MicroRNAs with a nucleolar location

RNA

Volumn 15, Issue 9, 2009, Pages 1705-1715

  Ritland Politz, Joan C ^a,b   Hogan, Eric M ^a   Pederson, Thoru ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

In situ nucleic acid hybridization; microRNAs; Muscle; Nuclear RNAs; Nucleolus; Nucleus

Indexed keywords

MICRORNA; SMALL NUCLEOLAR RNA; UNTRANSLATED RNA;

ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CELL FRACTIONATION; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; MYOBLAST; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; RAT; RNA PROCESSING;

ANIMALS; CELL NUCLEOLUS; CELLS, CULTURED; MICROARRAY ANALYSIS; MICRORNAS; MYOBLASTS; RATS; TISSUE DISTRIBUTION;

RATTUS;

EID: 69049118109     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1470409     Document Type: Article

References (95)

1. Andersen JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Mann M, Lamond AI. 2002. Directed proteomic analysis of the human nucleolus. Curr Biol 12: 1-11.
2. Ason B, Darnell DK, Wittbrodt B, Berezikov E, Kloosterman WP, Wittbrodt J, Antin PB, Plasterk RH. 2006. Differences in vertebrate microRNA expression. Proc Natl Acad Sci 103: 14385-14389.
3. Bártová E, Harnicarová A, Krejcí J, Strasák L, Kozubek S. 2008. Single-cell c-myc gene expression in relationship to nuclear domains. Chromosome Res 16: 325-343.
4. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. 2007. Mammalian mirtron genes. Mol Cell 28: 328-336.
5. Bhorjee JS, Pederson T. 1972. Nonhistone chromosomal proteins in synchronized HeLa cells. Proc Natl Acad Sci 69: 3345-3349.
6. Bhorjee JS, Pederson T. 1973. Chromatin: Its isolation from cultured mammalian cells with particular reference to contamination by nuclear ribonucleoprotein particles. Biochemistry 12: 2766-2773.
7. Blow, M.J., Grocock, R.J., van Dongen, S., Enright, A.J., Dicks, E., Futreal, P.A., Wooster, R., Stratton, M.R. 2006. RNA editing of human microRNAs. Genome Biol 7: R27.1-R27.8.
8. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. 2007. The multifunctional nucleolus. Nat Rev Mol Cell Biol 8: 574-585.
9. Bond VC, Wold B. 1993. Nucleolar localization of myc transcripts. Mol Cell Biol 13: 3221-3230.
10. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, et al. 2005. A microRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 353: 1793-1801.
11. Carthew RW, Sontheimer EJ. 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136: 642-655.
12. Castoldi M, Schmidt S, Benes V, Hentze MW, Muckenthaler MU. 2008. miChip: An array-based method for microRNA expression profiling using locked nucleic acid capture probes. Nat Protocols 3: 321-329.
13. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, et al. 2005. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33: e179. doi: 10.1093/nar/gni178.
14. Du T, Zamore PD. 2005. microPrimer: The biogenesis and function of microRNA. Development 132: 4645-4652.
15. Eisenberg I, Eran A, Nishino I, Moggio M, Lamperti C, Amato AA, Lidov HG, Kang PB, North KN, Mitrani-Rosenbaum S, et al. 2007. Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci 104: 17016-17021.
16. Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G. 2008. A human snoRNA with microRNA-like functions. Mol Cell 32: 519-528.
17. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9: 102-114.
18. Ganesan G, Rao SM. 2008. A novel noncoding RNA processed by Drosha is restricted to nucleus in mouse. RNA 14: 1399-1410.
19. Ganot P, Jady BE, Bortolin ML, Darzacq X, Kiss T. 1999. Nucleolar factors direct the 2′-O-ribose methylation and pseudouridylation of U6 spliceosomal RNA. Mol Cell Biol 19: 6906-6917.
20. Gerbi SA, Borovjagin AV, Lange TS. 2003. The nucleolus: A site of ribonucleoprotein maturation. Curr Opin Cell Biol 15: 318-325.
21. Guang S, Bochner AF, Pavelec DM, Burkhart KB, Harding S, Lachowiec J, Kennedy S. 2008. An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science 321: 537-541.
