Cited by 1,366Cell death mechanisms and regulationAutophagy in Disease and TherapyDeath, Funerary Practices, and Mourning

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Crosstalk between apoptosis.; necrosis and autophagy

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Nikoletopoulou, Vassiliki, Markaki, Maria, Palikaras, Konstantinos, Tavernarakis, Nektarios·2013·Biochimica et Biophysica Acta (BBA) - Molecular Cell Research

DOI 10.1016/j.bbamcr.2013.06.001

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Abstract

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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1 retracted

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Santos, E. W., Khatoon, S., Mise, A. D., Zheng, Y., & Wang, Y.-X. (2023) · Biomedicines · doi:10.3390/biomedicines12010053 · Cited by 15
“The balance between these two processes is particularly important, as they control and regulate their formation and distribution, thereby mediating normal cellular functions and disease processes [1,2].”
Background
Decreasing mitochondrial fission ameliorates HIF-1α-dependent pathological retinal angiogenesis
Huang, S.-Q., Cao, K., Wang, C., Chen, P.-L., Chen, Y., Zhang, Y., Yu, S., Bai, Z.-X., Guo, S., Liao, M., et al. (2024) · Acta Pharmacologica Sinica · doi:10.1038/s41401-024-01262-3 · Cited by 20
“Mitochondria are the primary power source for cells and play a crucial role in energy production, signal transduction, cellular redox homeostasis, and other physiological processes [27 – 29].”
The Necrosis-Avid Small Molecule HQ4-DTPA as a Multimodal Imaging Agent for Monitoring Radiation Therapy-Induced Tumor Cell Death
Stammes, M. A., Maeda, A., Bu, J., Scollard, D. A., Kulbatski, I., Medeiros, P. J., Sinisi, R., Goun, E. A., Snoeks, T. J. A., van Beek, E. R., et al. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00221 · Cited by 15
“Second, necrosis is primarily induced by external factors that cause physiochemical damage compared to apoptosis that can occur in any tissues during normal development and cell turnover (10, 11), making necrosis-based imaging method suitable to distinguish cell death induced by antitumor therapies.”
Background
Activation of endoplasmic reticulum stress and the extrinsic apoptotic pathway in human lung cancer cells by the new synthetic flavonoid, LZ-205
Zhang, Y., Xu, X., Li, W., Miao, H., Huang, S., Zhou, Y., Sun, Y., Li, Z., Guo, Q., & Zhao, L. (2016) · Oncotarget · doi:10.18632/oncotarget.13535 · Cited by 15
“Apoptosis is well-known as a process of regulated cell death, which plays a major role not only in cell damage or stress, but also in normal development and morphogenesis [2].”
Genetic Polymorphisms of Tumor Necrosis Factor Alpha and Susceptibility to Dengue Virus Infection in a Mexican Population
Sánchez-Leyva, M., Sánchez‐Zazueta, J. G., Osuna‐Ramos, J. F., Rendón‐Aguilar, H., Félix-Espinoza, R., Becerra‐Loaiza, D. S., Sánchez-García, D. C., Romero-Quintana, J. G., Castillo-Ureta, H., Velarde-Rodríguez, I., et al. (2017) · Viral Immunology · doi:10.1089/vim.2017.0029 · Cited by 15
“Tumor necrosis factor alpha (TNF-a ) is a key proin-ﬂammatory cytokine that participates in many processes, such as lipid metabolism (13), host defense (28), coagulation (14), regulation of apoptosis (36), endothelial function (39), and transcriptional induction of some cytokines (42).”
