Inflammasomes in cancer: a double-edged sword

Ryan Kolb, Guang-Hui Liu, Ann M. Janowski, Fayyaz S. Sutterwala, Weizhou Zhang

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Protein Cell ›› 2014, Vol. 5 ›› Issue (1) : 12-20. DOI: 10.1007/s13238-013-0001-4
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Inflammasomes in cancer: a double-edged sword

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Abstract

Chronic inflammatory responses have long been observed to be associated with various types of cancer and play decisive roles at different stages of cancer development. Inflammasomes, which are potent inducers of interleukin (IL)-1β and IL-18 during inflammation, are large protein complexes typically consisting of a Nod-like receptor (NLR), the adapter protein ASC, and Caspase-1. During malignant transformation or cancer therapy, the inflammasomes are postulated to become activated in response to danger signals arising from the tumors or from therapy-induced damage to the tumor or healthy tissue. The activation of inflammasomes plays diverse and sometimes contrasting roles in cancer promotion and therapy depending on the specific context. Here we summarize the role of different inflammasome complexes in cancer progression and therapy. Inflammasome components and pathways may provide novel targets to treat certain types of cancer; however, using such agents should be cautiously evaluated due to the complex roles that inflammasomes and proinflammatory cytokines play in immunity.

Keywords

inflammasome / cancer / inflammation

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Ryan Kolb, Guang-Hui Liu, Ann M. Janowski, Fayyaz S. Sutterwala, Weizhou Zhang. Inflammasomes in cancer: a double-edged sword. Protein Cell, 2014, 5(1): 12‒20 https://doi.org/10.1007/s13238-013-0001-4

References

[1]
AllenIC, TeKippeEM, WoodfordRM, UronisJM, HollEK, RogersAB, HerfarthHH, JobinC, TingJP (2010) The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J Exp Med207: 1045-1056
CrossRef Google scholar
[2]
AllenIC, WilsonJE, SchneiderM, LichJD, RobertsRA, ArthurJC, WoodfordRM, DavisBK, UronisJM, HerfarthHH (2012) NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-κB signaling. Immunity36: 742-754
CrossRef Google scholar
[3]
BassoD, ScrignerM, TomaA, NavagliaF, Di MarioF, RuggeM, PlebaniM (1996) Helicobacter pylori infection enhances mucosal interleukin-1 beta, interleukin-6, and the soluble receptor of interleukin-2. Int J Clin Lab Res26: 207-210
CrossRef Google scholar
[4]
BauerC, DuewellP, MayerC, LehrHA, FitzgeraldKA, DauerM, TschoppJ, EndresS, LatzE, SchnurrM (2010) Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut59: 1192-1199
CrossRef Google scholar
[5]
BauernfeindF, HornungV (2013) Of inflammasomes and pathogens -sensing of microbes by the inflammasome. EMBO Mol Med5: 814-826
CrossRef Google scholar
[6]
BauernfeindFG, HorvathG, StutzA, AlnemriES, MacDonaldK, SpeertD, Fernandes-AlnemriT, WuJ, MonksBG, FitzgeraldKA (2009) Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol183: 787-791
CrossRef Google scholar
[7]
BauernfeindF, AblasserA, BartokE, KimS, Schmid-BurgkJ, CavlarT, HornungV (2011) Inflammasomes: current understanding and open questions. Cell Mol Life Sci68: 765-783