22. Habig JW, Dale T, Bass BL. 2007. miRNA editing - we should have inosine this coming. Mol Cell 25: 792-793.
23. Hendrick JP, Wolin SL, Rinke J, Lerner MR, Steitz JA. 1981. Ro small cytoplasmic ribonucleoproteins are a subclass of La ribonucleoproteins: Further characterization of the Ro and La small ribonucleoproteins from uninfected mammalian cells. Mol Cell Biol 1: 1138-1149.
24. Huang S. 2002. Building an efficient factory: Where is pre-rRNA synthesized in the nucleolus? J Cell Biol 157: 739-741.
25. Hwang HW, Wentzel EA, Mendell JT. 2007. A hexanucleotide element directs microRNA nuclear import. Science 315: 97-100.
26. Jacobson MR, Pederson T. 1998. Localization of signal recognition particle RNA in the nucleolus of mammalian cells. Proc Natl Acad Sci 95: 7981-7986.
27. John HA, Patrinou-Georgoulas M, Jones KW. 1977. Detection of myosin heavy chain mRNA during myogenesis in tissue culture by in vitro and in situ hybridization. Cell 12: 501-508.
28. Karayan L, Riou JF, Seite P, Migeon J, Cantereau A, Larsen CJ. 2001. Human ARF protein interacts with topoisomerase I and stimulates its activity. Oncogene 20: 836-848.
29. Kawahara Y, Zinshteyn B, Chendrimada TP, Shiekhattar R, Nishikura K. 2007. RNA editing of the microRNA-151 precursor blocks cleavage by the Dicer-TRBP complex. EMBO Rep 8: 763-769.
30. Kawahara Y, Megraw M, Kreider E, Iizasa H, Valente L, Hatzigeorgiou AG, Nishikura K. 2008. Frequency and fate of microRNA editing in human brain. Nucleic Acids Res 36: 5270-5280.
31. Kim J, Krichevsky A, Grad Y, Hayes GD, Kosik KS, Church GM, Ruvkun G. 2004. Identification of many microRNAs that copurify with polyribosomes in mammalian neurons. Proc Natl Acad Sci 101: 360-365.
32. Kim HK, Lee YS, Sivaprasad U, Malhotra A, Dutta A. 2006. Muscle-specific microRNA miR-206 promotes muscle differentiation. J Cell Biol 174: 677-687.
33. Kim DH, Saetrom P, Snove O Jr, Rossi JJ. 2008. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci 105: 16230-16235.
34. Kim SH, Koroleva OA, Lewandowska D, Pendle AF, Clark GP, Simpson CG, Shaw PJ, Brown JWS. 2009. Aberrant mRNA transcripts and the nonsense-mediated decay proteins UPF2 and UPF3 are enriched in the Arabidopsis nucleolus. Plant Cell 21: (in press). doi: 10.1105/tpc.109.067736.
35. Kiss AM, Jady BE, Bertrand E, Kiss T. 2004. Human box H/ACA pseudouridylation guide RNA machinery. Mol Cell Biol 24: 5797-5807.
36. Kiss T, Fayet E, Jady BE, Richard P, Weber M. 2006. Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb Symp Quant Biol 71: 407-417.
37. Lee EJ, Baek M, Gusev Y, Brackett DJ, Nuovo GJ, Schmittgen TD. 2008. Systematic evaluation of microRNA processing patterns in tissues, cell lines, and tumors. RNA 14: 35-42.
38. Luciano DJ, Mirsky H, Vendetti NJ, Maas S. 2004. RNA editing of a miRNA precursor. RNA 10: 1174-1177.
39. Ma H, Pederson T. 2008a. Nucleophosmin is a binding partner of nucleostemin in human osteosarcoma cells. Mol Biol Cell 19: 2870-2875.
40. Ma H, Pederson T. 2008b. Nucleostemin: A multiplex regulator of cell-cycle progression. Trends Cell Biol 18: 575-579.
41. Maggio R, Siekevitz P, Palade GE. 1963. Studies in isolated nuclei. I. Isolation and chemical characterization of a nuclear fraction from guinea pig liver. J Cell Biol 18: 267-291.
42. Marcon E, Babak T, Chua G, Hughes T, Moens PB. 2008. miRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Res 16: 243-260.
43. Matera AG, Tycowski KT, Steitz JA, Ward DC. 1994. Organization of small nucleolar ribonucleoproteins (snoRNPs) by fluorescence in situ hybridization and immunocytochemistry. Mol Biol Cell 5: 1289-1299.
44. Matera AG, Terns RM, Terns MP. 2007. Non-coding RNAs: Lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol 8: 209-220.
45. Matranga C, Zamore P. 2007. Small silencing RNAs. Curr Biol 17: R789-R793.
46. Mayer C, Neubert M, Grummt I. 2008. The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep 9: 774-780.
