., Saeki, Y., Tanaka, K., Matsuda, N., Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature, 510, 2014, 162.
74. [74] Chen, Y., Dorn, G.W., PINK1-phosphorylated mitofusin 2 is a parkin receptor for culling damaged mitochondria. Science 340 (2013), 471–475.
75. [75] Lazarou, M., Sliter, D.A., Kane, L.A., Sarraf, S.A., Wang, C.X., Burman, J.L., Sideris, D.P., Fogel, A.I., Youle, R.J., The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature, 524, 2015, 309.
76. [76] Clark, I.E., Dodson, M.W., Jiang, C.G., Cao, J.H., Huh, J.R., Seol, J.H., Yoo, S.J., Hay, B.A., Guo, M., Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441 (2006), 1162–1166.
77. [77] Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., Shimizu, N., Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392 (1998), 605–608.
78. [78] Park, J., Lee, S.B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M.H., Kim, J.M., Chung, J.K., Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441 (2006), 1157–1161.
79. [79] Yang, Y.F., Gehrke, S., Imai, Y., Huang, Z.N., Ouyang, Y., Wang, J.W., Yang, L.C., Beal, M.F., Vogel, H., Lu, B.W., Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused inactivation of Drosophila Pink1 is rescued by by Parkin. Proc. Natl. Acad. Sci. USA 103 (2006), 10793–10798.
80. [80] Gegg, M.E., Cooper, J.M., Chau, K.Y., Rojo, M., Schapira, A.H.V., Taanman, J.W., Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy (vol. 19, pp. 4861, 2010). Hum. Mol. Genet., 22, 2013, 1697.
81. [81] Tanaka, A., Cleland, M.M., Xu, S., Narendra, D.P., Suen, D.F., Karbowski, M., Youle, R.J., Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 191 (2010), 1367–1380.
82. [82] Wang, X.N., Winter, D., Ashrafi, G., Schlehe, J., Wong, Y.L., Selkoe, D., Rice, S., Steen, J., LaVoie, M.J., Schwarz, T.L., PINK1 and parkin target miro for phosphorylation and degradation to arrest mitochondrial motility. Cell 147 (2011), 893–906.
83. [83] Kanki, T., Wang, K., Cao, Y., Baba, M., Klionsky, D.J., Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17 (2009), 98–109.
84. [84] Okamoto, K., Kondo-Okamoto, N., Ohsumi, Y., Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17 (2009), 87–97.
85. [85] Kondo-Okamoto, N., Noda, N.N., Suzuki, S.W., Nakatogawa, H., Takahashi, I., Matsunami, M., Hashimoto, A., Inagaki, F., Ohsumi, Y., Okamoto, K., Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J. Biol. Chem. 287 (2012), 10631–10638.
86. [86] Kurihara, Y., Kanki, T., Aoki, Y., Hirota, Y., Saigusa, T., Uchiumi, T., Kang, D.C., 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 (2012), 3265–3272.
87. [87] Titorenko, V., Beach, A., Richard, V., Leonov, A., Piano, A., Feldman, R., Macromitophagy is a longevity assurance process that in chronologically aging yeast limited in calorie supply sustains functional mitochondria and maintains cellular lipid homeostasis. FASEB J., 28, 2014.
88. [88] Kissova, I.B., Camougrand, N., Glutathione participates in the regulation of mitophagy in yeast. Autophagy 5 (2009), 872–873.
89. [89] Sakakibara, K., Eiyama, A., Suzuki, S.W., Sakoh-Nakatogawa, M., Okumura, N., Tani, M., Hashimoto, A., Nagumo, S., Kondo-Okamoto, N., Kondo-Kakuta, C., Asai, E., Kirisako, H., Nakatogawa, H., Kuge, O., Takao, T., Ohsumi, Y., Okamoto, K., Phospholipid methylation controls Atg32-mediated mitophagy and Atg8 recycling. Embo J. 34 (2015), 2703–2719.
