Sp1 Suppresses miR-3178 to Promote the Metastasis Invasion Cascade via Upregulation of TRIOBP
Open accessAbstract
Specificity protein (Sp1) plays an important role in invasion-metastasis cascade. Sp1 regulation on protein coding genes has been extensively investigated; however, little is known about its regulation on protein non-coding genes. In this study, miR-3178 is reported as a novel target of Sp1 in multiple cancer cell models. Sp1 functions as its transcriptional suppressor as evidenced by luciferase reporter and chromatin immunoprecipitation (ChIP) assays. In line with the pro-metastatic role of Sp1, miR-3178 exerts anti-metastasis function. Overexpression of miR-3178 inhibits both migration and invasion of highly metastatic prostate, lung, and breast cancer cells whereas antagonizing miR-3178 promotes those events in their lowly metastatic counterparts. The in vivo study demonstrates that miR-3178 suppresses the tail vein inoculated prostate cancer cells to form colonies in lung, lymph node, and liver of BALB/c nude mice. miR-3178 directly targets the 3' UTR of TRIOBP-1 and TRIOBP-5, two isoforms of TRIOBP expressed in prostate, lung, and breast cancer cells. Overexpression of TRIOBP-1 could rescue miR-3178 inhibition on cell migration and invasion. Collectively, our findings reveal the regulatory axis of Sp1/miR-3178/TRIOBP in metastasis cascade. Our results suggest miR-3178 as a promising application to suppress metastasis in Sp1-overexpressed cancers.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Bortezomib induces downregulation of miR-33b-3p.
“downregulation of miR-33b-3p was induced by bortezomib, the clinically used proteasome inhibitor”
From miR-33b-3p Acts as a Tumor Suppressor by Targeting DOCK4 in Prostate Cancer (2021) · cites this paper as [14]
The Materials and Methods (Microarray; page unavailable) describe bortezomib treatment, and the Results (Sp1 Is a Transcriptional Suppressor of miR-3178; page unavailable) report that treatment downregulated SP1 and upregulated miR-3178. Searches for miR-33b-3p and bortezomib-induced miRNA downregulation found no passage stating what happened to miR-33b-3p. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Cawley, S., Bekiranov, S., Ng, H. H., Kapranov, P., Sekinger, E. A., Kampa, D., Piccolboni, A., Sementchenko, V., Cheng, J., Williams, A. J., et al. (2004) · Cell · doi:10.1016/s0092-8674(04)00127-8 · Cited by 1,095 · see citing works
Flagged first, then by citations
Research works printed but not linked: 46
- [1]Cai Y. Yu X. Hu S. Yu J. A brief review on the mechanisms of miRNA regulation Genomics Proteomics Bioinformatics 7 2009 147 154 20172487 PMC5054406
- [2]Nam E.H. Lee Y. Zhao X.F. Park Y.K. Lee J.W. Kim S. ZEB2-Sp1 cooperation induces invasion by upregulating cadherin-11 and integrin α5 expression Carcinogenesis 35 2014 302 314 24130169
- [3]Kolesnikoff N. Attema J.L. Roslan S. Bert A.G. Schwarz Q.P. Gregory P.A. Goodall G.J. Specificity protein 1 (Sp1) maintains basal epithelial expression of the miR-200 family: implications for epithelial-mesenchymal transition J. Biol. Chem. 289 2014 11194 11205 24627491 PMC4036258
- [4]Qian Y. Yao W. Yang T. Yang Y. Liu Y. Shen Q. Zhang J. Qi W. Wang J. aPKC-ι/P-Sp1/Snail signaling induces epithelial-mesenchymal transition and immunosuppression in cholangiocarcinoma Hepatology 66 2017 1165 1182 28574228
- [5]Xu K. Shu H.K. EGFR activation results in enhanced cyclooxygenase-2 expression through p38 mitogen-activated protein kinase-dependent activation of the Sp1/Sp3 transcription factors in human gliomas Cancer Res. 67 2007 6121 6129 17616668