47. McCarthy JJ. 2008. MicroRNA-206: The skeletal muscle-specific myomiR. Biochim Biophys Acta 1779: 682-691.
48. Mellon I, Bhorjee J. 1982. Isolation and characterization of nuclei and purification of chromatin from differentiating cultures of rat skeletal muscle. Exp Cell Res 137: 141-154.
49. Mishra RK, Eliceiri GL. 1997. Three small nucleolar RNAs that are involved in ribosomal RNA precursor processing. Proc Natl Acad Sci 94: 4972-4977.
50. Morlando M, Ballarino M, Gromak N, Pagano F, Bozzoni I, Proudfoot NJ. 2008. Primary microRNA transcripts are processed co-transcriptionally. Nat Struct Mol Biol 15: 902-909.
51. Muramatsu M, Smetana K, Busch H. 1963. Quantitative aspects of isolation of nucleoli of Walker carcinosarcoma and liver of the rat. Cancer Res 23: 510-518.
52. Newman MA, Thomson JM, Hammond SM. 2008. Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14: 1539-1549.
53. Ochs RL, Lischwe MA, Spohn WH, Busch H. 1985. Fibrillarin: A new protein of the nucleolus identified by autoimmune sera. Biol Cell 54: 123-133.
54. Ohrt T, Mutze J, Staroske W, Weinmann L, Hock J, Crell K, Meister G, Schwille P. 2008. Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy reveal the cytoplasmic origination of loaded nuclear RISC in vivo in human cells. Nucleic Acids Res 36: 6439-6449.
55. Pawlicki JM, Steitz JA. 2008. Primary microRNA transcript retention at sites of transcription leads to enhanced microRNA production. J Cell Biol 182: 61-76.
56. Pederson T. 1974. Proteins associated with heterogeneous nuclear RNA in eukaryotic cells. J Mol Biol 83: 163-183.
57. Pederson T. 1998. Growth factors in the nucleolus? J Cell Biol 143: 279-281.
58. Pederson T, Tsai RY. 2009. In search of nonribosomal nucleolar protein function and regulation. J Cell Biol 184: 771-776.
59. Penman S, Smith I, Holtzman E. 1966. Ribosomal RNA synthesis and processing in a particulate site in the HeLa cell nucleus. Science 154: 786-789.
60. Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. 2008. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci 105: 1608-1613.
61. Pogacic V, Dragon F, Filipowicz W. 2000. Human H/ACA small nucleolar RNPs and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol Cell Biol 20: 9028-9040.
62. Politz J, Yarovoi S, Kilroy S, Gowda K, Zwieb C, Pederson T. 2000. Signal recognition particle components in the nucleolus. Proc Natl Acad Sci 97: 55-60.
63. Politz J, Lewandowski L, Pederson T. 2002. Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis. J Cell Biol 159: 411-418.
64. Politz J, Polena I, Trask I, Bazett-Jones D, Pederson T. 2005. A nonribosomal landscape in the nucleolus revealed by the stem cell protein nucleostemin. Mol Biol Cell 16: 3401-3410.
65. Politz JC, Zhang F, Pederson T. 2006. MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Proc Natl Acad Sci 103: 18957-18962.
66. Raska I, Shaw PJ, Cmarko D. 2006. New insights into nucleolar architecture and activity. Int Rev Cytol 255: 177-235.
67. Robertus JL, Harms G, Blokzijl T, Booman M, de Jong D, van Imhoff G, Rosati S, Schuuring E, Kluin P, van den Berg A. 2009. Specific expression of miR-17-5p and miR-127 in testicular and central nervous system diffuse large B-cell lymphoma. Mod Pathol 22: 547-555.
68. Rosenberg MI, Georges SA, Asawachaicharn A, Analau E, Tapscott SJ. 2006. MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. J Cell Biol 175: 77-85.
69. Saraiya AA, Wang CC. 2008. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4: e1000224. doi: 10.1371/ journal.ppat.1000224.
70. Schmittgen TD, Lee EJ, Jiang J, Sarkar A, Yang L, Elton TS, Chen C. 2008. Real-time PCR quantification of precursor and mature microRNA. Methods 44: 31-38.
71. Schneiter R, Kadowski T, Tartakoff AM. 1995. mRNA transport in yeast: Time to reinvestigate the functions of the nucleolus. Mol Biol Cell 6: 357-370.