CrossRef Google scholar
[8]
BuntSK, ClementsVK, HansonEM, SinhaP, Ostrand-RosenbergS (2009) Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J Leukoc Biol85: 996-1004
CrossRef Google scholar
[9]
BurdetteD, HaskettA, PresserL, McRaeS, IqbalJ, WarisG (2012) Hepatitis C virus activates interleukin-1beta via caspase-1- inflammasome complex. J Gen Virol93: 235-246
CrossRef Google scholar
[10]
ChaveyC, BibeauF, Gourgou-BourgadeS, BurlinchonS, BoissiereF, LauneD, RoquesS, LazennecG (2007) Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res9: R15
CrossRef Google scholar
[11]
ChenGY, NunezG (2011) Inflammasomes in intestinal inflammation and cancer. Gastroenterology141: 1986-1999
CrossRef Google scholar
[12]
ChenGY, LiuM, WangF, BertinJ, NunezG (2011) A functional role for Nlrp6 in intestinal inflammation and tumorigenesis. J Immunol186: 7187-7194
CrossRef Google scholar
[13]
ChowMT, SceneayJ, PagetC, WongCS, DuretH, TschoppJ, MollerA, SmythMJ (2012) NLRP3 suppresses NK cell-mediated responses to carcinogen-induced tumors and metastases. Cancer Res72: 5721-5732
CrossRef Google scholar
[14]
CoussensLM, ZitvogelL, PaluckaAK (2013) Neutralizing tumorpromoting chronic inflammation: a magic bullet? Science339: 286-291
CrossRef Google scholar
[15]
Di VirgilioF (2013) The therapeutic potential of modifying inflammasomes and NOD-Like receptors. Pharmacol Rev65: 872-905
CrossRef Google scholar
[16]
DinarelloCA (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol27: 519-550
CrossRef Google scholar
[17]
DinarelloCA (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood117: 3720-3732
CrossRef Google scholar
[18]
DostertC, PetrilliV, Van BruggenR, SteeleC, MossmanBT, TschoppJ (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science320: 674-677
CrossRef Google scholar
[19]
DrexlerSK, BonsignoreL, MasinM, TardivelA, JackstadtR, HermekingH, SchneiderP, GrossO, TschoppJ, YazdiAS (2012) Tissue-speciflc opposing functions of the inflammasome adaptor ASC in the regulation of epithelial skin carcinogenesis. Proc Natl Acad Sci USA109: 18384-18389
CrossRef Google scholar
[20]
DunnJH, EllisLZ, FujitaM (2012) Inflammasomes as molecular mediators of inflammation and cancer: potential role in melanoma. Cancer Lett314: 24-33
CrossRef Google scholar
[21]
Dupaul-ChicoineJ, YeretssianG, DoironK, BergstromKS, McIntireCR, LeBlancPM, MeunierC, TurbideC, GrosP, BeaucheminN (2010) Control of intestinal homeostasis, colitis, and colitisassociated colorectal cancer by the inflammatory caspases. Immunity32: 367-378
CrossRef Google scholar
[22]
EisenbarthSC, FlavellRA (2009) Innate instruction of adaptive immunity revisited: the inflammasome. EMBO Mol Med1: 92-98
CrossRef Google scholar
[23]
ElinavE, StrowigT, KauAL, Henao-MejiaJ, ThaissCA, BoothCJ, PeaperDR, BertinJ, EisenbarthSC, GordonJI (2011) NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell145: 745-757
CrossRef Google scholar
[24]
ElkabetsM, RibeiroVS, DinarelloCA, Ostrand-RosenbergS, Di SantoJP, ApteRN, VosshenrichCA (2010) IL-1beta regulates a novel myeloid-derived suppressor cell subset that impairs NK cell development and function. Eur J Immunol40: 3347-3357
CrossRef Google scholar
[25]
