Cited by 23MicroRNA in disease regulationMechanisms of cancer metastasisCancer-related molecular mechanisms research

Sp1 Suppresses miR-3178 to Promote the Metastasis Invasion Cascade via Upregulation of TRIOBP

Open access
Wang, Hui, Li, Kai, Mei, Yu, Huang, Xuemei, Li, Zhenglin, Yang, Qingzhu, Yang, Huanjie·2018·Molecular Therapy Nucleic Acids

Abstract

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.omtn.2018.04.008

Cites

1 of 1 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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

Flagged first, then by citations

Research works printed but not linked: 46

  1. [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. [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. [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. [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. [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. [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. [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. [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. [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. [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
  11. [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
  12. [13]Esquela-Kerscher A. Slack F.J. Oncomirs - microRNAs with a role in cancer Nat. Rev. Cancer 6 2006 259 269 16557279
  13. [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
  14. [15]Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297 14744438
  15. [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
  16. [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
  17. [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
  18. [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
  19. [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
  20. [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
  21. [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
  22. [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
  23. [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
  24. [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
  25. [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
  26. [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
  27. [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
  28. [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
  29. [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
  30. [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
  31. [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
  32. [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
  33. [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
  34. [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
  35. [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
  36. [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
  37. [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
  38. [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
  39. [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
  40. [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
  41. [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
  42. [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
  43. [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
  44. [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
  45. [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
  46. [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

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)
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
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