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PMID: 19801681 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

The miR200 family of microRNAs regulates WAVE3-dependent cancer cell invasion.

The Journal of biological chemistry ·Vol. 284 ·No. 48 ·2009-11-27 ·Pages 33019-29

Sossey-Alaoui K, Bialkowska K, Plow EF

Abstract

MicroRNAs are small non-coding RNAs that are directly involved in the regulation of gene expression by either translational repression or degradation of target mRNAs. Because of the high level of conservation of the target motifs, known as seed sequences, within the 3'-untranslated regions, a single microRNA can regulate numerous target genes simultaneously, making this class of RNAs a powerful regulator of gene expression. The miR200 family of microRNAs has recently been shown to regulate the process of epithelial to mesenchymal transition during tumor progression and metastasis. Here, we report that the expression of WAVE3, an actin cytoskeleton remodeling and metastasis promoter protein, is regulated by miR200 microRNAs. We show a clear inverse correlation between expression levels of WAVE3 and miR200 microRNAs in invasive versus non-invasive cancer cells. miR200 directly targets the 3'-untranslated regions of the WAVE3 mRNA and inhibits its expression. The miR200-mediated down-regulation of WAVE3 results in a significant reduction in the invasive phenotype of cancer cells, which is specific to the loss of WAVE3 expression. Re-expression of a miR200-resistant WAVE3 reverses miR200-mediated inhibition of cancer cell invasion. Loss of WAVE3 expression downstream of miR200 also results in a dramatic change in cell morphology resembling that of a mesenchymal to epithelial transition. In conclusion, a novel mechanism for the regulation of WAVE3 expression in cancer cells has been identified, which controls the invasive properties and morphology of cancer cells associated with their metastatic potential.