90. [90] Eiyama, A., Okamoto, K., Protein N-terminal acetylation by the NatA complex is critical for selective mitochondrial degradation. J. Biol. Chem. 290 (2015), 25034–25044.
91. [91] Aihara, M., Jin, X.L., Kurihara, Y., Yoshida, Y., Matsushima, Y., Oku, M., Hirota, Y., Saigusa, T., Aoki, Y., Uchiumi, T., Yamamoto, T., Sakai, Y., Kang, D.C., Kanki, T., Tor and the Sin3–Rpd3 complex regulate expression of the mitophagy receptor protein Atg32 in yeast. J. Cell Sci. 127 (2014), 3184–3196.
92. [92] Aoki, Y., Kanki, T., Hirota, Y., Kurihara, Y., Saigusa, T., Uchiumi, T., Kang, D.C., Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 22 (2011), 3206–3217.
93. [93] Kanki, T., Kurihara, Y., Jin, X.L., Goda, T., Ono, Y., Aihara, M., Hirota, Y., Saigusa, T., Aoki, Y., Uchiumi, T., Kang, D., Casein kinase 2 is essential for mitophagy. Embo Rep. 14 (2013), 788–794.
94. [94] Mao, K., Wang, K., Zhao, M.T., Xu, T., Klionsky, D.J., Two MAPK-signaling pathways are required for mitophagy in Saccharomyces cerevisiae. J. Cell Biol. 193 (2011), 755–767.
95. [95] Wang, K., Jin, M.Y., Liu, X., Klionsky, D.J., Proteolytic processing of Atg32 by the mitochondrial i-AAA protease Yme1 regulates mitophagy. Autophagy 9 (2013), 1828–1836.
96. [96] Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q.X., Song, P.P., Ma, Q., Zhu, C.Z., Wang, R., Qi, W.J., Huang, L., Xue, P., Li, B.W., Wang, X.H., Jin, H.J., Wang, J., Yang, F.Q., Liu, P.S., Zhu, Y.S., Sui, S.F., Chen, Q., Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14 (2012), 177–185.
97. [97] Chen, G., Han, Z., Feng, D., Chen, Y.F., Chen, L.B., Wu, H., Huang, L., Zhou, C.Q., Cai, X.Y., Fu, C.Y., Duan, L.W., Wang, X.H., Liu, L., Liu, X.Q., Shen, Y.Q., Zhu, Y.S., Chen, Q., A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol. Cell 54 (2014), 362–377.
98. [98] Wu, W.X., Tian, W.L., Hu, Z., Chen, G., Huang, L., Li, W., Zhang, X.L., Xue, P., Zhou, C.Q., Liu, L., Zhu, Y.S., Zhang, X.L., Li, L.X., Zhang, L.Q., Sui, S.F., Zhao, B., Feng, D., ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. Embo Rep. 15 (2014), 566–575.
99. [99] Wu, H., Xue, D.F., Chen, G., Han, Z., Huang, L., Zhu, C.Z., Wang, X.H., Jin, H.J., Wang, J., Zhu, Y.S., Liu, L., Chen, Q., The BCL2L1 and PGAM5 axis defines hypoxia-induced receptor-mediated mitophagy. Autophagy 10 (2014), 1712–1725.
100. [100] Wu, H., Chen, Q., Hypoxia activation of mitophagy and its role in disease pathogenesis. Antioxid. Redox Signal. 22 (2015), 1032–1046.
101. [101] Kataoka, T., Holler, N., Micheau, O., Martinon, F., Tinel, A., Hofmann, K., Tschopp, J., Bcl-rambo, a novel Bcl-2 homologue that induces apoptosis via its unique C-terminal extension. J. Biol. Chem. 276 (2001), 19548–19554.
