Nuclear accumulation of an uncapped RNA produced by Drosha cleavage of a transcript encoding miR-10b and Hoxd4

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Phua, Sze Lynn Calista ^a   Sivakamasundari, V ^b   Shao, Yu ^a   Cai, Xiaohan ^a   Zhang, Li Feng ^a   Lufkin, Thomas ^b   Featherstone, Mark ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b GENOME INSTITUTE OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPED RNA; MICRORNA; MICRORNA 10B; UNCLASSIFIED DRUG; DROSHA PROTEIN, MOUSE; HOXD4 PROTEIN, MOUSE; MESSENGER RNA; MIRN10 MICRORNA, MOUSE; RIBONUCLEASE III; TRANSCRIPTION FACTOR;

5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYONAL CARCINOMA STEM CELL; GENE; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENETIC REGULATION; GENETIC TRANSCRIPTION; HOX GENE; HOXD4 GENE; INTERNAL RIBOSOME ENTRY SITE; MIR 10B GENE; MOUSE; NERVE CELL; NONHUMAN; RNA CLEAVAGE; ANIMAL; ANIMAL EMBRYO; CELL NUCLEUS; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS; RIBOSOME; RNA TRANSPORT;

ANIMALIA; MURINAE;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL NUCLEUS; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; PROTEIN BIOSYNTHESIS; RIBONUCLEASE III; RIBOSOMES; RNA CAPS; RNA TRANSPORT; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 80053437781     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025689     Document Type: Article

References (60)

