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Crosstalk between apoptosis.; necrosis and autophagy
Open accessAbstract
Apoptosis and necrosis are the two major modes of cell death, the molecular mechanisms of which have been extensively studied. Although initially thought to constitute mutually exclusive cellular states, recent findings reveal cellular contexts that require a balanced interplay between these two modes of cellular demise. Several death initiator and effector molecules, signaling pathways and subcellular sites have been identified as key mediators in both processes, either by constituting common modules or alternatively by functioning as a switch allowing cells to decide which route to take, depending on the specific situation. Importantly, autophagy, which is a predominantly cytoprotective process, has been linked to both types of cell death, serving either a pro-survival or pro-death function. Here we review the recent literature that highlights the intricate interplay between apoptosis, necrosis and autophagy, focusing on the relevance and impact of this crosstalk in normal development and in pathology. This article is part of a Special Section entitled: Cell Death Pathways.
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“While autophagy is implicated in several paradigms of life extension and is generally considered an antiaging mechanism, autophagy is also a well-defined mechanism of cell death, autophagy-dependent cell death, ADCD [153,154,155].”
From The mitochondrial permeability transition: Nexus of aging, disease and longevity (2021) · cites this paper as [153]
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“A regulated necrosis process mediated by the RIP kinase family members can be induced, in some cell lines, under certain circumstances, such as the use of caspase inhibitors [16], downregulation of cIAPs [17], and acidic extracellular pH [18].”
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“Autophagy induction in response to stressful stimuli is involved in adaptation of the cells to various stressful conditions, such as shortage of nutrients and oxygen [13], or it can also cause dysregulated cell death [14].”
BackgroundAdipose tissue glycogen accumulation is associated with obesity-linked inflammation in humans
Ceperuelo‐Mallafré, V., Ejarque, M., Serena, C., Durán, X., Montori-Grau, M., Rodriguez, M. A., Yanes, Ó., Núñez‐Roa, C., Roche, K., Puthanveetil, P., et al. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.10.001 · Cited by 71
“Generally activated by nutrient deprivation, autophagy flux in glycogenloaded adipocytes correlates with a negative regulation of the nutrientsensing kinase mTOR, which has been previously associated with autophagy activation [57], but not with ER stress or NFKb signaling, as detected in other cellular systems [58,59].”
BackgroundCell Death Pathways and Phthalocyanine as an Efficient Agent for Photodynamic Cancer Therapy
Mfouo-Tynga, I. S., & Abrahamse, H. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160510228 · Cited by 70
“Unlike apoptosis, autophagy is not well understood, but has also been reported to be involved in either cell survival or death function [19].”
BackgroundLu, X., Liu, T., Chen, K., Xia, Y., Dai, W., Xu, S., Xu, L., Wang, F., Wu, L., Li, J., et al. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.04.016 · Cited by 70
Toxicity assessment of the herbicide acetochlor in the human liver carcinoma (HepG2) cell line
Huang, T., Huang, Y., Huang, Y. H., Yang, Y., Zhao, Y. H., & Martyniuk, C. J. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.125345 · Cited by 69
Blue Light Action on Mitochondria Leads to Cell Death by Necroptosis
del Olmo‐Aguado, S., Núñez‐Álvarez, C., & Osborne, N. N. (2016) · Neurochemical Research · doi:10.1007/s11064-016-1946-5 · Cited by 68
Vazirpanah, N., Ottria, A., van der Linden, M., Wichers, C. G. K., Schuiveling, M., van Lochem, E. G., Phipps‐Green, A. J., Merriman, T. R., Zimmermann, M., Jansen, M., et al. (2019) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2018-214656 · Cited by 70
“27 It is established that necrosis leads to NACHT, LRR and PYD domains–containing protein 3 (NLRP3) activation and increased IL-1 β production, an important feature of gout and also observed in our study.”