- [6]Hertel J. Hirche C. Wissmann C. Ebert M.P. Höcker M. Transcription of the vascular endothelial growth factor receptor-3 (VEGFR3) gene is regulated by the zinc finger proteins Sp1 and Sp3 and is under epigenetic control: transcription of vascular endothelial growth factor receptor 3 Cell Oncol. (Dordr.) 37 2014 131 145 24710631 PMC13004477
- [7]Li Y. Wang Y. Bioinformatics analysis of gene expression data for the identification of critical genes in breast invasive carcinoma Mol. Med. Rep. 16 2017 8657 8664 28990063 PMC5779935
- [8]Guan H. Cai J. Zhang N. Wu J. Yuan J. Li J. Li M. Sp1 is upregulated in human glioma, promotes MMP-2-mediated cell invasion and predicts poor clinical outcome Int. J. Cancer 130 2012 593 601 21469139
- [9]Jiang N.Y. Woda B.A. Banner B.F. Whalen G.F. Dresser K.A. Lu D. Sp1, a new biomarker that identifies a subset of aggressive pancreatic ductal adenocarcinoma Cancer Epidemiol. Biomarkers Prev. 17 2008 1648 1652 18628415
- [10]Briggs M.R. Kadonaga J.T. Bell S.P. Tjian R. Purification and biochemical characterization of the promoter-specific transcription factor, Sp1 Science 234 1986 47 52 3529394
- [12]Olive V. Minella A.C. He L. Outside the coding genome, mammalian microRNAs confer structural and functional complexity Sci. Signal. 8 2015 re2 25783159 PMC4425368
- [13]Esquela-Kerscher A. Slack F.J. Oncomirs - microRNAs with a role in cancer Nat. Rev. Cancer 6 2006 259 269 16557279
- [14]Hurst D.R. Edmonds M.D. Welch D.R. Metastamir: the field of metastasis-regulatory microRNA is spreading Cancer Res. 69 2009 7495 7498 19773429 PMC2756311
- [15]Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297 14744438
- [16]Filipowicz W. Bhattacharyya S.N. Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9 2008 102 114 18197166
- [17]Yen W.H. Ke W.S. Hung J.J. Chen T.M. Chen J.S. Sun H.S. Sp1-mediated ectopic expression of T-cell lymphoma invasion and metastasis 2 in hepatocellular carcinoma Cancer Med. 5 2016 465 477 26763486 PMC4799941
- [18]Rhodes D.R. Kalyana-Sundaram S. Mahavisno V. Varambally R. Yu J. Briggs B.B. Barrette T.R. Anstet M.J. Kincead-Beal C. Kulkarni P. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles Neoplasia 9 2007 166 180 17356713 PMC1813932
- [19]Liu Y. Zheng J. Fang W. You J. Wang J. Cui X. Wu B. [Isolation and characterization of human prostate cancer cell subclones with different metastatic potential] Zhonghua Bing Li Xue Za Zhi 28 1999 361 364 11869550
- [21]Rizwan A. Cheng M. Bhujwalla Z.M. Krishnamachary B. Jiang L. Glunde K. Breast cancer cell adhesome and degradome interact to drive metastasis NPJ Breast Cancer 1 2015 15017 28721370 PMC5515192
- [22]Soule H.D. Vazguez J. Long A. Albert S. Brennan M. A human cell line from a pleural effusion derived from a breast carcinoma J. Natl. Cancer Inst. 51 1973 1409 1416 4357757
- [23]Chadalapaka G. Jutooru I. Safe S. Celastrol decreases specificity proteins (Sp) and fibroblast growth factor receptor-3 (FGFR3) in bladder cancer cells Carcinogenesis 33 2012 886 894 22334592 PMC3324448
- [24]Liu S. Liu Z. Xie Z. Pang J. Yu J. Lehmann E. Huynh L. Vukosavljevic T. Takeki M. Klisovic R.B. Bortezomib induces DNA hypomethylation and silenced gene transcription by interfering with Sp1/NF-kappaB-dependent DNA methyltransferase activity in acute myeloid leukemia Blood 111 2008 2364 2373 18083845 PMC2234064
