Small RNA expression and deep sequencing analyses of the nucleolus reveal the presence of nucleolus-associated microRNAs

FEBS Open Bio

Volumn 4, Issue , 2014, Pages 441-449

  Bai, Baoyan ^a,c   Liu, Hester ^a   Laiho, Marikki ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Deep sequencing; MiRNA expression profiling; Nucleolus; Small RNA

Indexed keywords

DICER; DNA DIRECTED RNA POLYMERASE; MICRORNA; SMALL NUCLEOLAR RNA; SMALL UNTRANSLATED RNA; EXPORTIN 1;

ARTICLE; CANCER CELL; CELL ISOLATION; CYTOPLASM; DENATURATION; FEMALE; GENE SEQUENCE; HUMAN; HUMAN CELL; HYBRIDIZATION; NORTHERN HYBRIDIZATION; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; CELL FRACTIONATION; NORTHERN BLOTTING; RNA HYBRIDIZATION; RNA ISOLATION; RNA SEQUENCE; RNA TRANSCRIPTION;

EID: 84901243830     PISSN: 22115463     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fob.2014.04.010     Document Type: Article

References (58)

1. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
2. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
3. Kim V.N., Han J., Siomi M.C. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10:126-139.
4. Siomi H., Siomi M.C. Posttranscriptional regulation of microRNA biogenesis in animals. Mol Cell 2010, 38:323-332.
5. Newman M.A., Hammond S.M. Emerging paradigms of regulated microRNA processing. Genes Dev 2010, 24:1086-1092.
6. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11:597-610.
7. Croce C.M. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009, 10:704-714.
8. Dimmeler S., Nicotera P. MicroRNAs in age-related diseases. EMBO Mol Med 2013, 5:180-190.
9. Liu N., Olson E.N. MicroRNA regulatory networks in cardiovascular development. Dev Cell 2010, 18:510-525.
10. O'Connell R.M., Rao D.S., Chaudhuri A.A., Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010, 10:111-122.
11. Eacker S.M., Dawson T.M., Dawson V.L. Understanding microRNAs in neurodegeneration. Nat Rev Neurosci 2009, 10:837-841.
12. Hwang H.W., Wentzel E.A., Mendell J.T. A hexanucleotide element directs microRNA nuclear import. Science 2007, 315:97-100.
13. 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.
14. Kim D.H., Saetrom P., Snøve O., Rossi J.J. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci U S A 2008, 105:16230-16235.
15. Place R.F., Li L.C., Pookot D., Noonan E.J., Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci U S A 2008, 105:1608-1613.
16. Politz J.C., Zhang F., Pederson T. MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Proc Natl Acad Sci U S A 2006, 103:18957-18962.
17. Politz J.C., Hogan E.M., Pederson T. MicroRNAs with a nucleolar location. RNA 2009, 15:1705-1715.
18. Li Z.F., Liang Y.M., Lau P.N., Shen W., Wang D.K., Cheung W.T., Xue C.J., Poon L.M., Lam Y.W. Dynamic localisation of mature microRNAs in Human nucleoli is influenced by exogenous genetic materials. PLoS ONE 2013, 8:e70869.
19. Marcon E., Babak T., Chua G., Hughes T., Moens P.B. MiRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Res 2008, 16:243-260.
20. Scott M.S., Avolio F., Ono M., Lamond A.I., Barton G.J. Human miRNA precursors with box H/ACA snoRNA features. PLoS Comput Biol 2009, 5:e1000507.
21. Ono M., Scott M.S., Yamada K., Avolio F., Barton G.J., Lamond A.I. Identification of human miRNA precursors that resemble box C/D snoRNAs. Nucleic Acids Res 2011, 39:3879-3891.
22. 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.
23. Pickering B.F., Yu D., Van Dyke M.W. Nucleolin protein interacts with microprocessor complex to affect biogenesis of microRNAs 15a and 16. J Biol Chem 2011, 286:44095-44103.
24. Jeffries C.D., Fried H.M., Perkins D.O. Nuclear and cytoplasmic localization of neural stem cell microRNAs. RNA 2011, 17:675-686.
25. Haag J.R., Pikaard C.S. RNA polymerase I: a multifunctional molecular machine. Cell 2007, 131:1224-1225.
26. Russell J., Zomerdijk J.C. The RNA polymerase I transcription machinery. Biochem Soc Symp 2006, 203-216.
27. Fatica A., Tollervey D. Making ribosomes. Curr Opin Cell Biol 2002, 14:313-318.
28. Boulon S., Westman B.J., Hutten S., Boisvert F.M., Lamond A.I. The nucleolus under stress. Mol Cell 2010, 40:216-227.
29. Hernandez-Verdun D. Nucleolus: from structure to dynamics. Histochem Cell Biol 2006, 125:127-137.
30. Kiss T., Fayet-Lebaron E., Jady B.E. Box H/ACA small ribonucleoproteins. Mol Cell 2010, 37:597-606.
31. Watkins N.J., Bohnsack M.T. The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev RNA 2012, 3:397-414.
