A genomic analysis of RNA polymerase II modification and chromatin architecture related to 3′ end RNA polyadenylation

Genome Research

Volumn 18, Issue 8, 2008, Pages 1224-1237

  Lian, Zheng ^a   Karpikov, Alexander ^b   Lian, Jin ^a   Mahajan, Milind C ^a   Hartman, Stephen ^b   Gerstein, Mark ^b   Snyder, Michael ^b   Weissman, Sherman M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DNA; MESSENGER RNA; RNA; RNA POLYMERASE II;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; DNA FLANKING REGION; DNA MICROARRAY; DNA MODIFICATION; ENZYME PHOSPHORYLATION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTRON; METHYLATION; POLYADENYLATION; PRIORITY JOURNAL;

CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENOMICS; HELA CELLS; HISTONES; HUMANS; LYSINE; METHYLATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYADENYLATION; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 48949092575     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.075804.107     Document Type: Article

References (75)

1. Ahn, S.H., Kim, M., and Buratowski, S. 2004. Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell 13: 67-76.
2. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
3. Beaudoing, E., Freier, S., Wyatt, J.R., Claverie, J.M., and Gautheret, D. 2000. Patterns of variant polyadenylation signal usage in human genes. Genome Res. 10: 1001-1010.
4. Bernstein, B.E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D.K., Huebert, D.J., McMahon, S., Karlsson, E.K., Kulbokas III, E.J., Gingeras, T.R., et al. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181.
5. Bertone, P., Stolc, V., Royce, T.E., Rozowsky, J.S., Urban, A.E., Zhu, X., Rinn, J.L., Tongprasit, W., Samanta, M., Weissman, S., et al. 2004. Global identification of human transcribed sequences with genome tiling arrays. Science 306: 2242-2246.
6. Birse, C.E., Lee, B.A., Hansen, K., and Proudfoot, N.J. 1997. Transcriptional termination signals for RNA polymerase II in fission yeast. EMBO J. 16: 3633-3643.
7. Brodsky, A.S., Meyer, C.A., Swinburne, I.A., Hall, G., Keenan, B.J., Liu, X.S., Fox, E.A., and Silver, P.A. 2005. Genomic mapping of RNA polymerase II reveals sites of co-transcriptional regulation in human cells. Genome Biol. 6: R64. doi: 10.1186/gb-2005-6-8-r64.
8. Buratowski, S. 2003. The CTD code. Nat. Struct. Biol. 10: 679-680.
9. Buratowski, S. 2005. Connections between mRNA 3′ end processing and transcription termination. Curr. Opin. Cell Biol. 17: 257-261.
10. Carninci, P. and Hayashizaki, Y. 2007. Noncoding RNA transcription beyond annotated genes. Curr. Opin. Genet. Dev. 17: 139-144.
11. Carrozza, M.J., Li, B., Florens, L., Suganuma, T., Swanson, S.K., Lee, K.K., Shia, W.J., Anderson, S., Yates, J., Washburn, M.P., et al. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581-592.
12. Cheng, J., Kapranov, P., Drenkow, J., Dike, S., Brubaker, S., Patel, S., Long, J., Stern, D., Tammana, H., Helt, G., et al. 2005. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308: 1149-1154.
13. Cheng, Y., Miura, R.M., and Tian, B. 2006. Prediction of mRNA polyadenylation sites by support vector machine. Bioinformatics 22: 2320-2325.
14. Choi, Y.H. and Hagedorn, C.H. 2003. Purifying mRNAs with a high-affinity eIF4E mutant identifies the short 3′ poly(A) end phenotype. Proc. Natl. Acad. Sci. 100: 7033-7038.
15. Cuthbert, G.L., Daujat, S., Snowden, A.W., Erdjument-Bromage, H., Hagiwara, T., Yamada, N., Schneider, R., Gregory, P.D., Tempst, P., Bannister, A.J., et al. 2004. Histone deimination antagonizes arginine methylation. Cell 118: 545-553.
16. De Gobbi, M., Viprakasit, V., Hughes, J.R., Fisher, C., Buckle, V.J., Ayyub, H., Gibbons, R.J., Vernimmen, D., Yoshinaga, Y., de Jong, P., et al. 2006. A regulatory SNP causes a human genetic disease by creating a new transcriptional promoter. Science 312: 1215-1217.
17. Denoeud, F., Kapranov, P., Ucla, C., Frankish, A., Castelo, R., Drenkow, J., Lagarde, J., Alioto, T., Manzano, C., Chrast, J., et al. 2007. Prominent use of distal 5′ transcription start sites and discovery of a large number of additional exons in ENCODE regions. Genome Res. 17: 746-759.
