The bin3 RNA methyltransferase targets 7SK RNA to control transcription and translation

Wiley Interdisciplinary Reviews: RNA

Volumn 3, Issue 5, 2012, Pages 633-647

  Cosgrove, Michael S ^a   Ding, Ye ^b   Rennie, William A ^b   Lane, Michael J ^a   Hanes, Steven D ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BIN3; RNA; RNA METHYLTRANSFERASE; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG;

DROSOPHILA; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SUBSTRATE; GENE CONTROL; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; REVIEW; RNA TRANSCRIPTION; RNA TRANSLATION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; YEAST;

ANIMALS; CONSERVED SEQUENCE; DROSOPHILA; HUMANS; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; SCHIZOSACCHAROMYCES; TRANSCRIPTION, GENETIC;

EID: 84867595496     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1123     Document Type: Review

References (94)

1. Zhu W. Isolation and characterization of bicoid-interacting proteins: Bin1 a homolog of human SAP18 and Bin3, a putative protein methyltransferase. Ph.D. Thesis, Department of Biomedical Sciences, School of Public Health, State University of New York; 2000.
2. Singh N, Morlock H, Hanes SD. The Bin3 RNA methyltransferase is required for repression of caudal translation in the Drosophila embryo. Dev Biol 2011, 352:104-115.
3. Jeronimo C, Forget D, Bouchard A, Li Q, Chua G, Poitras C, Therien C, Bergeron D, Bourassa S, Greenblatt J, Chabot B, Poirier GG, Hughes TR, Blanchette M, Price DH, Coulombe B. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol Cell 2007, 27:262-274.
4. Zhu W, Hanes SD. Identification of Drosophila Bicoid-interacting proteins using a custom two-hybrid selection. Gene 2000, 245:329-339.
5. Gelbart WM, Emmert DB. FlyBase High Throughput Expression Pattern Data Beta Version. Available at: http://flybase.org/reports/FBgn0263144.html. (Accessed October 13, 2010).
6. Kagan RM, Clarke S. Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch Biochem Biophys. 1994, 310:417-427.
7. Driever W, Nusslein-Volhard C. A gradient of bicoid protein in Drosophila embryos. Cell 1988, 54:83-93.
8. Driever W, Nusslein-Volhard C. The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 1988, 54: 95-104.
9. Driever W, Nusslein-Volhard C. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo. Nature 1989, 337:138-143.
10. Dubnau J, Struhl G. RNA recognition and translational regulation by a homeodomain protein. Nature 1996, 379:694-699.
11. Rivera-Pomar R, Niessing D, Schmidt-Ott U, Gehring WJ, Jackle H. RNA binding and translational suppression by bicoid. Nature 1996, 379:746-749.
12. Mlodzik M, Gehring WJ. Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell 1987, 48:465-478.
13. Mlodzik M, Gibson G, Gehring WJ. Effects of ectopic expression of caudal during Drosophila development. Development 1990, 109:271-277.
14. Marz M, Donath A, Verstraete N, Nguyen VT, Stadler PF, Bensaude O. Evolution of 7SK RNA and its protein partners in metazoa. Mol Biol Evol 2009, 26:2821-2830.
15. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:D225-D229.
16. Chen X, Sullivan DS, Huffaker TC. Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc Natl Acad Sci USA 1994, 91:9111-9115.
17. Shumyatsky GP, Tillib SV, Kramerov DA. B2 RNA and 7SK RNA, RNA polymerase III transcripts, have a cap-like structure at their 5′ end. Nucleic Acids Res 1990, 18:6347-6351.
18. Gupta S, Busch RK, Singh R, Reddy R. Characterization of U6 small nuclear RNA cap-specific antibodies. Identification of gamma-monomethyl-GTP cap structure in 7SK and several other human small RNAs. J Biol Chem 1990, 265:19137-19142.
19. Hamm J, Darzynkiewicz E, Tahara SM, Mattaj IW. The trimethylguanosine cap structure of U1 snRNA is a component of a bipartite nuclear targeting signal. Cell 1990, 62:569-577.
20. Xue Y, Yang Z, Chen R, Zhou Q. A capping-independent function of MePCE in stabilizing 7SK snRNA and facilitating the assembly of 7SK snRNP. Nucleic Acids Res 2010, 38:360-369.