32. Kiss T. SnoRNP biogenesis meets pre-mRNA splicing. Mol Cell 2006, 23:775-776.
33. Boulon S., Verheggen C., Jady B.E., Girard C., Pescia C., Paul C., Ospina J.K., Kiss T., Matera A.G., Bordonne R., et al. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 2004, 16:777-787.
34. Fornerod M., van Deursen J., van Baal S., Reynolds A., Davis D., Murti K.G., Fransen J., Grosveld G. The human homologue of yeast CRM1 is in a dynamic subcomplex with CAN/Nup214 and a novel nuclear pore component Nup88. EMBO J 1997, 16:807-816.
35. Thomas F., Kutay U. Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J Cell Sci 2003, 116:2409-2419.
36. Trotta C.R., Lund E., Kahan L., Johnson A.W., Dahlberg J.E. Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates. EMBO J 2003, 22:2841-2851.
37. Ernoult-Lange M., Wilczynska A., Harper M., Aigueperse C., Dautry F., Kress M., Weil D. Nucleocytoplasmic traffic of CPEB1 and accumulation in Crm1 nucleolar bodies. Mol Biol Cell 2009, 20:176-187.
38. Latonen L., Moore H.M., Bai B., Jaamaa S., Laiho M. Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene 2011, 30:790-805.
39. Bai B., Moore H.M., Laiho M. CRM1 and its ribosome export adaptor NMD3 localize to the nucleolus and affect rRNA synthesis. Nucleus 2013, 4:315-325.
40. Ender C., Krek A., Friedlander M.R., Beitzinger M., Weinmann L., Chen W., Pfeffer S., Rajewsky N., Meister G. A human snoRNA with microRNA-like functions. Mol Cell 2008, 32:519-528.
41. Saraiya A.A., Wang C.C. SnoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 2008, 4:e1000224.
42. Taft R.J., Glazov E.A., Lassmann T., Hayashizaki Y., Carninci P., Mattick J.S. Small RNAs derived from snoRNAs. RNA 2009, 15:1233-1240.
43. Brameier M., Herwig A., Reinhardt R., Walter L., Gruber J. Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res 2011, 39:675-686.
44. Scott M.S., Ono M. From snoRNA to miRNA: dual function regulatory non-coding RNAs. Biochimie 2011, 93:1987-1992.
45. Bai B., Laiho M. Efficient sequential recovery of nucleolar macromolecular components. Proteomics 2012, 12:3044-3048.
46. Cummins J.M., He Y., Leary R.J., Pagliarini R., Diaz L.A., Sjoblom T., Barad O., Bentwich Z., Szafranska A.E., Labourier E., et al. The colorectal microRNAome. Proc Natl Acad Sci U S A 2006, 103:3687-3692.
47. Moore H.M., Bai B., Boisvert F.M., Latonen L., Rantanen V., Simpson J.C., Pepperkok R., Lamond A.I., Laiho M. Quantitative proteomics and dynamic imaging of the nucleolus reveal distinct responses to UV and ionizing radiation. Mol Cell Proteomics 2011, 10(M111):009241.
48. Turner A.J., Knox A.A., Watkins N.J. Nucleolar disruption leads to the spatial separation of key 18S rRNA processing factors. RNA Biol 2012, 9:175-186.
49. Castanotto D., Lingeman R., Riggs A.D., Rossi J.J. CRM1 mediates nuclear-cytoplasmic shuttling of mature microRNAs. Proc Natl Acad Sci U S A 2009, 106:21655-21659.
50. Kohler A., Hurt E. Exporting RNA from the nucleus to the cytoplasm. Nat Rev Mol Cell Biol 2007, 8:761-773.
51. Vitali P., Basyuk E., Le Meur E., Bertrand E., Muscatelli F., Cavaillé J., Huttenhofer A. ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs. J Cell Biol 2005, 169:745-753.
52. Chiang H.R., Schoenfeld L.W., Ruby J.G., Auyeung V.C., Spies N., Baek D., Johnston W.K., Russ C., Luo S., Babiarz J.E., et al. Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes Dev 2010, 24:992-1009.
53. van Wolfswinkel J.C., Ketting R.F. The role of small non-coding RNAs in genome stability and chromatin organization. J Cell Sci 2010, 123:1825-1839.
54. Pontes O., Li C.F., Costa Nunes P., Haag J., Ream T., Vitins A., Jacobsen S.E., Pikaard C.S. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 2006, 126:79-92.
55. Grummt I., Längst G. Epigenetic control of RNA polymerase I transcription in mammalian cells. Biochim Biophys Acta 2013, 1829:393-404.
56. Höck J., Weinmann L., Ender C., Rüdel S., Kremmer E., Raabe M., Urlaub H., Meister G. Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep 2007, 8:1052-1060.
57. Mourelatos Z., Dostie J., Paushkin S., Sharma A., Charroux B., Abel L., Rappsilber J., Mann M., Dreyfuss G. MiRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev 2002, 16:720-788.
58. Kressler D., Bange G., Ogawa Y., Stjepanovic G., Bradatsch B., Pratte D., Amlacher S., Strauß D., Yoneda Y., Katahira J., et al. Synchronizing nuclear import of ribosomal proteins with ribosome assembly. Science 2012, 338:666-671.