18. Ebraliddze, A. and Tenen, D.G. 2006. Regulation of the PU.1 gene by sense and functional antisense RNAs generated through the same chromatin architecture. Blood 108 (Suppl.): 234a.
19. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
20. Furuno, M., Pang, K.C., Ninomiya, N., Fukuda, S., Frith, M.C., Bult, C., Kai, C., Kawai, J., Carninci, P., Hayashizaki, Y., et al. 2006. Clusters of internally primed transcripts reveal novel long noncoding RNAs. PLoS Genet. 2: e37. doi: 10.1371/journal.pgen.0020037.
21. Gingeras, T.R. 2007. Origin of phenotypes: Genes and transcripts. Genome Res. 17: 682-690.
22. Goodrich, J.A. and Kugel, J.F. 2006. Non-coding-RNA regulators of RNA polymerase II transcription. Nat. Rev. Mol. Cell Biol. 7: 612-616.
23. Hayashizaki, Y. and Carninci, P. 2006. Genome network and FANTOM3: Assessing the complexity of the transcriptome. PLoS Genet. 2: e63. doi: 10.1371/journal.pgen.0020063.
24. Heintzman, N.D., Stuart, R.K., Hon, G., Fu, Y., Ching, C.W., Hawkins, R.D., Barrera, L.O., Van Calcar, S., Qu, C., Ching, K.A., et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39: 311-318.
25. Ho, Y., Elefant, F., Liebhaber, S.A., and Cooke, N.E. 2006. Locus control region transcription plays an active role in long-range gene activation. Mol. Cell 23: 365-375.
26. Hoogenkamp, M., Krysinska, H., Ingram, R., Huang, G., Barlow, R., Clarke, D., Ebralidze, A., Zhang, P., Tagoh, H., Cockerill, P.N., et al. 2007. The Pu.1 locus is differentially regulated at the level of chromatin structure and noncoding transcription by alternate mechanisms at distinct developmental stages of hematopoiesis. Mol. Cell. Biol. 27: 7425-7438.
27. Joshi, A.A. and Struhl, K. 2005. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20: 971-978.
28. Kampa, D., Cheng, J., Kapranov, P., Yamanaka, M., Brubaker, S., Cawley, S., Drenkow, J., Piccolboni, A., Bekiranov, S., Helt, G., et al. 2004. Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res. 14: 331-342.
29. Kapranov, P., Cawley, S.E., Drenkow, J., Bekiranov, S., Strausberg, R.L., Fodor, S.P., and Gingeras, T.R. 2002. Large-scale transcriptional activity in chromosomes 21 and 22. Science 296: 916-919.
30. Kapranov, P., Drenkow, J., Cheng, J., Long, J., Helt, G., Dike, S., and Gingeras, T.R. 2005. Examples of the complex architecture of the human transcriptome revealed by RACE and high-density tiling arrays. Genome Res. 15: 987-997.
31. Kapranov, P., Willingham, A.T., and Gingeras, T.R. 2007a. Genome-wide transcription and the implications for genomic organization. Nat. Rev. Genet. 8: 413-423.
32. Kapranov, P., Cheng, J., Dike, S., Nix, D.A., Duttagupta, R., Willingham, A.T., Stadler, P.F., Hertel, J., Hackermüller, J., Hofacker, I.L., et al. 2007b. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316: 1484-1488.
33. Kelley, R.L. and Kuroda, M.I. 2000. Noncoding RNA genes in dosage compensation and imprinting. Cell 103: 9-12.
34. Keogh, M.C., Kurdistani, S.K., Morris, S.A., Ahn, S.H., Podolny, V., Collins, S.R., Schuldiner, M., Chin, K., Punna, T., Thompson, N.J., et al. 2005. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605.
35. Khanna-Gupta, A., Kolibaba, K., Zibello, T.A., and Berliner, N. 1994. NB4 cells show bilineage potential and an aberrant pattern of neutrophil secondary granule protein gene expression. Blood 84: 294-302.
36. Kizer, K.O., Phatnani, H.P., Shibata, Y., Hall, H., Greenleaf, A.L., and Strahl, B.D. 2005. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol. Cell. Biol. 25: 3305-3316.
37. Koch, C.M., Andrews, R.M., Flicek, P., Dillon, S.C., Karaöz, U., Clelland, G.K., Wilcox, S., Beare, D.M., Fowler, J.C., Couttet, P., et al. 2007. The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res. 17: 691-707.
