Impaired OMA1-dependent cleavage of OPA1 and reduced DRP1 fission activity combine to prevent mitophagy in cells that are dependent on oxidative phosphorylation

Journal of Cell Science

Volumn 127, Issue 10, 2014, Pages 2313-2325

  MacVicar, Thomas D B ^a   Lane, Jon D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Autophagy; DRP1; Mitochondrial dynamics; Mitophagy; OMA1; OPA1

Indexed keywords

CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; DYNAMIN RELATED PROTEIN 1; OMA 1 PROTEIN; OPA 1 PROTEIN; PARKIN; PROTEIN; UNCLASSIFIED DRUG; DNM1L PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE; METALLOPROTEINASE; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL PROTEIN; MOLECULE METALLOPROTEASE-RELATED PROTEIN-1, HUMAN; OPA1 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; MEMBRANE FUSION; MEMBRANE POTENTIAL; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; MITOPHAGY; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; QUALITY CONTROL; UPREGULATION; ANIMAL; APOPTOSIS; CELL LINE; ENZYMOLOGY; GENETICS; METABOLISM; MITOCHONDRION; MOUSE; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL LINE; GTP PHOSPHOHYDROLASES; HUMANS; METALLOENDOPEPTIDASES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; OXIDATIVE PHOSPHORYLATION;

EID: 84900801787     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.144337     Document Type: Article

References (61)

