RNAi factors are present and active in human cell nuclei

Cell Reports

Volumn 6, Issue 1, 2014, Pages 211-221

  Gagnon, KeithT ^a   Li, Liande ^a   Chu, Yongjun ^a   Janowski, BethanyA ^a   Corey, DavidR ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; CELL PROTEIN; DICER; DOUBLE STRANDED RNA; MICRORNA; NUCLEAR RNA; TAR RNA BINDING PROTEIN; TRNC6A PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE SILENCING; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; RNA CLEAVAGE; RNA INTERFERENCE; RNA STABILITY;

MAMMALIA;

ARGONAUTE PROTEINS; AUTOANTIGENS; CELL NUCLEUS; CYTOPLASM; DEAD-BOX RNA HELICASES; HELA CELLS; HUMANS; PROTEIN BINDING; RIBONUCLEASE III; RNA INTERFERENCE; RNA-BINDING PROTEINS;

EID: 84892544892     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.12.013     Document Type: Article

References (58)

1. Alló M., Buggiano V., Fededa J.P., Petrillo E., Schor I., de la Mata M., Agirre E., Plass M., Eyras E., Elela S.A., et al. Control of alternative splicing through siRNA-mediated transcriptional gene silencing. Nat. Struct. Mol. Biol. 2009, 16:717-724.
2. Ando Y., Tomaru Y., Morinaga A., Burroughs A.M., Kawaji H., Kubosaki A., Kimura R., Tagata M., Ino Y., Hirano H., et al. Nuclear pore complex protein mediated nuclear localization of dicer protein in human cells. PLoS ONE 2011, 6:e23385.
3. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
4. Braasch D.A., Jensen S., Liu Y., Arar K., White M.A., Corey D.R. RNA interference in mammalian cells by chemically modified RNA. Biochemistry 2003, 42:7967-7975.
5. Calhoun K.A., Swartz J.R. Energy systems for ATP regeneration in cell-free protein synthesis reactions. Methods Mol. Biol. 2007, 375:3-17.
6. Castel S.E., Martienssen R.A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 2013, 14:100-112.
7. Chu Y., Yue X., Younger S.T., Janowski B.A., Corey D.R. Involvement of argonaute proteins in gene silencing and activation by RNAs complementary to a non-coding transcript at the progesterone receptor promoter. Nucleic Acids Res. 2010, 38:7736-7748.
8. Daniels S.M., Gatignol A. The multiple functions of TRBP, at the hub of cell responses to viruses, stress, and cancer. Microbiol. Mol. Biol. Rev. 2012, 76:652-666.
9. Dodd D.W., Gagnon K.T., Corey D.R. Digital quantitation of potential therapeutic target RNAs. Nucleic Acid Ther. 2013, 23:188-194.
10. Doyle M., Badertscher L., Jaskiewicz L., Güttinger S., Jurado S., Hugenschmidt T., Kutay U., Filipowicz W. The double-stranded RNA binding domain of human Dicer functions as a nuclear localization signal. RNA 2013, 19:1238-1252.
11. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.
12. Gagnon K.T., Corey D.R. Argonaute and the nuclear RNAs: new pathways for RNA-mediated control of gene expression. Nucleic Acid Ther. 2012, 22:3-16.
13. Gurtan A.M., Sharp P.A. The role of miRNAs in regulating gene expression networks. J.Mol. Biol. 2013, 425:3582-3600. 10.1016/j.jmb.2013.03.007.
14. Hammond S.M., Bernstein E., Beach D., Hannon G.J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000, 404:293-296.
15. Harel-Bellan A., Zazoua M.A., Rachez C., Muchardt C., Batsche E. 10-million-years AGO: Argonaute on chromatin in yeast and human, a conserved mode of action?. Transcription 2013, 4. Published online April 12, 2013.
16. Hetzer M.W. The nuclear envelope. Cold Spring Harb. Perspect. Biol. 2010, 2:a000539.
17. Holding C. RNAi active in the nucleus?. Genome Biol. 2004, 6. 10.1186/gb-spotlight-20050112-01.