StandardizedOlea europaeaL. leaf extract exhibits protective activity in carbon tetrachloride-induced acute liver injury in rats: the insight into potential mechanisms
Vidičević, S., Tasić, J., Stanojević, Ž., Isaković, A., Mitić, D. M., Ristić, D., & Dekanski, D. (2019) · Archives of Physiology and Biochemistry · doi:10.1080/13813455.2018.1550095 · Cited by 15
Targeting inhibitors of apoptosis in oral squamous cell carcinoma in vitro
Scheurer, M., Seher, A., Steinacker, V. C., Linz, C., Hartmann, S., Kübler, A. C., Müller-Richter, U. D. A., & Brands, R. C. (2019) · Journal of Cranio-Maxillofacial Surgery · doi:10.1016/j.jcms.2019.07.022 · Cited by 15
Physiological Functions of Mitochondrial Reactive Oxygen Species
Choi, T. G., & Kim, S. S. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.88386 · Cited by 22
“[15] Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N.”
Background
RETRACTED ARTICLE: Downregulation of miR-483-5p decreases hypoxia-induced injury in human cardiomyocytes by targeting MAPK3
Hao, Y., Yuan, H., & Yu, H. (2020) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-020-00213-0 · Cited by 15
“To the best of our knowledge, myocardial apoptosis has been extensively researched in terms of its effect on cardiomyocyte death and survival [18, 19].”
Background
Retracted
Photoreceptor Degeneration in Pro23His Transgenic Rats (Line 3) Involves Autophagic and Necroptotic Mechanisms
Kakavand, K., Jobling, A. I., Greferath, U., Vessey, K. A., de Iongh, R. U., & Fletcher, E. L. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.581579 · Cited by 15
“The well-known tumor suppressor, p53 (TP53), has been associated with not only caspase-dependent and caspase-independent pathways of apoptosis, but also with non-apoptotic mechanisms of cell death, including programmed necrosis (necroptosis) (Nikoletopoulou et al., 2013; Ranjan and Iwakuma, 2016).”
Background
Nomad Jellyfish Rhopilema nomadica Venom Induces Apoptotic Cell Death and Cell Cycle Arrest in Human Hepatocellular Carcinoma HepG2 Cells
Tawfik, M. M., Eissa, N., Althobaiti, F., Fayad, E., & Almaaty, A. H. A. (2021) · Molecules · doi:10.3390/molecules26175185 · Cited by 15
“Apoptosis is a significant mode of programmed cell death characterized by distinct hallmarks and controlled by essential extrinsic and intrinsic regulatory proteins [48,49].”
Background
Acrylamide impairs the developmental potential of germinal vesicle oocytes by inducing mitochondrial dysfunction and autophagy/apoptosis in mice
Gao, J., Yang, J., Zhu, L., Xu, C., & Nie, L. (2021) · Human & Experimental Toxicology · doi:10.1177/09603271211045956 · Cited by 15
“According to previous studies, autophagy and apoptosis are two important cellular processes for determining cell fate.(52) ROS accumulation can induce oxidative damage, which is accompanied by apoptotic and autophagic cell death.”
Pharmacological Activities of Ginkgolic Acids in Relation to Autophagy
Ding, Y. F., Ding, Z., Xu, J., Li, Y., & Chen, M. (2022) · Pharmaceuticals · doi:10.3390/ph15121469 · Cited by 15
Rheb may complex with RASSF1A to coordinate Hippo and TOR signaling
Nelson, N. C., & Clark, G. J. (2016) · Oncotarget · doi:10.18632/oncotarget.8447 · Cited by 15
“This should not be surprising, as there are clearly links between autophagy and apoptotic death [28].”
Background
Palliative Care for Salivary Gland Dysfunction Highlights the Need for Regenerative Therapies: A Review on Radiation and Salivary Gland Stem Cells
Chibly, A. M. (2014) · Journal of Palliative Care & Medicine · doi:10.4172/2165-7386.1000180 · Cited by 16
“It is likely that all three pathways interact to determine the overall response of the salivary epithelium to radiation damage [21,23].”
