Advanced search
Publication Cover
Expert Review of Anticancer Therapy Volume 13, 2013 - Issue 7
Submit an article Journal homepage
525
Views
27
CrossRef citations to date
0
Altmetric
Review

The role of necroptosis, an alternative form of cell death, in cancer therapy

Xinfang Yu Cancer Research Institute, Xiangya School of Medicine, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China; Cancer Research Institute, Xiangya School of Medicine, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China
,
Qipan Deng Cancer Research Institute, Xiangya School of Medicine, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China; The Hormel Institute, University of Minnesota, 801 16th Avenue NE, Austin, MN 55912, USA
,
Ann M Bode The Hormel Institute, University of Minnesota, 801 16th Avenue NE, Austin, MN 55912, USA; The Hormel Institute, University of Minnesota, 801 16th Avenue NE, Austin, MN 55912, USA
,
Zigang Dong The Hormel Institute, University of Minnesota, 801 16th Avenue NE, Austin, MN 55912, USA; The Hormel Institute, University of Minnesota, 801 16th Avenue NE, Austin, MN 55912, USA
&
Ya Cao Cancer Research Institute, Xiangya School of Medicine, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China. [email protected]; Molecular Imaging Center, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China; Cancer Research Institute, Xiangya School of Medicine, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China. [email protected]; Molecular Imaging Center, Central South University, 110 Xiang Ya Road, Changsha 410078, Hunan, China
Pages 883-893 | Published online: 10 Jan 2014

References

  • Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 147(4), 742–758 (2011).
  • Galluzzi L, Vitale I, Abrams JM et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 19(1), 107–120 (2012).
  • Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26(4), 239–257 (1972).
  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell 147(4), 728–741 (2011).
  • Mathew R, White E. Autophagy, stress, and cancer metabolism: what doesn’t kill you makes you stronger. Cold Spring Harb. Symp. Quant. Biol. 76, 389–396 (2011).
  • Eguchi Y, Shimizu S, Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57(10), 1835–1840 (1997).
  • Vandenabeele P, Galluzzi L, Vanden Berghe T, Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 11(10), 700–714 (2010).
  • Galluzzi L, Kepp O, Kroemer G. RIP kinases initiate programmed necrosis. J. Mol. Cell Biol. 1(1), 8–10 (2009).
  • Li J, McQuade T, Siemer AB et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150(2), 339–350 (2012).
  • Degterev A, Huang Z, Boyce M et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1(2), 112–119 (2005).
  • Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity 38(2), 209–223 (2013).
  • Welz PS, Wullaert A, Vlantis K et al. FADD prevents RIP3-mediated epithelial cell necrosis and chronic intestinal inflammation. Nature 477(7364), 330–334 (2011).
  • Bonnet MC, Preukschat D, Welz PS et al. The adaptor protein FADD protects epidermal keratinocytes from necroptosis in vivo and prevents skin inflammation. Immunity 35(4), 572–582 (2011).
  • Günther C, Martini E, Wittkopf N et al. Caspase-8 regulates TNF-a-induced epithelial necroptosis and terminal ileitis. Nature 477(7364), 335–339 (2011).
  • Vercammen D, Beyaert R, Denecker G et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187(9), 1477–1485 (1998).
  • Zhang DW, Shao J, Lin J et al. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325(5938), 332–336 (2009).
  • Vanlangenakker N, Bertrand MJ, Bogaert P, Vandenabeele P, Vanden Berghe T. TNF-induced necroptosis in L929 cells is tightly regulated by multiple TNFR1 complex I and II members. Cell Death Dis. 2, e230 (2011).
  • Ye YC, Yu L, Wang HJ, Tashiro S, Onodera S, Ikejima T. TNFα-induced necroptosis and autophagy via suppression of the p38-NF-κB survival pathway in L929 cells. J. Pharmacol. Sci. 117(3), 160–169 (2011).
  • Jouan-Lanhouet S, Arshad MI, Piquet-Pellorce C et al. TRAIL induces necroptosis involving RIPK1/RIPK3-dependent PARP-1 activation. Cell Death Differ. 19(12), 2003–2014 (2012).
  • Thapa RJ, Basagoudanavar SH, Nogusa S et al. NF-κB protects cells from γ interferon-induced RIP1-dependent necroptosis. Mol. Cell. Biol. 31(14), 2934–2946 (2011).
  • Lamkanfi M, Dixit VM. Manipulation of host cell death pathways during microbial infections. Cell Host Microbe 8(1), 44–54 (2010).
  • He S, Liang Y, Shao F, Wang X. Toll-like receptors activate programmed necrosis in macrophages through a receptor-interacting kinase-3-mediated pathway. Proc. Natl Acad. Sci. USA 108(50), 20054–20059 (2011).
