During autophagy mitochondria elongate, are spared from degradation and sustain cell viability

Nature Cell Biology

Volumn 13, Issue 5, 2011, Pages 589-598

  Gomes, Ligia C ^a,b,c   Benedetto, Giulietta Di ^b,d   Scorrano, Luca ^a,b,e  

^a DULBECCO TELETHON INSTITUTE   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d CNR Consiglio Nazionale delle Ricerche   (Italy)

^e UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DYNAMIN; DYNAMIN RELATED PROTEIN 1; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL DEATH; CELL FATE; CELL STRAIN HEPG2; CELL VIABILITY; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; EMBRYO; FIBROBLAST; HELA CELL; HUMAN; HUMAN CELL; LIVER CELL; MITOCHONDRIAL ELONGATION; MITOCHONDRION; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STARVATION; TIBIALIS ANTERIOR MUSCLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; AUTOPHAGY; CELL DEATH; CELL LINE; HUMANS; MICE; MITOCHONDRIA;

EUKARYOTA;

EID: 79955623510     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb2220     Document Type: Article

References (65)

1. Bereiter-Hahn, J. & Voth, M. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and-ssion of mitochondria. Microsc. Res. Tech. 27, 198-219 (1994). (Pubitemid 24062014)
2. Cipolat, S., de Brito, O. M., Dal Zilio, B. & Scorrano, L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc. Natl Acad. Sci. USA 101, 15927-15932 (2004). (Pubitemid 39507904)
3. Santel, A. & Fuller, M. T. Control of mitochondrial morphology by a human mitofusin. J. Cell Sci. 114, 867-874 (2001). (Pubitemid 32266258)
4. Smirnova, E., Griparic, L., Shurland, D. L. & van der Bliek, A. M. Dynaminrelated protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256 (2001). (Pubitemid 33051954)
5. Cereghetti, G. M. et al. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc. Natl Acad. Sci. USA 105, 15803-15808 (2008).
6. Cribbs, J. T. & Strack, S. Reversible phosphorylation of Drp1 by cyclic AMPdependent protein kinase and calcineurin regulates mitochondrial-ssion and cell death. EMBO Rep. 8, 939-944 (2007). (Pubitemid 47500477)
7. Chang, C. R. & Blackstone, C. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 282, 21583-21587 (2007). (Pubitemid 47195725)
8. Harder, Z., Zunino, R. & McBride, H. Sumo1 conjugates mitochondrial substrates and participates in mitochondrial-ssion. Curr. Biol. 14, 340-345 (2004). (Pubitemid 38300214)
9. Braschi, E., Zunino, R. & McBride, H. M. MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial-ssion. EMBO Rep. 10, 748-754 (2009).
10. Scorrano, L. et al. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2, 55-67 (2002). (Pubitemid 34065906)
11. Martinou, I. et al. The release of cytochrome c from mitochondria during apoptosis of NGF-deprived sympathetic neurons is a reversible event. J. Cell Biol. 144, 883-889 (1999). (Pubitemid 29238965)
12. Frank, S. et al. The role of dynamin-related protein 1, a mediator of mitochondrial-ssion, in apoptosis. Dev. Cell 1, 515-525 (2001). (Pubitemid 33586103)
13. Szabadkai, G. et al. Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2C waves and protects against Ca2C-mediated apoptosis. Mol. Cell 16, 59-68 (2004). (Pubitemid 39330152)
14. Li, Z., Okamoto, K., Hayashi, Y. & Sheng, M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887 (2004). (Pubitemid 40017692)
15. Campello, S. et al. Orchestration of lymphocyte chemotaxis by mitochondrial dynamics. J. Exp. Med. 203, 2879-2886 (2006). (Pubitemid 46026165)
16. Mitra, K., Wunder, C., Roysam, B., Lin, G. & Lippincott-Schwartz, J. A hyperfused mitochondrial state achieved at G1-S regulates cyclin E buildup and entry into S phase. Proc. Natl Acad. Sci. USA 106, 11960-11965 (2009).
