Life, death, and autophagy in cancer: NF-κB turns up everywhere.
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
30 03 2020
30 03 2020
Historique:
received:
06
01
2020
accepted:
03
03
2020
revised:
27
02
2020
entrez:
2
4
2020
pubmed:
2
4
2020
medline:
14
4
2021
Statut:
epublish
Résumé
Escaping programmed cell death is a hallmark of cancer. NF-κB transcription factors are key regulator of cell survival and aberrant NF-κB signaling has been involved in the pathogenesis of most human malignancies. Although NF-κB is best known for its antiapoptotic role, other processes regulating the life/death balance, such as autophagy and necroptosis, seem to network with NF-κB. This review discusses how the reciprocal regulation of NF-κB, autophagy and programmed cell death affect cancer development and progression.
Identifiants
pubmed: 32231206
doi: 10.1038/s41419-020-2399-y
pii: 10.1038/s41419-020-2399-y
pmc: PMC7105474
doi:
Substances chimiques
NF-kappa B
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
210Subventions
Organisme : Medical Research Council
ID : MR/L005069/1
Pays : United Kingdom
Références
Beg, A. A., Sha, W. C., Bronson, R. T., Ghosh, S. & Baltimore, D. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa-B. Nature 376, 167–170 (1995).
pubmed: 7603567
doi: 10.1038/376167a0
pmcid: 7603567
Bonizzi, G. & Karin, M. The two NF-kappa B activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25, 280–288 (2004).
pubmed: 15145317
doi: 10.1016/j.it.2004.03.008
pmcid: 15145317
Siebenlist, U., Brown, K. & Claudio, E. Control of lymphocyte development by nuclear factor-kappa B. Nat. Rev. Immunol. 5, 435–445 (2005).
pubmed: 15905862
doi: 10.1038/nri1629
pmcid: 15905862
Karin, M. & Lin, A. NF-kappa B at the crossroads of life and death. Nat. Immunol. 3, 221–227 (2002).
pubmed: 11875461
doi: 10.1038/ni0302-221
pmcid: 11875461
Luo, J. L., Kamata, H. & Karin, M. IKK/NF-kappaB signaling: balancing life and death-a new approach to cancer therapy. J. Clin. Invest 115, 2625–2632 (2005).
pubmed: 16200195
pmcid: 1236696
doi: 10.1172/JCI26322
Baldwin, A. S. Regulation of cell death and autophagy by IKK and NF-kappa B: critical mechanisms in immune function and cancer. Immunol. Rev. 246, 327–345 (2012).
pubmed: 22435564
doi: 10.1111/j.1600-065X.2012.01095.x
pmcid: 22435564
De Smaele, E. et al. Induction of gadd45 beta by NF-kappa B downregulates pro-apoptotic JNK signalling. Nature 414, 308–313 (2001).
pubmed: 11713530
doi: 10.1038/35104560
pmcid: 11713530
Tang, G. L. et al. Inhibition of JNK activation through NF-kappa B target genes. Nature 414, 313–317 (2001).
pubmed: 11713531
doi: 10.1038/35104568
pmcid: 11713531
Chen, L. F. & Greene, W. C. Shaping the nuclear action of NF-kappa B. Nat. Rev. Mol. Cell Bio. 5, 392–401 (2004).
doi: 10.1038/nrm1368
Maeda, S. et al. IKK beta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNF alpha. Immunity 19, 725–737 (2003).
pubmed: 14614859
doi: 10.1016/S1074-7613(03)00301-7
pmcid: 14614859
Papa, S. et al. Gadd45 beta mediates the NF-kappa B suppression of JNK signalling by targeting MKK7/JNKK2. Nat. Cell Biol. 6, 146 (2004).
pubmed: 14743220
doi: 10.1038/ncb1093
pmcid: 14743220
Pham, C. G. et al. Ferritin heavy chain upregulation by NF-kappa B inhibits TNF alpha-induced apoptosis by suppressing reactive oxygen species. Cell 119, 529–542 (2004).
pubmed: 15537542
doi: 10.1016/j.cell.2004.10.017
pmcid: 15537542
Delhalle, S., Deregowski, V., Benoit, V., Merville, M. P. & Bours, V. NF-kappa B-dependent MnSOD expression protects adenocarcinoma cells from TNF-alpha-induced apoptosis. Oncogene 21, 3917–3924 (2002).
pubmed: 12032830
doi: 10.1038/sj.onc.1205489
pmcid: 12032830
Bernard, D., Quatannens, B., Begue, A., Vandenbunder, B. & Abbadie, C. Antiproliferative and antiapoptotic effects of cRel may occur within the same cells via the up-regulation of manganese superoxide dismutase. Cancer Res. 61, 2656–2664 (2001).
pubmed: 11289144
pmcid: 11289144
Papa, S. et al. The NF-kappa B-mediated control of the JNK cascade in the antagonism of programmed cell death in health and disease. Cell Death Differ. 13, 712–729 (2006).
pubmed: 16456579
doi: 10.1038/sj.cdd.4401865
pmcid: 16456579
Sasazuki, T. et al. Genome wide analysis of TNF-inducible genes reveals that antioxidant enzymes are induced by TNF and responsible for elimination of ROS. Mol. Immunol. 41, 547–551 (2004).
