Cotranscriptional processes and their influence on genome stability

Genes and Development

Volumn 20, Issue 14, 2006, Pages 1838-1847

  Li, Xialu ^a   Manley, James L ^a  

^a Columbia University ^*  (United States)

Author keywords

Cotranscriptional RNA processes; Genome stability; R loop

Indexed keywords

DNA HYBRID;

DNA STRAND BREAKAGE; DNA TRANSCRIPTION; GENE EXPRESSION; GENOMIC INSTABILITY; PRIORITY JOURNAL; REVIEW; RNA TRANSCRIPTION;

DNA DAMAGE; EVOLUTION; GENOMIC INSTABILITY; RNA; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC;

EID: 33746093492     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1438306     Document Type: Review

References (103)

1. Abruzzi, K.C., Lacadie, S., and Rosbash, M. 2004. Biochemical analysis of TREX complex recruitment to intronless and intron-containing yeast genes. EMBO J. 23: 2620-2631.
2. Aguilera, A. 2002. The connection between transcription and genomic instability. EMBO J. 21: 195-201.
3. _. 2005a. Cotranscriptional mRNP assembly: From the DNA to the nuclear pore. Curr. Opin. Cell Biol. 17: 242-250.
4. _. 2005b. mRNA processing and genomic instability. Nat. Struct. Mol. Biol. 12: 737-738.
5. Aguilera, A. and Klein, H.L. 1988. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 119: 779-790.
6. Baaklini, I., Hraiky, C., Rallu, F., Tse-Dinh, Y.C., and Drolet, M. 2004. RNase HI overproduction is required for efficient fulllength RNA synthesis in the absence of topoisomerase I in Escherichia coli. Mol. Microbiol. 54: 198-211.
7. Beale, R.C., Petersen-Mahrt, S.K., Watt, I.N., Harris, R.S., Rada, C., and Neuberger, M.S. 2004. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: Correlation with mutation spectra in vivo. J. Mol. Biol. 337: 585-596.
8. Bottaro, A., Lansford, R., Xu, L., Zhang, J., Rothman, P., and Alt, F.W. 1994. S region transcription per se promotes basal IgE class switch recombination but additional factors regulate the efficiency of the process. EMBO J. 13: 665-674.
9. Broccoli, S., Rallu, F., Sanscartier, P., Cerritelli, S.M., Crouch, R.J., and Drolet, M. 2004. Effects of RNA polymerase modifications on transcription-induced negative supercoiling and associated R-loop formation. Mol. Microbiol. 52: 1769-1779.
10. Brock, R.D. 1971. Differential mutation of the β-galactosidase gene of Escherichia coli. Mutat. Res. 11: 181-186.
11. Chaudhuri, J., Tian, M., Khuong, C., Chua, K., Pinaud, E., and Alt, F.W. 2003. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422: 726-730.
12. Chaudhuri, J., Khuong, C., and Alt, F.W. 2004. Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature 430: 992-998.
13. Chavez, S., Beilharz, T., Rondon, A.G., Erdjument-Bromage, H., Tempst, P., Svejstrup, J.Q., Lithgow, T., and Aguilera, A. 2000. A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae. EMBO J. 19: 5824-5834.
14. Chavez, S., Garcia-Rubio, M., Prado, F., and Aguilera, A. 2001. Hpr1 is preferentially required for transcription of either long or G + C-rich DNA sequences in Saccharomyces cerevisiae. Mol. Cell. Biol. 21: 7054-7064.
15. Daneholt, B. 2001. Assembly and transport of a premessenger RNP particle. Proc. Natl. Acad. Sci. 98: 7012-7017.
16. Di Noia, J. and Neuberger, M.S. 2002. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419: 43-48.
17. Dickerson, S.K., Market, E., Besmer, E., and Papavasiliou, F.N. 2003. AID mediates hypermutation by deaminating single stranded DNA. J. Exp. Med. 197: 1291-1296.
18. Dreyfuss, G., Kim, V.N., and Kataoka, N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3: 195-205.
19. Drlica, K. 1992. Control of bacterial DNA supercoiling. Mol. Microbiol. 6: 425-433.
20. Drolet, M. 2006. Growth inhibition mediated by excess negative supercoiling: The interplay between transcription elongation, R-loop formation and DNA topology. Mol. Microbiol. 59: 723-730.
