NLRC3 regulates cellular proliferation and apoptosis to attenuate the development of colorectal cancer

References

• Kanneganti TD, Lamkanfi M, Nunez G. Intracellular NOD-like receptors in host defense and disease. Immunity 2007; 27:549-59; PMID:17967410; https://doi.org/10.1016/j.immuni.2007.10.002
   PubMed Web of Science ®Google Scholar
• Van Gorp H, Kuchmiy A, Van Hauwermeiren F, Lamkanfi M. NOD-like receptors interfacing the immune and reproductive systems. FEBS J 2014; 281:4568-82; PMID:25154302; https://doi.org/10.1111/febs.13014
   PubMed Web of Science ®Google Scholar
• Zaki MH, Boyd KL, Vogel P, Kastan MB, Lamkanfi M, Kanneganti TD. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 2010; 32:379-91; PMID:20303296; https://doi.org/10.1016/j.immuni.2010.03.003
   PubMed Web of Science ®Google Scholar
• Zaki MH, Vogel P, Body-Malapel M, Lamkanfi M, Kanneganti TD. IL-18 production downstream of the Nlrp3 inflammasome confers protection against colorectal tumor formation. J Immunol 2010; 185:4912-20; PMID:20855874; https://doi.org/10.4049/jimmunol.1002046
   PubMed Web of Science ®Google Scholar
• Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145:745-57; PMID:21565393; https://doi.org/10.1016/j.cell.2011.04.022
   PubMed Web of Science ®Google Scholar
• Man SM, Zhu Q, Zhu L, Liu Z, Karki R, Malik A, Sharma D, Li L, Malireddi RK, Gurung P, et al. Critical Role for the DNA Sensor AIM2 in Stem Cell Proliferation and Cancer. Cell 2015; 162:45-58; PMID:26095253; https://doi.org/10.1016/j.cell.2015.06.001
   PubMed Web of Science ®Google Scholar
• Hu B, Elinav E, Huber S, Booth CJ, Strowig T, Jin C, Eisenbarth SC, Flavell RA. Inflammation-induced tumorigenesis in the colon is regulated by caspase-1 and NLRC4. Proc Natl Acad Sci U S A 2010; 107:21635-40; PMID:21118981; https://doi.org/10.1073/pnas.1016814108
   PubMed Web of Science ®Google Scholar
• Allen IC, Wilson JE, Schneider M, Lich JD, Roberts RA, Arthur JC, Woodford RM, Davis BK, Uronis JM, Herfarth HH, et al. NLRP12 suppresses colon inflammation and tumorigenesis through the negative regulation of noncanonical NF-kappaB signaling. Immunity 2012; 36:742-54; PMID:22503542; https://doi.org/10.1016/j.immuni.2012.03.012
   PubMed Web of Science ®Google Scholar
• Allen IC, TeKippe EM, Woodford RM, Uronis JM, Holl EK, Rogers AB, Herfarth HH, Jobin C, Ting JP. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J Exp Med 2010; 207:1045-56; PMID:20385749; https://doi.org/10.1084/jem.20100050
   PubMed Web of Science ®Google Scholar
• Wlodarska M, Thaiss CA, Nowarski R, Henao-Mejia J, Zhang JP, Brown EM, Frankel G, Levy M, Katz MN, Philbrick WM, et al. NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 2014; 156:1045-59; PMID:24581500; https://doi.org/10.1016/j.cell.2014.01.026
   PubMed Web of Science ®Google Scholar
• Wilson JE, Petrucelli AS, Chen L, Koblansky AA, Truax AD, Oyama Y, Rogers AB, Brickey WJ, Wang Y, Schneider M, et al. Inflammasome-independent role of AIM2 in suppressing colon tumorigenesis via DNA-PK and Akt. Nat Med 2015; 21:906-13; PMID:26107252; https://doi.org/10.1038/nm.3908
   PubMed Web of Science ®Google Scholar
• Harton JA, Linhoff MW, Zhang J, Ting JP. Cutting edge: CATERPILLER: a large family of mammalian genes containing CARD, pyrin, nucleotide-binding, and leucine-rich repeat domains. J Immunol 2002; 169:4088-93; PMID:12370334; https://doi.org/10.4049/jimmunol.169.8.4088
