Regulation of mRNA cap methylation

Biochemical Journal

Volumn 425, Issue 2, 2010, Pages 295-302

  Cowling, Victoria H ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Gene regulation; mRNA cap methylation; Transcription; Translation

Indexed keywords

BIOLOGICAL PROCESS; CAP METHYLATION; CELL VIABILITY; CELLULAR ENZYMES; CELLULAR MRNAS; EUKARYOTIC ORGANISMS; EXPERIMENTAL SYSTEM; GENE REGULATIONS; GUANOSINES; MRNA CAP METHYLATION; NUCLEAR EXPORT; POLYADENYLATION;

ALKYLATION; METHYLATION; SYNTHESIS (CHEMICAL);

TRANSCRIPTION;

7 METHYLGUANOSINE; ABD1 PROTEIN; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 34; KARYOPHERIN ALPHA; MESSENGER RNA; MYC PROTEIN; RNA METHYLTRANSFERASE; RNA POLYMERASE II; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG;

CARBOXY TERMINAL SEQUENCE; CELL LINEAGE; CELL SURVIVAL; CELL VIABILITY; DEMETHYLATION; HUMAN; NONHUMAN; NUCLEAR EXPORT SIGNAL; POINT MUTATION; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; RNA DEGRADATION; RNA METHYLATION; RNA PROCESSING; RNA SPLICING; RNA STABILITY; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TRANSCRIPTION REGULATION;

GENE EXPRESSION REGULATION; GUANOSINE; METHYLATION; RNA CAPS; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 73849107519     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20091352     Document Type: Review

References (84)