- [25]Kitajiri S. Sakamoto T. Belyantseva I.A. Goodyear R.J. Stepanyan R. Fujiwara I. Bird J.E. Riazuddin S. Riazuddin S. Ahmed Z.M. Actin-bundling protein TRIOBP forms resilient rootlets of hair cell stereocilia essential for hearing Cell 141 2010 786 798 20510926 PMC2879707
- [26]Seipel K. O’Brien S.P. Iannotti E. Medley Q.G. Streuli M. Tara, a novel F-actin binding protein, associates with the Trio guanine nucleotide exchange factor and regulates actin cytoskeletal organization J. Cell Sci. 114 2001 389 399 11148140
- [27]Shahin H. Walsh T. Sobe T. Abu Sa’ed J. Abu Rayan A. Lynch E.D. Lee M.K. Avraham K.B. King M.C. Kanaan M. Mutations in a novel isoform of TRIOBP that encodes a filamentous-actin binding protein are responsible for DFNB28 recessive nonsyndromic hearing loss Am. J. Hum. Genet. 78 2006 144 152 16385458 PMC1380212
- [28]Bradshaw N.J. Yerabham A.S.K. Marreiros R. Zhang T. Nagel-Steger L. Korth C. An unpredicted aggregation-critical region of the actin-polymerizing protein TRIOBP-1/Tara, determined by elucidation of its domain structure J. Biol. Chem. 292 2017 9583 9598 28438837 PMC5465484
- [29]Peng M. Hu Y. Song W. Duan S. Xu Q. Ding Y. Geng J. Zhou J. MIER3 suppresses colorectal cancer progression by down-regulating Sp1, inhibiting epithelial-mesenchymal transition Sci. Rep. 7 2017 11000 28887525 PMC5591250
- [30]Bajpai R. Nagaraju G.P. Specificity protein 1: its role in colorectal cancer progression and metastasis Crit. Rev. Oncol. Hematol. 113 2017 1 7 28427500
- [31]Tan Y. Yin H. Zhang H. Fang J. Zheng W. Li D. Li Y. Cao W. Sun C. Liang Y. Sp1-driven up-regulation of miR-19a decreases RHOB and promotes pancreatic cancer Oncotarget 6 2015 17391 17403 26041879 PMC4627316
- [32]Yang W.B. Chen P.H. Hsu T. Fu T.F. Su W.C. Liaw H. Chang W.C. Hung J.J. Sp1-mediated microRNA-182 expression regulates lung cancer progression Oncotarget 5 2014 740 753 24519909 PMC3996653
- [33]Yan L. Yu J. Tan F. Ye G.T. Shen Z.Y. Liu H. Zhang Y. Wang J.F. Zhu X.J. Li G.X. SP1-mediated microRNA-520d-5p suppresses tumor growth and metastasis in colorectal cancer by targeting CTHRC1 Am. J. Cancer Res. 5 2015 1447 1459 26101709 PMC4473322
- [34]Xia S.S. Zhang G.J. Liu Z.L. Tian H.P. He Y. Meng C.Y. Li L.F. Wang Z.W. Zhou T. MicroRNA-22 suppresses the growth, migration and invasion of colorectal cancer cells through a Sp1 negative feedback loop Oncotarget 8 2017 36266 36278 28422727 PMC5482653
- [35]Zhang K. Li X.Y. Wang Z.M. Han Z.F. Zhao Y.H. miR-22 inhibits lung cancer cell EMT and invasion through targeting Snail Eur. Rev. Med. Pharmacol. Sci. 21 2017 3598 3604 28925484
- [36]Nagao-Kitamoto H. Nagata M. Nagano S. Kitamoto S. Ishidou Y. Yamamoto T. Nakamura S. Tsuru A. Abematsu M. Fujimoto Y. GLI2 is a novel therapeutic target for metastasis of osteosarcoma Int. J. Cancer 136 2015 1276 1284 25082385
- [37]Dang D.T. Chen X. Feng J. Torbenson M. Dang L.H. Yang V.W. Overexpression of Krüppel-like factor 4 in the human colon cancer cell line RKO leads to reduced tumorigenecity Oncogene 22 2003 3424 3430 12776194 PMC2275074
- [38]Montagner M. Enzo E. Forcato M. Zanconato F. Parenti A. Rampazzo E. Basso G. Leo G. Rosato A. Bicciato S. SHARP1 suppresses breast cancer metastasis by promoting degradation of hypoxia-inducible factors Nature 487 2012 380 384 22801492
- [39]Asanoma K. Liu G. Yamane T. Miyanari Y. Takao T. Yagi H. Ohgami T. Ichinoe A. Sonoda K. Wake N. Kato K. Regulation of the mechanism of TWIST1 transcription by BHLHE40 and BHLHE41 in cancer cells Mol. Cell. Biol. 35 2015 4096 4109 26391953 PMC4648814