17. Scheckhuber, C. Q. et al. Reducing mitochondrial-ssion results in increased life span and-tness of two fungal ageing models. Nat. Cell Biol. 9, 99-105 (2007). (Pubitemid 46024203)
18. Twig, G. et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27, 433-446 (2008). (Pubitemid 351161653)
19. Gomes, L. C. & Scorrano, L. High levels of Fis1, a pro-ssion mitochondrial protein, trigger autophagy. Biochim. Biophys. Acta 1777, 860-866 (2008).
20. Klionsky, D. J. & Emr, S. D. Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721 (2000). (Pubitemid 32004796)
21. Cecconi, F. & Levine, B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev. Cell 15, 344-357 (2008).
22. Ravikumar, B., Duden, R. & Rubinsztein, D. C. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11, 1107-1117 (2002). (Pubitemid 34521091)
23. Zheng, Y. T. et al. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. 183, 5909-5916 (2009).
24. Tuttle, D. L., Lewin, A. S. & Dunn, W. A. Jr Selective autophagy of peroxisomes in methylotrophic yeasts. Eur. J. Cell Biol. 60, 283-290 (1993). (Pubitemid 23139646)
25. Bernales, S., McDonald, K. L. & Walter, P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 4, e423 (2006).
26. Elmore, S. P., Qian, T., Grissom, S. F. & Lemasters, J. J. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15, 2286-2287 (2001).
27. Tooze, S. A. & Yoshimori, T. The origin of the autophagosomal membrane. Nat. Cell Biol. 12, 831-835 (2010).
28. Scherz-Shouval, R. et al. Reactive oxygen species are essential for autophagy and speci-cally regulate the activity of Atg4. EMBO J. 26, 1749-1760 (2007). (Pubitemid 46624042)
29. Hailey, D. W. et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141, 656-667 (2010).
30. de Brito, O. M. & Scorrano, L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610 (2008).
31. Karbowski, M. et al. Quantitation of mitochondrial dynamics by photolabelling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164, 493-499 (2004). (Pubitemid 38233310)
32. Song, Z., Chen, H., 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, 749-755 (2007). (Pubitemid 47347360)
33. Chen, H., Chomyn, A. & Chan, D. C. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280, 26185-26192 (2005). (Pubitemid 41022214)
34. Ishihara, N. et al. Mitochondrial-ssion factor Drp1 is essential for embryonic development and synapse formation in mice. Nat. Cell Biol. 11, 958-966 (2009).
35. Jouaville, L. S., Pinton, P., Bastianutto, C., Rutter, G. A. & Rizzuto, R. Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc. Natl Acad. Sci. USA 96, 13807-13812 (1999).
36. Rich, P. Chemiosmotic coupling: the cost of living. Nature 421, 583 (2003).
37. Strauss, M., Hofhaus, G., Schroder, R. R. & Kuhlbrandt, W. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27, 1154-1160 (2008). (Pubitemid 351508145)
38. Giraud, M. F. et al. Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae? Biochim. Biophys. Acta 1555, 174-180 (2002).
39. Unger, R. H. Glucagon physiology and pathophysiology in the light of new advances. Diabetologia 28, 574-578 (1985). (Pubitemid 15017391)
40. Pan, X. & Heitman, J. Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Mol. Cell Biol. 19, 4874-4887 (1999). (Pubitemid 29289526)
41. Budovskaya, Y. V., Stephan, J. S., Reggiori, F., Klionsky, D. J. & Herman, P. K. The Ras/cAMP-dependent protein kinase signalling pathway regulates an early step of the autophagy process in Saccharomyces cerevisiae. J. Biol. Chem. 279, 20663-20671 (2004). (Pubitemid 38656461)