1. Acin-Perez, R., Salazar, E., Kamenetsky, M., Buck, J., Levin, L. R. and Manfredi, G. (2009). Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab. 9, 265-276.
2. Allen, G. F., Toth, R., James, J. and Ganley, I. G. (2013). Loss of iron triggers PINK1/Parkin-independent mitophagy. EMBO Rep. 14, 1127-1135.
3. An, H. J., Cho, G., Lee, J. O., Paik, S. G., Kim, Y. S. and Lee, H. (2013). Higd-1a interacts with Opa1 and is required for the morphological and functional integrity of mitochondria. Proc. Natl. Acad. Sci. USA 110, 13014-13019.
4. Aoki, Y., Kanki, T., Hirota, Y., Kurihara, Y., Saigusa, T., Uchiumi, T. and Kang, D. (2011). Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol. Biol. Cell 22, 3206-3217.
5. Bensinger, S. J. and Christofk, H. R. (2012). New aspects of the Warburg effect in cancer cell biology. Semin. Cell Dev. Biol. 23, 352-361.
6. Betin, V. M. and Lane, J. D. (2009). Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. J. Cell Sci. 122, 2554-2566.
7. Betin, V. M. S., MacVicar, T. D. B., Parsons, S. F., Anstee, D. J. and Lane, J. D. (2012). A cryptic mitochondrial targeting motif in Atg4D links caspase cleavage with mitochondrial import and oxidative stress. Autophagy 8, 664-676.
8. Cereghetti, G. M., Stangherlin, A., Martins de Brito, O., Chang, C. R., Blackstone, C., Bernardi, P. and Scorrano, L. (2008). Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl. Acad. Sci. USA 105, 15803-15808.
9. Cogliati, S., Frezza, C., Soriano, M. E., Varanita, T., Quintana-Cabrera, R., Corrado, M., Cipolat, S., Costa, V., Casarin, A., Gomes, L. C. et al. (2013). Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell 155, 160-171.
10. Delettre, C., Griffoin, J. M., Kaplan, J., Dollfus, H., Lorenz, B., Faivre, L., Lenaers, G., Belenguer, P. and Hamel, C. P. (2001). Mutation spectrum and splicing variants in the OPA1 gene. Hum. Genet. 109, 584-591.
11. Ehses, S., Raschke, I., Mancuso, G., Bernacchia, A., Geimer, S., Tondera, D., Martinou, J. C., Westermann, B., Rugarli, E. I. and Langer, T. (2009). Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J. Cell Biol. 187, 1023-1036.
12. Frank, M., Duvezin-Caubet, S., Koob, S., Occhipinti, A., Jagasia, R., Petcherski, A., Ruonala, M. O., Priault, M., Salin, B. and Reichert, A. S. (2012). Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim. Biophys. Acta 1823, 2297-2310.
13. Gautier, C. A., Kitada, T. and Shen, J. (2008). Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl. Acad. Sci. USA 105, 11364-11369.
14. Gomes, L. C. and Scorrano, L. (2013). Mitochondrial morphology in mitophagy and macroautophagy. Biochim. Biophys. Acta 1833, 205-212.
15. Gomes, L. C., Di Benedetto, G. and Scorrano, L. (2011). During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13, 589-598.
16. Graef, M. and Nunnari, J. (2011). Mitochondria regulate autophagy by conserved signalling pathways. EMBO J. 30, 2101-2114.
17. Griparic, L., Kanazawa, T. and van der Bliek, A. M. (2007). Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J. Cell Biol. 178, 757-764.
18. Hackenbrock, C. R., Rehn, T. G., Weinbach, E. C. and Lemasters, J. J. (1971). Oxidative phosphorylation and ultrastructural transformation in mitochondria in the intact ascites tumor cell. J. Cell Biol. 51, 123-137.
19. Head, B., Griparic, L., Amiri, M., Gandre-Babbe, S. and van der Bliek, A. M. (2009). Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J. Cell Biol. 187, 959-966.
20. Ishihara, N., Jofuku, A., Eura, Y. and Mihara, K. (2003). Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem. Biophys. Res. Commun. 301, 891-898.
21. Ishihara, N., Fujita, Y., Oka, T. and Mihara, K. (2006). Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J. 25, 2966-2977.
22. Jahani-Asl, A., Cheung, E. C., Neuspiel, M., MacLaurin, J. G., Fortin, A., Park, D. S., McBride, H. M. and Slack, R. S. (2007). Mitofusin 2 protects cerebellar granule neurons against injury-induced cell death. J. Biol. Chem. 282, 23788-23798.
23. Jin, S. M., Lazarou, M., Wang, C., Kane, L. A., Narendra, D. P. and Youle, R. J. (2010). Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL. J. Cell Biol. 191, 933-942.
24. Johansen,T.and Lamark,T.(2011). Selective autophagy mediated by autophagic adapter proteins. Autophagy 7, 279-296.
25. Kanki, T. and Klionsky, D. J. (2008). Mitophagy in yeast occurs through a selective mechanism. J. Biol. Chem. 283, 32386-32393.
26. Kanki, T., Wang, K., Cao, Y., Baba, M. and Klionsky, D. J. (2009). Atg32 is a mitochondrial protein that confers selectivity during mitophagy. Dev. Cell 17, 98-109.
27. Kaser, M., Kambacheld, M., Kisters-Woike, B. and Langer, T. (2003). Oma1, a novel membrane-bound metallopeptidase in mitochondria with activities overlapping with the m-AAA protease. J. Biol. Chem. 278, 46414-46423.
28. Khalimonchuk, O., Jeong, M. Y., Watts, T., Ferris, E. and Winge, D. R. (2012). Selective Oma1 protease-mediated proteolysis of Cox1 subunit of cytochrome oxidase in assembly mutants. J. Biol. Chem. 287, 7289-7300.
29. Kim, J. Y., Zhao, H., Martinez, J., Doggett, T. A., Kolesnikov, A. V., Tang, P. H., Ablonczy, Z., Chan, C. C., Zhou, Z., Green, D. R. et al. (2013). Noncanonical autophagy promotes the visual cycle. Cell 154, 365-376.
30. Lemasters, J. J. (2005). Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res. 8, 3-5.
31. Liu, L., Feng, D., Chen, G., Chen, M., Zheng, Q., Song, P., Ma, Q., Zhu, C., Wang, R., Qi, W. et al. (2012). Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat. Cell Biol. 14, 177-185.
