Matrin-3 acts as a potential biomarker and promotes hepatocellular carcinoma progression by interacting with cell cycle-regulating genes

References

• Villanueva A, Longo DL. Hepatocellular carcinoma. N Engl J Med. 2019;380(15):1450–1462. doi: 10.1056/NEJMra1713263
   PubMed Web of Science ®Google Scholar
• Llovet JM, Kelley RK, Villanueva A, et al. Hepatocellular carcinoma. Nat Rev Dis Primers. 2021;7(1):6. doi: 10.1038/s41572-020-00240-3
   PubMed Web of Science ®Google Scholar
• Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/caac.21660
   PubMed Web of Science ®Google Scholar
• Huber TC, Bochnakova T, Koethe Y, et al. Percutaneous therapies for hepatocellular carcinoma: evolution of liver directed therapies. J Hepatocell Carcinoma. 2021;8:1181–1193. doi: 10.2147/JHC.S268300
   PubMed Web of Science ®Google Scholar
• Koulouris A, Tsagkaris C, Spyrou V, et al. Hepatocellular carcinoma: an overview of the changing landscape of treatment options. J Hepatocell Carcinoma. 2021;8:387–401. doi: 10.2147/JHC.S300182
   PubMed Web of Science ®Google Scholar
• Yuen MF, Cheng CC, Lauder IJ, et al. Early detection of hepatocellular carcinoma increases the chance of treatment: Hong Kong experience. Hepatology. 2000;31(2):330–335. doi: 10.1002/hep.510310211
   PubMed Web of Science ®Google Scholar
• Slotta JE, Kollmar O, Ellenrieder V, et al. Hepatocellular carcinoma: Surgeon’s view on latest findings and future perspectives. World J Hepatol. 2015;7(9):1168–1183. doi: 10.4254/wjh.v7.i9.1168
   PubMedGoogle Scholar
• Beretta L. Comparative analysis of the liver and plasma proteomes as a novel and powerful strategy for hepatocellular carcinoma biomarker discovery. Cancer Lett. 2009;286(1):134–139. doi: 10.1016/j.canlet.2009.01.025
   PubMed Web of Science ®Google Scholar
• Rizzo A, Ricci AD, Di Federico A, et al. Predictive biomarkers for checkpoint inhibitor-based immunotherapy in hepatocellular carcinoma: where do we stand? Front Oncol. 2021;11:803133. doi: 10.3389/fonc.2021.803133
   PubMed Web of Science ®Google Scholar
• Di Federico A, Rizzo A, Carloni R, et al. Atezolizumab-bevacizumab plus Y-90 TARE for the treatment of hepatocellular carcinoma: preclinical rationale and ongoing clinical trials. Expert Opin Investig Drugs. 2022;31(4):361–369. doi: 10.1080/13543784.2022.2009455
   PubMed Web of Science ®Google Scholar
• Rizzo A, Cusmai A, Gadaleta-Caldarola G, et al. Which role for predictors of response to immune checkpoint inhibitors in hepatocellular carcinoma? Expert Rev Gastroenterol Hepatol. 2022;16(4):333–339. doi: 10.1080/17474124.2022.2064273
   PubMed Web of Science ®Google Scholar
• Wan KM, Nickerson JA, Krockmalnic G, et al. The nuclear matrix prepared by amine modification. Proc Natl Acad Sci U S A. 1999;96(3):933–938. doi: 10.1073/pnas.96.3.933
   PubMed Web of Science ®Google Scholar
• Gerner C, Gotzmann J, Fröhwein U, et al. Proteome analysis of nuclear matrix proteins during apoptotic chromatin condensation. Cell Death Differ. 2002;9(6):671–681. doi: 10.1038/sj.cdd.4401010
   PubMed Web of Science ®Google Scholar
• Barboro P, Repaci E, D’Arrigo C, et al. The role of nuclear matrix proteins binding to matrix attachment regions (Mars) in prostate cancer cell differentiation. PLoS One. 2012;7(7):e40617. doi: 10.1371/journal.pone.0040617
   PubMed Web of Science ®Google Scholar
• Durślewicz J, Klimaszewska-Wiśniewska A, Jóźwicki J, et al. Prognostic significance of MATR3 in stage I and II non-small cell lung cancer patients. J Cancer Res Clin Oncol. 2022;148(12):3313–3322. doi: 10.1007/s00432-022-04097-9
   PubMed Web of Science ®Google Scholar
• Nakayasu H, Berezney R. Nuclear matrins: identification of the major nuclear matrix proteins. Proc Natl Acad Sci U S A. 1991;88(22):10312–10316. doi: 10.1073/pnas.88.22.10312
   PubMed Web of Science ®Google Scholar
• Johnson JO, Pioro EP, Boehringer A, et al. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat Neurosci. 2014;17(5):664–666. doi: 10.1038/nn.3688