  • Robinson N, McComb S, Mulligan R, Dudani R, Krishnan L, Sad S. Type I interferon induces necroptosis in macrophages during infection with Salmonella enterica serovar Typhimurium. Nat. Immunol. 13(10), 954–962 (2012).
  • Radin JN, González-Rivera C, Ivie SE, McClain MS, Cover TL. Helicobacter pylori VacA induces programmed necrosis in gastric epithelial cells. Infect. Immun. 79(7), 2535–2543 (2011).
  • Festjens N, Vanden Berghe T, Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta 1757(9-10), 1371–1387 (2006).
  • Cho YS, Challa S, Moquin D et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137(6), 1112–1123 (2009).
  • Fliss PM, Brune W. Prevention of cellular suicide by cytomegaloviruses. Viruses 4(10), 1928–1949 (2012).
  • Upton JW, Kaiser WJ, Mocarski ES. Virus inhibition of RIP3-dependent necrosis. Cell Host Microbe 7(4), 302–313 (2010).
  • Upton JW, Kaiser WJ, Mocarski ES. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11(3), 290–297 (2012).
  • Peri P, Nuutila K, Vuorinen T, Saukko P, Hukkanen V. Cathepsins are involved in virus-induced cell death in ICP4 and Us3 deletion mutant herpes simplex virus type 1-infected monocytic cells. J. Gen. Virol. 92(Pt 1), 173–180 (2011).
  • Wu YT, Tan HL, Huang Q, Sun XJ, Zhu X, Shen HM. zVAD-induced necroptosis in L929 cells depends on autocrine production of TNFα mediated by the PKC-MAPKs-AP-1 pathway. Cell Death Differ. 18(1), 26–37 (2011).
  • Christofferson DE, Li Y, Hitomi J et al. A novel role for RIP1 kinase in mediating TNFα production. Cell Death Dis. 3, e320 (2012).
  • Chang L, Kamata H, Solinas G et al. The E3 ubiquitin ligase itch couples JNK activation to TNFα-induced cell death by inducing c-FLIP(L) turnover. Cell 124(3), 601–613 (2006).
  • Micheau O, Tschopp J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114(2), 181–190 (2003).
  • Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ. Activation of IKK by TNFα requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol. Cell 22(2), 245–257 (2006).
  • Fan Y, Yu Y, Shi Y et al. Lysine 63-linked polyubiquitination of TAK1 at lysine 158 is required for tumor necrosis factor α- and interleukin-1β-induced IKK/NF-κB and JNK/AP-1 activation. J. Biol. Chem. 285(8), 5347–5360 (2010).
  • Bertrand MJ, Milutinovic S, Dickson KM et al. cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell 30(6), 689–700 (2008).
  • Wertz IE, O’Rourke KM, Zhou H et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature 430(7000), 694–699 (2004).
  • Christofferson DE, Yuan J. Necroptosis as an alternative form of programmed cell death. Curr. Opin. Cell Biol. 22(2), 263–268 (2010).
  • Hitomi J, Christofferson DE, Ng A et al. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135(7), 1311–1323 (2008).
  • Shembade N, Ma A, Harhaj EW. Inhibition of NF-κB signaling by A20 through disruption of ubiquitin enzyme complexes. Science 327(5969), 1135–1139 (2010).
  • Kreuzaler P, Watson CJ. Killing a cancer: what are the alternatives? Nat. Rev. Cancer 12(6), 411–424 (2012).
  • Wang L, Du F, Wang X. TNF-α induces two distinct caspase-8 activation pathways. Cell 133(4), 693–703 (2008).
  • Degterev A, Hitomi J, Germscheid M et al. Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat. Chem. Biol. 4(5), 313–321 (2008).
  • Zheng W, Degterev A, Hsu E, Yuan J, Yuan C. Structure-activity relationship study of a novel necroptosis inhibitor, necrostatin-7. Bioorg. Med. Chem. Lett. 18(18), 4932–4935 (2008).
  • Degterev A, Maki JL, Yuan J. Activity and specificity of necrostatin-1, small-molecule inhibitor of RIP1 kinase. Cell Death Differ. 20(2), 366 (2013).
  • Xie T, Peng W, Liu Y et al. Structural basis of RIP1 inhibition by necrostatins. Structure 21(3), 493–499 (2013).
  • O’Donnell MA, Perez-Jimenez E, Oberst A et al. Caspase 8 inhibits programmed necrosis by processing CYLD. Nat. Cell Biol. 13(12), 1437–1442 (2011).
  • Oberst A, Dillon CP, Weinlich R et al. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature 471(7338), 363–367 (2011).