38. Kodzius, R., Kojima, M., Nishiyori, H., Nakamura, M., Fukuda, S., Tagami, M., Sasaki, D., Imamura, K., Kai, C., Harbers, M., et al. 2006. CAGE: Cap Analysis of Gene Expression. Nat. Methods 3: 211-222.
39. Lanotte, M., Martin-Thouvenin, V., Najman, S., Balerini, P., Valensi, F., and Berger, R. 1991. NB4, a maturation inducible cell line with t(15;17) marker isolated from a human acute promyelocytic leukemia (M3). Blood 77: 1080-1086.
40. Le Texier, V., Riethoven, J.J., Kumanduri, V., Gopalakrishnan, C., Lopez, F., and Thanaraj, T.A. 2006. AltTrans: Transcript pattern variants annotated for both alternative splicing and alternative polyadenylation. BMC Bioinformatics 7: 169. doi: 10.1186/1471-2105-7-169.
41. Li, B., Gogol, M., Carey, M., Lee, D., Seidel, C., and Workman, J.L. 2007. Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316: 1050-1054.
42. Liang, G., Klose, R.J., Gardner, K.E., and Zhang, Y. 2007. Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat. Struct. Mol. Biol. 14: 243-245.
43. Maeda, N., Kasukawa, T., Oyama, R., Gough, J., Frith, M., Engström, P.G., Lenhard, B., Aturaliya, R.N., Batalov, S., Beisel, K.W., et al. 2006. Transcript annotation in FANTOM3: Mouse gene catalog based on physical cDNAs. PLoS Genet. 2: e62. doi: 10.1371/journal.pgen.0020062.
44. Maruyama, K. and Sugano, S. 1994. Oligo-capping: A simple method to replace the cap structure of eukaryotic mRNAs with oligoribonucleotides. Gene 138: 171-174.
45. Mattick, J.S. and Makunin, I.V. 2006. Non-coding RNA. Hum. Mol. Genet. 15: R17-R29. doi: 10.1093/hmg/ddl046.
46. Migliaccio, G., Di Pietro, R., di Giacomo, V., Di Baldassarre, A., Migliaccio, A.R., Maccioni, L., Galanello, R., and Papayannopoulou, T. 2002. In vitro mass production of human erythroid cells from the blood of normal donors and of thalassemic patients. Blood Cells Mol. Dis. 28: 169-180.
47. Morillon, A., Karabetsou, N., Nair, A., and Mellor, J. 2005. Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol. Cell 18: 723-734.
48. Moucadel, V., Lopez, F., Ara, T., Benech, P., and Gautheret, D. 2007. Beyond the 3′ end: Experimental validation of extended transcript isoforms. Nucleic Acids Res. 35: 1947-1957.
49. Nag, A., Narsinh, K., Kazerouninia, A., and Martinson, H.G. 2006. The conserved AAUAAA hexamer of the poly(A) signal can act alone to trigger a stable decrease in RNA polymerase II transcription velocity. RNA 12: 1534-1544.
50. Ng, P., Tan, J.J., Ooi, H.S., Lee, Y.L., Chiu, K.P., Fullwood, M.J., Srinivasan, K.G., Perbost, C., Du, L., Sung, W.K., et al. 2006. Multiplex sequencing of paired-end ditags (MS-PET): A strategy for the ultra-high-throughput analysis of transcriptomes and genomes. Nucleic Acids Res. 34: e84. doi: 10.1093/nar/gkl444.
51. Osheim, Y.N., Sikes, M.L., and Beyer, A.L. 2002. EM visualization of Pol II genes in Drosophila: Most genes terminate without prior 3′ end cleavage of nascent transcripts. Chromosoma 111: 1-12.
52. Pang, K.C., Frith, M.C., and Mattick, J.S. 2006. Rapid evolution of noncoding RNAs: Lack of conservation does not mean lack of function. Trends Genet. 22: 1-5.
53. Pauler, F.M., Koerner, M.V., and Barlow, D.P. 2007. Silencing by imprinted noncoding RNAs: Is transcription the answer? Trends Genet. 23: 284-292.
54. Phatnani, H.P. and Greenleaf, A.L. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes & Dev. 20: 2922-2936.
55. Prasanth, K.V. and Spector, D.L. 2007. Eukaryotic regulatory RNAs: An answer to the "genome complexity" conundrum. Genes & Dev. 21: 11-42.
56. Prashar, Y. and Weissman, S.M. 1996. Analysis of differential gene expression by display of 3′ end restriction fragments of cDNAs. Proc. Natl. Acad. Sci. 93: 659-663.