1. Shuman, S. (2002) What messenger RNA capping tells us about eukaryotic evolution. Nat. Rev. Mol. Cell. Biol. 3, 619-625
2. Furuichi, Y. and Shatkin, A. J. (2000) Viral and cellular mRNA capping: past and prospects. Adv. Virus Res. 55, 135-184
3. Shatkin, A. J. (1976) Capping of eucaryotic mRNAs. Cell 9, 645-653
4. Shibagaki, Y., Itoh, N., Yamada, H., Nagata, S. and Mizumoto, K. (1992) mRNA capping enzyme. Isolation and characterization of the gene encoding mRNA guanylytransferase subunit from Saccharomyces cerevisiae. J. Biol. Chem. 267, 9521-9528
5. Tsukamoto, T., Shibagaki, Y., Imajoh-Ohmi, S., Murakoshi, T., Suzuki, M., Nakamura, A., Gotoh, H. and Mizumoto, K. (1997) Isolation and characterization of the yeast mRNA capping enzyme beta subunit gene encoding RNA 5′-triphosphatase, which is essential for cell viability. Biochem. Biophys. Res. Commun. 239, 116-122
6. Mao, X., Schwer, B. and Shuman, S. (1995) Yeast mRNA cap methyltransferase is a 50-kilodalton protein encoded by an essential gene. Mol. Cell. Biol. 15, 4167-4174
7. Yue, Z., Maldonado, E., Pillutla, R., Cho, H., Reinberg, D. and Shatkin, A. J. (1997) Mammalian capping enzyme complements mutant Saccharomyces cerevisiae lacking mRNA guanylyltransferase and selectively binds the elongating form of RNA polymerase II. Proc. Natl. Acad. Sci. U.S.A. 94, 12898-12903
8. Tsukamoto, T., Shibagaki, Y., Niikura, Y. and Mizumoto, K. (1998) Cloning and characterization of three human cDNAs encoding mRNA (guanine-7-)-methyltransferase, an mRNA cap methylase. Biochem. Biophys. Res. Commun. 251, 27-34
9. Yamada-Okabe, T., Doi, R., Shimmi, O., Arisawa, M. and Yamada-Okabe, H. (1998) Isolation and characterization of a human cDNA for mRNA 5′-capping enzyme. Nucleic Acids Res. 26, 1700-1706
10. Pillutla, R. C., Shimamoto, A., Furuichi, Y. and Shatkin, A. J. (1998) Human mRNA capping enzyme (RNGTT) and cap methyltransferase (RNMT) map to 6q16 and 18p11.22-p11.23, respectively. Genomics 54, 351-353
11. Ishikawa, K., Nagase, T., Nakajima, D., Seki, N., Ohira, M., Miyajima, N., Tanaka, A., Kotani, H., Nomura, N. and Ohara, O. (1997) Prediction of the coding sequences of unidentified human genes. VIII. 78 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 4, 307-313
12. Moteki, S. and Price, D. (2002) Functional coupling of capping and transcription of mRNA. Mol. Cell 10, 599-609
13. Cole, M. D. and Cowling, V. H. (2008) Transcription-independent functions of MYC: regulation of translation and DNA replication. Nat. Rev. Mol. Cell. Biol. 9, 810-815
14. Konarska, M. M., Padgett, R. A. and Sharp, P. A. (1984) Recognition of cap structure in splicing in vitro of mRNA precursors. Cell 38, 731-736
15. Edery, I. and Sonenberg, N. (1985) Cap-dependent RNA splicing in a HeLa nuclear extract. Proc. Natl. Acad. Sci. U.S.A. 82, 7590-7594
16. Ohno, M., Sakamoto, H. and Shimura, Y. (1987) Preferential excision of the 5′ proximal intron from mRNA precursors with two introns as mediated by the cap structure. Proc. Natl. Acad. Sci. U.S.A. 84, 5187-5191
17. Inoue, K., Ohno, M., Sakamoto, H. and Shimura, Y. (1989) Effect of the cap structure on pre-mRNA splicing in Xenopus oocyte nuclei. Genes Dev. 3, 1472-1479
18. Fresco, L. D. and Buratowski, S. (1996) Conditional mutants of the yeast mRNA capping enzyme show that the cap enhances, but is not required for, mRNA splicing. RNA 2, 584-596
19. Schwer, B. and Shuman, S. (1996) Conditional inactivation of mRNA capping enzyme affects yeast pre-mRNA splicing in vivo. RNA 2, 574-583
20. Schwer, B., Mao, X. and Shuman, S. (1998) Accelerated mRNA decay in conditional mutants of yeast mRNA capping enzyme. Nucleic Acids Res. 26, 2050-2057
21. Izaurralde, E., Lewis, J., McGuigan, C., Jankowska, M., Darzynkiewicz, E. and Mattaj, I. W. (1994) A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell 78, 657-668