ElliottMR, ChekeniFB, TrampontPC, LazarowskiER, KadlA, WalkSF, ParkD, WoodsonRI, OstankovichM, SharmaP (2009) Nucleotides released by apoptotic cells act as a flnd-me signal to promote phagocytic clearance. Nature461: 282-286
CrossRef Google scholar
[26]
El-OmarEM, CarringtonM, ChowWH, McCollKE, BreamJH, YoungHA, HerreraJ, LissowskaJ, YuanCC, RothmanN (2000) Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature404: 398-402
CrossRef Google scholar
[27]
Fernandes-AlnemriT, YuJW, DattaP, WuJ, AlnemriES (2009) AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature458: 509-513
CrossRef Google scholar
[28]
Fernandes-AlnemriT, YuJW, JulianaC, SolorzanoL, KangS, WuJ, DattaP, McCormickM, HuangL, McDermottE (2010) The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat Immunol11: 385-393
CrossRef Google scholar
[29]
FerroneC, DranoffG (2010) Dual roles for immunity in gastrointestinal cancers. J Clin Oncol28: 4045-4051
CrossRef Google scholar
[30]
FranchiL, NunezG (2012) Immunology. Orchestrating inflammasomes. Science337: 1299-1300
CrossRef Google scholar
[31]
FranchiL, AmerA, Body-MalapelM, KannegantiTD, OzorenN, JagirdarR, InoharaN, VandenabeeleP, BertinJ, CoyleA (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol7: 576-582
CrossRef Google scholar
[32]
GhiringhelliF, ApetohL, TesniereA, AymericL, MaY, OrtizC, VermaelenK, PanaretakisT, MignotG, UllrichE (2009) Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med15: 1170-1178
CrossRef Google scholar
[33]
GreenDR, KroemerG (2005) Pharmacological manipulation of cell death: clinical applications in sight? J Clin Invest115: 2610-2617
CrossRef Google scholar
[34]
GringhuisSI, KapteinTM, WeversBA, TheelenB, van der VlistM, BoekhoutT, GeijtenbeekTB (2012) Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1beta via a noncanonical caspase-8 inflammasome. Nat Immunol13: 246-254
CrossRef Google scholar
[35]
GrivennikovSI, GretenFR, KarinM (2010) Immunity, inflammation, and cancer. Cell140: 883-899
CrossRef Google scholar
[36]
HornungV, AblasserA, Charrel-DennisM, BauernfeindF, HorvathG, CaffreyDR, LatzE, FitzgeraldKA (2009) AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature458: 514-518
CrossRef Google scholar
[37]
HuB, ElinavE, HuberS, BoothCJ, StrowigT, JinC, EisenbarthSC, FlavellRA (2010) Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc Natl Acad Sci USA107: 21635-21640
CrossRef Google scholar
[38]
HuB, ElinavE, FlavellRA (2011) Inflammasome-mediated suppression of inflammation-induced colorectal cancer progression is mediated by direct regulation of epithelial cell proliferation. Cell Cycle10: 1936-1939
CrossRef Google scholar
[39]
IdzkoM, DichmannS, FerrariD, Di VirgilioF, la SalaA, GirolomoniG, PantherE, NorgauerJ (2002) Nucleotides induce chemotaxis and actin polymerization in immature but not mature human dendritic cells via activation of pertussis toxin-sensitive P2y receptors. Blood100: 925-932
CrossRef Google scholar
[40]
IyerSS, PulskensWP, SadlerJJ, ButterLM, TeskeGJ, UllandTK, EisenbarthSC, FlorquinS, FlavellRA, LeemansJC (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA106: 20388-20393
CrossRef Google scholar
[41]
JeeCD, LeeHS, BaeSI, YangHK, LeeYM, RhoMS, KimWH (2005) Loss of caspase-1 gene expression in human gastric carcinomas and cell lines. Int J Oncol26: 1265-1271
[42]