42. Stephan, J. S., Yeh, Y. Y., Ramachandran, V., Deminoff, S. J. & Herman, P. K. The Tor and PKA signalling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc. Natl Acad. Sci. 106, 17049-17054 (2009).
43. Mavrakis, M., Lippincott-Schwartz, J., Stratakis, C. A. & Bossis, I. Depletion of type IA regulatory subunit (RIalpha) of protein kinase A (PKA) in mammalian cells and tissues activates mTOR and causes autophagic de-ciency. Hum. Mol. Genet. 15, 2962-2971 (2006). (Pubitemid 44446815)
44. Slattery, M. G., Liko, D. & Heideman, W. Protein kinase A, TOR, and glucose transport control the response to nutrient repletion in Saccharomyces cerevisiae. Eukaryot. Cell 7, 358-367 (2008). (Pubitemid 351959703)
45. Tondera, D. et al. SLP-2 is required for stress-induced mitochondrial hyperfusion. EMBO J. 28, 1589-1600 (2009).
46. Karbowski, M. & Youle, R. J. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 10, 870-880 (2003). (Pubitemid 36939697)
47. Cereghetti, G. M., Costa, V. & Scorrano, L. Inhibition of Drp1-dependent mitochondrial fragmentation and apoptosis by a polypeptide antagonist of calcineurin. Cell Death Differ. 17, 1785-1794 (2010).
48. Wasiak, S., Zunino, R. & McBride, H. M. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177, 439-450 (2007). (Pubitemid 46718273)
49. Nakamura, N., Kimura, Y., Tokuda, M., Honda, S. & Hirose, S. MARCH-V is a novel mitofusin 2-and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7, 1019-1022 (2006). (Pubitemid 44480517)
50. Karbowski, M., Neutzner, A. & Youle, R. J. The mitochondrial E3 ubiquitin ligase MARCH5 is required for Drp1 dependent mitochondrial division. J. Cell Biol. 178, 71-84 (2007). (Pubitemid 47026403)
51. Tanaka, A. et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 191, 1367-1380 (2010).
52. Ziviani, E., Tao, R. N. & Whitworth, A. J. Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl Acad. Sci. USA 107, 5018-5023 (2010).
53. 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, 795-803 (2008).
54. Costa, V. et al. Mitochondrial-ssion and cristae disruption increase the response of cell models of Huntington's disease to apoptotic stimuli. EMBO Mol. Med. 2, 490-503 (2010).
55. Brown, G. C. Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J. 284, 1-13 (1992).
56. Frezza, C. et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126, 177-189 (2006).
57. Meeusen, S. et al. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 127, 383-395 (2006). (Pubitemid 44572371)
58. Mopert, K. et al. Loss of Drp1 function alters OPA1 processing and changes mitochondrial membrane organization. Exp. Cell Res. 315, 2165-2180 (2009).
59. Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (2004). (Pubitemid 40052234)
60. Nikolaev, V. O., Bünemann, M., Hein, L., Hannawacker, A. & Lohse, M. J. Novel single chain cAMP sensors for receptor-induced signal propagation. J. Biol. Chem. 279, 37215-37218 (2004). (Pubitemid 39195424)
61. de Brito, O. M. & Scorrano, L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605-610 (2008).
62. Scorrano, L. et al. BAX and BAK regulation of endoplasmic reticulum Ca2C: a control point for apoptosis. Science 300, 135-139 (2003). (Pubitemid 36423046)
63. Danial, N. N. et al. BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424, 952-956 (2003). (Pubitemid 37051687)
64. Frezza, C., Cipolat, S. & Scorrano, L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured-broblasts. Nat. Protoc. 2, 287-295 (2007). (Pubitemid 47040043)
65. Alirol, E. et al. The mitochondrial-ssion protein hFis1 requires the endoplasmic reticulum gateway to induce apoptosis. Mol. Biol. Cell 17, 4593-4605 (2006). (Pubitemid 44665731)