102. [102] Yang, Y.L., Lin, S.R., Chen, J.S., Lin, S.W., Yu, S.L., Chen, H.Y., Yen, C.T., Lin, C.Y., Lin, J.F., Lin, K.H., Jou, S.T., Hu, C.Y., Chang, S.K., Lu, M.Y., Chang, H.H., Chang, W.H., Lin, K.S., Lin, D.T., Expression and prognostic significance of the apoptotic genes BCL2L13, Livin, and CASP8AP2 in childhood acute lymphoblastic leukemia. Leuk. Res. 34 (2010), 18–23.
103. [103] Jensen, S.A., Calvert, A.E., Volpert, G., Kouri, F.M., Hurley, L.A., Luciano, J.P., Wu, Y.F., Chalastanis, A., Futerman, A.H., Stegh, A.H., Bcl2L13 is a ceramide synthase inhibitor in glioblastoma. Proc. Natl. Acad. Sci. USA 111 (2014), 5682–5687.
104. [104] Murakawa, T., Yamaguchi, O., Hashimoto, A., Hikoso, S., Takeda, T., Oka, T., Yasui, H., Ueda, H., Akazawa, Y., Nakayama, H., Taneike, M., Misaka, T., Omiya, S., Shah, A.M., Yamamoto, A., Nishida, K., Ohsumi, Y., Okamoto, K., Sakata, Y., Otsu, K., Bcl-2-like protein 13 is a mammalian Atg32 homologue that mediates mitophagy and mitochondrial fragmentation. Nat. Commun., 6, 2015.
105. [105] Otsu, K., Murakawa, T., Yamaguchi, O., BCL2L13 is a mammalian homolog of the yeast mitophagy receptor Atg32. Autophagy 11 (2015), 1932–1933.
106. [106] Boyd. Adenovirus-E1b 19-Kda and Bcl-2 proteins interact with a common set of cellular proteins (vol. 79, pp. 341, 1994). Cell, 79, 1994, 1121.
107. [107] Chen, G., Cizeau, J., Velde, C.V., Park, J.H., Bozek, G., Bolton, J., Shi, L., Dubik, D., Greenberg, A., Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins. J. Biol. Chem. 274 (1999), 7–10.
108. [108] Imazu, T., Shimizu, S., Tagami, S., Matsushima, M., Nakamura, Y., Miki, T., Okuyama, A., Tsujimoto, Y., Bcl-2/E1B 19 kDa-interacting protein 3-like protein (Bnip3L) interacts with bcl-2/Bcl-xL and induces apoptosis by altering mitochondrial membrane permeability. Oncogene 18 (1999), 4523–4529.
109. [109] Yasuda, M., Theodorakis, P., Subramanian, T., Chinnadurai, G., Adenovirus E1B-19K/BCL-2 interacting protein BNIP3 contains a BH3 domain and a mitochondrial targeting sequence. J. Biol. Chem. 273 (1998), 12415–12421.
110. [110] Bellot, G., Garcia-Medina, R., Gounon, P., Chiche, J., Roux, D., Pouyssegur, J., Mazure, N.M., Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 29 (2009), 2570–2581.
111. [111] Hamacher-Brady, A., Brady, N.R., Logue, S.E., Sayen, M.R., Jinno, M., Kirshenbaum, L.A., Gottlieb, R.A., Gustafsson, A.B., Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ. 14 (2007), 146–157.
112. [112] Maiuri, M.C., Criollo, A., Tasdemir, E., Vicencio, J.M., Tajeddine, N., Hickman, J.A., Geneste, O., Kroemer, G., BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X-L. Autophagy 3 (2007), 374–376.
113. [113] Maiuri, M.C., Zalckvar, E., Kimchi, A., Kroemer, G., Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 8 (2007), 741–752.
114. [114] Novak, I., Kirkin, V., McEwan, D.G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Lohr, F., Popovic, D., Occhipinti, A., Reichert, A.S., Terzic, J., Dotsch, V., Ney, P.A., Dikic, I., Nix is a selective autophagy receptor for mitochondrial clearance. Embo Rep. 11 (2010), 45–51.