18. Ikeda K., Satoh M., Pauley K.M., Fritzler M.J., Reeves W.H., Chan E.K.L. Detection of the argonaute protein Ago2 and microRNAs in the RNA induced silencing complex (RISC) using a monoclonal antibody. J.Immunol. Methods 2006, 317:38-44.
19. Iwasaki S., Kobayashi M., Yoda M., Sakaguchi Y., Katsuma S., Suzuki T., Tomari Y. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell 2010, 39:292-299.
20. Janowski B.A., Younger S.T., Hardy D.B., Ram R., Huffman K.E., Corey D.R. Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat. Chem. Biol. 2007, 3:166-173.
21. Jeffries C.D., Fried H.M., Perkins D.O. Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 2011, 17:675-686.
22. Katahira J., Yoneda Y. Nucleocytoplasmic transport of microRNAs and related small RNAs. Traffic 2011, 12:1468-1474.
23. Katikireddy K.R., O'Sullivan F. Immunohistochemical and immunofluorescence procedures for protein analysis. Methods Mol. Biol. 2011, 784:155-167.
24. Klouwen H.M., Appelman A.W.M. Synthesis of adenosine triphosphate in isolated nuclei and intact cells. Biochem. J. 1967, 102:878-884.
25. Lazzaretti D., Tournier I., Izaurralde E. The C-terminal domains of human TNRC6A, TNRC6B, and TNRC6C silence bound transcripts independently of Argonaute proteins. RNA 2009, 15:1059-1066.
26. Li L.C., Okino S.T., Zhao H., Pookot D., Place R.F., Urakami S., Enokida H., Dahiya R. Small dsRNAs induce transcriptional activation in human cells. Proc. Natl. Acad. Sci. USA 2006, 103:17337-17342.
27. Liao J.Y., Ma L.M., Guo Y.H., Zhang Y.C., Zhou H., Shao P., Chen Y.Q., Qu L.H. Deep sequencing of human nuclear and cytoplasmic small RNAs reveals an unexpectedly complex subcellular distribution of miRNAs and tRNA 3' trailers. PLoS ONE 2010, 5:e10563.
28. Liu J., Carmell M.A., Rivas F.V., Marsden C.G., Thomson J.M., Song J.J., Hammond S.M., Joshua-Tor L., Hannon G.J. Argonaute2 is the catalytic engine of mammalian RNAi. Science 2004, 305:1437-1441.
29. Liu Y., Ye X., Jiang F., Liang C., Chen D., Peng J., Kinch L.N., Grishin N.V., Liu Q. C3PO, an endoribonuclease that promotes RNAi by facilitating RISC activation. Science 2009, 325:750-753.
30. Liu J., Hu J., Corey D.R. Expanding the action of duplex RNAs into the nucleus: redirecting alternative splicing. Nucleic Acids Res. 2012, 40:1240-1250.
31. Ma E., Zhou K., Kidwell M.A., Doudna J.A. Coordinated activities of human dicer domains in regulatory RNA processing. J.Mol. Biol. 2012, 422:466-476.
32. MacRae I.J., Ma E., Zhou M., Robinson C.V., Doudna J.A. Invitro reconstitution of the human RISC-loading complex. Proc. Natl. Acad. Sci. USA 2008, 105:512-517.
33. Malone C.D., Hannon G.J. Small RNAs as guardians of the genome. Cell 2009, 136:656-668.
34. Martinez N.J., Chang H.M., Borrajo Jde.R., Gregory R.I. The co-chaperones Fkbp4/5 control Argonaute2 expression and facilitate RISC assembly. RNA 2013, 19:1583-1593.
35. Matranga C., Tomari Y., Shin C., Bartel D.P., Zamore P.D. Passenger-strand cleavage facilitates assembly of siRNA into Ago2-containing RNAi enzyme complexes. Cell 2005, 123:607-620.
36. Matsui M., Zhang H., Chu Y., Gagnon K.T., Shaikh S., Kuchimanchi S., Manoharan M., Corey D.R., Janowski B.A. Promoter RNA links transcriptional regulation of inflammatory pathway genes. Nucleic Acids Res. 2013, 41:10086-10109.
37. Meister G., Landthaler M., Patkaniowska A., Dorsett Y., Teng G., Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 2004, 15:185-197.
