Chemical Inhibition of the Mitochondrial Division Dynamin Reveals Its Role in Bax/Bak-Dependent Mitochondrial Outer Membrane Permeabilization

Developmental Cell

Volumn 14, Issue 2, 2008, Pages 193-204

  Cassidy Stone, Ann ^a   Chipuk, Jerry E ^b   Ingerman, Elena ^a   Song, Cheng ^a   Yoo, Choong ^a   Kuwana, Tomomi ^c   Kurth, Mark J ^a   Shaw, Jared T ^d   Hinshaw, Jenny E ^e   Green, Douglas R ^b   Nunnari, Jodi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

CELLBIO; CELLCYCLE; CHEMBIO

Indexed keywords

CYTOCHROME C; DYNAMIN; MITOCHONDRIAL PROTEIN; PROTEIN BAK; PROTEIN BAX; PROTEIN BID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; INHIBITION KINETICS; MAMMAL CELL; MEMBRANE PERMEABILITY; MITOCHONDRION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; YEAST CELL;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CERCOPITHECUS AETHIOPS; COS CELLS; DYNAMINS; FLOW CYTOMETRY; HELA CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PERMEABILITY; QUINAZOLINONES; SACCHAROMYCES CEREVISIAE; STRUCTURE-ACTIVITY RELATIONSHIP;

MAMMALIA;

EID: 38849099158     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2007.11.019     Document Type: Article

References (61)