   PubMed Web of Science ®Google Scholar
• Salton M, Lerenthal Y, Wang S-Y, et al. Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle. 2010;9(8):1568–1576. doi: 10.4161/cc.9.8.11298
   PubMed Web of Science ®Google Scholar
• Zhang Z, Carmichael GG. The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell. 2001;106(4):465–475. doi: 10.1016/S0092-8674(01)00466-4
   PubMed Web of Science ®Google Scholar
• Attig J, Agostini F, Gooding C, et al. Heteromeric RNP Assembly at LINEs controls lineage-specific RNA processing. Cell. 2018;174(5):1067–1081.e17. doi: 10.1016/j.cell.2018.07.001
   PubMed Web of Science ®Google Scholar
• Pollini D, Loffredo R, Maniscalco F, et al. Multilayer and MATR3-dependent regulation of mRnas maintains pluripotency in human induced pluripotent stem cells. iScience. 2021;24(3):102197. doi: 10.1016/j.isci.2021.102197
   PubMed Web of Science ®Google Scholar
• Sarracino A, Gharu L, Kula A, et al. Posttranscriptional regulation of HIV-1 gene expression during replication and reactivation from latency by nuclear matrix protein MATR3. MBio. 2018;9(6). doi: 10.1128/mBio.02158-18
   PubMed Web of Science ®Google Scholar
• Valencia CA, Ju W, Liu R. Matrin 3 is a Ca2+/calmodulin-binding protein cleaved by caspases. Biochem Biophys Res Commun. 2007;361(2):281–286. doi: 10.1016/j.bbrc.2007.06.156
   PubMed Web of Science ®Google Scholar
• Sun J, Bai J, Jiang T, et al. Modulation of PDCD1 exon 3 splicing. RNA Biol. 2019;16(12):1794–1805. doi: 10.1080/15476286.2019.1659080
   PubMed Web of Science ®Google Scholar
• Przygodzka P, Boncela J, Cierniewski CS. Matrin 3 as a key regulator of endothelial cell survival. Exp Cell Res. 2011;317(6):802–811. doi: 10.1016/j.yexcr.2010.12.009
   PubMed Web of Science ®Google Scholar
• Kuriyama H, Fukushima S, Kimura T, et al. Matrin-3 plays an important role in cell cycle and apoptosis for survival in malignant melanoma. J Dermatol Sci. 2020;100(2):110–119. doi: 10.1016/j.jdermsci.2020.08.013
   PubMed Web of Science ®Google Scholar
• Yang T-W, Sahu D, Chang Y-W, et al. RNA-Binding proteomics reveals MATR3 interacting with lncRNA SNHG1 to enhance neuroblastoma progression. J Proteome Res. 2019;18(1):406–416. doi: 10.1021/acs.jproteome.8b00693
   PubMed Web of Science ®Google Scholar
• Chaudhary R, Gryder B, Woods WS, et al. Prosurvival long noncoding RNA PINCR regulates a subset of p53 targets in human colorectal cancer cells by binding to matrin 3. Elife. 2017;6:6. doi: 10.7554/eLife.23244
   Web of Science ®Google Scholar
• Chandrashekar DS, Bashel B, Balasubramanya SAH, et al. UALCAN: a portal for facilitating tumor subgroup gene expression and survival analyses. Neoplasia. 2017;19(8):649–658. doi: 10.1016/j.neo.2017.05.002
   PubMed Web of Science ®Google Scholar
• Vasaikar SV, Straub P, Wang J, et al. LinkedOmics: analyzing multi-omics data within and across 32 cancer types. Nucleic Acids Res. 2018;46(D1):D956–D963. doi: 10.1093/nar/gkx1090
   PubMed Web of Science ®Google Scholar
• Zhou Y, Zhou B, Pache L, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10(1):1523. doi: 10.1038/s41467-019-09234-6
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Franceschini A, Wyder S, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447–D452. doi: 10.1093/nar/gku1003
   PubMed Web of Science ®Google Scholar
• Shannon P, Markiel A, Ozier O, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–2504. doi: 10.1101/gr.1239303
   PubMed Web of Science ®Google Scholar
• Tang Z, Li C, Kang B, et al. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 2017;45(W1):W98–W102. doi: 10.1093/nar/gkx247
   PubMed Web of Science ®Google Scholar
• Newman AM, Liu CL, Green MR, et al. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12(5):453–457. doi: 10.1038/nmeth.3337
   PubMed Web of Science ®Google Scholar
• Li T, Fan J, Wang B, et al. TIMER: a web server for comprehensive analysis of tumor-infiltrating immune cells. Cancer Res. 2017;77(21):e108–e110. doi: 10.1158/0008-5472.CAN-17-0307