pubmed: 15183933
doi: 10.1016/j.molimm.2004.03.030
pmcid: 15183933
DiDonato, J. A., Mercurio, F., Karin, M. & NF-kappa, B. and the link between inflammation and cancer. Immunol. Rev. 246, 379–400 (2012).
pubmed: 22435567
doi: 10.1111/j.1600-065X.2012.01099.x
pmcid: 22435567
Xia, L. et al. Role of the NFkappaB-signaling pathway in cancer. Onco Targets Ther. 11, 2063–2073 (2018).
pubmed: 29695914
pmcid: 5905465
doi: 10.2147/OTT.S161109
Capece, D. et al. Cancer secretome and inflammation: the bright and the dark sides of NF-kappaB. Semin Cell Dev. Biol. 78, 51–61 (2018).
pubmed: 28779979
doi: 10.1016/j.semcdb.2017.08.004
pmcid: 28779979
Taniguchi, K. & Karin, M. NF-kappaB, inflammation, immunity and cancer: coming of age. Nat. Rev. Immunol. 18, 309–324 (2018).
pubmed: 29379212
doi: 10.1038/nri.2017.142
pmcid: 29379212
Staudt, L. M. Oncogenic activation of NF-kappaB. Cold Spring Harb. Perspect. Biol. 2, a000109 (2010).
pubmed: 20516126
pmcid: 2869521
doi: 10.1101/cshperspect.a000109
Bennett, J. et al. NF-kappaB in the crosshairs: Rethinking an old riddle. Int J. Biochem Cell Biol. 95, 108–112 (2018).
pubmed: 29277662
pmcid: 6562234
doi: 10.1016/j.biocel.2017.12.020
Begalli, F. et al. Unlocking the NF-kappaB Conundrum: embracing complexity to achieve specificity. Biomedicines 5, E50 (2017).
pubmed: 28829404
doi: 10.3390/biomedicines5030050
pmcid: 28829404
Mayo, M. W. et al. Requirement of NF-kappaB activation to suppress p53-independent apoptosis induced by oncogenic Ras. Science 278, 1812–1815 (1997).
pubmed: 9388187
doi: 10.1126/science.278.5344.1812
pmcid: 9388187
Basseres, D. S., Ebbs, A., Levantini, E. & Baldwin, A. S. Requirement of the NF-kappaB subunit p65/RelA for K-Ras-induced lung tumorigenesis. Cancer Res. 70, 3537–3546 (2010).
pubmed: 20406971
pmcid: 2862109
doi: 10.1158/0008-5472.CAN-09-4290
Greten, F. R. et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118, 285–296 (2004).
pubmed: 15294155
doi: 10.1016/j.cell.2004.07.013
pmcid: 15294155
Pikarsky, E. et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 431, 461–466 (2004).
pubmed: 15329734
doi: 10.1038/nature02924
pmcid: 15329734
Luo, J. L., Maeda, S., Hsu, L. C., Yagita, H. & Karin, M. Inhibition of NF-kappaB in cancer cells converts inflammation- induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression. Cancer Cell 6, 297–305 (2004).
pubmed: 15380520
doi: 10.1016/j.ccr.2004.08.012
pmcid: 15380520
Davis, R. E., Brown, K. D., Siebenlist, U. & Staudt, L. M. Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J. Exp. Med. 194, 1861–1874 (2001).
pubmed: 11748286
pmcid: 2193582
doi: 10.1084/jem.194.12.1861
Tornatore, L. et al. Cancer-selective targeting of the NF-kappaB survival pathway with GADD45beta/MKK7 inhibitors. Cancer Cell 26, 495–508 (2014).
pubmed: 25314077
pmcid: 4197335
doi: 10.1016/j.ccr.2014.07.027
Tornatore, L. et al. Preclinical toxicology and safety pharmacology of the first-in-class GADD45beta/MKK7 inhibitor and clinical candidate, DTP3. Toxicol. Rep. 6, 369–379 (2019).
pubmed: 31080744
pmcid: 6502747
doi: 10.1016/j.toxrep.2019.04.006
Tornatore, L. et al. Clinical proof of concept for a safe and effective NF-kappaB-targeting strategy in multiple myeloma. Br. J. Haematol. 185, 588–592 (2019).
pubmed: 30255568
doi: 10.1111/bjh.15569
Galluzzi, L. et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 22, 58–73 (2015).
pubmed: 25236395
doi: 10.1038/cdd.2014.137
Galluzzi, L., Buque, A., Kepp, O., Zitvogel, L. & Kroemer, G. Immunogenic cell death in cancer and infectious disease. Nat. Rev. Immunol. 17, 97–111 (2017).
pubmed: 27748397
doi: 10.1038/nri.2016.107
Choi, A. M., Ryter, S. W. & Levine, B. Autophagy in human health and disease. N. Engl. J. Med. 368, 651–662 (2013).
pubmed: 23406030
doi: 10.1056/NEJMra1205406
Yun, C. W. & Lee, S. H. The roles of autophagy in cancer. Int. J. Mol. Sci. 19, 3466 (2018).
pmcid: 6274804
doi: 10.3390/ijms19113466
pubmed: 6274804
Ben-Neriah, Y. & Karin, M. Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat. Immunol. 12, 715–723 (2011).