57. Rinn, J.L., Euskirchen, G., Bertone, P., Martone, R., Luscombe, N.M., Hartman, S., Harrison, P.M., Nelson, F.K., Miller, P., Gerstein, M., et al. 2003. The transcriptional activity of human chromosome 22. Genes & Dev. 17: 529-540.
58. Roma, G., Cobellis, G., Claudiani, P., Maione, F., Cruz, P., Tripoli, G., Sardiello, M., Peluso, I., and Stupka, E. 2007. A novel view of the transcriptome revealed from gene trapping in mouse embryonic stem cells. Genome Res. 17: 1051-1060.
59. Rozowsky, J., Wu, J., Lian, Z., Nagalakshmi, U., Korbel, J.O., Kapranov, P., Zheng, D., Dyke, S., Newburger, P., Miller, P., et al. 2006. Novel transcribed regions in the human genome. Cold Spring Harb. Symp. Quant. Biol. 71: 111-116.
60. Saha, S., Sparks, A.B., Rago, C., Akmaev, V., Wang, C.J., Vogelstein, B., Kinzler, K.W., and Velculescu, V.E. 2002. Using the transcriptome to annotate the genome. Nat. Biotechnol. 20: 508-512.
61. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J., and Kouzarides, T. 2002. Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411.
62. Schneider, R., Bannister, A.J., Myers, F.A., Thorne, A.W., Crane-Robinson, C., and Kouzarides, T. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 6: 73-77.
63. Secombe, J., Li, L., Carlos, L., and Eisenman, R.N. 2007. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes & Dev. 21: 537-551.
64. Shamovsky, I. and Nudler, E. 2006. Gene control by large noncoding RNAs. Sci. STKE 2006: pe40. doi: 10.1126/stke.3552006pe40.
65. Sims III, R.J., Belotserkovskaya, R., and Reinberg, D. 2004. Elongation by RNA polymerase II: The short and long of it. Genes & Dev. 18: 2437-2468.
66. Subrahmanyam, Y.V., Yamaga, S., Prashar, Y., Lee, H.H., Hoe, N.P., Kluger, Y., Gerstein, M., Goguen, J.D., Newburger, P.E., and Weissman, S.M. 2001. RNA expression patterns change dramatically in human neutrophils exposed to bacteria. Blood 97: 2457-2468.
67. Taft, R.J., Pheasant, M., and Mattick, J.S. 2007. The relationship between non-protein-coding DNA and eukaryotic complexity. BioEssays 29: 288-299.
68. Tsukahara, Y., Lian, Z., Zhang, X., Whitney, C., Kluger, Y., Tuck, D., Yamaga, S., Nakayama, Y., Weissman, S.M., and Newburger, P.E. 2003. Gene expression in human neutrophils during activation and priming by bacterial lipopolysaccharide. J. Cell. Biochem. 89: 848-861.
69. Venkataraman, K., Brown, K.M., and Gilmartin, G.M. 2005. Analysis of a noncanonical poly(A) site reveals a tripartite mechanism for vertebrate poly(A) site recognition. Genes & Dev. 19: 1315-1327.
70. Wei, C.L., Ng, P., Chiu, K.P., Wong, C.H., Ang, C.C., Lipovich, L., Liu, E.T., and Ruan, Y. 2004. 5′ Long serial analysis of gene expression (LongSAGE) and 3′ LongSAGE for transcriptome characterization and genome annotation. Proc. Natl. Acad. Sci. 101: 11701-11706.
71. West, S., Zaret, K., and Proudfoot, N.J. 2006. Transcriptional termination sequences in the mouse serum albumin gene. RNA 12: 655-665.
72. Xiang, P., Fang, X., Yin, W., Barkess, G., and Li, Q. 2006. Non-coding transcripts far upstream of the epsilon-globin gene are distinctly expressed in human primary tissues and erythroleukemia cell lines. Biochem. Biophys. Res. Commun. 344: 623-630.
73. Yang, P.K. and Kuroda, M.I. 2007. Noncoding RNAs and intranuclear positioning in monoallelic gene expression. Cell 128: 777-786.
74. Zhang, Z.D., Rozowsky, J., Lam, H.Y., Du, J., Snyder, M., and Gerstein, M. 2007. Tilescope: Online analysis pipeline for high-density tiling microarray data. Genome Biol. 8: R81. doi: 10.1186/gb-2007-8-5-r81.
75. Zhao, H., Kim, A., Song, S.H., and Dean, A. 2006. Enhancer blocking by chicken beta-globin 5′-HS4: Role of enhancer strength and insulator nucleosome depletion. J. Biol. Chem. 281: 30573-30580.