Fission and selective fusion govern mitochondrial segregation and elimination by autophagy

EMBO Journal

Volumn 27, Issue 2, 2008, Pages 433-446

  Twig, Gilad ^a   Elorza, Alvaro ^a   Molina, Anthony J A ^a,b   Mohamed, Hibo ^a   Wikstrom, Jakob D ^a   Walzer, Gil ^a   Stiles, Linsey ^a   Haigh, Sarah E ^a   Katz, Steve ^a   Las, Guy ^a   Alroy, Joseph ^c   Wu, Min ^d   Py, Bénédicte F ^e   Yuan, Junying ^e   Deeney, Jude T ^b   Corkey, Barbara E ^b   Shirihai, Orian S ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS MEDICAL CENTER   (United States)

^d Seahorse Bioscience   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

cell; Autophagy; Fission; Fusion; Mitochondria

Indexed keywords

BAFILOMYCIN; HYBRID PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN OPA1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGY; CELL STRAIN COS7; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEPOLARIZATION; FIBROBLAST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INSULIN METABOLISM; INSULIN RELEASE; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; QUANTITATIVE ANALYSIS;

ANIMALS; AUTOPHAGY; CELL LINE; GENOTYPE; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; INSULIN; INSULIN-SECRETING CELLS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MUTATION; REACTIVE OXYGEN SPECIES;

EID: 38549110110     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601963     Document Type: Article

References (39)