21. Shuman S. Transcriptional networking cap-tures the 7SK RNA 5′-gamma-methyltransferase. Mol Cell 2007, 27:517-519.
22. Mattaj IW. Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding. Cell 1986, 46:905-911.
23. Epstein P, Reddy R, Henning D, Busch H. The nucleotide sequence of nuclear U6 (4.7 S) RNA. J Biol Chem 1980, 255:8901-8906.
24. Singh R, Gupta S, Reddy R. Capping of mammalian U6 small nuclear RNA in vitro is directed by a conserved stem-loop and AUAUAC sequence: conversion of a noncapped RNA into a capped RNA. Mol Cell Biol 1990, 10:939-946.
25. Shimba S, Reddy R. Purification of human U6 small nuclear RNA capping enzyme. Evidence for a common capping enzyme for gamma-monomethyl-capped small RNAs. J Biol Chem 1994, 269:12419-12423.
26. http://www.sgc.utoronto.ca/pmwiki/pmwiki.php?n=Crystallography. HomePage (PDB ID 3G07).
27. http://swissmodel.expasy.org/.
28. Zieve G, Penman S. Small RNA species of the HeLa cell: metabolism and subcellular localization. Cell 1976, 8:19-31.
29. Zieve G, Benecke BJ, Penman S. Synthesis of two classes of small RNA species in vivo and in vitro. Biochemistry 1977, 16:4520-4525.
30. Murphy S, Tripodi M, Melli M. A sequence upstream from the coding region is required for the transcription of the 7SK RNA genes. Nucleic Acids Res 1986, 14:9243-9260.
31. Reddy R, Henning D, Subrahmanyam CS, Busch H. Primary and secondary structure of 7-3 (K) RNA of Novikoff hepatoma. J Biol Chem 1984, 259: 12265-12270.
32. Prasanth KV, Camiolo M, Chan G, Tripathi V, Denis L, Nakamura T, Hubner MR, Spector DL. Nuclear organization and dynamics of 7SK RNA in regulating gene expression. Mol Biol Cell 2010, 21:4184-4196.
33. Chen Y, Sinha K, Perumal K, Gu J, Reddy R. Accurate 3' end processing and adenylation of human signal recognition particle RNA and alu RNA in vitro. J Biol Chem 1998, 273:35023-35031.
34. He N, Jahchan NS, Hong E, Li Q, Bayfield MA, Maraia RJ, Luo K, Zhou Q. A La-related protein modulates 7SK snRNP integrity to suppress P-TEFb-dependent transcriptional elongation and tumorigenesis. Mol Cell 2008, 29:588-599.
35. Ullu E, Esposito V, Melli M. Evolutionary conservation of the human 7 S RNA sequences. J Mol Biol 1982, 161:195-201.
36. Gruber AR, Kilgus C, Mosig A, Hofacker IL, Hennig W, Stadler PF. Arthropod 7SK RNA. Mol Biol Evol 2008, 25:1923-1930.
37. Copeland CS, Marz M, Rose D, Hertel J, Brindley PJ, Santana CB, Kehr S, Attolini CS, Stadler PF. Homology-based annotation of non-coding RNAs in the genomes of Schistosoma mansoni and Schistosoma japonicum. BMC Genomics 2009, 10:464.
38. Diribarne G, Bensaude O. 7SK RNA, a non-coding RNA regulating P-TEFb, a general transcription factor. RNABiology 2009, 6:122-128.
39. Kohoutek J. P-TEFb- the final frontier. Cell Division 2009, 4:19.
40. Peterlin BM, Brogie JE, Price DH. 7SK snRNA: a noncoding RNA that plays a major role in regulating eukaryotic transcription. WIRes RNA 2012, 3:92-103.
41. Blencowe BJ. Transcription: surprising role for an elusive small nuclear RNA. Curr Biol 2002, 12: R147-R149.
42. Wassarman DA, Steitz JA. Structural analyses of the 7SK ribonucleoprotein (RNP), the most abundant human small RNP of unknown function. Mol Cell Biol 1991, 11:3432-3445.
43. Krueger BJ, Jeronimo C, Roy BB, Bouchard A, Barrandon C, Byers SA, Searcey CE, Cooper JJ, Bensaude O, Cohen EA, Coulombe B, Price DH. LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated. Nucleic Acids Res 2008, 36:2219-2229.
44. Krueger BJ, Varzavand K, Cooper JJ, Price DH. The mechanism of release of P-TEFb and HEXIM1 from the 7SK snRNP by viral and cellular activators includes a conformational change in 7SK. PloS One 2010, 5:e12335.
45. Lebars I, Martinez-Zapien D, Durand A, Coutant J, Kieffer B, Dock-Bregeon AC. HEXIM1 targets a repeated GAUC motif in the riboregulator of transcription 7SK and promotes base pair rearrangements. Nucleic Acids Res 2010, 38:7749-7763.