  • Feoktistova M, Geserick P, Kellert B et al. cIAPs block Ripoptosome formation, a RIP1/caspase-8 containing intracellular cell death complex differentially regulated by cFLIP isoforms. Mol. Cell 43(3), 449–463 (2011).
  • Tourneur L, Chiocchia G. FADD: a regulator of life and death. Trends Immunol. 31(7), 260–269 (2010).
  • Osborn SL, Diehl G, Han SJ et al. Fas-associated death domain (FADD) is a negative regulator of T-cell receptor-mediated necroptosis. Proc. Natl Acad. Sci. USA 107(29), 13034–13039 (2010).
  • Meylan E, Tschopp J. The RIP kinases: crucial integrators of cellular stress. Trends Biochem. Sci. 30(3), 151–159 (2005).
  • Narayan N, Lee IH, Borenstein R et al. The NAD-dependent deacetylase SIRT2 is required for programmed necrosis. Nature 492(7428), 199–204 (2012).
  • Duprez L, Bertrand MJ, Vanden Berghe T, Dondelinger Y, Festjens N, Vandenabeele P. Intermediate domain of receptor-interacting protein kinase 1 (RIPK1) determines switch between necroptosis and RIPK1 kinase-dependent apoptosis. J. Biol. Chem. 287(18), 14863–14872 (2012).
  • He S, Wang L, Miao L et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137(6), 1100–1111 (2009).
  • Sun L, Wang H, Wang Z et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148(1–2), 213–227 (2012).
  • Zhao J, Jitkaew S, Cai Z et al. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl Acad. Sci. USA 109(14), 5322–5327 (2012).
  • Arduíno DM, Esteves AR, Cortes L et al. Mitochondrial metabolism in Parkinson’s disease impairs quality control autophagy by hampering microtubule-dependent traffic. Hum. Mol. Genet. 21(21), 4680–4702 (2012).
  • Kim YS, Morgan MJ, Choksi S, Liu ZG. TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol. Cell 26(5), 675–687 (2007).
  • Yazdanpanah B, Wiegmann K, Tchikov V et al. Riboflavin kinase couples TNF receptor 1 to NADPH oxidase. Nature 460(7259), 1159–1163 (2009).
  • Byun HS, Won M, Park KA et al. Prevention of TNF-induced necrotic cell death by rottlerin through a Nox1 NADPH oxidase. Exp. Mol. Med. 40(2), 186–195 (2008).
  • Davis CW, Hawkins BJ, Ramasamy S et al. Nitration of the mitochondrial complex I subunit NDUFB8 elicits RIP1- and RIP3-mediated necrosis. Free Radic. Biol. Med. 48(2), 306–317 (2010).
  • Irrinki KM, Mallilankaraman K, Thapa RJ et al. Requirement of FADD, NEMO, and BAX/BAK for aberrant mitochondrial function in tumor necrosis factor α-induced necrosis. Mol. Cell. Biol. 31(18), 3745–3758 (2011).
  • Soldani C, Scovassi AI. Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 7(4), 321–328 (2002).
  • Ha HC, Snyder SH. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl Acad. Sci. USA 96(24), 13978–13982 (1999).
  • Baines CP, Kaiser RA, Purcell NH et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434(7033), 658–662 (2005).
  • Temkin V, Huang Q, Liu H, Osada H, Pope RM. Inhibition of ADP/ATP exchange in receptor-interacting protein-mediated necrosis. Mol. Cell. Biol. 26(6), 2215–2225 (2006).
  • Tesniere A, Schlemmer F, Boige V et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 29(4), 482–491 (2010).
  • Obeid M, Tesniere A, Ghiringhelli F et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13(1), 54–61 (2007).
  • Vakkila J, Lotze MT. Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol. 4(8), 641–648 (2004).
  • Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell 140(6), 883–899 (2010).
  • Galluzzi L, Kroemer G. Necroptosis: a specialized pathway of programmed necrosis. Cell 135(7), 1161–1163 (2008).
  • Gamrekelashvili J, Krüger C, von Wasielewski R et al. Necrotic tumor cell death in vivo impairs tumor-specific immune responses. J. Immunol. 178(3), 1573–1580 (2007).
  • Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 4(10), 757–768 (2004).
  • Kasof GM, Prosser JC, Liu D, Lorenzi MV, Gomes BC. The RIP-like kinase, RIP3, induces apoptosis and NF-κB nuclear translocation and localizes to mitochondria. FEBS Lett. 473(3), 285–291 (2000).
  • Yang Y, Hu W, Feng S, Ma J, Wu M. RIP3 β and RIP3 γ, two novel splice variants of receptor-interacting protein 3 (RIP3), downregulate RIP3-induced apoptosis. Biochem. Biophys. Res. Commun. 332(1), 181–187 (2005).