pubmed: 21772280
doi: 10.1038/ni.2060
Hayden, M. S. & Ghosh, S. NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26, 203–234 (2012).
pubmed: 22302935
pmcid: 3278889
doi: 10.1101/gad.183434.111
Verzella, D. et al. Targeting the NF-kappaB pathway in prostate cancer: a promising therapeutic approach? Curr. Drug Targets 17, 311–320 (2016).
pubmed: 26343112
doi: 10.2174/1389450116666150907100715
Salminen, A., Hyttinen, J. M., Kauppinen, A. & Kaarniranta, K. Context-dependent regulation of autophagy by IKK-NF-kappaB signaling: impact on the aging process. Int J. Cell Biol. 2012, 849541 (2012).
pubmed: 22899934
pmcid: 3412117
doi: 10.1155/2012/849541
Trocoli, A. & Djavaheri-Mergny, M. The complex interplay between autophagy and NF-kappaB signaling pathways in cancer cells. Am. J. Cancer Res. 1, 629–649 (2011).
pubmed: 21994903
pmcid: 3189824
Nivon, M., Richet, E., Codogno, P., Arrigo, A. P. & Kretz-Remy, C. Autophagy activation by NFkappaB is essential for cell survival after heat shock. Autophagy 5, 766–783 (2009).
pubmed: 19502777
doi: 10.4161/auto.8788
Copetti, T., Bertoli, C., Dalla, E., Demarchi, F. & Schneider, C. p65/RelA modulates BECN1 transcription and autophagy. Mol. Cell Biol. 29, 2594–2608 (2009).
pubmed: 19289499
pmcid: 2682036
doi: 10.1128/MCB.01396-08
Comb, W. C., Hutti, J. E., Cogswell, P., Cantley, L. C. & Baldwin, A. S. p85alpha SH2 domain phosphorylation by IKK promotes feedback inhibition of PI3K and Akt in response to cellular starvation. Mol. Cell 45, 719–730 (2012).
pubmed: 22342344
pmcid: 3319231
doi: 10.1016/j.molcel.2012.01.010
Comb, W. C., Cogswell, P., Sitcheran, R. & Baldwin, A. S. IKK-dependent, NF-kappaB-independent control of autophagic gene expression. Oncogene 30, 1727–1732 (2011).
pubmed: 21151171
doi: 10.1038/onc.2010.553
Criollo, A. et al. The IKK complex contributes to the induction of autophagy. Embo. J. 29, 619–631 (2010).
pubmed: 19959994
doi: 10.1038/emboj.2009.364
Sarkar, S. et al. Complex inhibitory effects of nitric oxide on autophagy. Mol. Cell 43, 19–32 (2011).
pubmed: 21726807
pmcid: 3149661
doi: 10.1016/j.molcel.2011.04.029
Balaburski, G. M., Hontz, R. D. & Murphy, M. E. p53 and ARF: unexpected players in autophagy. Trends Cell Biol. 20, 363–369 (2010).
pubmed: 20303758
pmcid: 2891045
doi: 10.1016/j.tcb.2010.02.007
Djavaheri-Mergny, M. et al. NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J. Biol. Chem. 281, 30373–30382 (2006).
pubmed: 16857678
doi: 10.1074/jbc.M602097200
Qing, G., Yan, P. & Xiao, G. Hsp90 inhibition results in autophagy-mediated proteasome-independent degradation of IkappaB kinase (IKK). Cell Res. 16, 895–901 (2006).
pubmed: 17088896
doi: 10.1038/sj.cr.7310109
Qing, G., Yan, P., Qu, Z., Liu, H. & Xiao, G. Hsp90 regulates processing of NF-kappa B2 p100 involving protection of NF-kappa B-inducing kinase (NIK) from autophagy-mediated degradation. Cell Res 17, 520–530 (2007).
pubmed: 17563756
doi: 10.1038/cr.2007.47
Niida, M., Tanaka, M. & Kamitani, T. Downregulation of active IKK beta by Ro52-mediated autophagy. Mol. Immunol. 47, 2378–2387 (2010).
pubmed: 20627395
pmcid: 2918734
doi: 10.1016/j.molimm.2010.05.004
Kim, J. E. et al. Suppression of NF-kappaB signaling by KEAP1 regulation of IKKbeta activity through autophagic degradation and inhibition of phosphorylation. Cell Signal 22, 1645–1654 (2010).
pubmed: 20600852
doi: 10.1016/j.cellsig.2010.06.004
Colleran, A. et al. Autophagosomal IkappaB alpha degradation plays a role in the long term control of tumor necrosis factor-alpha-induced nuclear factor-kappaB (NF-kappaB) activity. J. Biol. Chem. 286, 22886–22893 (2011).
pubmed: 21454695
pmcid: 3123056
doi: 10.1074/jbc.M110.199950
Singh, R. & Cuervo, A. M. Autophagy in the cellular energetic balance. Cell Metab. 13, 495–504 (2011).
pubmed: 21531332
pmcid: 3099265
doi: 10.1016/j.cmet.2011.04.004
Kroemer, G. & Levine, B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 9, 1004–1010 (2008).