   PubMed Web of Science ®Google Scholar
• Schneider M, Zimmermann AG, Roberts RA, Zhang L, Swanson KV, Wen H, Davis BK, Allen IC, Holl EK, Ye Z, et al. The innate immune sensor NLRC3 attenuates Toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-kappaB. Nat Immunol 2012; 13:823-31; PMID:22863753; https://doi.org/10.1038/ni.2378
   PubMed Web of Science ®Google Scholar
• Conti BJ, Davis BK, Zhang J, O'Connor W, Jr., Williams KL, Ting JP. CATERPILLER 16.2 (CLR16.2), a novel NBD/LRR family member that negatively regulates T cell function. J Biol Chem 2005; 280:18375-85; PMID:15705585; https://doi.org/10.1074/jbc.M413169200
   PubMed Web of Science ®Google Scholar
• Zhang L, Mo J, Swanson KV, Wen H, Petrucelli A, Gregory SM, Zhang Z, Schneider M, Jiang Y, Fitzgerald KA, et al. NLRC3, a member of the NLR family of proteins, is a negative regulator of innate immune signaling induced by the DNA sensor STING. Immunity 2014; 40:329-41; PMID:24560620; https://doi.org/10.1016/j.immuni.2014.01.010
   PubMed Web of Science ®Google Scholar
• Liu R, Truax AD, Chen L, Hu P, Li Z, Chen J, Song C, Chen L, Ting JP. Expression profile of innate immune receptors, NLRs and AIM2, in human colorectal cancer: correlation with cancer stages and inflammasome components. Oncotarget 2015; 6:33456-69; PMID:26378020
   PubMed Web of Science ®Google Scholar
• Karki R, Man SM, Malireddi RK, Kesavardhana S, Zhu Q, Burton AR, Sharma BR, Qi X, Pelletier S, Vogel P, et al. NLRC3 is an inhibitory sensor of PI3K-mTOR pathways in cancer. Nature 2016; 540:583-587; PMID:27951586; https://doi.org/10.1038/nature20597
   PubMed Web of Science ®Google Scholar
• Linares JF, Duran A, Yajima T, Pasparakis M, Moscat J, Diaz-Meco MT. K63 polyubiquitination and activation of mTOR by the p62-TRAF6 complex in nutrient-activated cells. Mol Cell 2013; 51:283-96; PMID:23911927; https://doi.org/10.1016/j.molcel.2013.06.020
   PubMed Web of Science ®Google Scholar
• Man SM, Kanneganti TD. Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat Rev Immunol 2016; 16:7-21; PMID:26655628; https://doi.org/10.1038/nri.2015.7
   PubMed Web of Science ®Google Scholar
• Karki R, Man SM, Kanneganti TD. Inflammasomes and Cancer. Cancer Immunol Res 2017; 5(2):94-99; PMID:28093447
   PubMed Web of Science ®Google Scholar
• Anti M, Armuzzi A, Morini S, Iascone E, Pignataro G, Coco C, Lorenzetti R, Paolucci M, Covino M, Gasbarrini A, et al. Severe imbalance of cell proliferation and apoptosis in the left colon and in the rectosigmoid tract in subjects with a history of large adenomas. Gut 2001; 48:238-46; PMID:11156647; https://doi.org/10.1136/gut.48.2.238
   PubMed Web of Science ®Google Scholar
• Zhu J, Blenis J, Yuan J. Activation of PI3K/Akt and MAPK pathways regulates Myc-mediated transcription by phosphorylating and promoting the degradation of Mad1. Proc Natl Acad Sci U S A 2008; 105:6584-9; PMID:18451027; https://doi.org/10.1073/pnas.0802785105
   PubMed Web of Science ®Google Scholar
• Sander S, Calado DP, Srinivasan L, Kochert K, Zhang B, Rosolowski M, Rodig SJ, Holzmann K, Stilgenbauer S, Siebert R, et al. Synergy between PI3K signaling and MYC in Burkitt lymphomagenesis. Cancer Cell 2012; 22:167-79; PMID:22897848; https://doi.org/10.1016/j.ccr.2012.06.012