21. Drolet, M., Bi, X., and Liu, L.F. 1994. Hypernegative supercoiling of the DNA template during transcription elongation in vitro. J. Biol. Chem. 269: 2068-2074.
22. Drolet, M., Phoenix, P., Menzel, R., Masse, E., Liu, L.F., and Crouch, R.J. 1995. Overexpression of RNase H partially complements the growth defect of an Escherichia coli Δ topA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc. Natl. Acad. Sci. 92: 3526-3530.
23. Drolet, M., Broccoli, S., Rallu, F., Hraiky, C., Fortin, C., Masse, E., and Baaklini, I. 2003. The problem of hypernegative supercoiling and R-loop formation in transcription. Front. Biosci. 8: d210-d221.
24. Dunnick, W., Hertz, G.Z., Scappino, L., and Gritzmacher, C. 1993. DNA sequences at immunoglobulin switch region recombination sites. Nucleic Acids Res. 21: 365-372.
25. Duquette, M.L., Handa, P., Vincent, J.A., Taylor, A.F., and Maizels, N. 2004. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes & Dev. 18: 1618-1629.
26. Fan, H.Y., Merker, R.J., and Klein, H.L. 2001. High-copy-number expression of Sub2p, a member of the RNA helicase superfamily, suppresses hpr1-mediated genomic instability. Mol. Cell. Biol. 21: 5459-5470.
27. French, S. 1992. Consequences of replication fork movement through transcription units in vivo. Science 258: 1362-1365.
28. Fu, X.D. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1: 663-680.
29. Ge, H. and Manley, J.L. 1990. A protein factor, ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro. Cell 62: 25-34.
30. Garcia-Rubio, M., Huertas, P., Gonzalez-Barrera, S., and Aguilera, A. 2003. Recombinogenic effects of DNA-damaging agents are synergistically increased by transcription in Saccharomyces cerevisiae. New insights into transcription-associated recombination. Genetics 165: 457-466.
31. Gilbert, D.E. and Feigon, J. 1999. Multistranded DNA structures. Curr. Opin. Struct. Biol. 9: 305-314.
32. Gnatt, A.L., Cramer, P., Fu, J., Bushnell, D.A., and Kornberg, R.D. 2001. Structural basis of transcription: An RNA polymerase II elongation complex at 3.3 A resolution. Science 292: 1876-1882.
33. Gowrishankar, J. and Harinarayanan, R. 2004. Why is transcription coupled to translation in bacteria? Mol. Microbiol. 54: 598-603.
34. Graveley, B.R. 2000. Sorting out the complexity of SR protein functions. RNA 6: 1197-1211.
35. Gritzmacher, C.A. 1989. Molecular aspects of heavy-chain class switching. Crit. Rev. Immunol. 9: 173-200.
36. Harriman, G.R., Bradley, A., Das, S., Rogers-Fani, P., and Davis, A.C. 1996. IgA class switch in I α exon-deficient mice. Role of germline transcription in class switch recombination. J. Clin. Invest. 97: 477-485.
37. Herman, R.K. and Dworkin, N.B. 1971. Effect of gene induction on the rate of mutagenesis by ICR-191 in Escherichia coli. J. Bacteriol. 106: 543-550.
38. Hirose, Y. and Manley, J.L. 2000. RNA polymerase II and the integration of nuclear events. Genes & Dev. 14: 1415-1429.
39. Hraiky, C., Raymond, M.A., and Drolet, M. 2000. RNase H overproduction corrects a defect at the level of transcription elongation during rRNA synthesis in the absence of DNA topoisomerase I in Escherichia coli. J. Biol. Chem. 275: 11257-11263.
40. Huang, Y., Gattoni, R., Stevenin, J., and Steitz, J.A. 2003. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11: 837-843.
41. Huang, F.T., Yu, K., Hsieh, C.L., and Lieber, M.R. 2006. Downstream boundary of chromosomal R-loops at murine switch regions: Implications for the mechanism of class switch recombination. Proc. Natl. Acad. Sci. 103: 5030-5035.
42. Huertas, P. and Aguilera, A. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 12: 711-721.
43. Itoh, T. and Tomizawa, J. 1980. Formation of an RNA primer for initiation of replication of ColE1 DNA by ribonuclease H. Proc. Natl. Acad. Sci. 77: 2450-2454.
44. Jimeno, S., Rondon, A.G., Luna, R., and Aguilera, A. 2002. The yeast THO complex and mRNA export factors link RNA metabolism with transcription and genome instability. EMBO J. 21: 3526-3535.
