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Original Research

NEAT1 paraspeckle promotes human hepatocellular carcinoma progression by strengthening IL-6/STAT3 signaling

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Article: e1503913 | Received 30 May 2018, Accepted 20 Jul 2018, Published online: 06 Aug 2018

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018 Jan;68(1):7–30. doi:10.3322/caac.21442. Epub 2018 Jan 4. PubMed PMID: 29313949.
  • Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M. Gender disparity in liver cancer due to sex differences in Myd88-dependent IL-6 production. Science. 2007;37(5834):121–124. PMID:17615358. doi:10.1126/science.1140485
  • Bergmann J, Muller M, Baumann N, Reichert M, Heneweer C, Bolik J, Lucke K, Gruber S, Carambia A, Boretius S, et al. IL-6 trans-signaling is essential for the development of hepatocellular carcinoma in mice. Hepatology 2017. 2017;65(1):89–103. PMID:27770462. doi:10.1002/hep.28874
  • Wan S, Zhao E, Kryczek I, Vatan L, Sadovskaya A, Ludema G, Simeone DM, Zou W, Welling TH. Tumor-associated macrophages produce interleukin 6 and signal via STAT3 to promote expansion of human hepatocellular carcinoma stem cells. Gastroenterology. 2014;147(6):1393–1404. PMID:25181692. doi:10.1053/j.gastro.2014.08039
  • Lee H, Herrmann A, Deng JH, Kujawski M, Niu G, Li Z, Forman S, Jove R, Pardoll DM, Yu H. Persistently activated Stat3 maintains constitutive NF-kappaB activity in tumors. Cancer Cell. 2009;15:283–293. PMID:19345327. doi:10.1016/j.ccr.2009.02.015
  • Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell JE Jr. Stat3 as an oncogene. Cell. 1999;98:295–303. PMID:10458605.
  • Lesina M, Kurkowski MU, Ludes K, Rose-John S, Treiber M, Kloppel G, Yoshimura A, Reindl W, Sipos B, Akira S. Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer. Cancer Cell. 2011;19:456–469. PMID:21481788. doi:10.1016/j.ccr.2011.03.009
  • Fukuda A, Wang SC, Morris JP 4th, Folias AE, Liou A, Kim GE, Akira S, Boucher KM, Firpo MA, Mulvihill SJ, et al. Stat3 and MMP7 contribute to pancreatic ductal adenocarcinoma initiation and progression. Cancer Cell. 2011;19:441–455. PMID:21481787. j.ccr.2011.03.002.
  • Yang X, Liang L, Zhang XF, Jia HL, Qin Y, Zhu XC, Gao XM, Qiao P, Zheng Y, Sheng YY, et al. MicroRNA-26a suppresses tumor growth and metastasis of human hepatocellular carcinoma by targeting interleukin-6-Stat3 pathway. Hepatology. 2013;58(1):158–170. PMID:23398948. doi:10.1002/hep.26305
  • Wang H, Su X, Yang M, Chen T, Hou J, Li N, Cao X. Reciprocal control of miR-197 and IL-6/STAT3 pathway reveals miR-197 as potential therapeutic target for hepatocellular carcinoma. Oncoimmunology. 2015;4(6):e1031440. PMID:26451302. doi:10.1080/2162402X.2015.1008371
  • Khorkova O, Hsiao J, Wahlestedt C. Basic biology and therapeutic implications of lncRNA. Adv Drug Deliv Rev. 2015;87:15–24. PMID:26024979. doi:10.1016/j.addr.2015.05012
  • Hou J, Lin L, Zhou W, Wang Z, Ding G, Dong Q, Qin L, Wu X, Zheng Y, Yang Y, et al. Identification of miRNomes in human liver and hepatocellular carcinoma reveals miR-199a/b-3p as therapeutic target for hepatocellular carcinoma. Cancer Cell. 2011;19(2):232–243. PMID:21316602. doi:10.1016/j.ccr.2011.01.001
  • Li Z, Zhang J, Liu X, Li S, Wang Q, Chen D, Hu Z, Yu T, Ding J, Li J, et al. The LINC01138 drives malignancies via activating arginine methyltransferase 5 in hepatocellular carcinoma. Nat Commun. 2018;20:9(1):1572. PMID:29679004. doi:10.1038/s41467-018-04006-0
  • Yuan JH, Liu XN, Wang TT, Pan W, Tao GF, Zhou WP, Wang F, Sun SH. The MBNL3 splicing factor promotes hepatocellular carcinoma by increasing PXN expression through the alternative splicing of lncRNA-PXN-AS1. Nat Cell Biol. 2017;19(7):820–832. PMID:28553938. doi:10.1038/ncb3538
