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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“Caspase-8 down regulation is essential for caspase independent cell death because it cleaves the substrates necessary for autophagy and necroptosis [36].”
Anticancer activity of gomisin�J from Schisandra chinensis fruit
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“For a long time, eukaryotic cell death was divided into two types: programmed cell death (PCD) of apoptosis and accidental cell death of necrosis (1-5).”
Targeting autophagy in thyroid cancers
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Autophagy and Cathepsin D mediated apoptosis contributing to ovarian follicular atresia in the Nile tilapia
Sales, C. F., Melo, R. M. C., Pinheiro, A. P. B., Luz, R. K., Bazzoli, N., & Rizzo, E. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23245 · Cited by 26
“In fact, recent evidence demonstrates that the caspases may act on the cleavage of autophagic proteins such as Beclin1 and Atg3, inhibiting the pro‐autophagic activity of these proteins (Cassel et al., 2017; Luo & Rubinsztein, 2010; Oral et al., 2012; Zhu et al., 2010).”
Background
Doxorubicin selectively induces apoptosis through the inhibition of a novel isoform of Bcl‑2 in acute myeloid leukaemia MOLM‑13 cells with reduced Beclin 1 expression
Vu, M., Kassouf, N., Ofili, R., Lund, T., Bell, C., & Appiah, S. S. (2020) · International Journal of Oncology · doi:10.3892/ijo.2020.5052 · Cited by 24
Xylocarpus Moluccensis Induces Cytotoxicity in Human Hepatocellular Carcinoma HepG2 Cell Line via Activation of the Extrinsic Pathway
Chaudhry, G.-E.-S., Sohimi, N. K. A., Mohamad, H., Zafar, M. N., Ahmed, A., Sung, Y. Y., & Muhammad, T. S. T. (2021) · Asian Pacific Journal of Cancer Prevention · doi:10.31557/apjcp.2021.22.s1.17 · Cited by 25
“Biochemical alterations include DNA fragmentation and activation of cysteine aspartyl proteases, called caspases, which leads to the destruction of the cell (Nikoletopoulou et al., 2013).”
Background
Inhibition of autophagy by YC-1 promotes gefitinib induced apoptosis by targeting FOXO1 in gefitinib-resistant NSCLC cells
Hu, H., Zhang, X., Lin, L., Hu, M.-N., Hu, W.-Q., Zhang, J., Miao, X., Yang, W., & Mou, L. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.174346 · Cited by 25
Tanshinone IIA exerts autophagic cell death through down-regulation of β-catenin in renal cell carcinoma cells
Kim, N. Y., Jung, Y. Y., Yang, M. H., Chinnathambi, A., Govindasamy, C., Narula, A. S., Namjoshi, O. A., Blough, B. E., & Ahn, K. S. (2022) · Biochimie · doi:10.1016/j.biochi.2022.05.018 · Cited by 24
Resveratrol inhibits hepatic stellate cell activation by regulating autophagy and apoptosis through the SIRT1 and JNK signaling pathways
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Cytotoxicity induced by cypermethrin in Human Neuroblastoma Cell Line SH-SY5Y
Raszewski, G., Lemieszek, M. K., & Łukawski, K. (2015) · Annals of Agricultural and Environmental Medicine · doi:10.5604/12321966.1196863 · Cited by 24
“Apoptosis may be triggered either by extrinsic stimuli through cell surface death receptors, such as TNFα (tumour necrosis factor-α), Fas (CD95/APO1) and TRAIL (TNF related apoptosis inducing ligand), or by intrinsic stimuli via the mitochondrial signaling pathway [18].”
BackgroundInfluential
Cucurbitacin-I induces hypertrophy in H9c2 cardiomyoblasts through activation of autophagy via MEK/ERK1/2 signaling pathway
Yao, W., Chen, H., Li, R., Wang, X., Li, H., Xin, J., Liu, Z., Wu, S., Jiang, W., & Zhu, L. Y. (2016) · Toxicology Letters · doi:10.1016/j.toxlet.2016.11.003 · Cited by 24
Goniothalamin induces mitochondria-mediated apoptosis associated with endoplasmic reticulum stress-induced activation of JNK in HeLa cells
Sophonnithiprasert, T., Mahabusarakam, W., Nakamura, Y., & Watanapokasin, R. Y. (2016) · Oncology Letters · doi:10.3892/ol.2016.5381 · Cited by 24
“Apoptosis can be activated either by cell surface death receptor-or mitochon-dria-mediated apoptosis signaling pathways (14,15).”
N-Glycosylation of Lipocalin 2 Is Not Required for Secretion or Exosome Targeting
Borkham‐Kamphorst, E., de Leur, E. V., Meurer, S. K., Buhl, E. M., & Weiskirchen, R. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00426 · Cited by 24
“(Nikoletopoulou et al., 2013; Su et al., 2015).”