1. Abdelwahid E., Yokokura T., Krieser R.J., Balasundaram S., Fowle W.H., and White K. Mitochondrial disruption in Drosophila apoptosis. Dev. Cell 12 (2007) 793-806
2. Adams J.M., and Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 281 (1998) 1322-1326
3. Antignani A., and Youle R.J. How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane?. Curr. Opin. Cell Biol. 18 (2006) 685-689
4. Bleazard W., McCaffery J.M., King E.J., Bale S., Mozdy A., Tieu Q., Nunnari J., and Shaw J.M. The dynamin-related GTPases, Dnm1, regulates mitochondrial fission in yeast. Nat. Cell Biol. 1 (1999) 298-304
5. Breckenridge D.G., Stojanovic M., Marcellus R.C., and Shore G.C. Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J. Cell Biol. 160 (2003) 1115-1127
6. Chan D.C. Mitochondria: dynamic organelles in disease, aging, and development. Cell 125 (2006) 1241-1252
7. Chan D.C. Mitochondrial fusion and fission in mammals. Annu. Rev. Cell. Dev. Biol. 22 (2006) 79-99
8. Chen H., and Chan D.C. Critical dependence of neurons on mitochondrial dynamics. Curr. Opin. Cell Biol. 18 (2006) 453-459
9. Chen H., Chomyn A., and Chan D.C. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280 (2005) 26185-26192
10. Chipuk J.E., Bouchier-Hayes L., and Green D.R. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13 (2006) 1396-1402
11. Danino D., and Hinshaw J.E. Dynamin family of mechanoenzymes. Curr. Opin. Cell Biol. 13 (2001) 454-460
12. Delivani P., Adrain C., Taylor R.C., Duriez P.J., and Martin S.J. Role for CED-9 and Egl-1 as regulators of mitochondrial fission and fusion dynamics. Mol. Cell 21 (2006) 761-773
13. Estaquier J., and Arnoult D. Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ. 14 (2007) 1086-1094
14. Fadok V.A., and Henson P.M. Apoptosis: giving phosphatidylserine recognition an assist-with a twist. Curr. Biol. 13 (2003) R655-R657
15. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W., Robert E.G., Catez F., Smith C.L., and Youle R.J. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1 (2001) 515-525
16. Frezza C., Cipolat S., Martins de Brito O., Micaroni M., Beznoussenko G.V., Rudka T., Bartoli D., Polishuck R.S., Danial N.N., De Strooper B., et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126 (2006) 177-189
17. Germain M., Mathai J.P., McBride H.M., and Shore G.C. Endoplasmic reticulum BIK initiates DRP1-regulated remodelling of mitochondrial cristae during apoptosis. EMBO J. 24 (2005) 1546-1556
18. Goyal G., Fell B., Sarin A., Youle R.J., and Sriram V. Role of mitochondrial remodeling in programmed cell death in Drosophila melanogaster. Dev. Cell 12 (2007) 807-816
19. Griffin E.E., and Chan D.C. Domain interactions within Fzo1 oligomers are essential for mitochondrial fusion. J. Biol. Chem. 281 (2006) 16599-16606
20. Harder Z., Zunino R., and McBride H. Sumo1 conjugates mitochondrial substrates and participates in mitochondrial fission. Curr. Biol. 14 (2004) 340-345
21. Hermann G.J., Thatcher J.W., Mills J.P., Hales K.G., Fuller M.T., Nunnari J., and Shaw J.M. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J. Cell Biol. 143 (1998) 359-374
22. Hoppins S., Lackner L., and Nunnari J. The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76 (2007) 751-780
23. Ingerman E., Perkins E.M., Marino M., Mears J.A., McCaffery J.M., Hinshaw J.E., and Nunnari J. Dnm1 forms spirals that are structurally tailored to fit mitochondria. J. Cell Biol. 170 (2005) 1021-1027
24. Ishihara N., Eura Y., and Mihara K. Mitofusin 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J. Cell Sci. 117 (2004) 6535-6546
25. Jagasia R., Grote P., Westermann B., and Conradt B. DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature 433 (2005) 754-760
26. Karbowski M., and Youle R.J. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 10 (2003) 870-880
27. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., and Youle R.J. Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis. J. Cell Biol. 159 (2002) 931-938
28. Karbowski M., Arnoult D., Chen H., Chan D.C., Smith C.L., and Youle R.J. Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis. J. Cell Biol. 164 (2004) 493-499 Published online February 9, 2004
29. Karbowski M., Norris K., Cleland M., Jeong S., and Youle R. Role of Bax and Bak in mitochondrial morphogenesis. Nature 443 (2006) 658-662
30. Koshiba T., Detmer S., Kaiser J., Chen H., McCaffery J., and Chan D. Structural basis of mitochondrial tethering by mitofusin complexes acting in trans. Science 305 (2004) 858-862
31. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., and Newmeyer D.D. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111 (2002) 331-342
32. Labrousse A.M., Zappaterra M.D., Rube D.A., and 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
33. Lee Y.J., Jeong S.Y., Karbowski M., Smith C.L., and Youle R.J. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol. Biol. Cell 15 (2004) 5001-5011
34. Macia E., Ehrlich M., Massol R., Boucrot E., Brunner C., and Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10 (2006) 839-850
35. Martinou J.C., and Youle R.J. Which came first, the cytochrome c release or the mitochondrial fission?. Cell Death Differ. 13 (2006) 1291-1295
36. McConnell S.J., Stewart L.C., Talin A., and Yaffe M.P. Temperature-sensitive mutants defective in mitochondrial inheritance. J. Cell Biol. 111 (1990) 967-976
37. Meeusen S., McCaffery J.M., and Nunnari J. Mitochondrial fusion intermediates revealed in vitro. Science 305 (2004) 1747-1752
38. Meeusen S., Devay R., Block J., Cassidy-Stone A., Wayson S., McCaffery J.M., and Nunnari J. Mitochondrial inner-membrane fusion and crista maintenance requires the dynamin-related GTPase Mgm1. Cell 127 (2006) 383-395
39. Monod J., Wyman J., and Changeux J.P. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12 (1965) 88-118
40. Morton W.M., Ayscough K.R., and McLaughlin P.J. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2 (2000) 376-378
41. Nakamura N., Kimura Y., Tokuda M., Honda S., and Hirose S. MARCH-V is a novel mitofusin 2- and Drp1-binding protein able to change mitochondrial morphology. EMBO Rep. 7 (2006) 1019-1022
42. Naylor K., Ingerman E., Okreglak V., Marino M., Hinshaw J.E., and Nunnari J. Mdv1 interacts with assembled dnm1 to promote mitochondrial division. J. Biol. Chem. 281 (2006) 2177-2183
43. Neuspiel M., Zunino R., Gangaraju S., Rippstein P., and McBride H. Activated mitofusin 2 signals mitochondrial fusion, interferes with Bax activation, and reduces susceptibility to radical induced depolarization. J. Biol. Chem. 280 (2005) 25060-25070
44. Newmeyer D.D., and Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112 (2003) 481-490
45. Nunnari J., Marshall W., Straight A., Murray A., Sedat J.W., and Walter P. Mitochondrial transmission during mating in S. cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mtDNA. Mol. Biol. Cell 8 (1997) 1233-1242
46. Olichon A., Baricault L., Gas N., Guillou E., Valette A., Belenguer P., and Lenaers G. Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J. Biol. Chem. 278 (2003) 7743-7746
47. Olichon A., Guillou E., Delettre C., Landes T., Arnaune-Pelloquin L., Emorine L.J., Mils V., Daloyau M., Hamel C., Amati-Bonneau P., et al. Mitochondrial dynamics and disease, OPA1. Biochim. Biophys. Acta 1763 (2006) 500-509
48. Parone P.A., James D.I., Da Cruz S., Mattenberger Y., Donze O., Barja F., and Martinou J.C. Inhibiting the mitochondrial fission machinery does not prevent Bax/Bak-dependent apoptosis. Mol. Cell. Biol. 26 (2006) 7397-7408
49. Rogers B., Decottignies A., Kolaczkowski M., Carvajal E., Balzi E., and Goffeau A. The pleitropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 3 (2001) 207-214
50. Rolland S., and Conradt B. The role of mitochondria in apoptosis induction in Caenorhabditis elegans: more than just innocent bystanders?. Cell Death Differ. 13 (2006) 1281-1286
51. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., and Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2 (2002) 55-67
52. Sesaki H., and Jensen R.E. Division versus fusion: Dnm1p and Fzo1p antagonistically regulate mitochondrial shape. J. Cell Biol. 147 (1999) 699-706
53. Smirnova E., Shurland D., Ryazantsev S., and Van Der Bliek A. A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143 (1998) 351-358
54. Smirnova E., Griparic L., Shurland D.L., and van Der Bliek A.M. Dynamin-related protein drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12 (2001) 2245-2256
55. Sugioka R., Shimizu S., and Tsujimoto Y. Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J. Biol. Chem. 279 (2004) 52726-52734
56. Taguchi N., Ishihara N., Jofuku A., Oka T., and Mihara K. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282 (2007) 11521-11529
57. Walensky L.D., Pitter K., Morash J., Oh K.J., Barbuto S., Fisher J., Smith E., Verdine G.L., and Korsmeyer S.J. A stapled BID BH3 helix directly binds and activates BAX. Mol. Cell 24 (2006) 199-210
58. Warnock D.E., Hinshaw J.E., and Schmid S.L. Dynamin self-assembly stimulates its GTPase activity. J. Biol. Chem. 271 (1996) 22310-22314
59. Wasiak S., Zunino R., and McBride H.M. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177 (2007) 439-450
60. Willis S.N., Fletcher J.I., Kaufmann T., van Delft M.F., Chen L., Czabotar P.E., Ierino H., Lee E.F., Fairlie W.D., Bouillet P., et al. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315 (2007) 856-859
61. Youle R.J. Morphology of mitochondria during apoptosis: worms-to-beetles in worms. Dev. Cell 8 (2005) 298-299