MiR-128 represses L1 retrotransposition by binding directly to L1 RNA

Nature Structural and Molecular Biology

Volumn 22, Issue 10, 2015, Pages 824-831

  Hamdorf, Matthias ^a   Idica, Adam ^a   Zisoulis, Dimitrios G ^b   Gamelin, Lindsay ^a   Martin, Charles ^a   Sanders, Katie J ^a   Pedersen, Irene M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b REGULUS THERAPEUTICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; DNA METHYLTRANSFERASE 3B; MICRORNA; MICRORNA 128; OCTAMER TRANSCRIPTION FACTOR 4; RNA; TRANSCRIPTION FACTOR FOXD3; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; LUCIFERASE; MIRN128 MICRORNA, HUMAN; PRIMER DNA;

ARTICLE; BINDING AFFINITY; CANCER CELL; CLINICAL ASSESSMENT; CONTROLLED STUDY; DNA INTEGRATION; DNA METHYLATION; GENE FUNCTION; GENE MUTATION; GENETIC TRANSFECTION; GENOMIC INSTABILITY; HELA CELL LINE; HUMAN; HUMAN CELL; INTERACTIONS WITH RNA; INTERSPERSED ELEMENT 1 RETROTRANSPOSON; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN BINDING; REPRESSOR GENE; RETROPOSON; RNA BINDING; TRANSIENT TRANSFECTION; TUMOR GROWTH; CFU COUNTING; FIBROBLAST; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOBLOTTING; LONG INTERSPERSED REPEAT; METABOLISM; NEOPLASM; NUCLEAR REPROGRAMMING; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELLULAR REPROGRAMMING; COLONY-FORMING UNITS ASSAY; DNA PRIMERS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; GENOMIC INSTABILITY; HELA CELLS; HUMANS; IMMUNOBLOTTING; INDUCED PLURIPOTENT STEM CELLS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; LUCIFERASES; MICRORNAS; MUTAGENESIS, INSERTIONAL; NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA;

EID: 84943457469     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3090     Document Type: Article

References (40)

1. Chekulaeva, M. &Filipowicz, W. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 21, 452-460 (2009).
2. Bartel, D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
3. Friedman, R.C., Farh, K.K., Burge, C.B. &Bartel, D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105 (2009).
4. Sood, P., Krek, A., Zavolan, M., Macino, G. &Rajewsky, N. Cell-type-specific signatures of microRNAs on target mRNA expression. Proc. Natl. Acad. Sci. USA 103, 2746-2751 (2006).
5. Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
6. Zisoulis, D.G. et al. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 17, 173-179 (2010).
7. Loeb, G.B. et al. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol. Cell 48, 760-770 (2012).
8. Sayed, D. &Abdellatif, M. MicroRNAs in development and disease. Physiol. Rev. 91, 827-887 (2011).
9. Adams, B.D., Kasinski, A.L. &Slack, F.J. Aberrant regulation and function of microRNAs in cancer. Curr. Biol. 24, R762-R776 (2014).
10. Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
11. Holmes, S.E., Singer, M.F. &Swergold, G.D. Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element. J. Biol. Chem. 267, 19765-19768 (1992).
12. Hattori, M., Kuhara, S., Takenaka, O. &Sakaki, Y. L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein. Nature 321, 625-628 (1986).
13. Xiong, Y. &Eickbush, T.H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9, 3353-3362 (1990).
14. Feng, Q., Moran, J.V., Kazazian, H.H. Jr. &Boeke, J.D. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87, 905-916 (1996).
15. Fanning, T. &Singer, M. The LINE-1 DNA sequences in four mammalian orders predict proteins that conserve homologies to retrovirus proteins. Nucleic Acids Res. 15, 2251-2260 (1987).
16. Xiong, Y. &Eickbush, T.H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol. Biol. Evol. 5, 675-690 (1988).
17. Beck, C.R., Garcia-Perez, J.L., Badge, R.M. &Moran, J.V. LINE-1 elements in structural variation and disease. Annu. Rev. Genomics Hum. Genet. 12, 187-215 (2011).
18. Cordaux, R. &Batzer, M.A. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 10, 691-703 (2009).
19. Shukla, R. et al. Endogenous retrotransposition activates oncogenic pathways in hepatocellular carcinoma. Cell 153, 101-111 (2013).
20. Lee, E. et al. Landscape of somatic retrotransposition in human cancers. Science 337, 967-971 (2012).
21. Aravin, A.A., Sachidanandam, R., Girard, A., Fejes-Toth, K. &Hannon, G.J. Developmentally regulated piRNA clusters implicate MILI in transposon control. science 316, 744-747 (2007).
22. Bourc'his, D. &Bestor, T.H. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99 (2004).
23. Smith, Z.D. et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344 (2012).
24. Muckenfuss, H. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 281, 22161-22172 (2006).
25. Horn, A.V. et al. Human LINE-1 restriction by APOBEC3C is deaminase independent and mediated by an ORF1p interaction that affects LINE reverse transcriptase activity. Nucleic Acids Res. 42, 396-416 (2014).
26. Heras, S.R. et al. The Microprocessor controls the activity of mammalian retrotransposons. Nat. Struct. Mol. Biol. 20, 1173-1181 (2013).
27. Ciaudo, C. et al. RNAi-dependent and independent control of LINE1 accumulation and mobility in mouse embryonic stem cells. PLoS Genet. 9, e1003791 (2013).
28. Wissing, S. et al. Reprogramming somatic cells into iPS cells activates LINE-1 retroelement mobility. Hum. Mol. Genet. 21, 208-218 (2012).
29. Fabris, S. et al. Biological and clinical relevance of quantitative global methylation of repetitive DNA sequences in chronic lymphocytic leukemia. Epigenetics 6, 188-194 (2011).
30. Carreira, P.E., Richardson, S.R. &Faulkner, G.J. L1 retrotransposons, cancer stem cells and oncogenesis. FEBS J. 281, 63-73 (2014).
31. Miyoshi, N. et al. Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8, 633-638 (2011).
32. Warren, L. et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7, 618-630 (2010).
33. Pedersen, I.M. et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449, 919-922 (2007).
34. Xie, Y., Rosser, J.M., Thompson, T.L., Boeke, J.D. &An, W. Characterization of L1 retrotransposition with high-throughput dual-luciferase assays. Nucleic Acids Res. 39, e16 (2011).
35. Kimberland, M.L. et al. Full-length human L1 insertions retain the capacity for high frequency retrotransposition in cultured cells. Hum. Mol. Genet. 8, 1557-1560 (1999).
36. Godlewski, J. et al. Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res. 68, 9125-9130 (2008).
37. Sikandar, S.S. et al. NOTCH signaling is required for formation and self-renewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res. 70, 1469-1478 (2010).
38. Macias, S. et al. DGCR8 HITS-CLIP reveals novel functions for the Microprocessor. Nat. Struct. Mol. Biol. 19, 760-766 (2012).
39. Hunter, S.E. et al. Functional genomic analysis of the let-7 regulatory network in Caenorhabditis elegans. PLoS Genet. 9, e1003353 (2013).
40. Hogan, D.J. et al. Anti-miRs competitively inhibit microRNAs in Argonaute complexes. PLoS ONE 9, e100951 (2014).