46. Nguyen D, Krueger BJ, Sedore SC, Brogie JE, Rogers JT, Rajendra TK, Saunders A, Matera AG, Lis JT, Uguen P, Price DH. The Drosophila 7SK snRNP and the essential role of dHEXIM in development. Nucleic Acids Res 2012. In press.
47. Ding Y, Chan CY, Lawrence CE. Sfold web server for statistical folding and rational design of nucleic acids. Nucleic Acids Res 2004, 32:W135-W141.
48. Ding Y, Lawrence CE. A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res 2003, 31:7280-7301.
49. Ding Y, Chan CY, Lawrence CE. RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble. RNA 2005, 11:1157-1166.
50. Markham NR, Zuker M. UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 2008, 453:3-31.
51. Muse GW, Gilchrist DA, Nechaev S, Shah R, Parker JS, Grissom SF, Zeitlinger J, Adelman K. RNA polymerase is poised for activation across the genome. Nat Genet 2007, 39:1507-1511.
52. Zeitlinger J, Stark A, Kellis M, Hong JW, Nechaev S, Adelman K, Levine M, Young RA. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 2007, 39:1512-1516.
53. Nechaev S, Fargo DC, dos Santos G, Liu L, Gao Y, Adelman K. Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 2010, 327:335-338.
54. Yang Z, Zhu Q, Luo K, Zhou Q. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 2001, 414:317-322.
55. Nguyen VT, Kiss T, Michels AA, Bensaude O. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 2001, 414:322-325.
56. Michels AA, Nguyen VT, Fraldi A, Labas V, Edwards M, Bonnet F, Lania L, Bensaude O. MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner. Mol Cell Biol 2003, 23:4859-4869.
57. Yik JH, Chen R, Nishimura R, Jennings JL, Link AJ, Zhou Q. Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell 2003, 12:971-982.
58. Ouchida R, Kusuhara M, Shimizu N, Hisada T, Makino Y, Morimoto C, Handa H, Ohsuzu F, Tanaka H. Suppression of NF-kappaB-dependent gene expression by a hexamethylene bisacetamide-inducible protein HEXIM1 in human vascular smooth muscle cells. Genes Cells 2003, 8:95-107.
59. Markert A, Grimm M, Martinez J, Wiesner J, Meyerhans A, Meyuhas O, Sickmann A, Fischer U. The La-related protein LARP7 is a component of the 7SK ribonucleoprotein and affects transcription of cellular and viral polymerase II genes. EMBO Rep 2008, 9:569-575.
60. Michels AA, Fraldi A, Li Q, Adamson TE, Bonnet F, Nguyen VT, Sedore SC, Price JP, Price DH, Lania L, Bensaude O. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. EMBO J 2004, 23:2608-2619.
61. Van Herreweghe E, Egloff S, Goiffon I, Jady BE, Froment C, Monsarrat B, Kiss T. Dynamic remodelling of human 7SK snRNP controls the nuclear level of active P-TEFb. EMBO J 2007, 26:3570-3580.
62. Barrandon C, Bonnet F, Nguyen VT, Labas V, Bensaude O. The transcription-dependent dissociation of P-TEFb-HEXIM1-7SK RNA relies upon formation of hnRNP-7SK RNA complexes. Mol Cell Biol 2007, 27:6996-7006.
63. Conaway JW, Conaway RC. Transcription elongation and human disease. Ann Rev Biochem 1999, 68:301-319.
64. Romano G, Giordano A. Role of the cyclin-dependent kinase 9-related pathway in mammalian gene expression and human diseases. Cell Cycle 2008, 7:3664-3668.
65. Espinoza-Derout J, Wagner M, Salciccioli L, Lazar JM, Bhaduri S, Mascareno E, Chaqour B, Siddiqui MA. Positive transcription elongation factor b activity in compensatory myocardial hypertrophy is regulated by cardiac lineage protein-1. Circ Res 2009, 104:1347-1354.
66. Ai N, Hu X, Ding F, Yu B, Wang H, Lu X, Zhang K, Li Y, Han A, Lin W, Liu R, Chen R. Signal-induced Brd4 release from chromatin is essential for its role transition from chromatin targeting to transcriptional regulation. Nucleic Acids Res 2011, 39:9592-9604.
67. Kim YK, Mbonye U, Hokello J, Karn J. T-cell receptor signaling enhances transcriptional elongation from latent HIV proviruses by activating P-TEFb through an ERK-dependent pathway. J Mol Biol 2011, 410:896-916.
68. Contreras X, Barboric M, Lenasi T, Peterlin BM. HMBA releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS Pathog 2007, 3:1459-1469.