   PubMed Web of Science ®Google Scholar
• Wang C, Lisanti MP, Liao DJ. Reviewing once more the c-myc and Ras collaboration: converging at the cyclin D1-CDK4 complex and challenging basic concepts of cancer biology. Cell Cycle 2011; 10:57-67; PMID:21200143; https://doi.org/10.4161/cc.10.1.14449
   PubMed Web of Science ®Google Scholar
• Obaya AJ, Mateyak MK, Sedivy JM. Mysterious liaisons: the relationship between c-Myc and the cell cycle. Oncogene 1999; 18:2934-41; PMID:10378690; https://doi.org/10.1038/sj.onc.1202749
   PubMed Web of Science ®Google Scholar
• Wang QS, Papanikolaou A, Sabourin CL, Rosenberg DW. Altered expression of cyclin D1 and cyclin-dependent kinase 4 in azoxymethane-induced mouse colon tumorigenesis. Carcinogenesis 1998; 19:2001-6; PMID:9855016; https://doi.org/10.1093/carcin/19.11.2001
   PubMed Web of Science ®Google Scholar
• Chiacchiera F, Simone C. The AMPK-FoxO3A axis as a target for cancer treatment. Cell Cycle 2010; 9:1091-6; PMID:20190568; https://doi.org/10.4161/cc.9.6.11035
   PubMed Web of Science ®Google Scholar
• Fu Z, Tindall DJ. FOXOs, cancer and regulation of apoptosis. Oncogene 2008; 27:2312-9; PMID:18391973; https://doi.org/10.1038/onc.2008.24
   PubMed Web of Science ®Google Scholar
• Tenbaum SP, Ordonez-Moran P, Puig I, Chicote I, Arques O, Landolfi S, Fernandez Y, Herance JR, Gispert JD, Mendizabal L, et al. beta-catenin confers resistance to PI3K and AKT inhibitors and subverts FOXO3a to promote metastasis in colon cancer. Nat Med 2012; 18:892-901; PMID:22610277; https://doi.org/10.1038/nm.2772
   PubMed Web of Science ®Google Scholar
• Fu Q, Du Y, Yang C, Zhang D, Zhang N, Liu X, Cho WC, Yang Y. An oncogenic role of miR-592 in tumorigenesis of human colorectal cancer by targeting Forkhead Box O3A (FoxO3A). Expert Opin Ther Targets 2016; 20:771-82; PMID:27167185; https://doi.org/10.1080/14728222.2016.1181753
   PubMed Web of Science ®Google Scholar
• Plas DR, Thompson CB. Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J Biol Chem 2003; 278:12361-6; PMID:12517744; https://doi.org/10.1074/jbc.M213069200
   PubMed Web of Science ®Google Scholar
• Fanali C, Lucchetti D, Farina M, Corbi M, Cufino V, Cittadini A, Sgambato A. Cancer stem cells in colorectal cancer from pathogenesis to therapy: controversies and perspectives. World J Gastroenterol 2014; 20:923-42; PMID:24574766; https://doi.org/10.3748/wjg.v20.i4.923
   PubMed Web of Science ®Google Scholar
• Espersen ML, Olsen J, Linnemann D, Hogdall E, Troelsen JT. Clinical implications of intestinal stem cell markers in colorectal cancer. Clin Colorectal Cancer 2015; 14:63-71; PMID:25657049; https://doi.org/10.1016/j.clcc.2014.12.004
   PubMed Web of Science ®Google Scholar
• Kreso A, van Galen P, Pedley NM, Lima-Fernandes E, Frelin C, Davis T, Cao L, Baiazitov R, Du W, Sydorenko N, et al. Self-renewal as a therapeutic target in human colorectal cancer. Nat Med 2014; 20:29-36; PMID:24292392; https://doi.org/10.1038/nm.3418
   PubMed Web of Science ®Google Scholar
• Yan KS, Chia LA, Li X, Ootani A, Su J, Lee JY, Su N, Luo Y, Heilshorn SC, Amieva MR, et al. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc Natl Acad Sci U S A 2012; 109:466-71; PMID:22190486; https://doi.org/10.1073/pnas.1118857109
