Activation of mitochondrial protease OMA1 by bax and bak promotes cytochrome c release during apoptosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 41, 2014, Pages 14782-14787

  Jiang, Xian ^a,b,c   Jiang, Hui ^a   Shen, Zhirong ^a   Wang, Xiaodong ^a,b,c  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^b GRADUATE SCHOOL OF PEKING UNION MEDICAL COLLEGE   (China)

^c PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

Caspase; Membrane potential; Permeability; Smac

Indexed keywords

CYTOCHROME C; GUANOSINE TRIPHOSPHATASE; METALLOPROTEINASE; MOLECULE METALLOPROTEASE-RELATED PROTEIN-1, HUMAN; OPA1 PROTEIN, HUMAN; PROTEIN BAK; PROTEIN BAX; PROTEIN BID;

APOPTOSIS; ENZYME ACTIVATION; ENZYMOLOGY; GENE SILENCING; HUMAN; METABOLISM; MITOCHONDRION; PROTEIN STABILITY; TUMOR CELL LINE;

APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CELL LINE, TUMOR; CYTOCHROMES C; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; GTP PHOSPHOHYDROLASES; HUMANS; METALLOENDOPEPTIDASES; MITOCHONDRIA; PROTEIN STABILITY;

EID: 84907919478     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1417253111     Document Type: Article

References (36)

1. Liu X, Kim CN, Yang J, Jemmerson R, Wang X (1996) Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochromec. Cell 86(1):147-157.
2. Li P, et al. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91(4):479-489.
3. Du C, Fang M, Li Y, Li L, Wang X (2000) Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102(1): 33-42.
4. Verhagen AM, et al. (2000) Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102(1):43-53.
5. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997) The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275(5303):1132-1136.
6. Yang J, et al. (1997) Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 275(5303):1129-1132.
7. Wei MC, et al. (2001) Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 292(5517):727-730.
8. Nechushtan A, Smith CL, Lamensdorf I, Yoon SH, Youle RJ (2001) Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J Cell Biol 153(6): 1265-1276.
9. Wei MC, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14(16):2060-2071.
10. Kuwana T, et al. (2005) BH3 domains of BH3-only proteins differentially regulate Baxmediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell 17(4):525-535.
11. Willis SN, et al. (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19(11):1294-1305.
12. Peng J, et al. (2006) tBid elicits a conformational alteration in membrane-bound Bcl-2 such that it inhibits Bax pore formation. J Biol Chem 281(47):35802-35811.
13. Ren D, et al. (2010) BID, BIM, and PUMA are essential for activation of the BAX- And BAK-dependent cell death program. Science 330(6009):1390-1393.
14. Eskes R, Desagher S, Antonsson B, Martinou JC (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20(3): 929-935.
15. Antonsson B, Montessuit S, Sanchez B, Martinou JC (2001) Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 276(15):11615-11623.
16. Annis MG, et al. (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J 24(12):2096-2103.
17. Czabotar PE, et al. (2013) Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 152(3):519-531.
18. Lovell JF, et al. (2008) Membrane binding by tBid initiates an ordered series of events culminating in membrane permeabilization by Bax. Cell 135(6):1074-1084.
19. Korsmeyer SJ, et al. (2000) Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7(12):1166-1173.
20. Basañez G, et al. (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 277(51): 49360-49365.
21. Kuwana T, et al. (2002) Bid, Bax, and lipids cooperate to form supra molecular openings in the outer mitochondrial membrane. Cell 111(3):331-342.
22. Martinez-Caballero S, et al. (2009) Assembly of the mitochondrial apoptosis-induced channel, MAC. J Biol Chem 284(18):12235-12245.
23. Schafer B, et al. (2009) Mitochondrial outer membrane proteins assist Bid in Baxmediated lipidic pore formation. Mol Biol Cell 20(8):2276-2285.
24. Frezza C, et al. (2006) OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 126(1):177-189.
25. Olichon A, et al. (2003) Loss of OPA1 perturbates the mitochondrial inner membrane structure and integrity, leading to cytochrome c release and apoptosis. J Biol Chem 278(10):7743-7746.
26. Yamaguchi R, et al. (2008) Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization. Mol Cell 31(4):557-569.
27. 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(5):749-755.
28. Cipolat S, et al. (2006) Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 126(1):163-175.
29. Ehses S, et al. (2009) Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J Cell Biol 187(7):1023-1036.
30. Stiburek L, et al. (2012) YME1L controls the accumulation of respiratory chain subunits and is required for apoptotic resistance, cristae morphogenesis, and cell proliferation. Mol Biol Cell 23(6):1010-1023.
31. Head B, Griparic L, Amiri M, Gandre-Babbe S, van der Bliek AM (2009) Inducible proteolytic inactivation of OPA1 mediated by the OMA1 protease in mammalian cells. J Cell Biol 187(7):959-966.
32. Dejean LM, et al. (2005) Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol Biol Cell 16(5): 2424-2432.
33. Arnoult D, Grodet A, Lee YJ, Estaquier J, Blackstone C (2005) Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J Biol Chem 280(42):35742-35750.
34. Baker MJ, et al. (2014) Stress-induced OMA1 activation and autocatalytic turnover regulate OPA1-dependent mitochondrial dynamics. EMBO J 33(6):578-593.
35. Gonzalvez F, et al. (2005) tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak. Cell Death Differ 12(6):614-626.
36. Quirós PM, 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(9): 2117-2133.