JinL, YuanRQ, FuchsA, YaoY, JosephA, SchwallR, SchnittSJ, GuidaA, HastingsHM, AndresJ (1997) Expression of interleukin-1beta in human breast carcinoma. Cancer80: 421-434
CrossRef Google scholar
[43]
JulianaC, Fernandes-AlnemriT, KangS, FariasA, QinF, AlnemriES (2012) Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J Biol Chem287: 36617-36622
CrossRef Google scholar
[44]
KanavyHE, GerstenblithMR (2011) Ultraviolet radiation and melanoma. Semin Cutan Med Surg30: 222-228
CrossRef Google scholar
[45]
KayagakiN, WarmingS, LamkanflM, Vande WalleL, LouieS, DongJ, NewtonK, QuY, LiuJ, HeldensS (2011) Non-canonical inflammasome activation targets caspase-11. Nature479: 117-121
CrossRef Google scholar
[46]
KimS, BauernfeindF, AblasserA, HartmannG, FitzgeraldKA, LatzE, HornungV (2010) Listeria monocytogenes is sensed by the NLRP3 and AIM2 inflammasome. Eur J Immunol40: 1545-1551
CrossRef Google scholar
[47]
LamkanflM, DixitVM (2009) The inflammasomes. PLoS Pathog5: e1000510
CrossRef Google scholar
[48]
LiY, WangL, PappanL, Galliher-BeckleyA, ShiJ (2012) IL-1beta promotes stemness and invasiveness of colon cancer cells through Zeb1 activation. Mol Cancer11: 87
CrossRef Google scholar
[49]
LiuX, WangZ, YuJ, LeiG, WangS (2010) Three polymorphisms in interleukin-1beta gene and risk for breast cancer: a metaanalysis. Breast Cancer Res Treat124: 821-825
CrossRef Google scholar
[50]
LiuW, LuoY, DunnJH, NorrisDA, DinarelloCA, FujitaM (2013) Dual role of apoptosis-associated speck-like protein containing a CARD (ASC) in tumorigenesis of human melanoma. J Invest Dermatol133: 518-527
CrossRef Google scholar
[51]
LocherC, ConfortiR, AymericL, MaY, YamazakiT, RusakiewiczS, TesniereA, GhiringhelliF, ApetohL, MorelY (2010) Desirable cell death during anticancer chemotherapy. Ann N Y Acad Sci1209: 99-108
CrossRef Google scholar
[52]
MachadoJC, PharoahP, SousaS, CarvalhoR, OliveiraC, FigueiredoC, AmorimA, SerucaR, CaldasC, CarneiroF (2001) Interleukin 1B and interleukin 1RN polymorphisms are associated with increased risk of gastric carcinoma. Gastroenterology121: 823-829
CrossRef Google scholar
[53]
MariathasanS, NewtonK, MonackDM, VucicD, FrenchDM, LeeWP, Roose-GirmaM, EricksonS, DixitVM (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature430: 213-218
CrossRef Google scholar
[54]
MariathasanS, WeissDS, NewtonK, McBrideJ, O’RourkeK, Roose-GirmaM, LeeWP, WeinrauchY, MonackDM, DixitVM (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature440: 228-232
CrossRef Google scholar
[55]
MartinonF, PetrilliV, MayorA, TardivelA, TschoppJ (2006) Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature440: 237-241
CrossRef Google scholar
[56]
MartinsI, TesniereA, KeppO, MichaudM, SchlemmerF, SenovillaL, SerorC, MetivierD, PerfettiniJL, ZitvogelL (2009) Chemotherapy induces ATP release from tumor cells. Cell Cycle8: 3723-3728
CrossRef Google scholar
[57]
MattarolloSR, LoiS, DuretH, MaY, ZitvogelL, SmythMJ (2011) Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res71: 4809-4820
CrossRef Google scholar
[58]
McNamaraD, El-OmarE (2008) Helicobacter pylori infection and the pathogenesis of gastric cancer: a paradigm for host-bacterial interactions. Dig Liver Dis40: 504-509
CrossRef Google scholar
[59]