   PubMed Web of Science ®Google Scholar
• Hu G, Pen W, Wang M. TRIM14 promotes breast cancer cell proliferation by inhibiting apoptosis. Oncol Res. 2019;27(4):439–447. doi: 10.3727/096504018X15214994641786
   PubMed Web of Science ®Google Scholar
• Huttlin EL, Bruckner RJ, Navarrete-Perea J, et al. Dual proteome-scale networks reveal cell-specific remodeling of the human interactome. Cell. 2021;184(11):3022–3040.e28. doi: 10.1016/j.cell.2021.04.011
   PubMed Web of Science ®Google Scholar
• Iradi MCG, Triplett JC, Thomas JD, et al. Characterization of gene regulation and protein interaction networks for Matrin 3 encoding mutations linked to amyotrophic lateral sclerosis and myopathy. Sci Rep. 2018;8(1):4049. doi: 10.1038/s41598-018-21371-4
   PubMedGoogle Scholar
• Kim J-S, He X, Liu J, et al. Systematic proteomics of endogenous human cohesin reveals an interaction with diverse splicing factors and RNA-binding proteins required for mitotic progression. J Biol Chem. 2019;294(22):8760–8772. doi: 10.1074/jbc.RA119.007832
   PubMed Web of Science ®Google Scholar
• Zhang X, Liu J, Yang X, et al. High expression of COL6A1 predicts poor prognosis and response to immunotherapy in bladder cancer. Cell Cycle. 2022;22(5):1–9. doi: 10.1080/15384101.2022.2154551
   PubMed Web of Science ®Google Scholar
• Chen D, Zhang H, Zhao L, et al. Prognostic value of RILPL2 and its correlation with tumor immune microenvironment and glycolysis in non-small cell lung cancer. Cell Cycle. 2022;22(7):841–857. doi: 10.1080/15384101.2022.2159203
   PubMed Web of Science ®Google Scholar
• Hirsch FR, Scagliotti GV, Mulshine JL, et al. Lung cancer: current therapies and new targeted treatments. Lancet. 2017;389(10066):299–311. doi: 10.1016/S0140-6736(16)30958-8
   PubMed Web of Science ®Google Scholar
• Maibach F, Sadozai H, Seyed Jafari SM, et al. Tumor-infiltrating lymphocytes and their prognostic value in cutaneous melanoma. Front Immunol. 2020;11:2105. doi: 10.3389/fimmu.2020.02105
   PubMed Web of Science ®Google Scholar
• Forner A, Reig M, Bruix J. Hepatocellular carcinoma. Lancet. 2018;391(10127):1301–1314. doi: 10.1016/S0140-6736(18)30010-2
   PubMed Web of Science ®Google Scholar
• Zeitz MJ, Malyavantham KS, Seifert B, et al. Matrin 3: chromosomal distribution and protein interactions. J Cell Biochem. 2009;108(1):125–133. doi: 10.1002/jcb.22234
   PubMed Web of Science ®Google Scholar
• Malyavantham KS, Bhattacharya S, Barbeitos M, et al. Identifying functional neighborhoods within the cell nucleus: proximity analysis of early S-phase replicating chromatin domains to sites of transcription, RNA polymerase II, HP1gamma, matrin 3 and SAF-A. J Cell Biochem. 2008;105(2):391–403. doi: 10.1002/jcb.21834
   PubMed Web of Science ®Google Scholar
• Senderek J, Garvey SM, Krieger M, et al. Autosomal-dominant distal myopathy associated with a recurrent missense mutation in the gene encoding the nuclear matrix protein, matrin 3. Am J Hum Genet. 2009;84(4):511–518. doi: 10.1016/j.ajhg.2009.03.006
   PubMed Web of Science ®Google Scholar
• Cha HJ, Uyan Ö, Kai Y, et al. Inner nuclear protein Matrin-3 coordinates cell differentiation by stabilizing chromatin architecture. Nat Commun. 2021;12(1):6241. doi: 10.1038/s41467-021-26574-4
   PubMed Web of Science ®Google Scholar
• Nho S-H, Yoon G, Seo J-H, et al. Licochalcone H induces the apoptosis of human oral squamous cell carcinoma cells via regulation of matrin 3. Oncol Rep. 2019;41(1):333–340. doi: 10.3892/or.2018.6784
   PubMed Web of Science ®Google Scholar
• Qie S, Diehl JA. Cyclin D1, cancer progression, and opportunities in cancer treatment. J Mol Med (Berl). 2016;94(12):1313–1326. doi: 10.1007/s00109-016-1475-3
   PubMed Web of Science ®Google Scholar
• Yoon M-K, Mitrea DM, Ou L, et al. Cell cycle regulation by the intrinsically disordered proteins p21 and p27. Biochem Soc Trans. 2012;40(5):981–988. doi: 10.1042/BST20120092
   PubMedGoogle Scholar