Background
ERK-mediated autophagy promotes inactivated Sendai virus (HVJ-E)-induced apoptosis in HeLa cells in an Atg3-dependent manner
Wang, T., Yu, N., Qian, M., Feng, J., Cao, S., Yin, J., & Zhang, Q. (2018) · Cancer Cell International · doi:10.1186/s12935-018-0692-y · Cited by 15
Sodium (±)‐5‐bromo‐2‐(α‐hydroxypentyl) benzoate ameliorates pressure overload‐induced cardiac hypertrophy and dysfunction through inhibiting autophagy
Wang, B., Shen, D., Tang, J., Li, J., Xiao, Y., Chen, X., Cao, C. Q., Han, D., Gao, E., Zhao, W., et al. (2019) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.14468 · Cited by 15
Regulatory effect of inflammatory mediators in spinal cord injury
Zeng, W.-C., & Zeng, F.-J. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1619337 · Cited by 14
“Il-1 b binds to the IL-1 receptor (IL-1R) on the surface of nerve cells, triggering a conformational change of the receptor and further recruitment of myeloid differentiation factor 88 (MyD88) (151).”
Effect of RFRP-3, the mammalian ortholog of GnIH, on apoptosis and autophagy in porcine ovarian granulosa cells via the p38MAPK pathway
Zhang, X., Li, M., Huang, M., Peng, H. F., Song, X., Chen, L., Hu, W., Xu, W., Luo, R., Han, D., et al. (2021) · Theriogenology · doi:10.1016/j.theriogenology.2021.12.024 · Cited by 14
2,3,4',5‑Tetrahydroxystilbene‑2‑O‑β‑D‑glucoside ameliorates gentamicin‑induced ototoxicity by modulating autophagy via Sesn2/AMPK/mTOR signaling
Wen, Y., Lin, H.-Y., Lin, J.-N., Tseng, G., Hwang, C., Lin, C.-C., Hsu, C., & Wu, H. (2022) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2022.5127 · Cited by 14
The Impact of Chrysin on The Folliculogenesis and Ovarian Apoptosis in Ischemia-Reperfusion Injury in The Rat Model.
Mohammadi, Z., Hosseinianvari, S., Ghazalian, N., Fani, M., Mahmoudian, A., Brazvan, B., Shokoohi, M., Abtahi-Evari, S.-H., & Moghimian, M. (2022) · PubMed Central · doi:10.22074/ijfs.2021.540364.1200 · Cited by 14
Galectin-9 in Gastroenterological Cancer
Morishita, A., Oura, K., Tadokoro, T., Shi, T., Fujita, K., Tani, J., Atsukawa, M., & Masaki, T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076174 · Cited by 14
“Apoptosis is a proposed type of programmed cell death [1] characterized by morphological changes occurring in response to extrinsic and intrinsic stress [21].”
Background
The Potential of Targeting Autophagy-Related Non-coding RNAs in the Treatment of Alzheimer’s and Parkinson’s Diseases
Taheri, A. T., Golshadi, Z., Zare, H., Alinaghipour, A., Faghihi, Z., Dadgostar, E., Tamtaji, Z., Aschner, M., Mirzaei, H., Tamtaji, O. R., et al. (2024) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-024-01461-w · Cited by 15
“…diseases is characterized by the accumulation of proteins (Menzies et al. 2015; Ravikumar et al. 2002), with autophagy contributing to disease progression (Menzies et al. 2015) and neuronal loss (Hara et al. 2006; Komatsu et al. 2006; Levine and Kroemer 2008; Nikoletopoulou et al. 2013).”
Background
Multimodal Imaging-Assisted Intravascular Theranostic Photoactivation on Atherosclerotic Plaque
Kim, J., Song, J., Kim, Y. H., Kim, H. J., Kim, R. H., Park, Y., Nam, H. S., Kang, D., Yoo, H., Park, K., et al. (2024) · Circulation Research · doi:10.1161/circresaha.123.323970 · Cited by 13
“Collectively, these data demonstrate that the intravascular LAM-Ce6 pho-toactivation possibly activates autophagic flux early and induces apoptosis by complex cross talk, 37 all of which were successfully terminated at 28 days post-treatment.”