22. Izaurralde, E., Lewis, J., Gamberi, C., Jarmolowski, A., McGuigan, C. and Mattaj, I. W. (1995) A cap-binding protein complex mediating U snRNA export. Nature 376, 709-712
23. Lewis, J. D., Izaurralde, E., Jarmolowski, A., McGuigan, C. and Mattaj, I. W. (1996) A nuclear cap-binding complex facilitates association of U1 snRNP with the cap-proximal 5′ splice site. Genes Dev. 10, 1683-1698
24. Colot, H. V., Stutz, F. and Rosbash, M. (1996) The yeast splicing factor Mud13p is a commitment complex component and corresponds to CBP20, the small subunit of the nuclear cap-binding complex. Genes Dev. 10, 1699-1708
25. Maniatis, T. and Reed, R. (2002) An extensive network of coupling among gene expression machines. Nature 416, 499-506
26. Spriggs, K. A., Stoneley, M., Bushell, M. and Willis, A. E. (2008) Re-programming of translation following cell stress allows IRES-mediated translation to predominate. Biol. Cell 100, 27-38
27. Muthukrishnan, S., Both, G. W., Furuichi, Y. and Shatkin, A. J. (1975) 5′-Terminal 7-methylguanosine in eukaryotic mRNA is required for translation. Nature 255, 33-37
28. Both, G. W., Banerjee, A. K. and Shatkin, A. J. (1975) Methylation-dependent translation of viral messenger RNAs in vitro. Proc. Natl. Acad. Sci. U.S.A. 72, 1189-1193
29. Drummond, D. R., Armstrong, J. and Colman, A. (1985) The effect of capping and polyadenylation on the stability, movement and translation of synthetic messenger RNAs in Xenopus oocytes. Nucleic Acids Res. 13, 7375-7394
30. Gillian-Daniel, D. L., Gray, N. K., Astrom, J., Barkoff, A. and Wickens, M. (1998) Modifications of the 5′ cap of mRNAs during Xenopus oocyte maturation: independence from changes in poly(A) length and impact on translation. Mol. Cell. Biol. 18, 6152-6163
31. Schwer, B., Saha, N., Mao, X., Chen, H. W. and Shuman, S. (2000) Structure-function analysis of yeast mRNA cap methyltransferase and high-copy suppression of conditional mutants by AdoMet synthase and the ubiquitin conjugating enzyme Cdc34p. Genetics 155, 1561-1576
32. Gingras, A. C., Raught, B. and Sonenberg, N. (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68, 913-963
33. von der Haar, T., Gross, J. D., Wagner, G. and McCarthy, J. E. (2004) The mRNA cap-binding protein eIF4E in post-transcriptional gene expression. Nat. Struct. Mol. Biol. 11, 503-511
34. Shatkin, A. J. and Manley, J. L. (2000) The ends of the affair: capping and polyadenylation. Nat. Struct. Biol. 7, 838-842
35. Flaherty, S. M., Fortes, P., Izaurralde, E., Mattaj, I. W. and Gilmartin, G. M. (1997) Participation of the nuclear cap binding complex in pre-mRNA 3′ processing. Proc. Natl. Acad. Sci. U.S.A. 94, 11893-11898
36. Glover-Cutter, K., Kim, S., Espinosa, J. and Bentley, D. L. (2008) RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes. Nat. Struct. Mol. Biol. 15, 71-78
37. Jarmolowski, A., Boelens, W. C., Izaurralde, E. and Mattaj, I. W. (1994) Nuclear export of different classes of RNA is mediated by specific factors. J. Cell Biol. 124, 627-635
38. Furuichi, Y., LaFiandra, A. and Shatkin, A. J. (1977) 5′-Terminal structure and mRNA stability. Nature 266, 235-239
39. Shimotohno, K., Kodama, Y., Hashimoto, J. and Miura, K. I. (1977) Importance of 5′-terminal blocking structure to stabilize mRNA in eukaryotic protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 74, 2734-2738
40. Murthy, K. G., Park, P. and Manley, J. L. (1991) A nuclear micrococcal-sensitive, ATP-dependent exoribonuclease degrades uncapped but not capped RNA substrates. Nucleic Acids Res. 19, 2685-2692
41. Bentley, D. L. (2005) Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr. Opin. Cell Biol. 17, 251-256
42. Ensinger, M. J. and Moss, B. (1976) Modification of the 5′ terminus of mRNA by an RNA (guanine-7-)-methyltransferase from HeLa cells. J. Biol. Chem. 251, 5283-5291