• Michaelis C, Ciosk R, Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997;91(1):35–45. doi: 10.1016/S0092-8674(01)80007-6
   PubMed Web of Science ®Google Scholar
• Guacci V, Koshland D, Strunnikov A. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell. 1997;91(1):47–57. doi: 10.1016/S0092-8674(01)80008-8
   PubMed Web of Science ®Google Scholar
• Haarhuis JH, Elbatsh AM, Rowland BD. Cohesin and its regulation: on the logic of X-shaped chromosomes. Dev Cell. 2014;31(1):7–18. doi: 10.1016/j.devcel.2014.09.010
   PubMed Web of Science ®Google Scholar
• Uhlmann F. SMC complexes: from DNA to chromosomes. Nat Rev Mol Cell Biol. 2016;17(7):399–412. doi: 10.1038/nrm.2016.30
   PubMed Web of Science ®Google Scholar
• Morales C, Losada A. Establishing and dissolving cohesion during the vertebrate cell cycle. Curr Opin Cell Biol. 2018;52:51–57. doi: 10.1016/j.ceb.2018.01.010
   PubMed Web of Science ®Google Scholar
• Canudas S, Smith S. Differential regulation of telomere and centromere cohesion by the Scc3 homologues SA1 and SA2, respectively, in human cells. J Cell Bio. 2009;187(2):165–173. doi: 10.1083/jcb.200903096
   PubMed Web of Science ®Google Scholar
• Remeseiro S, Cuadrado A, Carretero M, et al. Cohesin-SA1 deficiency drives aneuploidy and tumourigenesis in mice due to impaired replication of telomeres. EMBO J. 2012;31(9):2076–2089. doi: 10.1038/emboj.2012.11
   PubMed Web of Science ®Google Scholar
• Mondal G, Stevers M, Goode B, et al. A requirement for STAG2 in replication fork progression creates a targetable synthetic lethality in cohesin-mutant cancers. Nat Commun. 2019;10(1):1686. doi: 10.1038/s41467-019-09659-z
   PubMedGoogle Scholar
• Morales C, Ruiz-Torres M, Rodríguez-Acebes S, et al. PDS5 proteins are required for proper cohesin dynamics and participate in replication fork protection. J Biol Chem. 2020;295(1):146–157. doi: 10.1074/jbc.RA119.011099
   PubMed Web of Science ®Google Scholar
• Hu T, Shen H, Li J, et al. RFC2, a direct target of miR-744, modulates the cell cycle and promotes the proliferation of CRC cells. J Cell Physiol. 2020;235(11):8319–8333. doi: 10.1002/jcp.29676
   PubMed Web of Science ®Google Scholar
• Wang T, Tang T, Jiang Y, et al. PRIM2 promotes Cell cycle and tumor progression in p53-mutant lung cancer. Cancers (Basel). 2022;14(14):3370. doi: 10.3390/cancers14143370
   PubMed Web of Science ®Google Scholar
• Qiao L, Zheng J, Tian Y, et al. Regulator of chromatin condensation 1 abrogates the G1 cell cycle checkpoint via Cdk1 in human papillomavirus E7-expressing epithelium and cervical cancer cells. Cell Death Dis. 2018;9(6):583. doi: 10.1038/s41419-018-0584-z
   PubMedGoogle Scholar
• Fu Y, Liu S, Zeng S, et al. From bench to bed: the tumor immune microenvironment and current immunotherapeutic strategies for hepatocellular carcinoma. J Exp Clin Cancer Res. 2019;38(1):396. doi: 10.1186/s13046-019-1396-4
   PubMed Web of Science ®Google Scholar
• Yang L, Zhang Y. Tumor-associated macrophages: from basic research to clinical application. J Hematol Oncol. 2017;10(1):58. doi: 10.1186/s13045-017-0430-2
   PubMed Web of Science ®Google Scholar
• Pitt JM, Marabelle A, Eggermont A, et al. Targeting the tumor microenvironment: removing obstruction to anticancer immune responses and immunotherapy. Ann Oncol. 2016;27(8):1482–1492. doi: 10.1093/annonc/mdw168
   PubMed Web of Science ®Google Scholar
• Mantovani A, Marchesi F, Malesci A, et al. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14(7):399–416. doi: 10.1038/nrclinonc.2016.217
   PubMed Web of Science ®Google Scholar
• Ji D, Song C, Li Y, et al. Combination of radiotherapy and suppression of tregs enhances abscopal antitumor effect and inhibits metastasis in rectal cancer. J Immunother Cancer. 2020;8(2):e000826. doi: 10.1136/jitc-2020-000826
   PubMed Web of Science ®Google Scholar
• Kitamura T, Qian B-Z, Pollard JW. Immune cell promotion of metastasis. Nat Rev Immunol. 2015;15(2):73–86. doi: 10.1038/nri3789
   PubMed Web of Science ®Google Scholar