MiaoEA, Alpuche-ArandaCM, DorsM, ClarkAE, BaderMW, MillerSI, AderemA (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol7: 569-575
CrossRef Google scholar
[60]
MiaoEA, ErnstRK, DorsM, MaoDP, AderemA (2008) Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc Natl Acad Sci USA105: 2562-2567
CrossRef Google scholar
[61]
MiaoEA, RajanJV, AderemA (2011) Caspase-1-induced pyroptotic cell death. Immunol Rev243: 206-214
CrossRef Google scholar
[62]
NegashAA, RamosHJ, CrochetN, LauDT, DoehleB, PapicN, DelkerDA, JoJ, BertolettiA, HagedornCH (2013) IL-1beta production through the NLRP3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog9: e1003330
CrossRef Google scholar
[63]
NormandS, Delanoye-CrespinA, BressenotA, HuotL, GrandjeanT, Peyrin-BirouletL, LemoineY, HotD, ChamaillardM (2011) Nodlike receptor pyrin domain-containing protein 6 (NLRP6) controls epithelial self-renewal and colorectal carcinogenesis upon injury. Proc Natl Acad Sci USA108: 9601-9606
CrossRef Google scholar
[64]
OkamotoM, LiuW, LuoY, TanakaA, CaiX, NorrisDA, DinarelloCA, FujitaM (2010) Constitutively active inflammasome in human melanoma cells mediating autoinflammation via caspase-1 processing and secretion of interleukin-1beta. J Biol Chem285: 6477-6488
CrossRef Google scholar
[65]
PantschenkoAG, PushkarI, AndersonKH, WangY, MillerLJ, KurtzmanSH, BarrowsG, KreutzerDL (2003) The interleukin-1 family of cytokines and receptors in human breast cancer: implications for tumor progression. Int J Oncol23: 269-284
[66]
RamanD, BaugherPJ, ThuYM, RichmondA (2007) Role of chemokines in tumor growth. Cancer Lett256: 137-165
CrossRef Google scholar
[67]
RathinamVA, JiangZ, WaggonerSN, SharmaS, ColeLE, WaggonerL, VanajaSK, MonksBG, GanesanS, LatzE (2010) The AIM2 inflammasome is essential for host defense against cytosolic bacteria and DNA viruses. Nat Immunol11: 395-402
CrossRef Google scholar
[68]
ReedJR, LeonRP, HallMK, SchwertfegerKL (2009) Interleukin-1beta and flbroblast growth factor receptor 1 cooperate to induce cyclooxygenase-2 during early mammary tumourigenesis. Breast Cancer Res11:R21
CrossRef Google scholar
[69]
SagulenkoV, ThygesenSJ, SesterDP, IdrisA, CridlandJA, VajjhalaPR, RobertsTL, SchroderK, VinceJE, HillJM (2013) AIM2 and NLRP3 inflammasomes activate both apoptotic and pyroptotic death pathways via ASC. Cell Death Differ20: 1149-1160
CrossRef Google scholar
[70]
SakuraiT, HeG, MatsuzawaA, YuGY, MaedaS, HardimanG, KarinM (2008) Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell14: 156-165
CrossRef Google scholar
[71]
SalcedoR, WorschechA, CardoneM, JonesY, GyulaiZ, DaiRM, WangE, MaW, HainesD, O’HUiginC (2010) MyD88- mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J Exp Med207: 1625-1636
CrossRef Google scholar
[72]
SchroderK, TschoppJ (2010) The inflammasomes. Cell140: 821-832
CrossRef Google scholar
[73]
SchroderK, SagulenkoV, ZamoshnikovaA, RichardsAA, CridlandJA, IrvineKM, StaceyKJ, SweetMJ (2012) Acute lipopolysaccharide priming boosts inflammasome activation independently of inflammasome sensor induction. Immunobiology217: 1325-1329
CrossRef Google scholar
[74]
SevkoA, UmanskyV (2013) Myeloid-derived suppressor cells interact with tumors in terms of myelopoiesis, tumorigenesis and immunosuppression: thick as thieves. J Cancer4: 3-11
CrossRef Google scholar