MeSH Terms
3' Untranslated Regions/genetics Cadherins/metabolism Cell Line Cell Line, Tumor Cell Movement Cell Proliferation Gene Expression Regulation, Neoplastic Green Fluorescent Proteins/genetics,metabolism HT29 Cells Homeodomain Proteins/metabolism Humans Immunoblotting MicroRNAs/genetics Microscopy, Fluorescence Mutation Neoplasms/genetics,metabolism,pathology RNA Interference Repressor Proteins/metabolism Reverse Transcriptase Polymerase Chain Reaction Signal Transduction Transcription Factors/metabolism Wiskott-Aldrich Syndrome Protein Family/genetics,metabolism Zinc Finger E-box Binding Homeobox 2 Zinc Finger E-box-Binding Homeobox 1
Chemicals
3' Untranslated Regions Cadherins Homeodomain Proteins MIRN200 microRNA, human MIRN429 microRNA, human MicroRNAs Repressor Proteins Transcription Factors WASF3 protein, human Wiskott-Aldrich Syndrome Protein Family ZEB1 protein, human ZEB2 protein, human Zinc Finger E-box Binding Homeobox 2 Zinc Finger E-box-Binding Homeobox 1 Green Fluorescent Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sossey-Alaoui Khalid
Department of Molecular Cardiology, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio 44195, USA. [email protected]
Bialkowska Katarzyna
Plow Edward F
References (53)
53 references, click to expand
  1. Inclusion of Scar/WAVE3 in a similar complex to Scar/WAVE1 and 2.
    BMC Cell Biol. 2005 Mar 07;6(1):11 PMID: 15752430
  2. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors.
    Cell. 2006 Mar 24;124(6):1169-81 PMID: 16564011
  3. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells.
    EMBO Rep. 2008 Jun;9(6):582-9 PMID: 18483486
  4. The let-7 microRNA represses cell proliferation pathways in human cells.
    Cancer Res. 2007 Aug 15;67(16):7713-22 PMID: 17699775
  5. WAVE/Scars in platelets.
    Blood. 2005 Apr 15;105(8):3141-8 PMID: 15280206
  6. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2.
    J Biol Chem. 2008 May 30;283(22):14910-4 PMID: 18411277
  7. WAVE3-mediated cell migration and lamellipodia formation are regulated downstream of phosphatidylinositol 3-kinase.
    J Biol Chem. 2005 Jun 10;280(23):21748-55 PMID: 15826941
  8. The widespread impact of mammalian MicroRNAs on mRNA repression and evolution.
    Science. 2005 Dec 16;310(5755):1817-21 PMID: 16308420
  9. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs.
    Nature. 2005 Feb 17;433(7027):769-73 PMID: 15685193
  10. WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility.
    EMBO J. 2003 Jul 15;22(14):3602-12 PMID: 12853475
  11. WAVE3 promotes cell motility and invasion through the regulation of MMP-1, MMP-3, and MMP-9 expression.
    Exp Cell Res. 2005 Aug 1;308(1):135-45 PMID: 15907837
  12. Most mammalian mRNAs are conserved targets of microRNAs.
    Genome Res. 2009 Jan;19(1):92-105 PMID: 18955434
  13. MicroRNA targeting specificity in mammals: determinants beyond seed pairing.
    Mol Cell. 2007 Jul 6;27(1):91-105 PMID: 17612493
  14. Down-regulation of WAVE3, a metastasis promoter gene, inhibits invasion and metastasis of breast cancer cells.
    Am J Pathol. 2007 Jun;170(6):2112-21 PMID: 17525277
  15. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer.
    Clin Exp Metastasis. 2007;24(8):587-97 PMID: 17978854
  16. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression.
    Cell Cycle. 2009 Mar 15;8(6):843-52 PMID: 19221491
  17. Epithelial-mesenchymal and mesenchymal-epithelial transitions during cancer progression.
    Verh Dtsch Ges Pathol. 2007;91:21-8 PMID: 18314592
  18. Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration.
    Dev Cell. 2003 Oct;5(4):595-609 PMID: 14536061
  19. c-Abl-mediated phosphorylation of WAVE3 is required for lamellipodia formation and cell migration.
    J Biol Chem. 2007 Sep 7;282(36):26257-65 PMID: 17623672
  20. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis.
    Cancer Cell. 2006 Mar;9(3):189-98 PMID: 16530703
  21. Scar/WAVE-1, a Wiskott-Aldrich syndrome protein, assembles an actin-associated multi-kinase scaffold.
    EMBO J. 2000 Sep 1;19(17):4589-600 PMID: 10970852
  22. A microRNA polycistron as a potential human oncogene.
    Nature. 2005 Jun 9;435(7043):828-33 PMID: 15944707
  23. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing.
    N Engl J Med. 1986 Dec 25;315(26):1650-9 PMID: 3537791
  24. Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin.
    Cancer Res. 2007 Sep 1;67(17):7972-6 PMID: 17804704
  25. Non-coding RNAs take centre stage in epithelial-to-mesenchymal transition.
    Trends Cell Biol. 2008 Aug;18(8):357-9 PMID: 18585040
  26. Complex networks orchestrate epithelial-mesenchymal transitions.
    Nat Rev Mol Cell Biol. 2006 Feb;7(2):131-42 PMID: 16493418
  27. A novel neural Wiskott-Aldrich syndrome protein (N-WASP) binding protein, WISH, induces Arp2/3 complex activation independent of Cdc42.
    J Cell Biol. 2001 Feb 5;152(3):471-82 PMID: 11157975
  28. Characterization of the WAVE1 knock-out mouse: implications for CNS development.
    J Neurosci. 2003 Apr 15;23(8):3343-52 PMID: 12716942
  29. Oncomirs - microRNAs with a role in cancer.
    Nat Rev Cancer. 2006 Apr;6(4):259-69 PMID: 16557279
  30. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival.
    Cancer Res. 2004 Jun 1;64(11):3753-6 PMID: 15172979
  31. The emerging role of miR-200 family of microRNAs in epithelial-mesenchymal transition and cancer metastasis.
    RNA Biol. 2008 Jul-Sep;5(3):115-9 PMID: 19182522
  32. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition.
    Cancer Res. 2008 Oct 1;68(19):7846-54 PMID: 18829540
  33. Cellular motility driven by assembly and disassembly of actin filaments.
    Cell. 2003 Feb 21;112(4):453-65 PMID: 12600310
  34. let-7 microRNA functions as a potential growth suppressor in human colon cancer cells.
    Biol Pharm Bull. 2006 May;29(5):903-6 PMID: 16651716
  35. Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition.
    Bioessays. 2001 Oct;23(10):912-23 PMID: 11598958
  36. Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors.
    Cancer Res. 2004 Dec 1;64(23):8585-94 PMID: 15574765
  37. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2.
    Genes Dev. 2008 Apr 1;22(7):894-907 PMID: 18381893
  38. The prognostic significance of epithelial-mesenchymal transition in breast cancer.
    Anticancer Res. 2002 Nov-Dec;22(6A):3415-9 PMID: 12530097
  39. MicroRNAs as regulators of epithelial-mesenchymal transition.
    Cell Cycle. 2008 Oct;7(20):3112-8 PMID: 18927505
  40. The miR-200 family: central player for gain and loss of the epithelial phenotype.
    Gastroenterology. 2009 May;136(5):1835-7 PMID: 19324106
  41. Cell motility: braking WAVEs.
    Nature. 2002 Aug 15;418(6899):732-3 PMID: 12181548
  42. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome.
    Cell. 1994 Aug 26;78(4):635-44 PMID: 8069912
  43. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets.
    Cell. 2005 Jan 14;120(1):15-20 PMID: 15652477
  44. Genomic organization and expression profile of the human and mouse WAVE gene family.
    Mamm Genome. 2003 May;14(5):314-22 PMID: 12856283
  45. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia.
    Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15524-9 PMID: 12434020
  46. WAVE3, an actin-polymerization gene, is truncated and inactivated as a result of a constitutional t(1;13)(q21;q12) chromosome translocation in a patient with ganglioneuroblastoma.
    Oncogene. 2002 Aug 29;21(38):5967-74 PMID: 12185600
  47. Prediction of mammalian microRNA targets.
    Cell. 2003 Dec 26;115(7):787-98 PMID: 14697198
  48. Identification of two human WAVE/SCAR homologues as general actin regulatory molecules which associate with the Arp2/3 complex.
    Biochem Biophys Res Commun. 1999 Jun 24;260(1):296-302 PMID: 10381382
  49. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1.
    Nat Cell Biol. 2008 May;10(5):593-601 PMID: 18376396
  50. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10356-61 PMID: 11526241
  51. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation.
    Cell. 2005 Aug 26;122(4):553-63 PMID: 16122423
  52. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement.
    J Cell Sci. 2001 May;114(Pt 10):1801-9 PMID: 11329366
  53. WAVE2 is required for directed cell migration and cardiovascular development.
    Nature. 2003 Jul 24;424(6947):452-6 PMID: 12879075
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2009-11-27
Epub
2009-00-01
Pages
33019-29
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2785142
Subset
IM
Grants
NHLBI NIH HHS · P01 HL073311 · United States
NHLBI NIH HHS · P50 HL077107 · United States
NHLBI NIH HHS · P50HL077107 · United States
NHLBI NIH HHS · P01HL073311 · United States
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