  • Liu P, Xu B, Shen W et al. Dysregulation of TNFα-induced necroptotic signaling in chronic lymphocytic leukemia: suppression of CYLD gene by LEF1. Leukemia 26(6), 1293–1300 (2012).
  • Massoumi R, Chmielarska K, Hennecke K, Pfeifer A, Fässler R. Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-κB signaling. Cell 125(4), 665–677 (2006).
  • Alameda JP, Moreno-Maldonado R, Navarro M et al. An inactivating CYLD mutation promotes skin tumor progression by conferring enhanced proliferative, survival and angiogenic properties to epidermal cancer cells. Oncogene 29(50), 6522–6532 (2010).
  • Huang CY, Kuo WT, Huang YC, Lee TC, Yu LC. Resistance to hypoxia-induced necroptosis is conferred by glycolytic pyruvate scavenging of mitochondrial superoxide in colorectal cancer cells. Cell Death Dis. 4, e622 (2013).
  • Urtishak KA, Edwards AY, Wang LS et al. Potent obatoclax cytotoxicity and activation of triple death mode killing across infant acute lymphoblastic leukemia. Blood 121(14), 2689–2703 (2013).
  • Guido C, Panza S, Santoro M et al. Estrogen receptor beta (ERβ) produces autophagy and necroptosis in human seminoma cell line through the binding of the Sp1 on the phosphatase and tensin homolog deleted from chromosome 10 (PTEN) promoter gene. Cell Cycle 11(15), 2911–2921 (2012).
  • Horita H, Frankel AE, Thorburn A. Acute myeloid leukemia-targeted toxin activates both apoptotic and necroptotic death mechanisms. PLoS ONE 3(12), e3909 (2008).
  • Jang MS, Lee SJ, Kang NS, Kim E. Cooperative phosphorylation of FADD by Aur-A and Plk1 in response to taxol triggers both apoptotic and necrotic cell death. Cancer Res. 71(23), 7207–7215 (2011).
  • Nehs MA, Lin CI, Kozono DE et al. Necroptosis is a novel mechanism of radiation-induced cell death in anaplastic thyroid and adrenocortical cancers. Surgery 150(6), 1032–1039 (2011).
  • Krysko DV, Vanden Berghe T, D’Herde K, Vandenabeele P. Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44(3), 205–221 (2008).
  • de Bruin EC, Medema JP. Apoptosis and non-apoptotic deaths in cancer development and treatment response. Cancer Treat. Rev. 34(8), 737–749 (2008).
  • Hu X, Han W, Li L. Targeting the weak point of cancer by induction of necroptosis. Autophagy 3(5), 490–492 (2007).
  • Laukens B, Jennewein C, Schenk B et al. Smac mimetic bypasses apoptosis resistance in FADD- or caspase-8-deficient cells by priming for tumor necrosis factor a-induced necroptosis. Neoplasia 13(10), 971–979 (2011).
  • Vanlangenakker N, Vanden Berghe T, Bogaert P et al. cIAP1 and TAK1 protect cells from TNF-induced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 18(4), 656–665 (2011).
  • Dunai ZA, Imre G, Barna G et al. Staurosporine induces necroptotic cell death under caspase-compromised conditions in U937 cells. PLoS ONE 7(7), e41945 (2012).
  • Xuan Y, Hu X. Naturally-occurring shikonin analogues–a class of necroptotic inducers that circumvent cancer drug resistance. Cancer Lett. 274(2), 233–242 (2009).
  • Han W, Li L, Qiu S et al. Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol. Cancer Ther. 6(5), 1641–1649 (2007).
  • Tenev T, Bianchi K, Darding M et al. The Ripoptosome, a signaling platform that assembles in response to genotoxic stress and loss of IAPs. Mol. Cell 43(3), 432–448 (2011).
  • Wang G, Wang JJ, Yang GY et al. Effects of quercetin nanoliposomes on C6 glioma cells through induction of type III programmed cell death. Int. J. Nanomedicine 7, 271–280 (2012).
  • Hu J, Liu X, Hughes D et al. Herceptin conjugates linked by EDC boost direct tumor cell death via programmed tumor cell necrosis. PloS ONE 6(8), e23270 (2011).
  • Vanden Berghe T, Grootjans S, Goossens V et al. Determination of apoptotic and necrotic cell death in vitro and in vivo. Methods doi:10.1016/j.ymeth.2013.02.011 (2013) (Epub ahead of print).
  • Saddoughi SA, Gencer S, Peterson YK et al. Sphingosine analogue drug FTY720 targets I2PP2A/SET and mediates lung tumour suppression via activation of PP2A-RIPK1-dependent necroptosis. EMBO Mol. Med. 5(1), 105–121 (2013).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.