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Original Research

RNA Binding Motif Protein 3 Promotes Cell Metastasis and Epithelial–Mesenchymal Transition Through STAT3 Signaling Pathway in Hepatocellular Carcinoma

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Pages 405-422 | Published online: 09 May 2022

References

  • Zeng H, Zheng R, Guo Y, et al. Cancer survival in China, 2003–2005: a population-based study. Int J Cancer. 2015;136(8):1921–1930. doi:10.1002/ijc.29227
  • Fu J, Wang H. Precision diagnosis and treatment of liver cancer in China. Cancer Lett. 2018;412:283–288. doi:10.1016/j.canlet.2017.10.008
  • Siegel RL, Miller KD, Jemal A. Jemal A Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30. doi:10.3322/caac.21442
  • Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108. doi:10.3322/caac.21262
  • Graziani V, Rodriguez-Hernandez I, Maiques O, Sanz-Moreno V. The amoeboid state as part of the epithelial-to-mesenchymal transition programme. Trends Cell Biol. 2021;32(3):228–242. doi:10.1016/j.tcb.2021.10.004
  • Wagner J, Masek M, Jacobs A, et al. Mass cytometric and transcriptomic profiling of epithelial-mesenchymal transitions in human mammary cell lines. Sci Data. 2022;9(1):44. doi:10.1038/s41597-022-01137-4
  • Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871–890. doi:10.1016/j.cell.2009.11.007
  • Vu T, Datta PK. Regulation of EMT in colorectal cancer: a culprit in metastasis. Cancers. 2017;9(12):12. doi:10.3390/cancers9120171
  • Yang J, Antin P, Berx G, et al. Guidelines and definitions for research on epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2020;21(6):341–352. doi:10.1038/s41580-020-0237-9
  • Marcucci F, Stassi G, De MR. Epithelial-mesenchymal transition: a new target in anticancer drug discovery. Nat Rev Drug Discov. 2016;15(5):311–325. doi:10.1038/nrd.2015.13
  • Carroll CP, Bolland H, Vancauwenberghe E, et al. Targeting hypoxia regulated sodium driven bicarbonate transporters reduces triple negative breast cancer metastasis. Neoplasia. 2022;25:41–52. doi:10.1016/j.neo.2022.01.003
  • Wang J, Zhong Q, Zhang H, et al. Nogo-B promotes invasion and metastasis of nasopharyngeal carcinoma via RhoA-SRF-MRTFA pathway. Cell Death Dis. 2022;13(1):76. doi:10.1038/s41419-022-04518-0
  • Yu D, Pan M, Li Y, et al. RNA N6-methyladenosine reader IGF2BP2 promotes lymphatic metastasis and epithelial-mesenchymal transition of head and neck squamous carcinoma cells via stabilizing slug mRNA in an m6A-dependent manner. J Exp Clin Cancer Res. 2022;41(1):6. doi:10.1186/s13046-021-02212-1
  • Stehr AM, Wang G, Demmler R, et al. Neutrophil extracellular traps drive epithelial-mesenchymal transition of human colon cancer. J Pathol. 2021;256(4):455–467.
  • Dong T, Zhang Y, Chen Y, et al. FOXO1 inhibits the invasion and metastasis of hepatocellular carcinoma by reversing ZEB2-induced epithelial-mesenchymal transition. Oncotarget. 2017;8(1):1703–1713. doi:10.18632/oncotarget.13786
  • Han LL, Yin XR, Zhang SQ. miR-103 promotes the metastasis and EMT of hepatocellular carcinoma by directly inhibiting LATS2. Int J Oncol. 2018;53(6):2433–2444. doi:10.3892/ijo.2018.4580
  • Liu GM, Li Q, Zhang PF, et al. Restoration of FBP1 suppressed snail-induced epithelial to mesenchymal transition in hepatocellular carcinoma. Cell Death Dis. 2018;9(11):1132. doi:10.1038/s41419-018-1165-x
  • Zheng S, Liu J, Zhao Z, Song R. Role of STAT3/mTOR pathway in chronic kidney injury. Am J Transl Res. 2020;12(7):3302–3310.