Recent plant-synthesized gold nanoparticle advancements for gastric cancer therapy
Rojas-Cessa, M. A. (2024) · Nano TransMed · doi:10.1016/j.ntm.2024.100050 · Cited by 14
Small chaperons and autophagy protected neurons from necrotic cell death
Ye, L., Liu, K., Hou, L., Ding, L., Li, Y., & Liu, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-05995-6 · Cited by 14
Loss of Peter Pan (PPAN) Affects Mitochondrial Homeostasis and Autophagic Flux
Dannheisig, D. P., Beck, E., Calzia, E., Walther, P., Behrends, C., & Pfister, A. S. (2019) · Cells · doi:10.3390/cells8080894 · Cited by 14
“How the transition from autophagy to apoptosis is precisely regulated is still not fully understood [28,87].”
Background
ERas Enhances Resistance to Cisplatin-Induced Apoptosis by Suppressing Autophagy in Gastric Cancer Cell
Tian, H., Wang, W., Meng, X., Wang, M., Tan, J., Jia, W., Li, P., Li, J., & Zhou, Q. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00375 · Cited by 14
“(D) Cell apoptotic ratio of ERas knockdown and control BGC-823 cell was determined by flow cytometry (FACS) with Annexin V – FITC and PI double staining, quantification of apoptotic ratio on right panel (cisplatin 100 ng/ml for 12 h, *p < 0.05). tumor development in GC cells (Qian and Yang, 2016).”
MethodInfluential
APOPTOTIC EFFECTS OF BETA-CAROTENE, ALPHA-TOCOPHEROL AND ASCORBIC ACID ON PC-3 PROSTATE CANCER CELLS
Ayna, A. (2020) · Hacettepe Journal of Biology and Chemistry · doi:10.15671/hjbc.519212 · Cited by 14
Combined Extracts of Epimedii Folium and Ligustri Lucidi Fructus with Budesonide Attenuate Airway Remodeling in the Asthmatic Rats by Regulating Apoptosis and Autophagy
Ma, Z., Tang, X., Gao, Y., Wang, H., Yu, P., & Liu, R. (2020) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2020/2319409 · Cited by 14
“In addition, this interaction plays a key role in airway remodeling through maintaining cellular homeostasis and mediating cell death process [27], indicating that the dysregulated apoptosis and autophagy are involved in asthmatic pathogenesis [28, 29].”
Background
Differential Cytotoxicity of Rooibos and Green Tea Extracts against Primary Rat Hepatocytes and Human Liver and Colon Cancer Cells – Causal Role of Major Flavonoids
Samodien, S., de Kock, M., Joubert, E., Swanevelder, S. A., & Gelderblom, W. C. A. (2020) · Nutrition and Cancer · doi:10.1080/01635581.2020.1820054 · Cited by 14
Breast Cancer: a Global Concern, Diagnostic and Therapeutic Perspectives, Mechanistic Targets in Drug Development
Chaudhry, G.-E.-S., Jan, R., Akim, A. M., Zafar, M. N., Sung, Y. Y., & Muhammad, T. S. T. (2020) · Advanced Pharmaceutical Bulletin · doi:10.34172/apb.2021.068 · Cited by 14
Arsenic-induced autophagy regulates apoptosis in AML-12 cells
Yuan, M., Sun, Z., Manthari, R. K., Zhao, Y., Guo, Q., Yang, K., & Wang, J. (2020) · Toxicology in Vitro · doi:10.1016/j.tiv.2020.105074 · Cited by 14
Green tea and its active compound epigallocathechin-3-gallate (EGCG) inhibit neuronal apoptosis in a middle cerebral artery occlusion (MCAO) model
Machin, A., Susilo, I., & Purwanto, D. A. (2021) · Journal of Basic and Clinical Physiology and Pharmacology · doi:10.1515/jbcpp-2020-0454 · Cited by 14
An overview on the role of microalgal metabolites and pigments in apoptosis induction against copious diseases
Razack, S. A., Surendhiran, D., Kozani, P. S., Kozani, P. S., Hamidi, M., Cabrera‐Barjas, G., & Delattre, C. (2021) · Algal Research · doi:10.1016/j.algal.2021.102556 · Cited by 14
The Construction and Analysis of Immune Infiltration and Competing Endogenous RNA Network in Acute Ischemic Stroke
Ma, Z., Liu, C., Zhang, L., Xiang, N., Zhang, Y., & Chu, L. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.806200 · Cited by 15
“The C-fos level can then gradually return to normal levels within 24 h (Karch et al., 2013; Nikoletopoulou et al., 2013).”