43. Mizumoto, K. and Lipmann, F. (1979) Transmethylation and transguanylylation in 5′-RNA capping system isolated from rat liver nuclei. Proc. Natl. Acad. Sci. U.S.A. 76, 4961-4965
44. Saha, N., Schwer, B. and Shuman, S. (1999) Characterization of human, Schizosaccharomyces pombe, and Candida albicans mRNA cap methyltransferases and complete replacement of the yeast capping apparatus by mammalian enzymes. J. Biol. Chem. 274, 16553-16562
45. Pei, Y., Du, H., Singer, J., Stamour, C., Granitto, S., Shuman, S. and Fisher, R. P. (2006) Cyclin-dependent kinase 9 (Cdk9) of fission yeast is activated by the CDK-activating kinase Csk1, overlaps functionally with the TFIIH-associated kinase Mcs6, and associates with the mRNA cap methyltransferase Pcm1 in vivo. Mol. Cell. Biol. 26, 777-788
46. Shafer, B., Chu, C. and Shatkin, A. J. (2005) Human mRNA cap methyltransferase: alternative nuclear localization signal motifs ensure nuclear localization required for viability. Mol. Cell. Biol. 25, 2644-2649
47. Chu, C. and Shatkin, A. J. (2008) Apoptosis and autophagy induction in mammalian cells by small interfering RNA knockdown of mRNA capping enzymes. Mol. Cell. Biol. 28, 5829-5836
48. Wang, S. P. and Shuman, S. (1997) Structure-function analysis of the mRNA cap methyltransferase of Saccharomyces cerevisiae. J. Biol. Chem. 272, 14683-14689
49. Mao, X., Schwer, B. and Shuman, S. (1996) Mutational analysis of the Saccharomyces cerevisiae ABD1 gene: cap methyltransferase activity is essential for cell growth. Mol. Cell. Biol. 16, 475-480
50. Wen, Y. and Shatkin, A. J. (2000) Cap methyltransferase selective binding and methylation of GpppG-RNA are stimulated by importin-α. Genes Dev. 14, 2944-2949
51. Phatnani, H. P. and Greenleaf, A. L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20, 2922-2936
52. Moore, M. J. and Proudfoot, N. J. (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700
53. Chapman, R. D., Heidemann, M., Hintermair, C. and Eick, D. (2008) Molecular evolution of the RNA polymerase II CTD. Trends Genet. 24, 289-296
54. Egloff, S. and Murphy, S. (2008) Cracking the RNA polymerase II CTD code. Trends Genet. 24, 280-288
55. McCracken, S., Fong, N., Rosonina, E., Yankulov, K., Brothers, G., Siderovski, D., Hessel, A., Foster, S., Shuman, S. and Bentley, D. L. (1997) 5′-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11, 3306-3318
56. Ho, C. K., Sriskanda, V., McCracken, S., Bentley, D., Schwer, B. and Shuman, S. (1998) The guanylyltransferase domain of mammalian mRNA capping enzyme binds to the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 273, 9577-9585
57. Pillutla, R. C., Yue, Z., Maldonado, E. and Shatkin, A. J. (1998) Recombinant human mRNA cap methyltransferase binds capping enzyme/RNA polymerase IIo complexes. J. Biol. Chem. 273, 21443-21446
58. Pei, Y. and Shuman, S. (2002) Interactions between fission yeast mRNA capping enzymes and elongation factor Spt5. J. Biol. Chem. 277, 19639-19648
59. Wen, Y. and Shatkin, A. J. (1999) Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev. 13, 1774-1779
60. Lindstrom, D. L., Squazzo, S. L., Muster, N., Burckin, T. A., Wachter, K. C., Emigh, C. A., McCleery, J. A., Yates, 3rd, J. R. and Hartzog, G. A. (2003) Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol. Cell. Biol. 23, 1368-1378
61. Ho, C. K. and Shuman, S. (1999) Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 3, 405-411
62. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. and Young, R. A. (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88
63. Jove, R. and Manley, J. L. (1982) Transcription initiation by RNA polymerase II is inhibited by S-adenosylhomocysteine. Proc. Natl. Acad. Sci. U.S.A. 79, 5842-5846
64. Mandal, S. S., Chu, C., Wada, T., Handa, H., Shatkin, A. J. and Reinberg, D. (2004) Functional interactions of RNA-capping enzyme with factors that positively and negatively regulate promoter escape by RNA polymerase II. Proc. Natl. Acad. Sci. U.S.A. 101, 7572-7577