1. Griffiths-Jones S, (2004) The microRNA Registry. Nucleic Acids Res 32: D109-111.
2. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ, (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-144.
3. 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.
4. Kim DH, Saetrom P, Snove O Jr, Rossi JJ, (2008) MicroRNA-directed transcriptional gene silencing in mammalian cells. Proc Natl Acad Sci U S A 105: 16230-16235.
5. Mallo M, Wellik DM, Deschamps J, (2010) Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344: 7-15.
6. Durston AJ, Jansen HJ, Wacker SA, (2010) Review: Time-space translation regulates trunk axial patterning in the early vertebrate embryo. Genomics 95: 250-255.
7. Duboule D, (2007) The rise and fall of Hox gene clusters. Development 134: 2549-2560.
8. Woltering JM, Duboule D, (2010) The origin of digits: expression patterns versus regulatory mechanisms. Dev Cell 18: 526-532.
9. Tschopp P, Tarchini B, Spitz F, Zakany J, Duboule D, (2009) Uncoupling time and space in the collinear regulation of Hox genes. PLoS Genet 5: e1000398.
10. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T, (2001) Identification of novel genes coding for small expressed RNAs. Science 294: 853-858.
11. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, et al. (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12: 735-739.
12. Lagos-Quintana M, Rauhut R, Meyer J, Borkhardt A, Tuschl T, (2003) New microRNAs from mouse and human. RNA 9: 175-179.
13. Tan Y, Zhang B, Wu T, Skogerbo G, Zhu X, et al. (2009) Transcriptional inhibiton of Hoxd4 expression by miRNA-10a in human breast cancer cells. BMC Mol Biol 10: 12.
14. Ma L, Teruya-Feldstein J, Weinberg RA, (2007) Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688.
15. Ma L, Reinhardt F, Pan E, Soutschek J, Bhat B, et al. (2010) Therapeutic silencing of miR-10b inhibits metastasis in a mouse mammary tumor model. Nat Biotechnol 28: 341-347.
16. Ma L, Weinberg RA, (2008) MicroRNAs in malignant progression. Cell Cycle 7: 570-572.
17. Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E, (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J Cancer 125: 1407-1413.
18. Bloomston M, Frankel WL, Petrocca F, Volinia S, Alder H, et al. (2007) MicroRNA expression patterns to differentiate pancreatic adenocarcinoma from normal pancreas and chronic pancreatitis. JAMA 297: 1901-1908.
19. Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, et al. (2005) Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 334: 1351-1358.
20. Mansfield JH, Harfe BD, Nissen R, Obenauer J, Srineel J, et al. (2004) MicroRNA-responsive 'sensor' transgenes uncover Hox-like and other developmentally regulated patterns of vertebrate microRNA expression. Nat Genet 36: 1079-1083.
21. Kosman D, Mizutani CM, Lemons D, Cox WG, McGinnis W, et al. (2004) Multiplex detection of RNA expression in Drosophila embryos. Science 305: 846.
22. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, et al. (2005) MicroRNA expression in zebrafish embryonic development. Science 309: 310-311.
23. Kloosterman WP, Wienholds E, de Bruijn E, Kauppinen S, Plasterk RH, (2006) In situ detection of miRNAs in animal embryos using LNA-modified oligonucleotide probes. Nat Methods 3: 27-29.
24. Horan GS, Kovacs EN, Behringer RR, Featherstone MS, (1995) Mutations in paralogous Hox genes result in overlapping homeotic transformations of the axial skeleton: evidence for unique and redundant function. Dev Biol 169: 359-372.
25. Horan GS, Ramirez-Solis R, Featherstone MS, Wolgemuth DJ, Bradley A, et al. (1995) Compound mutants for the paralogous hoxa-4, hoxb-4, and hoxd-4 genes show more complete homeotic transformations and a dose-dependent increase in the number of vertebrae transformed. Genes Dev 9: 1667-1677.
26. Folberg A, Kovacs EN, Featherstone MS, (1997) Characterization and retinoic acid responsiveness of the murine Hoxd4 transcription unit. J Biol Chem 272: 29151-29157.
27. van Scherpenzeel Thim V, Remacle S, Picard J, Cornu G, Gofflot F, et al. (2005) Mutation analysis of the HOX paralogous 4-13 genes in children with acute lymphoid malignancies: identification of a novel germline mutation of HOXD4 leading to a partial loss-of-function. Hum Mutat 25: 384-395.
28. Nolte C, Amores A, Nagy Kovacs E, Postlethwait J, Featherstone M, (2003) The role of a retinoic acid response element in establishing the anterior neural expression border of Hoxd4 transgenes. Mech Dev 120: 325-335.
29. Morrison A, Moroni MC, Ariza-McNaughton L, Krumlauf R, Mavilio F, (1996) In vitro and transgenic analysis of a human HOXD4 retinoid-responsive enhancer. Development 122: 1895-1907.
30. Morrison A, Ariza-McNaughton L, Gould A, Featherstone M, Krumlauf R, (1997) HOXD4 and regulation of the group 4 paralog genes. Development 124: 3135-3146.