1. Alavi MV, Bette S, Schimpf S, Schuettauf F, Schraermeyer U, Wehrl HF, Ruttiger L, Beck SC, Tonagel F, Pichler BJ, Knipper M, Peters T, Laufs J, Wissinger B (2007) A splice site mutation in the murine Opa1 gene features pathology of autosomal dominant optic atrophy. Brain 130: 1029-1042
2. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci USA 101: 7805-7808
3. Barsoum MJ, Yuan H, Gerencser AA, Liot G, Kushnareva Y, Graber S, Kovacs I, Lee WD, Waggoner J, Cui J, White AD, Bossy B, Martinou JC, Youle RJ, Lipton SA, Ellisman MH, Perkins GA, Bossy-Wetzel E (2006) Nitric oxide-induced mitochondrial fission is regulated by dynamin-related GTPases in neurons. EMBO J 25: 3900-3911
4. Chan DC (2006) Mitochondria: dynamic organelles in disease, aging, and development. Cell 125: 1241-1252
5. Chen H, Chomyn A, Chan DC (2005) Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem 280: 26185-26192
6. Cipolat S, Martins de Brito O, Dal Zilio B, Scorrano L (2004) OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci USA 101: 15927-15932
7. Corkey BE, Duszynski J, Rich TL, Matschinsky B, Williamson JR (1986) Regulation of free and bound magnesium in rat hepatocytes and isolated mitochondria. J Biol Chem 261: 2567-2574
8. Duvezin-Caubet S, Jagasia R, Wagener J, Hofmann S, Trifunovic A, Hansson A, Chomyn A, Bauer MF, Attardi G, Larsson NG, Neupert W, Reichert AS (2006) Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J Biol Chem 281: 37972-37979
9. Elmore SP, Qian T, Grissom SF, Lemasters JJ (2001) The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15: 2286-2287
10. Griparic L, van der Wel NN, Orozco IJ, Peters PJ, van der Bliek AM (2004) Loss of the intermembrane space protein Mgm1/OPA1 induces swelling and localized constrictions along the lengths of mitochondria. J Biol Chem 279: 18792-18798
11. Heart E, Corkey RF, Wikstrom JD, Shirihai OS, Corkey BE (2006) Glucose-dependent increase in mitochondrial membrane potential, but not cytoplasmic calcium, correlates with insulin secretion in single islet cells. Am J Physiol Endocrinol Metab 290: E143-E148
12. Herlan M, Bornhovd C, Hell K, Neupert W, Reichert AS (2004) Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor. J Cell Biol 165: 167-173
13. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB (2000) Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49: 424-430
14. Ishihara N, Fujita Y, Oka T, Mihara K (2006) Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 25: 2966-2977
15. Ishihara N, Jofuku A, Eura Y, Mihara K (2003) Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1dependent fusion reaction in mammalian cells. Biochem Biophys Res Commun 301: 891-898
16. 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 (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169: 425-434
17. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N (2004) The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036
18. Lee S, Jeong SY, Lim WC, Kim S, Park YY, Sun X, Youle RJ, Cho H (2007) Mitochondrial fission and fusion mediators, hFis1 and OPA1, modulate cellular senescence. J Biol Chem 282: 22977-22983
19. Legros F, Lombes A, Frachon P, Rojo M (2002) Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins. Mol Biol Cell 13: 4343-4354
20. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115: 2679-2688
21. Lowell BB, Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387
22. Maechler P, Jornot L, Wollheim CB (1999) Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J Biol Chem 274: 27905-27913
23. Malka F, Guillery O, Cifuentes-Diaz C, Guillou E, Belenguer P, Lombes A, Rojo M (2005) Separate fusion of outer and inner mitochondrial membranes. EMBO Rep 6: 853-859
24. Meeusen S, McCaffery JM, Nunnari J (2004) Mitochondrial fusion intermediates revealed in vitro. Science 305: 1747-1752
25. Nakada K, Inoue K, Ono T, Isobe K, Ogura A, Goto YI, Nonaka I, Hayashi JI (2001) Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat Med 7: 934-940
26. Nicholls DG (2004) Mitochondrial membrane potential and aging. Aging Cell 3: 35-40
27. Noel RJ, Antinozzi PA, McGarry JD, Newgard CB (1997) Engineering of glycerol-stimulated insulin secretion in islet beta cells. Differential metabolic fates of glucose and glycerol provide insight into mechanisms of stimulus-secretion coupling. J Biol Chem 272: 18621-18627
28. Okamoto K, Shaw JM (2005) Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu Rev Genet 39: 503-536
29. Olichon A, Baricault L, Gas N, Guillou E, Valette A, Belenguer P, Lenaers G (2003) Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J Biol Chem 278: 7743-7746
30. Priault M, Salin B, Schaeffer J, Vallette FM, di Rago JP, Martinou JC (2005) Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ 12: 1613-1621
31. Pyo JO, Jang MH, Kwon YK, Lee HJ, Jun JI, Woo HN, Cho DH, Choi B, Lee H, Kim JH, Mizushima N, Oshumi Y, Jung YK (2005) Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J Biol Chem 280: 20722-20729
32. Skulachev VP (2001) Mitochondrial filaments and clusters as intracellular power-transmitting cables. Trends Biochem Sci 26: 23-29
33. Song Z, Chen H, Fiket M, Alexander C, Chan DC (2007) OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol 178: 749-755
34. Stojanovski D, Koutsopoulos OS, Okamoto K, Ryan MT (2004) Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology. J Cell Sci 117: 1201-1210
35. Stroikin Y, Dalen H, Loof S, Terman A (2004) Inhibition of autophagy with 3-methyladenine results in impaired turnover of lysosomes and accumulation of lipofuscin-like material. Eur J Cell Biol 83: 583-590
36. Twig G, Graf SA, Wikstrom JD, Mohamed H, Haigh SE, Elorza A, Deutsch M, Zurgil N, Reynolds N, Shirihai OS (2006) Tagging and tracking individual networks within a complex mitochondrial web with photoactivatable GFP. Am J Physiol Cell Physiol 291: C176-C184
37. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parslow D, Armistead S, Lemire K, Orrell J, Teich J, Chomicz S, Ferrick DA (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292: C125-C136
38. Yoon Y, Krueger EW, Oswald BJ, McNiven MA (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol 23: 5409-5420
39. Yoon YS, Yoon DS, Lim IK, Yoon SH, Chung HY, Rojo M, Malka F, Jou MJ, Martinou JC, Yoon G (2006) Formation of elongated giant mitochondria in DFO-induced cellular senescence: involvement of enhanced fusion process through modulation of Fis1. J Cell Physiol 209: 468-480