38. Michelsen U., von Hagen J. Isolation of subcellular organelles and structures. Methods Enzymol. 2009, 463:305-328.
39. Morris K.V., Chan S.W., Jacobsen S.E., Looney D.J. Small interfering RNA-induced transcriptional gene silencing in human cells. Science 2004, 305:1289-1292.
40. Ohrt T., Mütze J., Staroske W., Weinmann L., Höck J., Crell K., Meister G., Schwille P. Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy reveal the cytoplasmic origination of loaded nuclear RISC invivo in human cells. Nucleic Acids Res. 2008, 36:6439-6449.
41. Ohrt T., Muetze J., Svoboda P., Schwille P. Intracellular localization and routing of miRNA and RNAi pathway components. Curr. Top. Med. Chem. 2012, 12:79-88.
42. Pare J.M., LaPointe P., Hobman T.C. Hsp90 cochaperones p23 and FKBP4 physically interact with hAgo2 and activate RNA interference-mediated silencing in mammalian cells. Mol. Biol. Cell 2013, 24:2303-2310.
43. Rivas F.V., Tolia N.H., Song J.J., Aragon J.P., Liu J., Hannon G.J., Joshua-Tor L. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 2005, 12:340-349.
44. Robb G.B., Brown K.M., Khurana J., Rana T.M. Specific and potent RNAi in the nucleus of human cells. Nat. Struct. Mol. Biol. 2005, 12:133-137.
45. Rüdel S., Flatley A., Weinmann L., Kremmer E., Meister G. A multifunctional human Argonaute2-specific monoclonal antibody. RNA 2008, 14:1244-1253.
46. Shaw P.J. Comparison of widefield/deconvolution and confocal microscopy for three-dimensional imaging. Handbook of Biological Confocal Microscopy 2006, 453-467. Springer, New York. J.B. Pawley (Ed.).
47. Spector D.L. Immunofluorescence localization of nuclear proteins. Cold Spring Harb. Protoc. 2011, 2011:1276-1280.
48. Stalder L., Heusermann W., Sokol L., Trojer D., Wirz J., Hean J., Fritzsche A., Aeschimann F., Pfanzagl V., Basselet P., et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J. 2013, 32:1115-1127.
49. Till S., Lejeune E., Thermann R., Bortfeld M., Hothorn M., Enderle D., Heinrich C., Hentze M.W., Ladurner A.G. A conserved motif in Argonaute-interacting proteins mediates functional interactions through the Argonaute PIWI domain. Nat. Struct. Mol. Biol. 2007, 14:897-903.
50. Valencia-Sanchez M.A., Liu J., Hannon G.J., Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006, 20:515-524.
51. Vickers T.A., Koo S., Bennett C.F., Crooke S.T., Dean N.M., Baker B.F. Efficient reduction of target RNAs by small interfering RNA and RNase H-dependent antisense agents. A comparative analysis. J.Biol. Chem. 2003, 278:7108-7118.
52. Wang Y., Juranek S., Li H., Sheng G., Tuschl T., Patel D.J. Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 2008, 456:921-926.
53. Weinmann L., Höck J., Ivacevic T., Ohrt T., Mütze J., Schwille P., Kremmer E., Benes V., Urlaub H., Meister G. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 2009, 136:496-507.
54. Wilson R.C., Doudna J.A. Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 2013, 42:217-239.
55. Wuarin J., Schibler U. Physical isolation of nascent RNA chains transcribed by RNA polymerase II: evidence for cotranscriptional splicing. Mol. Cell. Biol. 1994, 14:7219-7225.
56. Ye X., Huang N., Liu Y., Paroo Z., Huerta C., Li P., Chen S., Liu Q., Zhang H. Structure of C3PO and mechanism of human RISC activation. Nat. Struct. Mol. Biol. 2011, 18:650-657.
57. Zamore P.D., Tuschl T., Sharp P.A., Bartel D.P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101:25-33.
58. Zeng Y., Cullen B.R. RNA interference in human cells is restricted to the cytoplasm. RNA 2002, 8:855-860.