72. Selvamurugan N, Joost OH, Haas ES, Brown JW, Galvin NJ, Eliceiri GL. 1997. Intracellular localization and unique conserved sequences of three small nucleolar RNAs. Nucleic Acids Res 25: 1591-1596.
73. Sempere, L.F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., and Ambros, V. 2004. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5: R13.1-R13.11.
74. Shaheen HH, Hopper AK. 2005. Retrograde movement of tRNAs from the cytoplasm to the nucleus in Saccharomyces cerevisiae. Proc Natl Acad Sci 102: 11290-11295.
75. Shaheen HH, Horetsky RL, Kimball SR, Murthi A, Jefferson LS, Hopper AK. 2007. Retrograde nuclear accumulation of cytoplasmic tRNA in rat hepatoma cells in response to amino acid deprivation. Proc Natl Acad Sci 104: 8845-8850.
76. Shiohama A, Sasaki T, Noda S, Minoshima S, Shimizu N. 2007. Nucleolar localization of DGCR8 and identification of eleven DGCR8-associated proteins. Exp Cell Res 313: 4196-4207.
77. Sommerville J, Brumwell C, Politz J, Pederson T. 2005. Signal recognition particle assembly in relation to the function of amplified nucleoli of Xenopus oocytes. J Cell Sci 118: 1299-1307.
78. Sweetman D, Goljanek K, Rathjen T, Oustanina S, Braun T, Dalmay T, Munsterberg A. 2008. Specific requirements of MRFs for the expression of muscle specific microRNAs, miR-1, miR-206, and miR-133. Dev Biol 321: 491-499.
79. Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS. 2009. Small RNAs derived from snoRNAs. RNA 15: 1233-1240.
80. Takano A, Endo T, Yoshihisa T. 2005. tRNA actively shuttles between the nucleus and cytosol in yeast. Science 309: 140-142.
81. Thomsen R, Nielsen PS, Jensen TH. 2005. Dramatically improved RNA in situ hybridization signals using LNA-modified probes. RNA 11: 1745-1748.
82. Thomsen R, Saguez C, Nasser T, Jensen TH. 2008. General, rapid, and transcription-dependent fragmentation of nucleolar antigens in S. cerevisiae mRNA export mutants. RNA 14: 706-716.
83. Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. 2006. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes & Dev 20: 2202-2207.
84. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S, et al. 2008. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456: 980-984.
85. Tong AW, Nemunaitis J. 2008. Modulation of miRNA activity in human cancer: A new paradigm for cancer gene therapy? Cancer Gene Ther 15: 341-355.
86. van Rooij E, Sutherland LB, Liu N, Williams AH, McAnally J, Gerard RD, Richardson JA, Olson EN. 2006. A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc Natl Acad Sci 103: 18255-18260.
87. van Rooij E, Liu N, Olson EN. 2008. MicroRNAs flex their muscles. Trends Genet 24: 159-166.
88. Visintin R, Amon A. 2000. The nucleolus: The magician's hat for cell cycle tricks. Curr Opin Cell Biol 12: 752.
89. Vitali P, Basyuk E, Le Meur E, Bertrand E, Muscatelli F, Cavaille J, Huttenhofer A. 2005. ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs. J Cell Biol 169: 745-753.
90. Wang B, Yanez A, Novina CD. 2008. MicroRNA-repressed mRNAs contain 40S but not 60S components. Proc Natl Acad Sci 105: 5343-5348.
91. Wulczyn FG, Smirnova L, Rybak A, Brandt C, Kwidzinski E, Ninnemann O, Strehle M, Seiler A, Schumacher S, Nitsch R. 2007. Post-transcriptional regulation of the let-7 microRNA during neural cell specification. FASEB J 21: 415-426.
92. Yang W, Wang Q, Howell KL, Lee JT, Cho DS, Murray JM, Nishikura K. 2005. ADAR1 RNA deaminase limits short interfering RNA efficacy in mammalian cells. J Biol Chem 280: 3946-3953.
93. Yang W, Chendrimada TP, Wang Q, Higuchi M, Seeburg PH, Shiekhattar R, Nishikura K. 2006. Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat Struct Mol Biol 13: 13-21.
94. Yeom KH, Lee Y, Han J, Suh MR, Kim VN. 2006. Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucleic Acids Res 34: 4622-4629.
95. Zeng Y, Yi R, Cullen BR. 2005. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J 24: 138-148.