Myc-Associated Zinc Finger Protein Regulates the Proinflammatory Response in Colitis and Colon Cancer via STAT3 Signaling

REFERENCES

• Reference deleted.
   Google Scholar
• Terzić J, Grivennikov S, Karin E, Karin M. 2010. Inflammation and colon cancer. Gastroenterology 138:2101–2114. https://doi.org/10.1053/j.gastro.2010.01.058.
   PubMed Web of Science ®Google Scholar
• Ray A, Kumar D, Shakya A, Brown CR, Cook JL, Ray BK. 2004. Serum amyloid A-activating factor-1 (SAF-1) transgenic mice are prone to develop a severe form of inflammation-induced arthritis. J Immunol 173:4684. https://doi.org/10.4049/jimmunol.173.7.4684.
   PubMed Web of Science ®Google Scholar
• Luo W, Zhu X, Liu W, Ren Y, Bei C, Qin L, Miao X, Tang F, Tang G, Tan S. 2016. MYC associated zinc finger protein promotes the invasion and metastasis of hepatocellular carcinoma by inducing epithelial mesenchymal transition. Oncotarget 7:86420–86432. https://doi.org/10.18632/oncotarget.11346.
   PubMedGoogle Scholar
• Jiao L, Li Y, Shen D, Xu C, Wang L, Huang G, Chen L, Yang Y, Yang C, Yu Y, Sun Y. 2013. The prostate cancer-up-regulated myc-associated zinc-finger protein (MAZ) modulates proliferation and metastasis through reciprocal regulation of androgen receptor. Medical Oncol 30:570. https://doi.org/10.1007/s12032-013-0570-3.
   PubMed Web of Science ®Google Scholar
• Zhu X, Luo W, Liang W, Tang F, Bei C, Ren Y, Qin L, Tan C, Zhang Y, Tan S. 2016. Overexpression and clinical significance of MYC-associated zinc finger protein in pancreatic carcinoma. OncoTargets Ther 9:7493–7501. https://doi.org/10.2147/OTT.S124118.
   PubMed Web of Science ®Google Scholar
• Ray A, Dhar S, Ray BK. 2011. Control of VEGF expression in triple-negative breast carcinoma cells by suppression of SAF-1 transcription Factor activity. Mol Cancer Res 9:1030. https://doi.org/10.1158/1541-7786.MCR-10-0598.
   PubMedGoogle Scholar
• Ray BK, Murphy R, Ray P, Ray A. 2002. SAF-2, a splice variant of SAF-1, acts as a negative regulator of transcription. J Biol Chem 277:46822–46830. https://doi.org/10.1074/jbc.M206299200.
   PubMedGoogle Scholar
• Ray A, Dhar S, Shakya A, Ray P, Okada Y, Ray BK. 2009. SAF-3, a novel splice variant of the SAF-1/MAZ/Pur-1 family, is expressed during inflammation. FEBS J 276:4276–4286. https://doi.org/10.1111/j.1742-4658.2009.07136.x.
   PubMedGoogle Scholar
• Triner D, Xue X, Schwartz AJ, Jung I, Colacino JA, Shah YM. 2017. Epithelial hypoxia-inducible factor 2α facilitates the progression of colon tumors through recruiting neutrophils. Mol Cell Biol 37:e00481-16. https://doi.org/10.1128/MCB.00481-16.
   Google Scholar
• Xue X, Ramakrishnan S, Anderson E, Taylor M, Zimmermann EM, Spence JR, Huang S, Greenson JK, Shah YM. 2013. Endothelial PAS domain protein 1 activates the inflammatory response in the intestinal epithelium to promote colitis in mice. Gastroenterology 145:831–841. https://doi.org/10.1053/j.gastro.2013.07.010.
   PubMedGoogle Scholar
• Xie L, Xue X, Taylor M, Ramakrishnan SK, Nagaoka K, Hao C, Gonzalez FJ, Shah YM. 2014. Hypoxia-inducible factor/MAZ-dependent induction of caveolin-1 regulates colon permeability through suppression of occludin, leading to hypoxia-induced inflammation. Mol Cell Biol 34:3013–3023. https://doi.org/10.1128/MCB.00324-14.
   PubMedGoogle Scholar
• Yu H, Pardoll D, Jove R. 2009. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9:798. https://doi.org/10.1038/nrc2734.
   PubMed Web of Science ®Google Scholar
• Dang EV, Barbi J, Yang H-Y, Jinasena D, Yu H, Zheng Y, Bordman Z, Fu J, Kim Y, Yen H-R, Luo W, Zeller K, Shimoda L, Topalian SL, Semenza GL, Dang CV, Pardoll DM, Pan F. 2011. Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell 146:772–784. https://doi.org/10.1016/j.cell.2011.07.033.