Zhao, M., Gu, L., Li, Y., Chen, S., You, J., Fan, L., Wang, Y., & Zhao, L. (2019) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2019.115171 · Cited by 68
Mi, X.-J., Choi, H. S., Perumalsamy, H., Rajeshkumar, S., Thangavelu, L. P., Balusamy, S. R., & Kim, Y.-J. (2022) · Phytomedicine · doi:10.1016/j.phymed.2022.154014 · Cited by 69
Gao, M., Zhu, H., Guo, J., Lei, Y., Sun, W., & Lin, H. (2022) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2022.09.062 · Cited by 69
Mitochondria: key players in the neurotoxic effects of amphetamines
Barbosa, D. J., Capela, J. P., Feio‐Azevedo, R., Gomes, A., Bastos, M. D. L., & Carvalho, F. D. (2015) · Archives of Toxicology · doi:10.1007/s00204-015-1478-9 · Cited by 70
“Upon an apoptosis trigger stimuli, AIF undergoes proteolysis by calpains or cathepsins into a soluble form (tAIF), and then translocates to the nuclei, via its carboxyl-terminal domain nuclear localization sequence, leading to chromatin condensation and largescale DNA degradation, in a caspase-independent manner (Kran…”
BackgroundInfluentialEvaluation on the antiviral activity of arctigenin against spring viraemia of carp virus
Shen, Y.-F., Liu, L., Chen, W., Hu, Y., Zhu, B., & Wang, G. (2017) · Aquaculture · doi:10.1016/j.aquaculture.2017.09.001 · Cited by 69
“Apoptosis plays an important role in normal development and regulation of various physiological processes (Nikoletopoulou et al., 2013) .”
Martínez, L. C., Plata‐Rueda, A., Gonçalves, W. G., Freire, A. F. P. A., Zanuncio, J. C., Bozdoğan, H., & Serrão, J. É. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.09.124 · Cited by 69
Luteolin Induces Apoptosis and Autophagy in HCT116 Colon Cancer Cells via p53-Dependent Pathway
Yoo, H. S., Won, S. B., & Kwon, Y. H. (2021) · Nutrition and Cancer · doi:10.1080/01635581.2021.1903947 · Cited by 68
“The crosstalk between autophagy and apoptosis, the two major mechanisms of cell death have been shown to regulate cancer development in multiple ways (Nikoletopoulou et al. 2013).”
BackgroundPengyue, Z., Guo, T., He, H., Liqiang, Y., & Yihao, D. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.03.039 · Cited by 68
Johnson, R., Shabalala, S. C., Louw, J., Kappo, A. P., & Muller, C. J. F. (2017) · Molecules · doi:10.3390/molecules22101589 · Cited by 69
“Under certain conditions, autophagy constitutes an adaptive response in order to avoid cell death and through this subdues apoptosis [4,6].”
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“The inter-relation between autophagy and apoptosis is complex and involves both harmful and beneficial effects in different conditions (Leber and Andrews, 2010; Nikoletopoulou et al., 2013).”
Yue, Z., Guan, X., Chao, R., Huang, C., Li, D., Yang, P., Liu, S., Hasegawa, T., Guo, J., & Li, M. (2019) · Molecules · doi:10.3390/molecules24142665 · Cited by 67
“Several studies have suggested that apoptosis and autophagy are interrelated and affect each other [18,19].”
BackgroundRole of necroptosis in traumatic brain and spinal cord injuries
Hu, X., Xu, Y. M., Zhang, H., Li, Y., Wang, X., Xu, C., Ni, W., & Zhou, K. (2021) · Journal of Advanced Research · doi:10.1016/j.jare.2021.12.002 · Cited by 68
“Moreover, zVAD (a short peptide that acts as a general caspase inhibitor) can robustly induce necroptosis and prevent autophagy through its inhibitory effect on lysosomal cathepsins, underscoring the prosurvival function of autophagy against necroptosis [88,89].”
BackgroundMetformin protects primary rat hepatocytes against oxidative stress‐induced apoptosis
de la Rosa, L. C., Vrenken, T. E., Buist‐Homan, M., Faber, K. N., & Moshage, H. J. (2015) · Pharmacology Research & Perspectives · doi:10.1002/prp2.125 · Cited by 66
“Apoptosis, or programmed cell death (Nieminen 2003; Nikoletopoulou et al. 2013; Stevens et .al. 2013), is an active process characterized by cell shrinkage, chromatin condensation, and activation of caspases (Riedl and Shi 2004; Shi 2002), and formation of apoptotic bodies.”
BackgroundInfluentialBlue light emitting diode induces apoptosis in lymphoid cells by stimulating autophagy
Oh, P., Hwang, H., Jeong, H.-S., Kwon, J., Kim, H., Kim, M., Lim, S. T., Sohn, M., & Jeong, H.-J. (2015) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2015.11.004 · Cited by 68
Kaboli, P. J., Leong, M. P.-Y., Ismail, P., & Ling, K. (2018) · Pharmacological Reports · doi:10.1016/j.pharep.2018.07.005 · Cited by 67
Tan, X., Zhu, H., Tao, Q., Guo, L., Jiang, T., Xu, L., Yang, R., Wei, X., Wu, J., Li, X., et al. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00556 · Cited by 67
“Studies demonstrate that HMGB1 plays an important role in the interaction of autophagy and apoptosis/necrosis in various disorders including AKI (Nikoletopoulou et al., 2013; Kim et al., 2014; Chen et al., 2016).”