115. [115] Novak, I., Dikic, I., Autophagy receptors in developmental clearance of mitochondria. Autophagy 7 (2011), 301–303.
116. [116] Schweers, R.L., Zhang, J., Randall, M.S., Loyd, M.R., Li, W., Dorsey, F.C., Kundu, M., Opferman, J.T., Cleveland, J.L., Miller, J.L., Ney, P.A., NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 104 (2007), 19500–19505.
117. [117] Sandoval, H., Thiagarajan, P., Dasgupta, S.K., Schumacher, A., Prchal, J.T., Chen, M., Wang, J., Essential role for Nix in autophagic maturation of erythroid cells. Nature, 454, 2008 (232-U266).
118. [118] Hanna, R.A., Quinsay, M.N., Orogo, A.M., Giang, K., Rikka, S., Gustafsson, A.B., 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 (2012), 19094–19104.
119. [119] Lee, Y., Lee, H.Y., Hanna, R.A., Gustafsson, A.B., Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes. Am. J. Physiol. – Heart Circ. 301 (2011), H1924–H1931.
120. [120] Quinsay, M.N., Thomas, R.L., Lee, Y., Gustafsson, A.B., Bnip3-mediated mitochondrial autophagy is independent of the mitochondrial permeability transition pore. Autophagy 6 (2010), 855–862.
121. [121] Sowter, H.M., Ratcliffe, P.J., Watson, P., Greenberg, A.H., Harris, A.L., HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res. 61 (2001), 6669–6673.
122. [122] Zhu, Y.Y., Massen, S., Terenzio, M., Lang, V., Chen-Lindner, S., Eils, R., Novak, I., Dikic, I., Hamacher-Brady, A., Brady, N.R., Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis. J. Biol. Chem. 288 (2013), 1099–1113.
123. [123] Fimia, G.M., Stoykova, A., Romagnoli, A., Giunta, L., Di Bartolomeo, S., Nardacci, R., Corazzari, M., Fuoco, C., Ucar, A., Schwartz, P., Gruss, P., Piacentini, M., Chowdhury, K., Cecconi, F., Ambra1 regulates autophagy and development of the nervous system. Nature, 447, 2007 (1121-U1114).
124. [124] Strappazzon, F., Vietri-Rudan, M., Campello, S., Nazio, F., Florenzano, F., Fimia, G.M., Piacentini, M., Levine, B., Cecconi, F., Mitochondrial BCL-2 inhibits AMBRA1-induced autophagy. Embo J. 30 (2011), 1195–1208.
125. [125] Van Humbeeck, C., Cornelissen, T., Hofkens, H., Mandemakers, W., Gevaert, K., De Strooper, B., Vandenberghe, W., Parkin interacts with Ambra1 to induce mitophagy. J. Neurosci. 31 (2011), 10249–10261.
126. [126] Van Humbeeck, C., Cornelissen, T., Vandenberghe, W., Ambra1, A., Parkin-binding protein involved in mitophagy. Autophagy 7 (2011), 1555–1556.
127. [127] Strappazzon, F., Nazio, F., Corrado, M., Cianfanelli, V., Romagnoli, A., Fimia, G.M., Campello, S., Nardacci, R., Piacentini, M., Campanella, M., Cecconi, F., AMBRA1 is able to induce mitophagy via LC3 binding, regardless of PARKIN and p62/SQSTM1. Cell Death Differ. 22 (2015), 419–432.
128. [128] Komatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., Ezaki, J., Mizushima, N., Ohsumi, Y., Uchiyama, Y., Kominami, E., Tanaka, K., Chiba, T., Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169 (2005), 425–434.
129. [129] Masiero, E., Agatea, L., Mammucari, C., Blaauw, B., Loro, E., Komatsu, M., Metzger, D., Reggiani, C., Schiaffino, S., Sandri, M., Autophagy is required to maintain muscle mass. Cell Metab. 10 (2009), 507–515.