pubmed: 18971948
pmcid: 2727358
doi: 10.1038/nrm2529
Yu, L. et al. Autophagic programmed cell death by selective catalase degradation. Proc. Natl Acad. Sci. USA 103, 4952–4957 (2006).
pubmed: 16547133
doi: 10.1073/pnas.0511288103
Mizushima, N. Autophagy in protein and organelle turnover. Cold Spring Harb. Symp. Quant. Biol. 76, 397–402 (2011).
pubmed: 21813637
doi: 10.1101/sqb.2011.76.011023
Rabinowitz, J. D. & White, E. Autophagy and metabolism. Science 330, 1344–1348 (2010).
pubmed: 21127245
pmcid: 3010857
doi: 10.1126/science.1193497
White, E. The role for autophagy in cancer. J. Clin. Invest 125, 42–46 (2015).
pubmed: 25654549
pmcid: 4382247
doi: 10.1172/JCI73941
Djavaheri-Mergny, M. et al. Regulation of autophagy by NFkappaB transcription factor and reactives oxygen species. Autophagy 3, 390–392 (2007).
pubmed: 17471012
doi: 10.4161/auto.4248
pmcid: 17471012
Huang, J., Lam, G. Y. & Brumell, J. H. Autophagy signaling through reactive oxygen species. Antioxid. Redox Signal 14, 2215–2231 (2011).
pubmed: 20874258
doi: 10.1089/ars.2010.3554
pmcid: 20874258
Salminen, A., Ojala, J., Kaarniranta, K. & Kauppinen, A. Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases. Cell Mol. Life Sci. 69, 2999–3013 (2012).
pubmed: 22446749
doi: 10.1007/s00018-012-0962-0
pmcid: 22446749
Zhang, H., Chen, Z., Miranda, R. N., Medeiros, L. J. & McCarty, N. TG2 and NF-kappaB signaling coordinates the survival of mantle cell lymphoma cells via IL6-mediated autophagy. Cancer Res. 76, 6410–6423 (2016).
pubmed: 27488529
pmcid: 5093039
doi: 10.1158/0008-5472.CAN-16-0595
Newman, A. C., Kemp, A. J., Drabsch, Y., Behrends, C. & Wilkinson, S. Autophagy acts through TRAF3 and RELB to regulate gene expression via antagonism of SMAD proteins. Nat. Commun. 8, 1537 (2017).
pubmed: 29146913
pmcid: 5691083
doi: 10.1038/s41467-017-00859-z
Dan, H. C., Adli, M. & Baldwin, A. S. Regulation of mammalian target of rapamycin activity in PTEN-inactive prostate cancer cells by I kappa B kinase alpha. Cancer Res. 67, 6263–6269 (2007).
pubmed: 17616684
doi: 10.1158/0008-5472.CAN-07-1232
pmcid: 17616684
Levine, B. & Kroemer, G. Autophagy in the pathogenesis of disease. Cell 132, 27–42 (2008).
pubmed: 18191218
pmcid: 2696814
doi: 10.1016/j.cell.2007.12.018
Chen, L., Liu, D., Zhang, Y., Zhang, H. & Cheng, H. The autophagy molecule Beclin 1 maintains persistent activity of NF-kappaB and Stat3 in HTLV-1-transformed T lymphocytes. Biochem Biophys. Res. Commun. 465, 739–745 (2015).
pubmed: 26319552
pmcid: 4580621
doi: 10.1016/j.bbrc.2015.08.070
Yoon, S. et al. NF-kappaB and STAT3 cooperatively induce IL6 in starved cancer cells. Oncogene 31, 3467–3481 (2012).
pubmed: 22105366
doi: 10.1038/onc.2011.517
pmcid: 22105366
Liu, K. et al. SKP2 attenuates NF-kappaB signaling by mediating IKKbeta degradation through autophagy. J. Mol. Cell Biol. 10, 205–215 (2018).
pubmed: 29474632
doi: 10.1093/jmcb/mjy012
pmcid: 29474632
Lee, D. F. et al. KEAP1 E3 ligase-mediated downregulation of NF-kappaB signaling by targeting IKKbeta. Mol. Cell 36, 131–140 (2009).
pubmed: 19818716
pmcid: 2770835
doi: 10.1016/j.molcel.2009.07.025
van der Wijst, M. G., Huisman, C., Mposhi, A., Roelfes, G. & Rots, M. G. Targeting Nrf2 in healthy and malignant ovarian epithelial cells: protection versus promotion. Mol. Oncol. 9, 1259–1273 (2015).
pubmed: 25841766
pmcid: 5528817
doi: 10.1016/j.molonc.2015.03.003
Leinonen, H. M., Kansanen, E., Polonen, P., Heinaniemi, M. & Levonen, A. L. Role of the Keap1-Nrf2 pathway in cancer. Adv. Cancer Res. 122, 281–320 (2014).
pubmed: 24974185
doi: 10.1016/B978-0-12-420117-0.00008-6
pmcid: 24974185
Lee, K. H., Lee, J., Woo, J., Lee, C. H. & Yoo, C. G. Proteasome inhibitor-induced IkappaB/NF-kappaB activation is mediated by Nrf2-dependent light chain 3B induction in lung cancer cells. Mol. Cells 41, 1008–1015 (2018).