[75]
SiegmundB, LehrHA, FantuzziG, DinarelloCA (2001) IL-1 betaconverting enzyme (caspase-1) in intestinal inflammation. Proc Natl Acad Sci USA98: 13249-13254
CrossRef Google scholar
[76]
SnoussiK, StrosbergAD, BouaouinaN, Ben AhmedS, ChouchaneL (2005) Genetic variation in pro-inflammatory cytokines (interleukin-1beta, interleukin-1alpha and interleukin-6) associated with the aggressive forms, survival, and relapse prediction of breast carcinoma. Eur Cytokine Netw16: 253-260
[77]
SrivastavaS, SalimN, RobertsonMJ (2010) Interleukin-18: biology and role in the immunotherapy of cancer. Curr Med Chem17: 3353-3357
CrossRef Google scholar
[78]
StehlikC, FiorentinoL, DorfleutnerA, BrueyJM, ArizaEM, SagaraJ, ReedJC (2002) The PAAD/PYRIN-family protein ASC is a dual regulator of a conserved step in nuclear factor kappaB activation pathways. J Exp Med196: 1605-1615
CrossRef Google scholar
[79]
SuzukiT, FranchiL, TomaC, AshidaH, OgawaM, YoshikawaY, MimuroH, InoharaN, SasakawaC, NunezG (2007) Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog3: e111
CrossRef Google scholar
[80]
TermeM, UllrichE, AymericL, MeinhardtK, DesboisM, DelahayeN, ViaudS, RyffelB, YagitaH, KaplanskiG (2011) IL-18 induces PD-1-dependent immunosuppression in cancer. Cancer Res71: 5393-5399
CrossRef Google scholar
[81]
TuS, BhagatG, CuiG, TakaishiS, Kurt-JonesEA, RickmanB, BetzKS, Penz-OesterreicherM, BjorkdahlO, FoxJG (2008) Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell14: 408-419
CrossRef Google scholar
[82]
van DeventerHW, BurgentsJE, WuQP, WoodfordRM, BrickeyWJ, AllenIC, McElvania-TekippeE, SerodyJS, TingJP (2010) The inflammasome component NLRP3 impairs antitumor vaccine by enhancing the accumulation of tumor-associated myeloid-derived suppressor cells. Cancer Res70: 10161-10169
CrossRef Google scholar
[83]
WangP, XiaHH, ZhangJY, DaiLP, XuXQ, WangKJ (2007) Association of interleukin-1 gene polymorphisms with gastric cancer: a meta-analysis. Int J Cancer120: 552-562
CrossRef Google scholar
[84]
ZakiMH, BoydKL, VogelP, KastanMB, LamkanflM, KannegantiTD (2010a) The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity32: 379-391
CrossRef Google scholar
[85]
ZakiMH, VogelP, Body-MalapelM, LamkanflM, KannegantiTD (2010b) IL-18 production downstream of the Nlrp3 inflammasome confers protection against colorectal tumor formation. J Immunol185: 4912-4920
CrossRef Google scholar
[86]
ZakiMH, VogelP, MalireddiRK, Body-MalapelM, AnandPK, BertinJ, GreenDR, LamkanflM, KannegantiTD (2011) The NOD-like receptor NLRP12 attenuates colon inflammation and tumorigenesis. Cancer Cell20: 649-660
CrossRef Google scholar
[87]
ZamboniDS, KobayashiKS, KohlsdorfT, OguraY, LongEM, VanceRE, KuidaK, MariathasanS, DixitVM, FlavellRA (2006) The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat Immunol7: 318-325
CrossRef Google scholar
[88]
ZhuY, ZhuM, LanceP (2012) IL1beta-mediated Stromal COX-2 signaling mediates proliferation and invasiveness of colonic epithelial cancer cells. Exp Cell Res318: 2520-2530
CrossRef Google scholar
[89]
ZitvogelL, KeppO, GalluzziL, KroemerG (2012) Inflammasomes in carcinogenesis and anticancer immune responses. Nat Immunol13: 343-351
CrossRef Google scholar

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