69. Zhu Y, Pe'ery T, Peng J, Ramanathan Y, Marshall N, Marshall T, Amendt B, Mathews MB, Price DH. Transcription elongation factor P-TEFb is required for HIV-1 tat transactivation in vitro. Genes Dev 1997, 11:2622-2632.
70. Mancebo HS, Lee G, Flygare J, Tomassini J, Luu P, Zhu Y, Peng J, Blau C, Hazuda D, Price D, Flores O. P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev 1997, 11:2633-2644.
71. Cho S, Schroeder S, Ott M. CYCLINg through transcription: posttranslational modifications of P-TEFb regulate transcription elongation. Cell Cycle 2010, 9:1697-1705.
72. Huang HD, Lee TY, Tzeng SW, Horng JT. KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites. Nucleic Acids Res 2005, 33:W226-W229.
73. Marshall NF, Price DH. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J Biol Chem 1995, 270:12335-12338.
74. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M, Pelisch F, Cramer P, Bentley D, Kornblihtt AR. A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 2003, 12:525-532.
75. Bird G, Zorio DA, Bentley DL. RNA polymerase II carboxy-terminal domain phosphorylation is required for cotranscriptional pre-mRNA splicing and 3'-end formation. Mol Cell Biol 2004, 24:8963-8969.
76. Kornblihtt AR. Coupling transcription and alternative splicing. Adv Expt Med Biol 2007, 623:175-189.
77. Dutertre M, Sanchez G, De Cian MC, Barbier J, Dardenne E, Gratadou L, Dujardin G, Le Jossic-Corcos C, Corcos L, Auboeuf D. Cotranscriptional exon skipping in the genotoxic stress response. Nat Struct Mol Biol 2010, 17:1358-1366.
78. Lenasi T, Barboric M. P-TEFb stimulates transcription elongation and pre-mRNA splicing through multilateral mechanisms. RNA Biol 2010, 7:145-150.
79. Barboric M, Lenasi T, Chen H, Johansen EB, Guo S, Peterlin BM. 7SK snRNP/P-TEFb couples transcription elongation with alternative splicing and is essential for vertebrate development. Proc Natl Acad Sci USA 2009, 106:7798-7803.
80. Eilebrecht S, Brysbaert G, Wegert T, Urlaub H, Benecke BJ, Benecke A. 7SK small nuclear RNA directly affects HMGA1 function in transcription regulation. Nucleic Acids Res 2011, 39:2057-2072.
81. Cleynen I, Van de Ven WJ. The HMGA proteins: a myriad of functions (Review). Int J Oncol 2008, 32:289-305.
82. Eilebrecht S, Becavin C, Leger H, Benecke BJ, Benecke A. HMGA1-dependent and independent 7SK RNA gene regulatory activity. RNA Biology 2011, 8:143-157.
83. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
84. Burrows C, Latip NA, Lam SJ, Carpenter L, Sawicka K, Tzolovsky G, Gabra H, Bushell M, Glover DM, Willis AE, Blagden SP. The RNA binding protein Larp1 regulates cell division, apoptosis and cell migration. Nucleic Acids Res 2009, 38:5542-5553.
85. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008, 9:102-114.
86. Duncan KE, Strein C, Hentze MW. The SXL-UNR corepressor complex uses a PABP-mediated mechanism to inhibit ribosome recruitment to msl-2 mRNA. Mol Cell 2009, 36:571-582.
87. Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H. Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol 2008, 181:639-653.
88. Clouse KN, Ferguson SB, Schupbach T. Squid, Cup, and PABP55B function together to regulate gurken translation in Drosophila. Dev Biol 2008, 313:713-724.
89. Kugler JM, Lasko P. Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly 2009, 3:15-28.
90. Lasko P. Posttranscriptional regulation in Drosophila oocytes and early embryos. WIRes RNA 2011, 2:408-416.
91. Chopra VS, Hong JW, Levine M. Regulation of Hox gene activity by transcriptional elongation in Drosophila. Curr Biol 2009, 19:688-693.
92. Harbison ST, Carbone MA, Ayroles JF, Stone EA, Lyman RF, Mackay TF. Co-regulated transcriptional networks contribute to natural genetic variation in Drosophila sleep. Nat Genet 2009, 41:371-375.
93. Wery M, Kwapisz M, Morillon A. Noncoding RNAs in gene regulation. WIRes Syst Biol Med 2011, 3:728-738.
94. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011, 43:904-914.