pubmed: 30396235
pmcid: 6315323
Xiao, G. Autophagy and NF-kappaB: fight for fate. Cytokine Growth Factor Rev. 18, 233–243 (2007).
pubmed: 17485237
pmcid: 2810660
doi: 10.1016/j.cytogfr.2007.04.006
Zuehlke, A. & Johnson, J. L. Hsp90 and co-chaperones twist the functions of diverse client proteins. Biopolymers 93, 211–217 (2010).
pubmed: 19697319
pmcid: 2810645
doi: 10.1002/bip.21292
Duran, A. et al. The signaling adaptor p62 is an important NF-kappaB mediator in tumorigenesis. Cancer Cell 13, 343–354 (2008).
pubmed: 18394557
doi: 10.1016/j.ccr.2008.02.001
pmcid: 18394557
Moscat, J. & Diaz-Meco, M. T. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 137, 1001–1004 (2009).
pubmed: 19524504
pmcid: 3971861
doi: 10.1016/j.cell.2009.05.023
Ren, F. et al. Knockdown of p62/sequestosome 1 attenuates autophagy and inhibits colorectal cancer cell growth. Mol. Cell Biochem. 385, 95–102 (2014).
pubmed: 24065390
doi: 10.1007/s11010-013-1818-0
pmcid: 24065390
Nguyen, T. D. et al. Loss of the selective autophagy receptor p62 impairs murine myeloid leukemia progression and mitophagy. Blood 133, 168–179 (2019).
pubmed: 30498063
doi: 10.1182/blood-2018-02-833475
pmcid: 30498063
Su, J. et al. p62 participates in the inhibition of NF-kappaB signaling and apoptosis induced by sulfasalazine in human glioma U251 cells. Oncol. Rep. 34, 235–p243 (2015).
pubmed: 25937318
doi: 10.3892/or.2015.3944
pmcid: 25937318
Sanz, L., Sanchez, P., Lallena, M. J., Diaz-Meco, M. T. & Moscat, J. The interaction of p62 with RIP links the atypical PKCs to NF-kappaB activation. Embo. J. 18, 3044–3053 (1999).
pubmed: 10356400
pmcid: 1171386
doi: 10.1093/emboj/18.11.3044
Wooten, M. W. et al. The p62 scaffold regulates nerve growth factor-induced NF-kappaB activation by influencing TRAF6 polyubiquitination. J Biol Chem 280, 35625–35629 (2005).
pubmed: 16079148
doi: 10.1074/jbc.C500237200
pmcid: 16079148
Yang, S., Qiang, L., Sample, A., Shah, P. & He, Y. Y. NF-kappaB signaling activation induced by chloroquine requires autophagosome, p62 protein, and c-Jun N-terminal kinase (JNK) signaling and promotes tumor cell resistance. J. Biol. Chem. 292, 3379–3388 (2017).
pubmed: 28082672
pmcid: 5336170
doi: 10.1074/jbc.M116.756536
Jia, L., Gopinathan, G., Sukumar, J. T. & Gribben, J. G. Blocking autophagy prevents bortezomib-induced NF-kappaB activation by reducing I-kappaBalpha degradation in lymphoma cells. PLoS ONE 7, e32584 (2012).
pubmed: 22393418
pmcid: 3290566
doi: 10.1371/journal.pone.0032584
Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646–674 (2011).
pubmed: 21376230
pmcid: 21376230
doi: 10.1016/j.cell.2011.02.013
Karin, M. Nuclear factor-kappaB in cancer development and progression. Nature 441, 431–436 (2006).
pubmed: 16724054
doi: 10.1038/nature04870
pmcid: 16724054
Hoesel, B. & Schmid, J. A. The complexity of NF-kappaB signaling in inflammation and cancer. Mol. Cancer 12, 86 (2013).
pubmed: 23915189
pmcid: 3750319
doi: 10.1186/1476-4598-12-86
Mancino, A. & Lawrence, T. Nuclear factor-kappaB and tumor-associated macrophages. Clin. Cancer Res. 16, 784–789 (2010).
pubmed: 20103670
pmcid: 6485421
doi: 10.1158/1078-0432.CCR-09-1015
Verzella, D. et al. GADD45beta loss ablates innate immunosuppression in cancer. Cancer Res. 78, 1275–1292 (2018).
pubmed: 29279355
doi: 10.1158/0008-5472.CAN-17-1833
pmcid: 29279355
Capece, D. et al. Turning an old GADDget into a troublemaker. Cell Death Differ. 25, 640–642 (2018).
pmcid: 5864189
doi: 10.1038/s41418-018-0087-6
Monkkonen, T. & Debnath, J. Inflammatory signaling cascades and autophagy in cancer. Autophagy 14, 190–198 (2018).
pubmed: 28813180
doi: 10.1080/15548627.2017.1345412
pmcid: 28813180
Chang, C. P., Su, Y. C., Lee, P. H. & Lei, H. Y. Targeting NFKB by autophagy to polarize hepatoma-associated macrophage differentiation. Autophagy 9, 619–621 (2013).
pubmed: 23360732
pmcid: 3627680
doi: 10.4161/auto.23546
Chang, C. P., Su, Y. C., Hu, C. W. & Lei, H. Y. TLR2-dependent selective autophagy regulates NF-kappaB lysosomal degradation in hepatoma-derived M2 macrophage differentiation. Cell Death Differ. 20, 515–523 (2013).