32. Losón, O. C., Song, Z., Chen, H. and Chan, D. C. (2013). Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 24, 659-667.
33. Maltecca, F., De Stefani, D., Cassina, L., Consolato, F., Wasilewski, M., Scorrano, L., Rizzuto, R. and Casari, G. (2012). Respiratory dysfunction by AFG3L2 deficiency causes decreased mitochondrial calcium uptake via organellar network fragmentation. Hum. Mol. Genet. 21, 3858-3870.
34. McBride, H. and Soubannier, V. (2010). Mitochondrial function: OMA1 and OPA1, the grandmasters of mitochondrial health. Curr. Biol. 20, R274-R276.
35. Melser, S., Chatelain, E. H., Lavie, J., Mahfouf, W., Jose, C., Obre, E., Goorden, S., Priault, M., Elgersma, Y., Rezvani, H. R. et al. (2013). Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab. 17, 719-730.
36. Narendra, D., Tanaka, A., Suen, D. F. and Youle, R. J. (2008). Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803.
37. Novak, I., Kirkin, V., McEwan, D. G., Zhang, J., Wild, P., Rozenknop, A., Rogov, V., Löhr, F., Popovic, D., Occhipinti, A. et al. (2010). Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 11, 45-51.
38. Okamoto, K., Kondo-Okamoto, N. and Ohsumi, Y. (2009). Mitochondria- anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev. Cell 17, 87-97.
39. Palmer, C. S., Elgass, K. D., Parton, R. G., Osellame, L. D., Stojanovski, D. and Ryan, M. T. (2013). Adaptor proteins MiD49 and MiD51 can act independently of Mff and Fis1 in Drp1 recruitment and are specific for mitochondrial fission. J. Biol. Chem. 288, 27584-27593.
40. Polson, H. E., de Lartigue, J., Rigden, D. J., Reedijk, M., Urbé, S., Clague, M. J. and Tooze, S. A. (2010). Mammalian Atg18 (WIPI2) localizes to omegasome- anchored phagophores and positively regulates LC3 lipidation. Autophagy 6, 506-522.
41. Quirós, P. M., Ramsay, A. J., Sala, D., Fernández-Vizarra, E., Rodríguez, F., Peinado, J. R., Fernández-García, M. S., Vega, J. A., EnrD́iquez, J. A., Zorzano, A. et al. (2012). Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J. 31, 2117-2133.
42. Rambold, A. S., Kostelecky, B., Elia, N. and Lippincott-Schwartz, J. (2011). Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. USA 108, 10190-10195.
43. Reitzer, L. J., Wice, B. M. and Kennell, D. (1979). Evidence that glutamine, not sugar, is the major energy source for cultured HeLa cells. J. Biol. Chem. 254, 2669-2676.
44. Rossignol, R., Gilkerson, R., Aggeler, R., Yamagata, K., Remington, S. J. and Capaldi, R. A. (2004). Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 64, 985-993.
45. Sandoval, H., Thiagarajan, P., Dasgupta, S. K., Schumacher, A., Prchal, J. T., Chen, M. and Wang, J. (2008). Essential role for Nix in autophagic maturation of erythroid cells. Nature 454, 232-235.
46. Scherz-Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L. and Elazar, Z. (2007). Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 26, 1749-1760.
47. 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. et al. (2007). NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl. Acad. Sci. USA 104, 19500-19505.
48. Shadrach, K. G., Rayborn, M. E., Hollyfield, J. G. and Bonilha, V. L. (2013). DJ- 1-dependent regulation of oxidative stress in the retinal pigment epithelium (RPE). PLoS ONE 8, e67983.
49. Slupe, A. M., Merrill, R. A., Flippo, K. H., Lobas, M. A., Houtman, J. C. and Strack, S. (2013). A calcineurin docking motif (LXVP) in dynamin-related protein 1 contributes to mitochondrial fragmentation and ischemic neuronal injury. J. Biol. Chem. 288, 12353-12365.
50. Song, Z., Chen, H., Fiket, M., Alexander, C. and Chan, D. C. (2007). OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J. Cell Biol. 178, 749-755.
51. Song, W., Bossy, B., Martin, O. J., Hicks, A., Lubitz, S., Knott, A. B. and Bossy-Wetzel, E. (2008). Assessing mitochondrial morphology and dynamics using fluorescence wide-field microscopy and 3D image processing. Methods 46, 295-303.
52. Strauss, O. (2005). The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845-881.
53. Tanaka, A., Cleland, M. M., Xu, S., Narendra, D. P., Suen, D. F., Karbowski, M. and Youle, R. J. (2010). Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 191, 1367-1380.
54. Tondera, D., Grandemange, S., Jourdain, A., Karbowski, M., Mattenberger, Y., Herzig, S., Da Cruz, S., Clerc, P., Raschke, I., Merkwirth, C. et al. (2009). SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J. 28, 1589-1600.
55. Twig, G., Elorza, A., Molina, A. J., Mohamed, H., Wikstrom, J. D., Walzer, G., Stiles, L., Haigh, S. E., Katz, S., Las, G. et al. (2008). Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446.
56. Unger, R. H. (1985). Glucagon physiology and pathophysiology in the light of new advances. Diabetologia 28, 574-578.
57. Van Laar, V. S., Arnold, B., Cassady, S. J., Chu, C. T., Burton, E. A. and Berman, S. B. (2011). Bioenergetics of neurons inhibit the translocation response of Parkin following rapid mitochondrial depolarization. Hum. Mol. Genet. 20, 927-940.
58. White, E. (2012). Deconvoluting the context-dependent role for autophagy in cancer. Nat. Rev. Cancer 12, 401-410.
59. Yamano, K. and Youle, R. J. (2013). PINK1 is degraded through the N-end rule pathway. Autophagy 9, 1758-1769.
60. Youle, R. J. and Narendra, D. P. (2011). Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14.
61. Youle, R. J. and van der Bliek, A. M. (2012). Mitochondrial fission, fusion, and stress. Science 337, 1062-1065.