BackgroundWang, X., Feng, S., Wang, Y., Yuan, Y., Li, Z., Chen, N., Wang, Z., & Zhang, Y. (2021) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-021-01039-w · Cited by 66
SARS-CoV-2 Accessory Protein ORF7b Mediates Tumor Necrosis Factor-α-Induced Apoptosis in Cells
Yang, R., Zhao, Q., Rao, J., Zeng, F., Yuan, S., Ji, M., Sun, X., Li, J., Yang, J., Cui, J., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.654709 · Cited by 66
Guo, C., Li, J., Chen, K., Li, S., Feng, J., Liu, T., Wang, F., Zhang, R., Xu, S., Zhou, Y., et al. (2016) · Drug Design Development and Therapy · doi:10.2147/dddt.s98740 · Cited by 66
“Beclin-1 usually promotes the occurrence of autophagy through an interaction with PI3K, which induces the conversion of LC3-I to LC3-II.(19,57) Following fucoidan treatment, the inhibition of TGF-β1 hindered the formation of autophagosomes, which degraded organelles to protect liver cells via the downregulated TGF-β1/…”
Ions, the Movement of Water and the Apoptotic Volume Decrease
Bortner, C. D., & Cidlowski, J. A. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.611211 · Cited by 65
Sárközy, M., Varga, Z., Gáspár, R., Szűcs, G., Kovács, M. G., Kovács, Z. Z. A., László, A., Kahán, Z., & Csont, T. (2021) · Clinical Research in Cardiology · doi:10.1007/s00392-021-01809-y · Cited by 72
Multiple Myeloma Tumor Cells are Selectively Killed by Pharmacologically-dosed Ascorbic Acid
Xia, J., Xu, H., Zhang, X., Allamargot, C., Coleman, K. L., Nessler, R., Frech, I., Tricot, G., & Zhan, F. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.02.011 · Cited by 63
“We focused our attention on apoptosis-inducing factor 1 (AIF1), because AIF1 induces cell death in caspase-dependent and caspase-independent manners (Nikoletopoulou et al., 2013).”
BackgroundBufalo, D. D., Desideri, M., Luca, T. D., Martile, M. D., Gabellini, C., Monica, V., Busso, S., Eramo, A., Maria, R. D., Milella, M., et al. (2014) · Molecular Cancer · doi:10.1186/1476-4598-13-230 · Cited by 63
“Since autophagy has been implicated in both inhibition and promotion of cell survival [46,47], we investigated whether a functional relationship exists between apoptosis and autophagy, by silencing the expression of proteins acting at the early steps of autophagy, such as Beclin1 or ATG7, as a genetic approach to inhi…”
BackgroundLiu, H., Sun, X., Gong, X., & Wang, G. (2019) · Journal of Cellular Biochemistry · doi:10.1002/jcb.28705 · Cited by 64
“Several signaling pathways that are induced by stresses of growth factor deprivation, limitation of nutrients and oxidative stress participate in the regulation of both autophagy and apoptosis.(38) mTOR, a serine/threonine kinase, can promote cell growth and inhibit autophagy via various pathways.”
Background
Metadata
- Authors
- Nikoletopoulou, V., Markaki, M., Palikaras, K., & Tavernarakis, N.
- Affiliations
- Foundation for Research and Technology Hellas (GR)
- Corresponding author
- Tavernarakis, Nektarios
- Venue
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 1833
- Issue
- 12
- Pages
- 3448-3459
- ISSN
- 0167-4889 (ISSN-L)
- OpenAlex
- W2059738518
- Cited by
- 1,366
- References
- 150
- Citations by year
- 2026: 43 · 2025: 58 · 2024: 80 · 2023: 91 · 2022: 113 · 2021: 147 · 2020: 133 · 2019: 146 · 2018: 136 · 2017: 141 · 2016: 122 · 2015: 107 · 2014: 43 · 2013: 5
- FWCI
- 8.50
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- European Research Council
- Ministry of National Education and Religious Affairs
- European Molecular Biology Organization
- Seventh Framework Programme
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Social Sciences › Anthropology › Death, Funerary Practices, and Mourning
- Keywords
- apoptosis, necrosis, autophagy, cell death crosstalk, cell death pathways, cell fate determination, development (biology), disease pathology
- MeSH terms
- Autophagy, Humans, Models, Biological, Necrosis, Signal Transduction, Apoptosis
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