   PubMed Web of Science ®Google Scholar
• Nacerddine K, Beaudry JB, Ginjala V, Westerman B, Mattiroli F, Song JY, van der Poel H, Ponz OB, Pritchard C, Cornelissen-Steijger P, et al. Akt-mediated phosphorylation of Bmi1 modulates its oncogenic potential, E3 ligase activity, and DNA damage repair activity in mouse prostate cancer. J Clin Invest 2012; 122:1920-32; PMID:22505453; https://doi.org/10.1172/JCI57477
   PubMed Web of Science ®Google Scholar
• Gersemann M, Becker S, Nuding S, Antoni L, Ott G, Fritz P, Oue N, Yasui W, Wehkamp J, Stange EF. Olfactomedin-4 is a glycoprotein secreted into mucus in active IBD. J Crohns Colitis 2012; 6:425-34; PMID:22398066; https://doi.org/10.1016/j.crohns.2011.09.013
   PubMed Web of Science ®Google Scholar
• Besson D, Pavageau AH, Valo I, Bourreau A, Belanger A, Eymerit-Morin C, Mouliere A, Chassevent A, Boisdron-Celle M, Morel A, et al. A quantitative proteomic approach of the different stages of colorectal cancer establishes OLFM4 as a new nonmetastatic tumor marker. Mol Cell Proteomics 2011; 10:1-14; PMID:21986994; https://doi.org/10.1074/mcp.M111.009712
   PubMed Web of Science ®Google Scholar
• Chin KL, Aerbajinai W, Zhu J, Drew L, Chen L, Liu W, Rodgers GP. The regulation of OLFM4 expression in myeloid precursor cells relies on NF-kappaB transcription factor. Br J Haematol 2008; 143:421-32; PMID:18764868; https://doi.org/10.1111/j.1365-2141.2008.07368.x
   PubMed Web of Science ®Google Scholar
• VanDussen KL, Carulli AJ, Keeley TM, Patel SR, Puthoff BJ, Magness ST, Tran IT, Maillard I, Siebel C, Kolterud A, et al. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 2012; 139:488-97; PMID:22190634; https://doi.org/10.1242/dev.070763
   PubMed Web of Science ®Google Scholar
• Rosenbauer F, Wagner K, Zhang P, Knobeloch KP, Iwama A, Tenen DG. pDP4, a novel glycoprotein secreted by mature granulocytes, is regulated by transcription factor PU.1. Blood 2004; 103:4294-301; PMID:14962908; https://doi.org/10.1182/blood-2003-08-2688
   PubMed Web of Science ®Google Scholar
• Liu W, Yan M, Liu Y, Wang R, Li C, Deng C, Singh A, Coleman WG, Jr., Rodgers GP. Olfactomedin 4 down-regulates innate immunity against Helicobacter pylori infection. Proc Natl Acad Sci U S A 2010; 107:11056-61; PMID:20534456; https://doi.org/10.1073/pnas.1001269107
   PubMed Web of Science ®Google Scholar
• Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001; 411:603-6; PMID:11385577; https://doi.org/10.1038/35079114
   PubMed Web of Science ®Google Scholar
• Hugot JP, Chamaillard M, Zouali H, Lesage S, Cezard JP, Belaiche J, Almer S, Tysk C, O'Morain CA, Gassull M, et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001; 411:599-603; PMID:11385576; https://doi.org/10.1038/35079107
   PubMed Web of Science ®Google Scholar
• Gagniere J, Raisch J, Veziant J, Barnich N, Bonnet R, Buc E, Bringer MA, Pezet D, Bonnet M. Gut microbiota imbalance and colorectal cancer. World J Gastroenterol 2016; 22:501-18; PMID:26811603; https://doi.org/10.3748/wjg.v22.i2.501
   PubMed Web of Science ®Google Scholar
• Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448:427-34; PMID:17653185; https://doi.org/10.1038/nature06005
   PubMed Web of Science ®Google Scholar
• Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013; 13:321-35; PMID:23618829; https://doi.org/10.1038/nri3430