Calcineurin regulates cyclin D1 stability through dephosphorylation at T286
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Toxicity Mechanism of Gadolinium Oxide Nanoparticles and Gadolinium Ions in Human Breast Cancer Cells
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The novel proautophagy anticancer drug ABTL0812 potentiates chemotherapy in adenocarcinoma and squamous nonsmall cell lung cancer
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“Accumulating evidence reveals that autophagy and nonapoptotic cell death can cooperate, antagonize or assist each other, thus differentially influencing cell fate.(37,38) Interestingly, autophagy appears to facilitate nonapoptotic cell death in certain instances.”
Background
Regulation on Beclin-1 expression by mTOR in CoCl2-induced HT22 cell ischemia-reperfusion injury
Yang, T., Li, D., Liu, F., Qi, L., Yan, G., & Wang, M. (2015) · Brain Research · doi:10.1016/j.brainres.2015.04.016 · Cited by 23
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SAHA and cisplatin sensitize gastric cancer cells to doxorubicin by induction of DNA damage, apoptosis and perturbation of AMPK-mTOR signalling
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The ER Stress Inducer l-Azetidine-2-Carboxylic Acid Elevates the Levels of Phospho-eIF2α and of LC3-II in a Ca2+-Dependent Manner
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Molecular modulation of autophagy: New venture to target resistant cancer stem cells
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Diosmetin alleviates hypoxia‑induced myocardial apoptosis by inducing autophagy through AMPK activation
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Knockout of VDAC1 in H9c2 Cells Promotes Oxidative Stress-Induced Cell Apoptosis through Decreased Mitochondrial Hexokinase II Binding and Enhanced Glycolytic Stress
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“Apoptosis and necrosis are the two major cell death pathways [29, 30].”
Background
Gemcitabine and Rapamycin Exhibit Additive Effect against Osteosarcoma by Targeting Autophagy and Apoptosis
Ando, T., Ichikawa, J., Fujimaki, T., Taniguchi, N., Takayama, Y., & Haro, H. (2020) · Cancers · doi:10.3390/cancers12113097 · Cited by 23
“In contrast, previous reports have shown that Rapa either suppresses [41,42] or induces [43,44] apoptosis, depending on the cell type and environment [45].”
Result
A selective CuII complex with 4-fluorophenoxyacetic acid hydrazide and phenanthroline displays DNA-cleaving and pro-apoptotic properties in cancer cells
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Ginsenoside Rg2 Ameliorates Myocardial Ischemia/Reperfusion Injury by Regulating TAK1 to Inhibit Necroptosis
Li, Y., Hao, H., Yu, H., Yu, L., Ma, H., & Zhang, H. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.824657 · Cited by 24
“Necroptosis, a regulated form of necrosis, is mediated by death receptors such as tumor necrosis factor receptor 1(TNFR1), and is executed through the induction of the RIP1–RIP3 necroptotic complex (5).”
Background
Liproxstatin‑1 induces cell cycle arrest, apoptosis, and caspase‑3/GSDME‑dependent secondary pyroptosis in K562 cells
Dong, H.-Q., Liang, S.-J., Xu, Y., Dai, Y., Sun, N., Deng, D., & Cheng, P. (2022) · International Journal of Oncology · doi:10.3892/ijo.2022.5409 · Cited by 23
Multifunctional role of dietary copper to regulate stress-responsive gene for mitigation of multiple stresses in Pangasianodon hypophthalmus
Kumar, N., Thorat, S. T., & Chavhan, S. R. (2024) · Scientific Reports · doi:10.1038/s41598-024-51170-z · Cited by 23
“It also has a critical role in removing damaged tissues or unwanted cells without affecting the other tissues 71,72 .”
Background
Silymarin induces a multi-targeted cell death process in the human colon cancer cell line HT-29
Khorsandi, L., Saki, G., Bavarsad, N., & Mombeini, M. A. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.08.015 · Cited by 23
Enhanced anticancer effects of low-dose curcumin with non-invasive pulsed electric field on PANC-1 cells
Lu, C., Lin, S., Hsieh, C.-H., Chen, W., & Chao, C. (2018) · OncoTargets and Therapy · doi:10.2147/ott.s166264 · Cited by 23
“41 Induction of apoptosis has been recognized as a major form of cell death and response to anticancer agents.”
