Cell survival, DNA damage, and oncogenic transformation after a transient and reversible apoptotic response
Open accessAbstract
Apoptosis serves as a protective mechanism by eliminating damaged cells through programmed cell death. After apoptotic cells pass critical checkpoints, including mitochondrial fragmentation, executioner caspase activation, and DNA damage, it is assumed that cell death inevitably follows. However, this assumption has not been tested directly. Here we report an unexpected reversal of late-stage apoptosis in primary liver and heart cells, macrophages, NIH 3T3 fibroblasts, cervical cancer HeLa cells, and brain cells. After exposure to an inducer of apoptosis, cells exhibited multiple morphological and biochemical hallmarks of late-stage apoptosis, including mitochondrial fragmentation, caspase-3 activation, and DNA damage. Surprisingly, the vast majority of dying cells arrested the apoptotic process and recovered when the inducer was washed away. Of importance, some cells acquired permanent genetic changes and underwent oncogenic transformation at a higher frequency than controls. Global gene expression analysis identified a molecular signature of the reversal process. We propose that reversal of apoptosis is an unanticipated mechanism to rescue cells from crisis and propose to name this mechanism “anastasis” (Greek for “rising to life”). Whereas carcinogenesis represents a harmful side effect, potential benefits of anastasis could include preservation of cells that are difficult to replace and stress-induced genetic diversity.
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At least some cells exposed to transient apoptotic stimuli appear to survive MOMP affecting a limited number of mitochondria and the partial activation of executioner caspases by a process called anastasis.
“Finally, at least some cells exposed to transient apoptotic stimuli appear to survive MOMP affecting a limited number of mitochondria and the partial activation of executioner caspases by a hitherto poorly characterized process called anastasis (most likely constituting a robust adaptative response upstream of the boundary between cellular life and death) [226–228].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [228]
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- Authors
- Tang, H. L., Tang, H. M., Mak, K. H., Hu, S., Wang, S. S., Wong, K. M., Wong, C. S. T., Wu, H. Y., Law, H. T., Liu, K., Talbot, C. C., Lau, W. K., Montell, D. J., & Fung, M. C.
- Affiliations
- Johns Hopkins University (US)
- Chinese University of Hong Kong (HK)
- School of Life Sciences, Chinese University of Hong Kong, Shatin, Hong Kong
- Corresponding author
- Tang, Ho Lam
- Montell, Denise J.
- Fung, Ming Chiu
- Venue
- Molecular Biology of the Cell
- Published
- 2012-06-15
- Volume
- 23
- Issue
- 12
- Pages
- 2240-2252
- ISSN
- 1059-1524 (ISSN-L)
- 1939-4586
- PMC
- PMC3374744
- OpenAlex
- W2166525237
- Cited by
- 293
- References
- 62
- Citations by year
- 2026: 18 · 2025: 22 · 2024: 31 · 2023: 25 · 2022: 26 · 2021: 16 · 2020: 24 · 2019: 28 · 2018: 27 · 2017: 20 · 2016: 14 · 2015: 20 · 2014: 13 · 2013: 3 · 2012: 5
- FWCI
- 5.28
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- Molecular Biology of the Cell (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Johns Hopkins University
- National Institute of General Medical Sciences (R01GM46425, R01GM046425)
- National Center for Research Resources (S10RR024550)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- anastasis, oncogenic transformation, DNA damage, caspase-3 activation, mitochondrial fragmentation, cell survival, carcinogenesis, hepatocytes, cardiomyocytes, macrophages, fibroblasts, HeLa cells, brain cells
- MeSH terms
- Ethanol, Animals, Animals, Newborn, Anti-Infective Agents, Local, Antineoplastic Agents, Cell Survival, Cell Transformation, Neoplastic, Cells, Cultured, DNA Damage, HeLa Cells, Humans, Liver, Mice, Inbred BALB C, Microscopy, Fluorescence, Rats, Sprague-Dawley, Apoptosis, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Myocytes, Cardiac, NIH 3T3 Cells, Depsipeptides, Mice, Rats, Transcriptome
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