pubmed: 23175187
doi: 10.1038/cdd.2012.146
pmcid: 23175187
Tan, H. Y. et al. Autophagy-induced RelB/p52 activation mediates tumour-associated macrophage repolarisation and suppression of hepatocellular carcinoma by natural compound baicalin. Cell Death Dis. 6, e1942 (2015).
pubmed: 26492375
pmcid: 4632300
doi: 10.1038/cddis.2015.271
Sun, K. et al. Autophagy-deficient Kupffer cells promote tumorigenesis by enhancing mtROS-NF-kappaB-IL1alpha/beta-dependent inflammation and fibrosis during the preneoplastic stage of hepatocarcinogenesis. Cancer Lett. 388, 198–207 (2017).
pubmed: 28011320
doi: 10.1016/j.canlet.2016.12.004
pmcid: 28011320
Capece, D. et al. NF-kappaB and mitochondria cross paths in cancer: mitochondrial metabolism and beyond. Semin Cell Dev. Biol. 98, 118–128 (2020).
pubmed: 31132468
doi: 10.1016/j.semcdb.2019.05.021
pmcid: 31132468
Martinez-Outschoorn, U. E., Lisanti, M. P. & Sotgia, F. Catabolic cancer-associated fibroblasts transfer energy and biomass t.o anabolic cancer cells, fueling tumor growth. Semin Cancer Biol. 25, 47–60 (2014).
pubmed: 24486645
doi: 10.1016/j.semcancer.2014.01.005
pmcid: 24486645
Weinlich, R., Oberst, A., Beere, H. M. & Green, D. R. Necroptosis in development, inflammation and disease. Nat. Rev. Mol. Cell Biol. 18, 127–136 (2017).
pubmed: 27999438
doi: 10.1038/nrm.2016.149
pmcid: 27999438
Park, H. H. et al. The death domain superfamily in intracellular signaling of apoptosis and inflammation. Annu Rev. Immunol. 25, 561–586 (2007).
pubmed: 17201679
pmcid: 2904440
doi: 10.1146/annurev.immunol.25.022106.141656
Dickens, L. S., Powley, I. R., Hughes, M. A. & MacFarlane, M. The ‘complexities’ of life and death: death receptor signalling platforms. Exp. Cell Res. 318, 1269–1277 (2012).
pubmed: 22542855
doi: 10.1016/j.yexcr.2012.04.005
pmcid: 22542855
Cho, Y. S. et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112–1123 (2009).
pubmed: 19524513
pmcid: 2727676
doi: 10.1016/j.cell.2009.05.037
Mompean, M. et al. The structure of the necrosome RIPK1-RIPK3 core, a human hetero-amyloid signaling complex. Cell 173, 1244–1253 e1210 (2018).
pubmed: 29681455
pmcid: 6002806
doi: 10.1016/j.cell.2018.03.032
He, S. et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha. Cell 137, 1100–1111 (2009).
pubmed: 19524512
doi: 10.1016/j.cell.2009.05.021
pmcid: 19524512
Wang, H. et al. Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol. Cell 54, 133–146 (2014).
pubmed: 24703947
doi: 10.1016/j.molcel.2014.03.003
pmcid: 24703947
Cai, Z. et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16, 55–65 (2014).
pubmed: 24316671
doi: 10.1038/ncb2883
pmcid: 24316671
Quarato, G. et al. Sequential engagement of distinct MLKL phosphatidylinositol-binding sites executes necroptosis. Mol. Cell 61, 589–601 (2016).
pubmed: 26853145
pmcid: 4769881
doi: 10.1016/j.molcel.2016.01.011
Yatim, N. et al. RIPK1 and NF-kappaB signaling in dying cells determines cross-priming of CD8(+) T cells. Science 350, 328–334 (2015).
pubmed: 26405229
pmcid: 4651449
doi: 10.1126/science.aad0395
Yatim, N., Cullen, S. & Albert, M. L. Dying cells actively regulate adaptive immune responses. Nat. Rev. Immunol. 17, 262–275 (2017).
pubmed: 28287107
doi: 10.1038/nri.2017.9
pmcid: 28287107
Daniels, B. P. et al. RIPK3 Restricts Viral Pathogenesis via Cell Death-Independent Neuroinflammation. Cell 169, 301–313 e311 (2017).
pubmed: 28366204
pmcid: 5405738
doi: 10.1016/j.cell.2017.03.011
Nailwal, H. & Chan, F. K. Necroptosis in anti-viral inflammation. Cell Death Differ. 26, 4–13 (2019).
pubmed: 30050058
doi: 10.1038/s41418-018-0172-x
pmcid: 30050058
Ea, C. K., Deng, L., Xia, Z. P., Pineda, G. & Chen, Z. J. Activation of IKK by TNFalpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22, 245–257 (2006).
pubmed: 16603398
doi: 10.1016/j.molcel.2006.03.026
pmcid: 16603398
Kanayama, A. et al. TAB2 and TAB3 activate the NF-kappaB pathway through binding to polyubiquitin chains. Mol. Cell 15, 535–548 (2004).