   PubMed Web of Science ®Google Scholar
• Pickert G, Neufert C, Leppkes M, Zheng Y, Wittkopf N, Warntjen M, Lehr H-A, Hirth S, Weigmann B, Wirtz S, Ouyang W, Neurath MF, Becker C. 2009. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 206:1465–1472. https://doi.org/10.1084/jem.20082683.
   PubMed Web of Science ®Google Scholar
• Liu JZ, van Sommeren S, Huang H, Ng SC, Alberts R, Takahashi A, Ripke S, Lee JC, Jostins L, Shah T, Abedian S, Cheon JH, Cho J, Dayani NE, Franke L, Fuyuno Y, Hart A, Juyal RC, Juyal G, Kim WH, Morris AP, Poustchi H, Newman WG, Midha V, Orchard TR, Vahedi H, Sood A, Sung JY, Malekzadeh R, Westra H-J, Yamazaki K, Yang S-K, The International Multiple Sclerosis Genetics Committee, The International IBD Genetics Consortium, Barrett JC, Alizadeh BZ, Parkes M, Bk T, Daly MJ, Kubo M, Anderson CA, Weersma RK. 2015. Association analyses identify 38 susceptibility loci for inflammatory bowel disease and highlight shared genetic risk across populations. Nat Genet 47:979–986. https://doi.org/10.1038/ng.3359.
   PubMed Web of Science ®Google Scholar
• Bollrath J, Phesse TJ, von Burstin VA, Putoczki T, Bennecke M, Bateman T, Nebelsiek T, Lundgren-May T, Canli Ö, Schwitalla S, Matthews V, Schmid RM, Kirchner T, Arkan MC, Ernst M, Greten FR. 2009. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell cycle progression during colitis-associated tumorigenesis. Cancer Cell 15:91–102. https://doi.org/10.1016/j.ccr.2009.01.002.
   PubMed Web of Science ®Google Scholar
• Grivennikov S, Karin E, Terzic J, Mucida D, Yu G-Y, Vallabhapurapu S, Scheller J, Rose-John S, Cheroutre H, Eckmann L, Karin M. 2009. IL-6 and STAT3 are required for survival of intestinal epithelial cells and development of colitis associated cancer. Cancer Cell 15:103–113. https://doi.org/10.1016/j.ccr.2009.01.001.
   PubMed Web of Science ®Google Scholar
• Kesselring R, Glaesner J, Hiergeist A, Naschberger E, Neumann H, Brunner SM, Wege AK, Seebauer C, Köhl G, Merkl S, Croner RS, Hackl C, Stürzl M, Neurath MF, Gessner A, Schlitt H-J, Geissler EK, Fichtner-Feigl S. 2016. IRAK-M expression in tumor cells supports colorectal cancer progression through reduction of antimicrobial defense and stabilization of STAT3. Cancer Cell 29:684–696. https://doi.org/10.1016/j.ccell.2016.03.014.
   PubMed Web of Science ®Google Scholar
• Suzuki A, Hanada T, Mitsuyama K, Yoshida T, Kamizono S, Hoshino T, Kubo M, Yamashita A, Okabe M, Takeda K, Akira S, Matsumoto S, Toyonaga A, Sata M, Yoshimura A. 2001. Cis3/Socs3/Ssi3 plays a negative regulatory role in Stat3 activation and intestinal inflammation. J Exp Med 193:471–482. https://doi.org/10.1084/jem.193.4.471.
   PubMed Web of Science ®Google Scholar
• Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. 2002. cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem 277:33275–33283. https://doi.org/10.1074/jbc.M204935200.
   PubMed Web of Science ®Google Scholar
• Matsuoka K, Kanai T. 2015. The gut microbiota and inflammatory bowel disease. Semin Immunopathol 37:47–55. https://doi.org/10.1007/s00281-014-0454-4.
   PubMed Web of Science ®Google Scholar
• Ray BK, Ray A. 1997. Involvement of an SAF-like transcription factor in the activation of serum amyloid A gene in monocyte/macrophage cells by lipopolysaccharide. Biochemistry 36:4662–4668. https://doi.org/10.1021/bi9624595.
   PubMedGoogle Scholar
• Barthel M, Hapfelmeier S, Quintanilla-Martínez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Rüssmann H, Hardt W-D. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71:2839–2858. https://doi.org/10.1128/IAI.71.5.2839-2858.2003.