130. [130] Mortensen, M., Ferguson, D.J.P., Edelmann, M., Kessler, B., Morten, K.J., Komatsu, M., Simon, A.K., Loss of autophagy in erythroid cells leads to defective removal of mitochondria and severe anemia in vivo. Proc. Natl. Acad. Sci. USA 107 (2010), 832–837.
131. [131] Poole, A.C., Thomas, R.E., Andrews, L.A., McBride, H.M., Whitworth, A.J., Pallanck, L.J., The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. USA 105 (2008), 1638–1643.
132. [132] Gautier, C.A., Kitada, T., Shen, J., Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl. Acad. Sci. USA 105 (2008), 11364–11369.
133. [133] Billia, F., Hauck, L., Konecny, F., Rao, V., Shen, J., Mak, T.W., PTEN-inducible kinase 1 (PINK1)/Park6 is indispensable for normal heart function. Proc. Natl. Acad. Sci. USA 108 (2011), 9572–9577.
134. [134] Glick, D., Zhang, W.S., Beaton, M., Marsboom, G., Gruber, M., Simon, M.C., Hart, J., Dorn, G.W., Brady, M.J., Macleod, K.F., BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol. Cell. Biol. 32 (2012), 2570–2584.
135. [135] Dorn, G.W., Mitochondrial pruning by Nix and BNip3: an essential function for cardiac-expressed death factors. J. Cardiovasc. Transl. 3 (2010), 374–383.
136. [136] Richard, V.R., Leonov, A., Beach, A., Burstein, M.T., Koupaki, O., Gomez-Perez, A., Levy, S., Pluska, L., Mattie, S., Rafeh, R., Iouk, T., Sheibani, S., Greenwood, M., Vali, H., Titorenko, V.I., Macromitophagy is a longevity assurance process that in chronologically aging yeast limited in calorie supply sustains functional mitochondria and maintains cellular lipid homeostasis. Aging-Us 5 (2013), 234–269.
137. [137] Youle, R.J., Narendra, D.P., Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12 (2011), 9–14.
138. [138] Kubli, D.A., Gustafsson, A.B., Mitochondria and mitophagy the Yin and Yang of cell death control. Circ. Res. 111 (2012), 1208–1221.
139. [139] Fischer, F., Hamann, A., Osiewacz, H.D., Mitochondrial quality control: an integrated network of pathways. Trends Biochem. Sci. 37 (2012), 284–292.
140. [140] Gomes, L.C., Di Benedetto, G., Scorrano, L., During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol., 13, 2011 (589-U207).
141. [141] Rambold, A.S., Kostelecky, B., Elia, N., Lippincott-Schwartz, J., Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. USA 108 (2011), 10190–10195.
142. [142] Twig, G., Elorza, A., Molina, A.J.A., Mohamed, H., Wikstrom, J.D., Walzer, G., Stiles, L., Haigh, S.E., Katz, S., Las, G., Alroy, J., Wu, M., Py, B.F., Yuan, J., Deeney, J.T., Corkey, B.E., Shirihai, O.S., Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. Embo J. 27 (2008), 433–446.
143. [143] Imai, Y., Lu, B.W., Mitochondrial dynamics and mitophagy in Parkinson's disease: disordered cellular power plant becomes a big deal in a major movement disorder. Curr. Opin. Neurobiol. 21 (2011), 935–941.
144. [144] Chen, H.C., Chan, D.C., Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18 (2009), R169–R176.
145. [145] Twig, G., Shirihai, O.S., The interplay between mitochondrial dynamics and mitophagy. Antioxid. Redox Signal. 14 (2011), 1939–1951.
146. [146] Kanki, T., Wang, K., Baba, M., Bartholomew, C.R., Lynch-Day, M.A., Du, Z., Geng, J.F., Mao, K., Yang, Z.F., Yen, W.L., Klionsky, D.J., A genomic screen for yeast mutants defective in selective mitochondria autophagy. Mol. Biol. Cell 20 (2009), 4730–4738.