  • Wong CM, Tsang FH, Ng IO. Non-coding RNAs in hepatocellular carcinoma: molecular functions and pathological implications. Nat Rev Gastroenterol Hepatol. 2018;15(3):137–151. PMID:29317776. doi:10.1038/nrgastro.2017.169
  • Klingenberg M, Matsuda A, Diederichs PT. Non-coding RNA in hepatocellular carcinoma: mechanisms, biomarkers and therapeutic targets. J Hepatol. 2017;67(3):603–618. PMID:28438689. doi:10.1016/j.jhep.2017.04.009
  • Wang Y, He L, Du Y, Huang G, Luo J, Yan X, Ye B, Li C, Xia P, Zhang G, et al. The long noncoding RNA lncTCF7 promotes self-renewal of human liver cancer stem cells through activation of Wnt signaling. Cell Stem Cell. 2015;16(4):413–425. PMID:25842979. doi:10.1016/j.stem.2015.03.003
  • Yuan JH, Yang F, Wang F, Ma JZ, Guo YJ, Tao QF, Liu F, Pan W, Wang TT, Zhou CC, et al. A long noncoding RNA activated by TGF-β promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell. 2014;25(5):666–681. PMID:24768205. doi:10.1016/j.ccr.2014.03.010
  • Zhu P, Wang Y, Huang G, Ye B, Liu B, Wu J, Du Y, He L, Fan Z. lnc-β-Catm elicits EZH2-dependent β-catenin stabilization and sustains liver CSC self-renewal. Nat Struct Mol Biol. 2016;23(7):631–639. PMID:27239797. doi:10.1038/nsmb.3235
  • Chen ZZ, Huang L, Wu YH, Zhai WJ, Zhu PP, Gao YF. LncSox4 promotes the self-renewal of liver tumour-initiating cells through Stat3-mediated Sox4 expression. Nat Commun. 2016;7:12598. PMID:27553854. doi:10.1038/ncomms12598
  • Naganuma T, Nakagawa S, Tanigawa A, Sasaki YF, Goshima N, Hirose T. Alternative 3ʹ-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J. 2012;31(20):4020–4034. PMID:22960638. doi:10.1038/emboj.2012.251
  • Naganuma T, Hirose T. Paraspeckle formation during the biogensis of long non-coding RNAs. RNA Biol. 2013;10(3):456–461. PMID:23324609. doi:10.4161/rna.23547
  • Fox AH, Bond CS, Lamond AI. P54nrb forms a heterodimer with PSP1 that localizes to paraspeckles in an RNA-dependent manner. Mol Biol Cell. 2005;16:5304–5315. PMID:16148043. doi:10.1091/mbc.E05-06-0587
  • West JA, Mito M, Kurosaka S, Takumi T, Tanegashima C, Chujo T, Yanaka K, Kingston RE, Hirose T, Bond C, et al. Structural, super-resolution microscopy analysis of paraspeckle nuclear body organization. J Cell Biol. 2016;214(7):817–830. PMID:27646274. doi:10.1083/jcb.201601071
  • Chen LL, Carmichael GG. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: functional role of a nuclear noncoding RNA. Mol Cell. 2009;35(4):467–478. PMID:19716791. doi:10.1016/j.molcel.2009.06.027
  • Imamura K, Imamachi N, Akizuki G, Kumakura M, Kawaguchi A, Nagata K, Kato A, Kawaguchi Y, Sato H, Yoneda M, et al. Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol Cell. 2014;53(3):393–406. PMID:24507715. doi:10.1016/j.molcel.2014.01.009
  • Sasaki YT, Ideue T, Sano M, Mituyama T, Hirose T. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci U S A. 2009;106(8):2525–2530. PMID:19188602. doi:10.1073/pnas.0807899106
  • Li R, Harvey AR, Hodgetts SI, Fox AH. Functional dissection of NEAT1 using genome editing reveals substantial localization of the NEAT1_1 isoform outside paraspeckles. RNA. 2017;23(6):872–881. PMID:28325845. doi:10.1261/rna.059477.116
  • Jiang L, Shao C, Qj W, Chen G, Zhou J, Yang B, Li H, Gou LT, Zhang Y, Wang Y, et al. NEAT1 scaffolds RNA-binding proteins and the microprocessor to globally enhance pri-miRNA processing. Nat Struct Mol Biol. 2017;24(10):816–824. PMID:28846091. doi:10.1038/nsmb.3455
  • Lee CJ, Evans J, Kim K, Chae H, Kim S. Determining the effect of DNA methylation on gene expression in cancer cells. Methods Mol Biol. 2014;1101:161–178. PMID:24233782. doi:10.1007/978-1-62703-1_9
  • Zhao S, Zhong Y, Fu X, Wang Y, Ye P, Cai J, Liu Y, Sun J, Mei Z, Jiang Y, et al. H3K4 methylation regulates LPS-induced proinflammatory cytokine expression and release in macrophages. Shock. 2018. [Epub ahead of print. PMID:29570119. doi:10.1097/SHK.0000000000001141.