pubmed: 15327770
doi: 10.1016/j.molcel.2004.08.008
pmcid: 15327770
Micheau, O., Lens, S., Gaide, O., Alevizopoulos, K. & Tschopp, J. NF-kappaB signals induce the expression of c-FLIP. Mol. Cell Biol. 21, 5299–5305 (2001).
pubmed: 11463813
pmcid: 87253
doi: 10.1128/MCB.21.16.5299-5305.2001
Kreuz, S., Siegmund, D., Scheurich, P. & Wajant, H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol. Cell Biol. 21, 3964–3973 (2001).
pubmed: 11359904
pmcid: 87059
doi: 10.1128/MCB.21.12.3964-3973.2001
Micheau, O. & Tschopp, J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181–190 (2003).
pubmed: 12887920
doi: 10.1016/S0092-8674(03)00521-X
pmcid: 12887920
Feng, S. et al. Cleavage of RIP3 inactivates its caspase-independent apoptosis pathway by removal of kinase domain. Cell Signal 19, 2056–2067 (2007).
pubmed: 17644308
doi: 10.1016/j.cellsig.2007.05.016
pmcid: 17644308
Degterev, A. et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4, 313–321 (2008).
pubmed: 18408713
pmcid: 5434866
doi: 10.1038/nchembio.83
Ofengeim, D. & Yuan, J. Regulation of RIP1 kinase signalling at the crossroads of inflammation and cell death. Nat. Rev. Mol. Cell Biol. 14, 727–736 (2013).
pubmed: 24129419
doi: 10.1038/nrm3683
pmcid: 24129419
Weinlich, R. & Green, D. R. The two faces of receptor interacting protein kinase-1. Mol. Cell 56, 469–480 (2014).
pubmed: 25459879
pmcid: 4254517
doi: 10.1016/j.molcel.2014.11.001
Li, J. et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150, 339–350 (2012).
pubmed: 22817896
pmcid: 3664196
doi: 10.1016/j.cell.2012.06.019
Fernald, K. & Kurokawa, M. Evading apoptosis in cancer. Trends Cell Biol. 23, 620–633 (2013).
pubmed: 23958396
pmcid: 4091735
doi: 10.1016/j.tcb.2013.07.006
He, S., Huang, S. & Shen, Z. Biomarkers for the detection of necroptosis. Cell Mol. Life Sci. 73, 2177–2181 (2016).
pubmed: 27066893
doi: 10.1007/s00018-016-2192-3
pmcid: 27066893
Kagoya, Y. et al. Positive feedback between NF-kappaB and TNF-alpha promotes leukemia-initiating cell capacity. J. Clin. Invest 124, 528–542 (2014).
pubmed: 24382349
pmcid: 3904603
doi: 10.1172/JCI68101
Chu, W. M. Tumor necrosis factor. Cancer Lett. 328, 222–225 (2013).
pubmed: 23085193
doi: 10.1016/j.canlet.2012.10.014
pmcid: 23085193
Gentle, I. E. & Silke, J. New perspectives in TNF-R1-induced NF-kappaB signaling. Adv. Exp. Med Biol. 691, 79–88 (2011).
pubmed: 21153311
doi: 10.1007/978-1-4419-6612-4_8
pmcid: 21153311
Laster, S. M., Wood, J. G. & Gooding, L. R. Tumor necrosis factor can induce both apoptic and necrotic forms of cell lysis. J. Immunol. 141, 2629–2634 (1988).
pubmed: 3171180
pmcid: 3171180
Sawai, H. Characterization of TNF-induced caspase-independent necroptosis. Leuk. Res. 38, 706–713 (2014).
pubmed: 24773756
doi: 10.1016/j.leukres.2014.02.002
pmcid: 24773756
Vanden Berghe, T. et al. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ. 17, 922–930 (2010).
pubmed: 20010783
doi: 10.1038/cdd.2009.184
pmcid: 20010783
Hernandez, L. et al. A dual role for Caspase8 and NF-kappaB interactions in regulating apoptosis and necroptosis of ovarian cancer, with correlation to patient survival. Cell Death Disco. 1, 15053 (2015).
doi: 10.1038/cddiscovery.2015.53
Shan, B., Pan, H., Najafov, A. & Yuan, J. Necroptosis in development and diseases. Genes Dev. 32, 327–340 (2018).
pubmed: 29593066
pmcid: 5900707
doi: 10.1101/gad.312561.118
Bozec, D., Iuga, A. C., Roda, G., Dahan, S. & Yeretssian, G. Critical function of the necroptosis adaptor RIPK3 in protecting from intestinal tumorigenesis. Oncotarget 7, 46384–46400 (2016).
pubmed: 27344176
pmcid: 5216805
doi: 10.18632/oncotarget.10135
Kondylis, V. et al. NEMO prevents steatohepatitis and hepatocellular carcinoma by inhibiting RIPK1 kinase activity-mediated hepatocyte apoptosis. Cancer Cell 28, 830 (2015).
pubmed: 28843278
pmcid: 5628166
doi: 10.1016/j.ccell.2015.11.007
Geisler, F., Algul, H., Paxian, S. & Schmid, R. M. Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology 132, 2489–2503 (2007).
pubmed: 17570221
doi: 10.1053/j.gastro.2007.03.033
Luedde, T. et al. Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 11, 119–132 (2007).