147. [147] Mao, K., Wang, K., Liu, X., Klionsky, D.J., The scaffold protein Atg11 recruits fission machinery to drive selective mitochondria degradation by autophagy. Dev. Cell 26 (2013), 9–18.
148. [148] Mao, K., Klionsky, D.J., Participation of mitochondrial fission during mitophagy. Cell Cycle 12 (2013), 3131–3132.
149. [149] Chen, M., Chen, Z.H., Wang, Y.Y., Tan, Z., Zhu, C.Z., Li, Y.J., Han, Z., Chen, L.B., Gao, R.Z., Liu, L., Chen, Q., Mitophagy receptor FUNDC1 regulates mitochondrial dynamics and mitophagy. Autophagy 12 (2016), 1–14.
150. [150] Lo, S.C., Hannink, M., PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp. Cell Res. 314 (2008), 1789–1803.
151. [151] Wang, Z.G., Jiang, H., Chen, S., Du, F.H., Wang, X.D., The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell 148 (2012), 228–243.
152. [152] Lin, H.Y., Lai, R.H., Lin, S.T., Lin, R.C., Wang, M.J., Lin, C.C., Lee, H.C., Wang, F.F., Chen, J.Y., Suppressor of cytokine signaling 6 (SOCS6) promotes mitochondrial fission via regulating DRP1 translocation. Cell Death Differ. 20 (2013), 139–153.
153. [153] Xu, W.J., Jing, L.L., Wang, Q.S., Lin, C.C., Chen, X.T., Diao, J.X., Liu, Y.L., Sun, X.G., Bax–PGAM5L–Drp1 complex is required for intrinsic apoptosis execution. Oncotarget 6 (2015), 30017–30034.
154. [154] Delivani, P., Adrain, C., Taylor, R.C., Duriez, P.J., Martin, S.J., Role for CED-9 and Egl-1 as regulators of mitochondrial fission and fusion dynamics. Mol. Cell 21 (2006), 761–773.
155. [155] Sheridan, C., Delivani, P., Cullen, S.P., Martin, S.J., Bax- or Bak-induced mitochondrial fission can be uncoupled from cytochrome c release. Mol. Cell 31 (2008), 570–585.
156. [156] Berman, S.B., Chen, Y.B., Qi, B., McCaffery, J.M., Rucker, E.B., Goebbels, S., Nave, K.A., Arnold, B.A., Jonas, E.A., Pineda, F.J., Hardwick, J.M., Bcl-x(L) increases mitochondrial fission, fusion, and biomass in neurons. J. Cell Biol. 184 (2009), 707–719.
157. [157] Cleland, M.M., Norris, K.L., Karbowski, M., Wang, C., Suen, D.F., Jiao, S., George, N.M., Luo, X., Li, Z., Youle, R.J., Bcl-2 family interaction with the mitochondrial morphogenesis machinery. Cell Death Differ. 18 (2011), 235–247.
158. [158] Li, H.M., Alavian, K.N., Lazrove, E., Mehta, N., Jones, A., Zhang, P., Licznerski, P., Graham, M., Uo, T., Guo, J.H., Rahner, C., Duman, R.S., Morrison, R.S., Jonas, E.A., A Bcl-x(L)–Drp1 complex regulates synaptic vesicle membrane dynamics during endocytosis. Nat. Cell Biol., 15, 2013, 773.
159. [159] Li, H., Chen, Y., Jones, A.F., Sanger, R.H., Collis, L.P., Flannery, R., McNay, E.C., Yu, T., Schwarzenbacher, R., Bossy, B., Bossy-Wetzel, E., Bennett, M.V., Pypaert, M., Hickman, J.A., Smith, P.J., Hardwick, J.M., Jonas, E.A., Bcl-xL induces Drp1-dependent synapse formation in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 105 (2008), 2169–2174.