31. Zhang F, Popperl H, Morrison A, Kovacs EN, Prideaux V, et al. (1997) Elements both 5′ and 3′ to the murine Hoxd4 gene establish anterior borders of expression in mesoderm and neurectoderm. Mech Dev 67: 49-58.
32. Zhang F, Nagy Kovacs E, Featherstone MS, (2000) Murine hoxd4 expression in the CNS requires multiple elements including a retinoic acid response element. Mech Dev 96: 79-89.
33. Rastegar M, Kobrossy L, Kovacs EN, Rambaldi I, Featherstone M, (2004) Sequential histone modifications at Hoxd4 regulatory regions distinguish anterior from posterior embryonic compartments. Mol Cell Biol 24: 8090-8103.
34. Nolte C, Rastegar M, Amores A, Bouchard M, Grote D, et al. (2006) Stereospecificity and PAX6 function direct Hoxd4 neural enhancer activity along the antero-posterior axis. Dev Biol 299: 582-593.
35. Woltering JM, Durston AJ, (2008) MiR-10 represses HoxB1a and HoxB3a in zebrafish. PLoS One 3: e1396.
36. Rudnicki MA, McBurney MW, (1987) Cell culture methods and induction of differentiation of embryonal carcinoma cell lines. In: Robertson EJ, editors. Teratocarcinomas and embryonic stem cells: a practical approach Oxford IRL Press pp. 19-49.
37. LaRosa GJ, Gudas LJ, (1988) Early Retinoic Acid-Induced F9 Teratocarcinoma Stem Cell Gene ERA-I: Alternate Splicing Creates Transcripts for a Homeobox-Containing Protein and One Lacking the Homeobox. Molecular and Cellular Biology 8: 3906-3917.
38. Wei Y, Harris T, Childs G, (2002) Global gene expression patterns during neural differentiation of P19 embryonic carcinoma cells. Differentiation 70: 204-219.
39. Baron A, Featherstone MS, Hill RE, Hall A, Galliot B, et al. (1987) Hox-1.6: A mouse homeobox-containing gene member of the Hox-1 complex. EMBO J 6: 2977-2986.
40. Featherstone MS, Baron A, Gaunt SJ, Mattei MG, Duboule D, (1988) Hox-5.1 defines a homeobox-containing gene locus on mouse chromosome 2. Proc Natl Acad Sci U S A 85: 4760-4764.
41. Han J, Lee Y, Yeom K-H, Nam J-W, Heo I, et al. (2006) Molecular Basis for the Recognition of Primary microRNAs by the Drosha-DGCR8 Complex. Cell 125: 887-901.
42. Rodriguez A, Griffiths-Jones S, Ashurst JL, Bradley A, (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res 14: 1902-1910.
43. Baskerville S, Bartel DP, (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11: 241-247.
44. Cai X, Hagedorn CH, Cullen BR, (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10: 1957-1966.
45. Gaunt SJ, Krumlauf R, Duboule D, (1989) Mouse homeo-genes within a subfamily, Hox-1.4,-2.6 and-5.1, display similar anteroposterior domains of expression in the embryo, but show stage- and tissue-dependent differences in their regulation. Development 107: 131-141.
46. Cianetti L, Di Cristofaro A, Zappavigna V, Bottero L, Boccoli G, et al. (1990) Molecular mechanisms underlying the expression of the human HOX-5.1 gene. Nucleic Acids Res 18: 4361-4368.
47. Myers RM, Stamatoyannopoulos J, Snyder M, Dunham I, Hardison RC, et al. (2011) A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 9: e1001046.
48. Woltering JM, Durston AJ, (2006) The zebrafish hoxDb cluster has been reduced to a single microRNA. Nat Genet 38: 601-602.
49. Simeone A, Pannese M, Acampora D, D'Esposito M, Boncinelli E, (1988) At least three human homeoboxes on chromosome 12 belong to the same transcription unit. Nucleic Acids Res 16: 5379-5390.
50. Mainguy G, Koster J, Woltering J, Jansen H, Durston A, (2007) Extensive polycistronism and antisense transcription in the mammalian Hox clusters. PLoS One 2: e356.
51. Hadrys T, Prince V, Hunter M, Baker R, Rinkwitz S, (2004) Comparative genomic analysis of vertebrate Hox3 and Hox4 genes. J Exp Zool B Mol Dev Evol 302: 147-164.
52. Franks TM, Lykke-Andersen J, (2008) The control of mRNA decapping and P-body formation. Mol Cell 32: 605-615.
53. Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, et al. (2002) Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420: 563-573.
54. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, et al. (2005) The transcriptional landscape of the mammalian genome. Science 309: 1559-1563.
55. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
56. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, et al. (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by Noncoding RNAs. Cell 129: 1311-1323.
57. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, et al. (2011) A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
58. Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH, et al. (2009) An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell 33: 717-726.
59. Tribioli C, Lufkin T, (1999) The murine Bapx1 homeobox gene plays a critical role in embryonic development of the axial skeleton and spleen. Development 126: 5699-5711.
60. Wang W, Chan EK, Baron S, Van de Water T, Lufkin T, (2001) Hmx2 homeobox gene control of murine vestibular morphogenesis. Development 128: 5017-5029.