pubmed: 17292824
doi: 10.1016/j.ccr.2006.12.016
Aigelsreiter, A. et al. NEMO expression in human hepatocellular carcinoma and its association with clinical outcome. Hum. Pathol. 43, 1012–1019 (2012).
pubmed: 22176836
doi: 10.1016/j.humpath.2011.08.009
Koppe, C. et al. IkappaB kinasealpha/beta control biliary homeostasis and hepatocarcinogenesis in mice by phosphorylating the cell-death mediator receptor-interacting protein kinase 1. Hepatology 64, 1217–1231 (2016).
pubmed: 27396433
doi: 10.1002/hep.28723
Koppe, C. et al. An NF-kappaB- and IKK-independent function of NEMO prevents hepatocarcinogenesis by suppressing compensatory liver regeneration. Cancers 11, E999 (2019).
pubmed: 31319593
doi: 10.3390/cancers11070999
Pescatore, A., Esposito, E., Draber, P., Walczak, H. & Ursini, M. V. NEMO regulates a cell death switch in TNF signaling by inhibiting recruitment of RIPK3 to the cell death-inducing complex II. Cell Death Dis. 7, e2346 (2016).
pubmed: 27560715
pmcid: 5108330
doi: 10.1038/cddis.2016.245
Irrinki, K. M. et al. Requirement of FADD, NEMO, and BAX/BAK for aberrant mitochondrial function in tumor necrosis factor alpha-induced necrosis. Mol. Cell Biol. 31, 3745–3758 (2011).
pubmed: 21746883
pmcid: 3165716
doi: 10.1128/MCB.05303-11
Pasparakis, M. & Vandenabeele, P. Necroptosis and its role in inflammation. Nature 517, 311–320 (2015).
pubmed: 25592536
doi: 10.1038/nature14191
Biswas, S. K. & Lewis, C. E. NF-kappaB as a central regulator of macrophage function in tumors. J. Leukoc. Biol. 88, 877–884 (2010).
pubmed: 20573802
doi: 10.1189/jlb.0310153
pmcid: 20573802
Aaes, T. L. et al. Vaccination with necroptotic cancer cells induces efficient anti-tumor immunity. Cell Rep. 15, 274–287 (2016).
pubmed: 27050509
doi: 10.1016/j.celrep.2016.03.037
pmcid: 27050509
Schmidt, S. V. et al. RIPK3 expression in cervical cancer cells is required for PolyIC-induced necroptosis, IL-1alpha release, and efficient paracrine dendritic cell activation. Oncotarget 6, 8635–8647 (2015).
pubmed: 25888634
pmcid: 4496172
Snyder, A. G. et al. Intratumoral activation of the necroptotic pathway components RIPK1 and RIPK3 potentiates antitumor immunity. Sci. Immunol. 4, eaaw2004 (2019).
pubmed: 31227597
pmcid: 6831211
doi: 10.1126/sciimmunol.aaw2004
Maycotte, P. & Thorburn, A. Autophagy and cancer therapy. Cancer Biol. Ther. 11, 127–137 (2011).
pubmed: 21178393
pmcid: 3047083
doi: 10.4161/cbt.11.2.14627
Gewirtz, D. A. Autophagy and senescence in cancer therapy. J. Cell Physiol. 229, 6–9 (2014).
pubmed: 23794221
pmcid: 23794221
Papademetrio, D. L. et al. Inhibition of survival pathways MAPK and NF-kB triggers apoptosis in pancreatic ductal adenocarcinoma cells via suppression of autophagy. Target Oncol. 11, 183–195 (2016).
pubmed: 26373299
doi: 10.1007/s11523-015-0388-3
pmcid: 26373299
Papademetrio, D. L. et al. Interplay between autophagy and apoptosis in pancreatic tumors in response to gemcitabine. Target Oncol. 9, 123–134 (2014).
pubmed: 23588416
doi: 10.1007/s11523-013-0278-5
pmcid: 23588416
Ravikumar, B. & Rubinsztein, D. C. Role of autophagy in the clearance of mutant huntingtin: a step towards therapy? Mol. Asp. Med 27, 520–527 (2006).
doi: 10.1016/j.mam.2006.08.008
Koo, G. B. et al. Methylation-dependent loss of RIP3 expression in cancer represses programmed necrosis in response to chemotherapeutics. Cell Res. 25, 707–725 (2015).
pubmed: 25952668
pmcid: 4456623
doi: 10.1038/cr.2015.56
Feng, X. et al. Receptor-interacting protein kinase 3 is a predictor of survival and plays a tumor suppressive role in colorectal cancer. Neoplasma 62, 592–601 (2015).
pubmed: 25997957
doi: 10.4149/neo_2015_071
Geserick, P. et al. Absence of RIPK3 predicts necroptosis resistance in malignant melanoma. Cell Death Dis. 6, e1884 (2015).
pubmed: 26355347
pmcid: 4650439
doi: 10.1038/cddis.2015.240
He, L., Peng, K., Liu, Y., Xiong, J. & Zhu, F. F. Low expression of mixed lineage kinase domain-like protein is associated with poor prognosis in ovarian cancer patients. Onco Targets Ther. 6, 1539–1543 (2013).
pubmed: 24204164
pmcid: 3817086