Ochratoxin A induces cytoprotective autophagy via blocking AKT/mTOR signaling pathway in PK-15 cells
Qian, G., Liu, D., Hou, L., Hamid, M., Chen, X., Gan, F., Song, S., & Huang, K. (2018) · Food and Chemical Toxicology · doi:10.1016/j.fct.2018.09.070 · Cited by 23
Autophagy and its regulation by ginseng components
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“The parallel activity in the mitogen activated protein kinase (MAPK) and AMPK signaling pathways initiates autophagy as follows: JNK phosphorylates Bcl-2 to dissociate with Beclin-1, inhibiting mTOR [42], whereas mTOR generally is inhibited by AMPK activation to initiate autophagy processes and negatively regulate the…”
Background
Mitochondrial dysfunction, autophagy stimulation and non-apoptotic cell death caused by nitric oxide-inducing Pt-coated Au nanoparticle in human lung carcinoma cells
Akhtar, M. J., Ahamed, M., Alhadlaq, H. A., Kumar, S., & Alrokayan, S. (2019) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2019.129452 · Cited by 23
Methyl methanesulfonate induces necroptosis in human lung adenoma A549 cells through the PIG-3-reactive oxygen species pathway
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Activation of TLR5 induces podocyte apoptosis
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“Under certain condition, the apoptosis programme may be initiated by exogenous or endogenous events; such as stress,(5) the binding of nuclear receptors by glucocorticoids,(6) heat,(7) radiation,(8) nutrient deprivation,(9) viral infection,(10) hypoxia(11) and damage of the cell membrane.(12) Podocytes are visceral ep…”
Background
Severe Asthma: Have we Made Progress?
Poon, A. H., & Hamid, Q. A. (2016) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201508-514mg · Cited by 22
Phosphatidylinositol 3-Kinase/AKT Pathway Inhibition by Doxazosin Promotes Glioblastoma Cells Death, Upregulation of p53 and Triggers Low Neurotoxicity
Gaelzer, M. M., Coelho, B. P., de Quadros, A. H., Hoppe, J. B., Terra, S. R., Guerra, M. C., Usach, V., Guma, F. T. C. R., Gonçalves, C. A., Setton-Avruj, C. P., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154612 · Cited by 22
“When Akt is inactive, cells can undergo apoptosis through loss of mitochondrial membrane potential, leading to activation of caspase-9 and caspase-3, resulting in apoptosis [49].”
Background
Altered expression of genes involved in programmed cell death in primary cultured rat cerebellar granule cells acutely challenged with tetrabromobisphenol A
Lenart, J., Ziemińska, E., Diamandakis, D., & Łazarewicz, J. W. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2017.09.014 · Cited by 22
“…the three major pathways of programmed cell death could partially result from a known phenomenon of the interplay between these signaling pathways (Nikoletopoulou et al., 2013) and from the diversity of sites of TBBPA interaction with neurotransmission in neurons leading to the induction of many…”
Background
Zn-doped CuO Nanocomposites Inhibit Tumor Growth By NF-κB Pathway cross-linked Autophagy and Apoptosis
Xu, H., Yuan, R., Liu, X., Li, X., Qiao, G., Li, C., Gedanken, A., & Lin, X. (2018) · Nanomedicine · doi:10.2217/nnm-2018-0366 · Cited by 22
Rapamycin Reduces Cervical Cancer Cells Viability in Hypoxic Condition: Investigation of the Role of Autophagy and Apoptosis
Rezazadeh, D., Norooznezhad, A. H., Mansouri, K., Jahani, M., Mostafaie, A., Modarressi, M. H., & Modarressi, M. H. (2020) · OncoTargets and Therapy · doi:10.2147/ott.s249985 · Cited by 22
The Crosstalk between Autophagy and Apoptosis Is Necessary for Myogenic Differentiation
Jiang, A., Guo, H., Wu, W., & Liu, H. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c00140 · Cited by 23
A Five Autophagy-Related Long Non-Coding RNA Prognostic Model for Patients with Lung Adenocarcinoma
Liu, B., Zhao, Y., & Yang, S. (2021) · International Journal of General Medicine · doi:10.2147/ijgm.s334601 · Cited by 20
Multiplicity of Glycosphingolipid-Enriched Microdomain-Driven Immune Signaling
Yokoyama, N., Hanafusa, K., Hotta, T., Oshima, E., Iwabuchi, K., & Nakayama, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179565 · Cited by 22
“Thus, apoptosis and autophagy can cooperate, antagonize or assist each other, differentially influencing the fate of cells [83].”
Background
Cytotoxic Effects of Hellebrigenin and Arenobufagin Against Human Breast Cancer Cells
Zhang, Y., Yuan, B., Bian, B., Zhao, H., Kiyomi, A., Hayashi, H., Iwatani, Y., Sugiura, M., & Takagi, N. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.711220 · Cited by 22
“Furthermore, cleavage of PARP, known as an early marker of chemotherapyinduced apoptosis (31), was observed concomitantly, indicating the onset of apoptosis.”
BackgroundInfluential
MicroRNA-483-5p accentuates cisplatin-induced acute kidney injury by targeting GPX3
Xia, Y., Pan, W., Xiao, X., Zhou, X., Gu, W., Liu, Y., Zhao, Y.-Y., Li, L., Zheng, C., Liu, J., et al. (2022) · Laboratory Investigation · doi:10.1038/s41374-022-00737-3 · Cited by 22

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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