- [40]Yang B. Jing C. Wang J. Guo X. Chen Y. Xu R. Peng L. Liu J. Li L. Identification of microRNAs associated with lymphangiogenesis in human gastric cancer Clin. Transl. Oncol. 16 2014 374 379 23881463
- [41]Li W. Shen S. Wu S. Chen Z. Hu C. Yan R. Regulation of tumorigenesis and metastasis of hepatocellular carcinoma tumor endothelial cells by microRNA-3178 and underlying mechanism Biochem. Biophys. Res. Commun. 464 2015 881 887 26182877
- [42]Sayagués J.M. Corchete L.A. Gutiérrez M.L. Sarasquete M.E. Del Mar Abad M. Bengoechea O. Fermiñán E. Anduaga M.F. Del Carmen S. Iglesias M. Genomic characterization of liver metastases from colorectal cancer patients Oncotarget 7 2016 72908 72922 27662660 PMC5341953
- [43]Bao J. Wang S. Gunther L.K. Kitajiri S. Li C. Sakamoto T. The actin-bundling protein TRIOBP-4 and -5 promotes the motility of pancreatic cancer cells Cancer Lett. 356 2 Pt B 2015 367 373 25130170
- [44]Bao J. Bielski E. Bachhawat A. Taha D. Gunther L.K. Thirumurugan K. Kitajiri S. Sakamoto T. R1 motif is the major actin-binding domain of TRIOBP-4 Biochemistry 52 2013 5256 5264 23789641
- [45]Yano T. Yamazaki Y. Adachi M. Okawa K. Fort P. Uji M. Tsukita S. Tsukita S. Tara up-regulates E-cadherin transcription by binding to the Trio RhoGEF and inhibiting Rac signaling J. Cell Biol. 193 2011 319 332 21482718 PMC3080255
- [46]Gao Y. Zhang Z. Li K. Gong L. Yang Q. Huang X. Hong C. Ding M. Yang H. Linc-DYNC2H1-4 promotes EMT and CSC phenotypes by acting as a sponge of miR-145 in pancreatic cancer cells Cell Death Dis. 8 2017 e2924 28703793 PMC5550858
- [47]Yang H. Chen D. Cui Q.C. Yuan X. Dou Q.P. Celastrol, a triterpene extracted from the Chinese “Thunder of God Vine,” is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice Cancer Res. 66 2006 4758 4765 16651429
- [48]Guo J. Huang X. Wang H. Yang H. Celastrol induces autophagy by targeting AR/miR-101 in prostate cancer cells PLoS One 10 2015 e0140745 26473737 PMC4608724
Cited by
Sorted by citations
miR-33b-3p Acts as a Tumor Suppressor by Targeting DOCK4 in Prostate Cancer
Mei, Y., Li, K., Zhang, Z., Li, M., Yang, H., Wang, H., Huang, X., Li, X., Shi, S., & Yang, H. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.740452 · Cited by 10 · see citing works
“Our previous studies showed that miR-33b-3p was downregulated in prostate cancer in response to proteasome inhibition (14).”
BackgroundMethodSelf-citation
- Authors
- Wang, H., Li, K., Mei, Y., Huang, X., Li, Z., Yang, Q., & Yang, H.
- Affiliations
- Harbin Institute of Technology (CN)
- Corresponding author
- Yang, Huanjie
- Venue
- Molecular Therapy Nucleic Acids
- Publisher
- Elsevier BV
- Published
- 2018-09
- Volume
- 12
- Pages
- 1-11
- ISSN
- 2162-2531 (ISSN-L)
- PMC
- PMC6023786
- OpenAlex
- W2802571217
- Cited by
- 23
- References
- 1
- Citations by year
- 2025: 3 · 2023: 1 · 2022: 3 · 2021: 6 · 2020: 8 · 2019: 2
- FWCI
- 1.21
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Molecular Therapy — Nucleic Acids (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Harbin Science and Technology Bureau (2017RAQXJ182)
- Heilongjiang Postdoctoral Science Foundation (LBH-Z16072)
- China Postdoctoral Science Foundation (2017M610201)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- Sp1, TRIOBP, metastasis, cell invasion, cell migration, microRNA regulation, transcriptional regulation, prostate cancer, lung cancer, breast cancer, 3' UTR target, metastasis suppression, protein isoforms, tumor xenografts
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review