  • Poholek CH, Raphael I, Wu D, et al. Noncanonical STAT3 activity sustains pathogenic Th17 proliferation and cytokine response to antigen. J Exp Med. 2020;217(10). doi:10.1084/jem.20191761
  • Wang C, Dou C, Wang Y, et al. TLX3 repressed SNAI1-induced epithelial-mesenchymal transition by directly constraining STAT3 phosphorylation and functionally sensitized 5-FU chemotherapy in hepatocellular carcinoma. Int J Biol Sci. 2019;15(8):1696–1711. doi:10.7150/ijbs.33844
  • Chen RY, Yen CJ, Liu YW, et al. CPAP promotes angiogenesis and metastasis by enhancing STAT3 activity. Cell Death Differ. 2020;27(4):1259–1273. doi:10.1038/s41418-019-0413-7
  • Balic JJ, Albargy H, Luu K, et al. STAT3 serine phosphorylation is required for TLR4 metabolic reprogramming and IL-1beta expression. Nat Commun. 2020;11(1):3816. doi:10.1038/s41467-020-17669-5
  • Goel RR, Nakabo S, Dizon BLP, et al. Lupus-like autoimmunity and increased interferon response in patients with STAT3-deficient hyper-IgE syndrome. J Allergy Clin Immunol. 2020;147(2):746–749.e9. doi:10.1016/j.jaci.2020.07.024
  • Guo R, Wu Z, Wang J, et al. Development of a non‐coding‐RNA‐based EMT/CSC inhibitory nanomedicine for in vivo treatment and monitoring of HCC. Adv Sci. 2019;6(9):1801885. doi:10.1002/advs.201801885
  • Sun XL, Ma J, Chen QZ, et al. SIX4 promotes metastasis through STAT3 activation in breast cancer. Am J Cancer Res. 2020;10(1):224.
  • Danno S, Nishiyama H, Higashitsuji H, et al. Increased transcript level of RBM3, a member of the glycine-rich RNA-binding protein family, in human cells in response to cold stress. Biochem Biophys Res Commun. 1997;236(3):804–807. doi:10.1006/bbrc.1997.7059
  • Zargar R, Urwat U, Malik F, et al. Molecular characterization of RNA binding motif protein 3 (RBM3) gene from Pashmina goat. Res Vet Sci. 2015;98:51–58. doi:10.1016/j.rvsc.2014.11.016
  • Boman K, Segersten U, Ahlgren G, et al. Decreased expression of RNA-binding motif protein 3 correlates with tumour progression and poor prognosis in urothelial bladder cancer. BMC Urol. 2013;13(1). doi:10.1186/1471-2490-13-17
  • Melling N, Simon R, Mirlacher M, et al. Loss of RNA-binding motif protein 3 expression is associated with right-sided localization and poor prognosis in colorectal cancer. Histopathology. 2016;68(2):191–198. doi:10.1111/his.12726
  • Melling N, Bachmann K, Hofmann B, et al. Prevalence and clinical significance of RBM3 immunostaining in non-small cell lung cancers. J Cancer Res Clin Oncol. 2019;145(4):873–879. doi:10.1007/s00432-019-02850-1
  • Ehlen A, Brennan DJ, Nodin B, et al. Expression of the RNA-binding protein RBM3 is associated with a favourable prognosis and cisplatin sensitivity in epithelial ovarian cancer. J Transl Med. 2010;8(1). doi:10.1186/1479-5876-8-78
  • Jonsson L, Gaber A, Ulmert D, et al. High RBM3 expression in prostate cancer independently predicts a reduced risk of biochemical recurrence and disease progression. Diagn Pathol. 2011;6(1). doi:10.1186/1746-1596-6-91
  • Zhang HT, Zhang ZW, Xue JH, et al. Differential expression of the RNA-binding motif protein 3 in human astrocytoma. Chin Med J. 2013;126(10):1948–1952.
  • Florianova L, Xu B, Traboulsi S, et al. Evaluation of RNA-binding motif protein 3 expression in urothelial carcinoma of the bladder: an immunohistochemical study. World J Surg Oncol. 2015;13(1). doi:10.1186/s12957-015-0730-3
  • Chen P, Yue X, Xiong H, Lu X, Ji Z. RBM3 upregulates ARPC2 by binding the 3ʹUTR and contributes to breast cancer progression. Int J Oncol. 2019. doi:10.3892/ijo.2019.4698
  • Kim MS, Lee HS, Kim YJ, et al. MEST induces twist-1-mediated EMT through STAT3 activation in breast cancers. Cell Death Differ. 2019;26(12):2594–2606. doi:10.1038/s41418-019-0322-9
  • Zhang X, Sai B, Wang F, et al. Hypoxic BMSC-derived exosomal miRNAs promote metastasis of lung cancer cells via STAT3-induced EMT. Mol Cancer. 2019;18(1):40. doi:10.1186/s12943-019-0959-5
  • Zhou RB, Lu XL, Zhang CY, Yin DC. RNA binding motif protein 3: a potential biomarker in cancer and therapeutic target in neuroprotection. Oncotarget. 2017;8(13):22235–22250. doi:10.18632/oncotarget.14755