  • Krishnan S, Horowitz S, Trievel RC. Structure and function of histone H3 lysine 9 methyltransferases and demethylases. Chembiochem. 2011;12(2):254–263. PMID:21243713. cbic.201000545.
  • Wang Z, Fan P, Zhao Y, Zhang S, Lu J, Xie W, Jiang Y, Lei F, Xu N, Zhang Y. NEAT1 modulates herpes simplex virus-1 replication by regulating viral gene transcription. Cell Mol Life Sci. 2017;74(6):1117–1131. PMID:27783096. doi:10.1007/s00018-016-2398-4
  • Anantharaman A, Jadaliha M, Tripathi V, Nakagawa S, Hirose T, Jantsch MF, Prasanth SG, Prasanth KV. Paraspeckles modulate the intranuclear distribution of paraspeckle-associated Ctn RNA. Sci Rep. 2016;6:34043. PMID:27665741. doi:10.1038/srep34043
  • Kanwal R, Pandey M, Bhaskaran N, Maclennan GT, Fu P, Ponsky LE, Gupta S. Protection against oxidative DNA damage and stress in human prostate by glutathione S-transferasse P1. Mol Carcinog. 2014;53(1):8–18. PMID:22833520. doi:10.1002/mc.21939
  • MacLennan GT, Eisenberg R, Fleshman RL, Taylor JM, Fu P, Resnick MI, Gupta S. The influence of chronic inflammation in prostatic carcinogenesis: a 5-year followup study. J Urol. 2006;176(3):1012–1016. PMID:16890681. j.juro.2006.04.033.
  • Tu J, Zhao Z, Xu M, Lu X, Chang L, Ji J. NEAT1 upregulates TGF-β1 to induce hepatocellular carcinoma progression by sponging has-mir-139-5p. J Cell Physiol. 2018. Epub ahead of print. PMID:29797561. doi:10.1002/jcp.26524
  • Choi HI, Ma SK, Bae EH, Lee J, Kim SW. Peroxiredoxin 5 protects TGF-β induced fibrosis by inhibiting Stat3 activation in rat kidney interstitial fibroblast cells. PloS One. 2016;11(2):e0149266. PMID:26872211. doi:10.1371/journal.pone.0149266
  • Mowel WK, Kotzin JJ, McCright SJ, Neal VD, Henao-Mejia J. Control of immune cells homeostasis and function by lncRNAs. Trends Immunol. 2018;39(1):55–69. PMID:28919048. doi:10.1016/j.it.2017.08.009
  • Liu X, Liang Y, Song R, Yang G, Han J, Lan Y, Pan S, Zhu M, Liu Y, Wang Y, et al. Long non-coding RNA NEAT1-modulated abnormal lipolysis via ATGL drives hepatocellular carcinoma proliferation. Mol Cancer. 2018;17(1):90. PMID:29764424. doi:10.1186/s12943-018-0838-5
  • Zheng X, Zhang Y, Liu Y, Fang L, Li L, Sun J, Pan Z, Xin W, Huang P. HIF-2α activated lncRNA NEAT1 promotes hepatocellular carcinoma cells invasion and metastasis by affecting the epithelial-mesenchymal transition. J Cell Biochem. 2018;119(4):3247–3256. PMID:29091312. doi:10.1002/jcb.26481
  • Guo S, Chen W, Luo Y, Ren F, Zhong T, Rong M, Dang Y, Feng Z, Chen G. Clinical implication of long non-coding RNA NEAT1 expression in hepatocellular carcinoma patients. Int J Clin Exp Pathol. 2015;8(5):5395–5402. PMID:26191242. eCollection2015.
  • Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumors, immune cells and microorganisms. Nat Rev Cancer. 2013;13(11):759–771. PMID:24154716. doi:10.1038/nrc3611
  • He G, Karin M. NF-kB and STAT3 – key players in liver inflammation and cancer. Cell Res. 2011;21(1):159–168. PMID:21187858. doi:10.1038/cr.2010.183
  • Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, Chess A, Lawrence JB. An architectural role for a nuclear noncoding RNA, NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell. 2009;33:717–726. PMID:19217333. doi:10.1016/j.molcel.2009.01.026
  • Yamazaki T, Hirose T. The building process of the functional paraspeckle with long non-coding RNAs. Front Biosci(Elite Ed). 2015;1(7):1–41. PMID:25553361.
  • Prasanth KV, Prasanth SG, Xuan Z, Hearn S, Freier SM, Bennett CF, Zhang MQ, Spector DL. Regulating gene expression through RNA nuclear retention. Cell. 2005;123:249–263. PMID:16239143. doi:10.1016/j.cell.2005.08.033
  • Hirose T, Virnicchi G, Tanigawa A, Naganuma T, Li R, Kimura H, Yokoi T, Nakagawa S, Benard M, Fox AH, et al. NEAT1 long noncoding RNA regulates transcription via protein sequestration within subnuclear bodies. Mol Biol Cell. 2014;25:169–183. PMID:24173718. doi:10.1091/mbc.E13-09-0558
  • Yu H, Lee H, Herrmann A, Buettner R, JoveR. Revisiting STAT3 signalling in cancer: new and unexpected biological functions. Nat Rev Cancer. 2014;14:736–746. PMID:25342631. doi:10.1038/nrc3818
  • Morchikh M, Cribier A, Raffel R, Amraoui S, Cau J, Severac D, Dubois E, Schwartz O, Bennasser Y, Benkirane M. HEXM1 and NEAT1 long non-coding RNA form a muti-subunit complex that regulates DNA-mediated innate immune response. Mol Cell. 2017;67(3):387–399. PMID:28712728. doi:10.1016/j.molcel.2017.06.020
  • Schnekenburger M, Karius T, Diederich M. Regulation of epigenetic traits of the glutathione S-transferase P1 gene: from detoxification toward cancer prevention and diagnosis. Front Pharmacol. 2014;16(5):170. PMID:25076909. doi:10.3389/fphar.2014.00170
  • Zhong S, Tang MW, Yeo W, Liu C, Lo YM, Johnson PJ. Silencing of GSTP1 gene by CpG island DNA hypermethylation in HBV-associated hepatocellular carcinomas. Clin Cancer Res. 2002;8(4):1087–1092. PMID:11948118.
  • Ruscoe JE, Rosario LA, Wang T, Gate L, Arifoglu P, Wolf CR, Henderson CJ, Ronai Z, Tew KD. Pharmacologic or genetic manipulation of glutathione S-transferase P1-1 (GSTpi) influences cell proliferation pathways. J Pharmacol Exp Ther. 2011;298:339–345. PMID:11408560.
  • Wu Y, Fan Y, Xue B, Luo L, Shen J, Zhang S, Jiang Y, Yin Z. Human glutathione S-transferase P1-1 interacts with TRAF2 and regulates TRAF2-ASK1 signals. Oncogene. 2006;25(42):5787–5800. PMID:16636664. sj.onc.1209576.
  • Kong KH, Takasu K, Inoue H, Takahashi K. Tyrosine-7 in human class Pi glutathione S-transferase is important for lowering the pKa of the thiol group of glutathione in the enzyme-glutathione complex. Biochem Biophys Res Commun. 1992;184(1):194–197. PMID:1567427.
  • Kou X, Chen N, Feng Z, Luo L, Yin Z. GSTP1 negatively regulates Stat3 activation in epidermal growth factor signaling. Oncol Lett. 2013;5(3):1053–1057. PMID:2346146. doi:10.3892/ol.2012.1098
  • Wang C, Wang Q, Xu X, Xie B, Zhao Y, Li N, Cao X. The methyltransferase NSD3 promotes antiviral innate immunity via direct lysine methylation of IRF3. J Exp Med. 2017;214(12):3597–3610. PMID:29101251. doi:10.1084/jem.20170856
  • Wang P, Xu J, Wang Y, Cao X. An interferon-independent lncRNA promotes viral replication by modulating cellular metabolism. Science. 2017;24;358(6366):1051–1055. PMID:29074580. doi:10.1126/science.aao0409

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