Background
The Effect of Ghrelin on Apoptosis, Necroptosis and Autophagy Programmed Cell Death Pathways in the Hippocampal Neurons of Amyloid-β 1–42-Induced Rat Model of Alzheimer’s Disease
Naseri, F., Sirati‐Sabet, M., Sarlaki, F., Keimasi, M., Mokarram, P., Siri, M., Ghasemi, R., Shahsavari, Z., & Goshadrou, F. (2022) · International Journal of Peptide Research and Therapeutics · doi:10.1007/s10989-022-10457-3 · Cited by 14
“Beclin-1 inhibits caspase-8 activation and subsequently blocks Bid to tBid cleavage, which triggers the reduction of mitochondrial membrane potential (Nikoletopoulou et al. 2013).”
Background
Lysosome-targeted cyclometalated iridium(III) complexes: JMJD inhibition, dual induction of apoptosis, and autophagy
Lu, J., Ma, X.-R., Xie, K. M., Chen, M., Huang, B., Li, R., & Ye, R. (2022) · Metallomics · doi:10.1093/mtomcs/mfac068 · Cited by 14
Shining light on cell death processes – a novel biosensor for necroptosis, a newly described cell death program
Sipieter, F., Ladik, M., Vandenabeele, P., & Riquet, F. B. (2014) · Biotechnology Journal · doi:10.1002/biot.201300200 · Cited by 14
Mechanism and Physiological Significance of Growth Factor-Related Autophagy
Li, T. Y., Lin, S., & Lin, S. (2013) · Physiology · doi:10.1152/physiol.00023.2013 · Cited by 16
High Inorganic Phosphate Intake Promotes Tumorigenesis at Early Stages in a Mouse Model of Lung Cancer
Lee, S., Kim, J., Hong, S., Lee, A.-Y., Park, E., Seo, H. W., Chae, C., Doble, P., Bishop, D., & Cho, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135582 · Cited by 13
“Apoptosis is a physiological process that removes damaged cellular components and thereby maintains tissue homeostasis [45].”
Background
MG132 plus apoptosis antigen-1 (APO-1) antibody cooperate to restore p53 activity inducing autophagy and p53-dependent apoptosis in HPV16 E6-expressing keratinocytes
Lagunas-Martínez, A., Garcı́a-Villa, E., Arellano-Gaytán, M., Contreras-Ochoa, C. O., Dimas-González, J., López‐Arellano, M. E., Madrid‐Marina, V., & Gariglio, P. (2016) · APOPTOSIS · doi:10.1007/s10495-016-1299-1 · Cited by 14
“logically and genetically [8] and contributes to the elimina-”
Background

Authors: Nikoletopoulou, V., Markaki, M., Palikaras, K., & Tavernarakis, N.
Affiliations: Foundation for Research and Technology Hellas (GR)
Corresponding author: Tavernarakis, Nektarios
ORCID: Nikoletopoulou, Vassiliki
Markaki, Maria
Palikaras, Konstantinos
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)
DOI: 10.1016/j.bbamcr.2013.06.001
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
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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Crosstalk between apoptosis.; necrosis and autophagy

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