160. [160] Kubl, D.A., Ycaza, J.E., Gustafsson, A.B., Bnip3 mediates mitochondrial dysfunction and cell death through Bax and Bak. Biochem. J. 405 (2007), 407–415.
161. [161] Romanello, V., Guadagnin, E., Gomes, L., Roder, I., Sandri, C., Petersen, Y., Milan, G., Masiero, E., Del Piccolo, P., Foretz, M., Scorrano, L., Rudolf, R., Sandri, M., Mitochondrial fission and remodelling contributes to muscle atrophy. Embo J. 29 (2010), 1774–1785.
162. [162] Landes, T., Emorine, L.J., Courilleau, D., Rojo, M., Belenguer, P., Arnaune-Pelloquin, L., The BH3-only Bnip3 binds to the dynamin Opa1 to promote mitochondrial fragmentation and apoptosis by distinct mechanisms. Embo Rep. 11 (2010), 459–465.
163. [163] Kim, J., Kundu, M., Viollet, B., Guan, K.L., AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol., 13, 2011 (132-U171).
164. [164] Egan, D.F., Shackelford, D.B., Mihaylova, M.M., Gelino, S., Kohnz, R.A., Mair, W., Vasquez, D.S., Joshi, A., Gwinn, D.M., Taylor, R., Asara, J.M., Fitzpatrick, J., Dillin, A., Viollet, B., Kundu, M., Hansen, M., Shaw, R.J., Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331 (2011), 456–461.
165. [165] Li, J., Wang, Y., Wen, X., Ma, X.N., Chen, W., Huang, F., Kou, J., Qi, L.W., Liu, B., Liu, K., Pharmacological activation of AMPK prevents Drp1-mediated mitochondrial fission and alleviates endoplasmic reticulum stress-associated endothelial dysfunction. J. Mol. Cell. Cardiol. 86 (2015), 62–74.
166. [166] Wikstrom, J.D., Israeli, T., Bachar-Wikstrom, E., Swisa, A., Ariav, Y., Waiss, M., Kaganovich, D., Dor, Y., Cerasi, E., Leibowitz, G., AMPK regulates ER morphology and function in stressed pancreatic beta-cells via phosphorylation of DRP1. Mol. Endocrinol. 27 (2013), 1706–1723.
167. [167] Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q., Song, P., Ma, Q., Zhu, C., Wang, R., Qi, W., Huang, L., Xue, P., Li, B., Wang, X., Jin, H., Wang, J., Yang, F., Liu, P., Zhu, Y., Sui, S., Chen, Q., Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14 (2012), 177–185.
168. [168] Chen, G., Han, Z., Feng, D., Chen, Y., Chen, L., Wu, H., Huang, L., Zhou, C., Cai, X., Fu, C., Duan, L., Wang, X., Liu, L., Liu, X., Shen, Y., Zhu, Y., Chen, Q., A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol. Cell 54 (2014), 362–377.
169. [169] Wu, H., Chen, Q., Hypoxia activation of mitophagy and its role in disease pathogenesis. Antioxid. Redox Signal. 22 (2015), 1032–1046.
170. [170] Kim, H., Scimia, M.C., Wilkinson, D., Trelles, R.D., Wood, M.R., Bowtell, D., Dillin, A., Mercola, M., Ronai, Z.A., Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol. Cell 44 (2011), 532–544.
171. [171] Chaanine, A.H., Jeong, D., Liang, L., Chemaly, E.R., Fish, K., Gordon, R.E., Hajjar, R.J., JNK modulates FOXO3a for the expression of the mitochondrial death and mitophagy marker BNIP3 in pathological hypertrophy and in heart failure. Cell Death Dis., 3, 2012, 265.
172. [172] Zhang, Q., Kuang, H., Chen, C., Yan, J., Do-Umehara, H.C., Liu, X.Y., Dada, L., Ridge, K.M., Chandel, N.S., Liu, J., The kinase Jnk2 promotes stress-induced mitophagy by targeting the small mitochondrial form of the tumor suppressor ARF for degradation. Nat. Immunol. 16 (2015), 458–466.
