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Mitochondrial Shape Governs BAX-Induced Membrane Permeabilization and Apoptosis
Open accessAbstract
Proapoptotic BCL-2 proteins converge upon the outer mitochondrial membrane (OMM) to promote mitochondrial outer membrane permeabilization (MOMP) and apoptosis. Here we investigated the mechanistic relationship between mitochondrial shape and MOMP and provide evidence that BAX requires a distinct mitochondrial size to induce MOMP. We utilized the terminal unfolded protein response pathway to systematically define proapoptotic BCL-2 protein composition after stress and then directly interrogated their requirement for a productive mitochondrial size. Complementary biochemical, cellular, in vivo, and ex vivo studies reveal that Mfn1, a GTPase involved in mitochondrial fusion, establishes a mitochondrial size that is permissive for proapoptotic BCL-2 family function. Cells with hyperfragmented mitochondria, along with size-restricted OMM model systems, fail to support BAX-dependent membrane association and permeabilization due to an inability to stabilize BAXα9·membrane interactions. This work identifies a mechanistic contribution of mitochondrial size in dictating BAX activation, MOMP, and apoptosis.
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“Finally, it is becoming increasingly evident that mitochondrial size and shape [139–141] as well as lipid composition [142, 143] can influence the likelihood of mitochondria to undergo irreversible MOMP.”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [140]
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Proapoptotic BAX and BAK: A Requisite Gateway to Mitochondrial Dysfunction and Death
Wei, M. C., Zong, W.-X., Cheng, E. H.-Y., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B., & Korsmeyer, S. J. (2001) · Science · doi:10.1126/science.1059108 · Cited by 3,988
Mitochondrial Fission, Fusion, and Stress
Youle, R. J., & van der Bliek, A. M. (2012) · Science · doi:10.1126/science.1219855 · Cited by 3,674
An inhibitor of Bcl-2 family proteins induces regression of solid tumours
Oltersdorf, T., Elmore, S. W., Shoemaker, A. R., Armstrong, R. C., Augeri, D. J., Belli, B., Bruncko, M., Deckwerth, T. L., Dinges, J., Hajduk, P. J., et al. (2005) · Nature · doi:10.1038/nature03579 · Cited by 3,407
Regulated Translation Initiation Controls Stress-Induced Gene Expression in Mammalian Cells
Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R. C., Schapira, M., & Ron, D. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00108-8 · Cited by 3,344
Chen, H., Detmer, S. A., Ewald, A. J., Griffin, E. E., Fraser, S. E., & Chan, D. C. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200211046 · Cited by 2,601
Mitofusin 2 tethers endoplasmic reticulum to mitochondria
de Brito, O. M., & Scorrano, L. (2008) · Nature · doi:10.1038/nature07534 · Cited by 2,442
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Bid, Bax, and Lipids Cooperate to Form Supramolecular Openings in the Outer Mitochondrial Membrane
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Self-citationER Stress Triggers Apoptosis by Activating BH3-Only Protein Bim
Puthalakath, H., O’Reilly, L. A., Gunn, P., Lee, L., Kelly, P. N., Huntington, N. D., Hughes, P., Michalak, E. M., McKimm‐Breschkin, J. L., Motoyama, N., et al. (2007) · Cell · doi:10.1016/j.cell.2007.04.027 · Cited by 1,493
Chipuk, J. E., Moldoveanu, T., Llambi, F., Parsons, M. J., & Green, D. R. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.025 · Cited by 1,476
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Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680
Self-citationTargeting apoptosis in cancer therapy
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Vyas, S., Zaganjor, E., & Haigis, M. C. (2016) · Cell · doi:10.1016/j.cell.2016.07.002 · Cited by 1,735
Bax, Bak and beyond — mitochondrial performance in apoptosis
Peña‐Blanco, A., & García‐Sáez, A. J. (2017) · FEBS Journal · doi:10.1111/febs.14186 · Cited by 987
Pernas, L. F., & Scorrano, L. (2015) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021115-105011 · Cited by 845
Metadata
- Authors
- Renault, T. T., Floros, K. V., Elkholi, R., Corrigan, K.-A., Kushnareva, Y., Wieder, S. Y., Lindtner, C., Serasinghe, M. N., Asciolla, J. J., Buettner, C., Newmeyer, D. D., & Chipuk, J. E.
- Affiliations
- Tisch Cancer Institute (US)
- Icahn School of Medicine at Mount Sinai (US)
- La Jolla Institute for Immunology (US)
- Mount Sinai Hospital (US)
- Corresponding author
- Chipuk, Jerry E.
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2015-01
- Volume
- 57
- Issue
- 1
- Pages
- 69-82
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC4289414
- OpenAlex
- W2049807952
- Cited by
- 217
- References
- 51
- Citations by year
- 2026: 13 · 2025: 11 · 2024: 13 · 2023: 14 · 2022: 20 · 2021: 23 · 2020: 22 · 2019: 21 · 2018: 18 · 2017: 23 · 2016: 24 · 2015: 15
- FWCI
- 8.48
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- Funders
- National Institutes of Health (5r01aa023416-04)
- National Institute on Alcohol Abuse and Alcoholism (NIH P20AA017067, P20AA017067, R01-AA-023416)
- National Cancer Institute (CA157740, R01CA157740)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK083568, R03DK082724, K08DK074873, DK-082724)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Keywords
- mitochondrial morphology, mitochondrial size, Bax, mitochondrial outer membrane permeabilization, apoptosis, Bcl-2 family proteins, Mfn1, mitochondrial fusion, mitochondrial outer membrane
- MeSH terms
- Bcl-2-Like Protein 11, Animals, Gene Expression Regulation, Membrane Proteins, Mitochondria, Liver, Permeability, Proto-Oncogene Proteins, Signal Transduction, Apoptosis, GTP Phosphohydrolases, bcl-2 Homologous Antagonist-Killer Protein, Apoptosis Regulatory Proteins, bcl-2-Associated X Protein, Mitochondrial Membranes, Mice, Membrane Potential, Mitochondrial, Organelle Shape, Unilamellar Liposomes, Mitochondrial Dynamics
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