  • Qin H, Ni H, Liu Y, et al. RNA-binding proteins in tumor progression. J Hematol Oncol. 2020;13(1):90. doi:10.1186/s13045-020-00927-w
  • Francart ME, Vanwynsberghe AM, Lambert J, et al. Vimentin prevents a miR-dependent negative regulation of tissue factor mRNA during epithelial-mesenchymal transitions and facilitates early metastasis. Oncogene. 2020;39(18):3680–3692. doi:10.1038/s41388-020-1244-1
  • Long H, Wang X, Chen Y, et al. Dysregulation of microRNAs in autoimmune diseases: pathogenesis, biomarkers and potential therapeutic targets. Cancer Lett. 2018;428:90–103. doi:10.1016/j.canlet.2018.04.016
  • Salomonsson A, Micke P, Mattsson JSM, et al. Comprehensive analysis of RNA binding motif protein 3 (RBM3) in non-small cell lung cancer. Cancer Med. 2020;9(15):5609–5619. doi:10.1002/cam4.3149
  • Dong W, Dai ZH, Liu FC, et al. The RNA-binding protein RBM3 promotes cell proliferation in hepatocellular carcinoma by regulating circular RNA SCD-circRNA 2 production. EBioMedicine. 2019;45:155–167. doi:10.1016/j.ebiom.2019.06.030
  • Kang SH, Cho J, Jeong H, Kwon SY. High RNA-binding motif protein 3 expression is associated with improved clinical outcomes in invasive breast cancer. J Breast Cancer. 2018;21(3):288–296. doi:10.4048/jbc.2018.21.e34
  • Boman K, Andersson G, Wennersten C, et al. Podocalyxin-like and RNA-binding motif protein 3 are prognostic biomarkers in urothelial bladder cancer: a validatory study. Biomark Res. 2017;5(1). doi:10.1186/s40364-017-0090-y
  • Grupp K, Wilking J, Prien K, et al. High RNA-binding motif protein 3 expression is an independent prognostic marker in operated prostate cancer and tightly linked to ERG activation and PTEN deletions. Eur J Cancer. 2014;50(4):852–861. doi:10.1016/j.ejca.2013.12.003
  • Grupp K, Hofmann B, Kutup A, et al. Reduced RBM3 expression is associated with aggressive tumor features in esophageal cancer but not significantly linked to patient outcome. BMC Cancer. 2018;18(1):1106. doi:10.1186/s12885-018-5032-z
  • Jingyu Z, Xiao-Jun T, Hang Z, et al. TGF-β-induced epithelial-to-mesenchymal transition proceeds through stepwise activation of multiple feedback loops. Sci Signal. 2014;7(345):ra91. doi:10.1126/scisignal.2005304
  • Pilotte J, Kiosses W, Chan SW, et al. Morphoregulatory functions of the RNA-binding motif protein 3 in cell spreading, polarity and migration. Sci Rep. 2018;8(1):7367. doi:10.1038/s41598-018-25668-2
  • Chai F, Li Y, Liu K, Li Q, Sun H. Caveolin enhances hepatocellular carcinoma cell metabolism, migration, and invasion in vitro via a hexokinase 2-dependent mechanism. J Cell Physiol. 2019;234(2):1937–1946. doi:10.1002/jcp.27074
  • Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141(1):52–67. doi:10.1016/j.cell.2010.03.015
  • Hannocks MJ, Zhang X, Gerwien H, et al. The gelatinases, MMP-2 and MMP-9, as fine tuners of neuroinflammatory processes. Matrix Biol. 2019;75–76:102–113. doi:10.1016/j.matbio.2017.11.007
  • Mahdi A, Darvishi B, Majidzadeh AK, Salehi M, Farahmand L. Challenges facing antiangiogenesis therapy: the significant role of hypoxia-inducible factor and MET in development of resistance to anti-vascular endothelial growth factor-targeted therapies. J Cell Physiol. 2019;234(5):5655–5663. doi:10.1002/jcp.27414
  • Zhu Y, Yan L, Zhu W, et al. MMP2/3 promote the growth and migration of laryngeal squamous cell carcinoma via PI3K/Akt-NF-kappaB-mediated epithelial-mesenchymal transformation. J Cell Physiol. 2019;234(9):15847–15855.
  • Zhang Q, Agoston AT, Pham TH, et al. Acidic bile salts induce epithelial to mesenchymal transition via VEGF signaling in non-neoplastic Barrett’s cells. Gastroenterology. 2019;156(1):130–144. doi:10.1053/j.gastro.2018.09.046
  • Bao Q, Zhang B, Suo Y, et al. Intermittent hypoxia mediated by TSP1 dependent on STAT3 induces cardiac fibroblast activation and cardiac fibrosis. eLife. 2020:9:e49923.
  • Wan P, Chi X, Du Q, et al. miR-383 promotes cholangiocarcinoma cell proliferation, migration, and invasion through targeting IRF1. J Cell Biochem. 2018;119(12):9720–9729. doi:10.1002/jcb.27286
  • Li J, Smith AR, Marquez RT, et al. MicroRNA-383 acts as a tumor suppressor in colorectal cancer by modulating CREPT/RPRD1B expression. Mol Carcinog. 2018;57(10):1408–1420. doi:10.1002/mc.22866