173. [173] Lupfer, C., Thomas, P.G., Anand, P.K., Vogel, P., Milasta, S., Martinez, J., Huang, G., Green, M., Kundu, M., Chi, H., Xavier, R.J., Green, D.R., Lamkanfi, M., Dinarello, C.A., Doherty, P.C., Kanneganti, T.D., Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat. Immunol. 14 (2013), 480–488.
174. [174] Wang, X.Q., Jiang, W., Yan, Y.Q., Gong, T., Han, J.H., Tian, Z.G., Zhou, R.B., RNA viruses promote activation of the NLRP3 inflammasome through a RIP1–RIP3–DRP1 signaling pathway. Nat. Immunol. 15 (2014), 1126–1133.
175. [175] Rayamajhi, M., Miao, E.A., The RIP1–RIP3 complex initiates mitochondrial fission to fuel NLRP3. Nat. Immunol. 15 (2014), 1100–1102.
176. [176] Hoyer-Hansen, M., Jaattela, M., Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14 (2007), 1576–1582.
177. [177] Imaizumi, K., Autophagy is activated for cell survival after ER stress. J. Pharmacol. Sci., 103, 2007, 45.
178. [178] Kouroku, Y., Fujita, E., Tanida, I., Ueno, T., Isoai, A., Kumagai, H., Ogawa, S., Kaufman, R.J., Kominami, E., Momoi, T., ER stress (PERK/eIF2 alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14 (2007), 230–239.
179. [179] Hoyer-Hansen, M., Bastholm, L., Szyniarowski, P., Campanella, M., Szabadkai, G., Farkas, T., Bianchi, K., Fehrenbacher, N., Elling, F., Rizzuto, R., Mathiasen, I.S., Jaattela, M., Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25 (2007), 193–205.
180. [180] Friedman, J.R., Lackner, L.L., West, M., DiBenedetto, J.R., Nunnari, J., Voeltz, G.K., ER tubules mark sites of mitochondrial division. Science 334 (2011), 358–362.
181. [181] Bockler, S., Westermann, B., Mitochondrial, E.R., Contacts are crucial for mitophagy in yeast. Dev. Cell 28 (2014), 450–458.
182. [182] Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., Amano, A., Yoshimori, T., Autophagosomes form at ER–mitochondria contact sites. Nature 495 (2013), 389–393.
183. [183] de Brito, O.M., Scorrano, L., Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature, 456, 2008 (605-U647).
184. [184] Nargund, A.M., Pellegrino, M.W., Fiorese, C.J., Baker, B.M., Haynes, C.M., Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science 337 (2012), 587–590.
185. [185] Pellegrino, M.W., Nargund, A.M., Haynes, C.M., Signaling the mitochondrial unfolded protein response. BBA – Mol. Cell Res. 1833 (2013), 410–416.
186. [186] Willems, P.H.G.M., Rossignol, R., Dieteren, C.E.J., Murphy, M.P., Koopman, W.J.H., Redox homeostasis and mitochondrial dynamics. Cell Metab. 22 (2015), 207–218.
187. [187] Lee, J., Giordano, S., Zhang, J.H., Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J. 441 (2012), 523–540.
188. 2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc. Natl. Acad. Sci. USA 105 (2008), 20728–20733.
189. [189] 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 alpha-induced phosphorylation of Drp1 regulates mitochondrial morphology. J. Cell Biol. 182 (2008), 573–585.
190. 2+ signals as causes or consequences of mitophagy induction. Autophagy 9 (2013), 1677–1686.
191. [191] Mishra, P., Carelli, V., Manfredi, G., Chan, D.C., Proteolytic cleavage of Opa1 stimulates mitochondrial inner membrane fusion and couples fusion to oxidative phosphorylation (vol. 19, pp. 630, 2014). Cell Metab., 19, 2014, 891.