65. Kim, H. J., Jeong, S. H., Heo, J. H., Jeong, S. J., Kim, S. T., Youn, H. D., Han, J. W., Lee, H. W. and Cho, E. J. (2004) mRNA capping enzyme activity is coupled to an early transcription elongation. Mol. Cell. Biol. 24, 6184-6193
66. Schroeder, S. C., Zorio, D. A., Schwer, B., Shuman, S. and Bentley, D. (2004) A function of yeast mRNA cap methyltransferase, Abd1, in transcription by RNA polymerase II. Mol. Cell 13, 377-387
67. Peterlin, B. M. and Price, D. H. (2006) Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23, 297-305
68. Pei, Y., Schwer, B. and Shuman, S. (2003) Interactions between fission yeast Cdk9, its cyclin partner Pch1, and mRNA capping enzyme Pct1 suggest an elongation checkpoint for mRNA quality control. J. Biol. Chem. 278, 7180-7188
69. Viladevall, L., St Amour, C. V., Rosebrock, A., Schneider, S., Zhang, C., Allen, J. J., Shokat, K. M., Schwer, B., Leatherwood, J. K. and Fisher, R. P. (2009) TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specific genes in fission yeast. Mol. Cell 33, 738-751
70. Guiguen, A., Soutourina, J., Dewez, M., Tafforeau, L., Dieu, M., Raes, M., Vandenhaute, J., Werner, M. and Hermand, D. (2007) Recruitment of P-TEFb (Cdk9-Pch1) to chromatin by the cap-methyl transferase Pcm1 in fission yeast. EMBO J. 26, 1552-1559
71. Takagi, T., Walker, A. K., Sawa, C., Diehn, F., Takase, Y., Blackwell, T. K. and Buratowski, S. (2003) The Caenorhabditis elegans mRNA 5′-capping enzyme. In vitro and in vivo characterization. J. Biol. Chem. 278, 14174-14184
72. Stewart, M. (2007) Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell. Biol. 8, 195-208
73. Cowling, V. H. and Cole, M. D. (2007) The Myc transactivation domain promotes global phosphorylation of the RNA polymerase II carboxy-terminal domain independently of direct DNA binding. Mol. Cell. Biol. 27, 2059-2073
74. Cole, M. D. and Cowling, V. H. (2009) Specific regulation of mRNA cap methylation by the c-Myc and E2F1 transcription factors. Oncogene 28, 1169-1175
75. Hulf, T., Bellosta, P., Furrer, M., Steiger, D., Svensson, D., Barbour, A. and Gallant, P. (2005) Whole-genome analysis reveals a strong positional bias of conserved dMyc-dependent E-boxes. Mol. Cell. Biol. 25, 3401-3410
76. Brown, S. J., Cole, M. D. and Erives, A. J. (2008) Evolution of the holozoan ribosome biogenesis regulon. BMC Genomics 9, 442
77. 2/M checkpoints. Genes Dev. 16, 245-256
78. Chiang, P. K., Gordon, R. K., Tal, J., Zeng, G. C., Doctor, B. P., Pardhasaradhi, K. and McCann, P. P. (1996) S-Adenosylmethionine and methylation. FASEB J. 10, 471-480
79. Radomski, N., Kaufmann, C. and Dreyer, C. (1999) Nuclear accumulation of S-adenosylhomocysteine hydrolase in transcriptionally active cells during development of Xenopus laevis. Mol. Biol. Cell. 10, 4283-4298
80. Radomski, N., Barreto, G., Kaufmann, C., Yokoska, J., Mizumoto, K. and Dreyer, C. (2002) Interaction of S-adenosylhomocysteine hydrolase of Xenopus laevis with mRNA(guanine-7-)methyltransferase: implication on its nuclear compartmentalisation and on cap methylation of hnRNA. Biochim. Biophys. Acta 1590, 93-102
81. Fernandez-Sanchez, M. E., Gonatopoulos-Pournatzis, T., Preston, G., Lawlor, M. A. and Cowling, V. H. (2009) S-Adenosyl homocysteine hydrolase (SAHH) is required for Myc-induced mRNA cap methylation, protein synthesis and cell proliferation. Mol. Cell. Biol. 29, 6182-6191
82. Franks, T. M. and Lykke-Andersen, J. (2008) The control of mRNA decapping and P-body formation. Mol. Cell 32, 605-615
83. Simon, E., Camier, S. and Seraphin, B. (2006) New insights into the control of mRNA decapping. Trends Biochem. Sci. 31, 241-243
84. Liu, H. and Kiledjian, M. (2006) Decapping the message: a beginning or an end. Biochem. Soc. Trans. 34, 35-38