   PubMed Web of Science ®Google Scholar
• Koroleva EP, Halperin S, Gubernatorova EO, Macho-Fernandez E, Spencer CM, Tumanov AV. 2015. Citrobacter rodentium-induced colitis: a robust model to study mucosal immune responses in the gut. J Immunol Methods 421:61–72. https://doi.org/10.1016/j.jim.2015.02.003.
   PubMed Web of Science ®Google Scholar
• Triner D, Shah YM. 2016. Hypoxia-inducible factors: a central link between inflammation and cancer. J Clin Invest 126:3689–3698. https://doi.org/10.1172/JCI84430.
   PubMed Web of Science ®Google Scholar
• Robertis MD, Massi E, Poeta ML, Carotti S, Morini S, Cecchetelli L, Signori E, Fazio VM. 2011. The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies. J Carcinog 10:9. https://doi.org/10.4103/1477-3163.78279.
   PubMedGoogle Scholar
• Dame MK, Jiang Y, Appelman HD, Copley KD, McClintock SD, Aslam MN, Attili D, Elmunzer BJ, Brenner DE, Varani J, Turgeon DK. 2014. Human colonic crypts in culture: segregation of immunochemical markers in normal versus adenoma-derived. Lab Invest 94:222–234. https://doi.org/10.1038/labinvest.2013.145.
   PubMedGoogle Scholar
• Phesse TJ, Buchert M, Stuart E, Flanagan DJ, Faux M, Afshar-Sterle S, Walker F, Zhang H-H, Nowell CJ, Jorissen R, Tan CW, Hirokawa Y, Eissmann MF, Poh AR, Malaterre J, Pearson HB, Kirsch DG, Provero P, Poli V, Ramsay RG, Sieber O, Burgess AW, Huszar D, Vincan E, Ernst M. 2014. Partial inhibition of gp130-Jak-Stat3 signaling prevents Wnt–β-catenin-mediated intestinal tumor growth and regeneration. Sci Signal 7:ra92. https://doi.org/10.1126/scisignal.2005411.
   PubMed Web of Science ®Google Scholar
• Putoczki TL, Thiem S, Loving A, Busuttil RA, Wilson NJ, Ziegler Paul K, Nguyen PM, Preaudet A, Farid R, Edwards KM, Boglev Y, Luwor RB, Jarnicki A, Horst D, Boussioutas A, Heath JK, Sieber OM, Pleines I, Kile BT, Nash A, Greten FR, McKenzie BS, Ernst M. 2013. Interleukin-11 is the dominant IL-6 family cytokine during gastrointestinal tumorigenesis and can be targeted therapeutically. Cancer Cell 24:257–271. https://doi.org/10.1016/j.ccr.2013.06.017.
   PubMed Web of Science ®Google Scholar
• Lu R, Wu S, Zhang Y-g, Xia Y, Zhou Z, Kato I, Dong H, Bissonnette M, Sun J. 2016. Salmonella protein AvrA activates the STAT3 signaling pathway in colon cancer. Neoplasia 18:307–316. https://doi.org/10.1016/j.neo.2016.04.001.
   PubMed Web of Science ®Google Scholar
• Yu H, Lee H, Herrmann A, Buettner R, Jove R. 2014. Revisiting STAT3 signaling in cancer: new and unexpected biological functions. Nat Rev Cancer 14:736. https://doi.org/10.1038/nrc3818.
   PubMed Web of Science ®Google Scholar
• Bossone SA, Asselin C, Patel AJ, Marcu KB. 1992. MAZ, a zinc finger protein, binds to c-MYC and C2 gene sequences regulating transcriptional initiation and termination. Proc Natl Acad Sci U S A 89:7452. https://doi.org/10.1073/pnas.89.16.7452.
   PubMed Web of Science ®Google Scholar
• Ray A, Bal BS, Ray BK. 2005. Transcriptional induction of matrix metalloproteinase-9 in the chondrocyte and synoviocyte cells is regulated via a novel mechanism: evidence for functional cooperation between serum amyloid A-activating factor-1 and AP-1. J Immunol 175:4039. https://doi.org/10.4049/jimmunol.175.6.4039.
   PubMedGoogle Scholar
• Ray A, Kuroki K, Cook JL, Bal BS, Kenter K, Aust G, Ray BK. 2003. Induction of matrix metalloproteinase 1 gene expression is regulated by inflammation-responsive transcription factor SAF-1 in osteoarthritis. Arthritis Rheum 48:134–145. https://doi.org/10.1002/art.10706.