   PubMed Web of Science ®Google Scholar
• Russo E, Taddei A, Ringressi MN, Ricci F, Amedei A. The interplay between the microbiome and the adaptive immune response in cancer development. Therap Adv Gastroenterol 2016; 9:594-605; PMID:27366226; https://doi.org/10.1177/1756283X16635082
   PubMed Web of Science ®Google Scholar
• Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci 2009; 122:3589-94; PMID:19812304; https://doi.org/10.1242/jcs.051011
   PubMed Web of Science ®Google Scholar
• Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, et al. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 2006; 126:955-68; PMID:16959574; https://doi.org/10.1016/j.cell.2006.06.055
   PubMed Web of Science ®Google Scholar
• Sullivan LB, Gui DY, Vander Heiden MG. Altered metabolite levels in cancer: implications for tumour biology and cancer therapy. Nat Rev Cancer 2016; 16:680-93; PMID:27658530; https://doi.org/10.1038/nrc.2016.85
   PubMed Web of Science ®Google Scholar
• Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2003; 2:28; PMID:14511394; https://doi.org/10.1186/1475-4924-2-28
   PubMedGoogle Scholar
• Nazio F, Cecconi F. mTOR, AMBRA1, and autophagy: an intricate relationship. Cell Cycle 2013; 12:2524-5; PMID:23907135; https://doi.org/10.4161/cc.25835
   PubMed Web of Science ®Google Scholar
• Nazio F, Strappazzon F, Antonioli M, Bielli P, Cianfanelli V, Bordi M, Gretzmeier C, Dengjel J, Piacentini M, Fimia GM, et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol 2013; 15:406-16; PMID:23524951; https://doi.org/10.1038/ncb2708
   PubMed Web of Science ®Google Scholar
• Jia G, Aroor AR, Martinez-Lemus LA, Sowers JR. Overnutrition, mTOR signaling, and cardiovascular diseases. Am J Physiol Regul Integr Comp Physiol 2014; 307:R1198-206; PMID:25253086; https://doi.org/10.1152/ajpregu.00262.2014
   PubMed Web of Science ®Google Scholar
• Cejka D, Hayer S, Niederreiter B, Sieghart W, Fuereder T, Zwerina J, Schett G. Mammalian target of rapamycin signaling is crucial for joint destruction in experimental arthritis and is activated in osteoclasts from patients with rheumatoid arthritis. Arthritis Rheum 2010; 62:2294-302; PMID:20506288; https://doi.org/10.1002/art.27504
   PubMed Web of Science ®Google Scholar
• Laudien M, Hasler R, Wohlers J, Bock J, Lipinski S, Bremer L, Podschun R, Ambrosch P, Lamprecht P, Rosenstiel P, et al. Molecular signatures of a disturbed nasal barrier function in the primary tissue of Wegener's granulomatosis. Mucosal Immunol 2011; 4:564-73; PMID:21412229; https://doi.org/10.1038/mi.2011.9
   PubMed Web of Science ®Google Scholar
• Karki R, Man SM, Malireddi RK, Gurung P, Vogel P, Lamkanfi M, Kanneganti TD. Concerted Activation of the AIM2 and NLRP3 Inflammasomes Orchestrates Host Protection against Aspergillus Infection. Cell host & microbe 2015; 17:357-68; https://doi.org/10.1016/j.chom.2015.01.006
   PubMed Web of Science ®Google Scholar
• Zhu Q, Man SM, Gurung P, Liu Z, Vogel P, Lamkanfi M, Kanneganti TD. Cutting edge: STING mediates protection against colorectal tumorigenesis by governing the magnitude of intestinal infla.mmation. J Immunol 2014; 193:4779-82; PMID:25320273; https://doi.org/10.4049/jimmunol.1402051
   PubMed Web of Science ®Google Scholar