   PubMedGoogle Scholar
• Ray A, Shakya A, Kumar D, Benson MD, Ray BK. 2006. Inflammation-responsive transcription factor SAF-1 activity is linked to the development of amyloid A amyloidosis. J Immunol 177:2601. https://doi.org/10.4049/jimmunol.177.4.2601.
   PubMedGoogle Scholar
• Ray A, Yu G-Y, Ray BK. 2002. Cytokine-responsive induction of SAF-1 activity is mediated by a mitogen-activated protein kinase signaling pathway. Mol Cell Biol 22:1027–1035. https://doi.org/10.1128/MCB.22.4.1027-1035.2002.
   PubMedGoogle Scholar
• Ray BK, Ray A. 1997. Induction of serum amyloid A (SAA) gene by SAA-activating sequence-binding factor (SAF) in monocyte/macrophage cells: evidence for a functional synergy between SAF and Sp1. J Biol Chem 272:28948–28953. https://doi.org/10.1074/jbc.272.46.28948.
   PubMedGoogle Scholar
• Ray A, Fields AP, Ray BK. 2000. Activation of transcription factor SAF involves its phosphorylation by protein kinase C. J Biol Chem 275:39727–39733. https://doi.org/10.1074/jbc.M007907200.
   PubMedGoogle Scholar
• Sears CL, Garrett WS. 2014. Microbes, microbiota and colon cancer. Cell Host Microbe 15:317–328. https://doi.org/10.1016/j.chom.2014.02.007.
   PubMed Web of Science ®Google Scholar
• Ray A, Ray BK. 2015. Induction of Ras by SAF-1/MAZ through a feed-forward loop promotes angiogenesis in breast cancer. Cancer Med 4:224–234. https://doi.org/10.1002/cam4.362.
   PubMed Web of Science ®Google Scholar
• Cogoi S, Zorzet S, Rapozzi V, Géci I, Pedersen EB, Xodo LE. 2013. MAZ-binding G4-decoy with locked nucleic acid and twisted intercalating nucleic acid modifications suppresses KRAS in pancreatic cancer cells and delays tumor growth in mice. Nucleic Acids Res 41:4049–4064. https://doi.org/10.1093/nar/gkt127.
   PubMedGoogle Scholar
• Miglietta G, Gouda AS, Cogoi S, Pedersen EB, Xodo LE. 2015. Nucleic acid targeted therapy: G4 oligonucleotides downregulate HRAS in bladder cancer cells through a decoy mechanism. ACS Med Chem Lett 6:1179–1183. https://doi.org/10.1021/acsmedchemlett.5b00315.
   PubMedGoogle Scholar
• Xue X, Ramakrishnan SK, Weisz K, Triner D, Xie L, Attili D, Pant A, Győrffy B, Zhan M, Carter-Su C, Hardiman KM, Wang TD, Dame MK, Varani J, Brenner D, Fearon ER, Shah YM. 2016. Iron uptake via DMT1 integrates cell cycle with JAK-STAT3 signaling to promote colorectal tumorigenesis. Cell Metab 24:447–461. https://doi.org/10.1016/j.cmet.2016.07.015.
   PubMed Web of Science ®Google Scholar
• Maity G, Haque I, Ghosh A, Dhar G, Gupta VG, Sarkar S, Azeem I, McGregor D, Choudhary A, Campbell DR, Kambhampati S, Banerjee SK, Banerjee S. 2018. The MAZ transcription factor is a downstream target of the oncoprotein Cyr61/CCN1 and promotes pancreatic cancer cell invasion via CRAF–ERK signaling. J Biol Chem 293:4334–4349. https://doi.org/10.1074/jbc.RA117.000333.
   PubMedGoogle Scholar
• Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V, Skrzypek E. 2015. PhosphoSitePlus, 2014: mutations, PTMs, and recalibrations. Nucleic Acids Res 43:D512–D520. https://doi.org/10.1093/nar/gku1267.
   PubMed Web of Science ®Google Scholar
• Zeng MY, Cisalpino D, Varadarajan S, Hellman J, Warren HS, Cascalho M, Inohara N, Núñez G. 2016. Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 44:647–658. https://doi.org/10.1016/j.immuni.2016.02.006.
   PubMed Web of Science ®Google Scholar
• Xue X, Shah YM. 2013. Hypoxia-inducible factor-2α is essential in activating the COX2/mPGES-1/PGE2 signaling axis in colon cancer. Carcinogenesis 34:163–169. https://doi.org/10.1093/carcin/bgs313.
   PubMed Web of Science ®Google Scholar
• Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. https://doi.org/10.1093/bioinformatics/bts635.
   PubMed Web of Science ®Google Scholar