45. Jung, S., Rajewsky, K., and Radbruch, A. 1993. Shutdown of class switch recombination by deletion of a switch region control element. Science 259: 984-987.
46. Kadesch, T.R. and Chamberlin, M.J. 1982. Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J. Biol. Chem. 257: 5286-5295.
47. Kettenberger, H., Armache, K.J., and Cramer, P. 2004. Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol. Cell 16: 955-965.
48. Kinoshita, K. and Honjo, T. 2000. Unique and unprecedented recombination mechanisms in class switching. Curr. Opin. Immunol. 12: 195-198.
49. Krainer, A.R., Conway, G.C., and Kozak, D. 1990. The essential pre-mRNA splicing factor SF2 influences 5′ splice site selection by activating proximal sites. Cell 62: 35-42.
50. Krasilnikova, M.M., Samadashwily, G.M., Krasilnikov, A.S., and Mirkin, S.M. 1998. Transcription through a simple DNA repeat blocks replication elongation. EMBO J. 17: 5095-5102.
51. Kruger, W. and Herskowitz, I. 1991. A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1. Mol. Cell. Biol. 11: 4135-4146.
52. Lee, C.G., Kondo, S., and Honjo, T. 1998. Frequent but biased class switch recombination in the S mu flanking regions. Curr. Biol. 8: 227-230.
53. Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J.L., and Lafyatis, R. 2002. Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: A novel function for SR proteins. Genes & Dev. 16: 594-607.
54. Li, X. and Manley, J.L. 2005a. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122: 365-378.
55. _. 2005b. New talents for an old acquaintance: The SR protein splicing factor ASF/SF2 functions in the maintenance of genome stability. Cell Cycle 4: 1706-1708.
56. Lindahl, T. and Nyberg, B. 1974. Heat-induced deamination of cytosine residues in deoxyribonucleic acid. Biochemistry 13: 3405-3410.
57. Liu, Z. and Gilbert, W. 1994. The yeast KEM1 gene encodes a nuclease specific for G4 tetraplex DNA: Implication of in vivo functions for this novel DNA structure. Cell 77: 1083-1092.
58. Liu, L.F. and Wang, J.C. 1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. 84: 7024-7027.
59. Liu, Z., Frantz, J.D., Gilbert, W., and Tye, B.K. 1993. Identification and characterization of a nuclease activity specific for G4 tetrastranded DNA. Proc. Natl. Acad. Sci. 90: 3157-3161.
60. Longerich, S., Basu, U., Alt, F., and Storb, U. 2006. AID in somatic hypermutation and class switch recombination. Curr. Opin. Immunol. 18: 164-174.
61. Luna, R., Jimeno, S., Marin, M., Huertas, P., Garcia-Rubio, M., and Aguilera, A. 2005. Interdependence between transcription and mRNP processing and export, and its impact on genetic stability. Mol. Cell 18: 711-722.
62. Maniatis, T. and Reed, R. 2002. An extensive network of coupling among gene expression machines. Nature 416: 499-506.
63. Manley, J.L. and Tacke, R. 1996. SR proteins and splicing control. Genes & Dev. 10: 1569-1579.
64. Masse, E. and Drolet, M. 1999. Escherichia coli DNA topoisomerase I inhibits R-loop formation by relaxing transcription-induced negative supercoiling. J. Biol. Chem. 274: 16659-16664.
65. Masse, E., Phoenix, P., and Drolet, M. 1997. DNA topoisomerases regulate R-loop formation during transcription of the rrnB operon in Escherichia coli. J. Biol. Chem. 272: 12816-12823.
66. Masuda, S., Das, R., Cheng, H., Hurt, E., Dorman, N., and Reed, R. 2005. Recruitment of the human TREX complex to mRNA during splicing. Genes & Dev. 19: 1512-1517.
67. Mizuta, R., Mizuta, M., and Kitamura, D. 2005. Guanine is indispensable for immunoglobulin switch region RNA-DNA hybrid formation. J. Electron Microsc. (Tokyo) 54: 403-408.
68. Muramatsu, M., Sankaranand, V.S., Anant, S., Sugai, M., Kinoshita, K., Davidson, N.O., and Honjo, T. 1999. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274: 18470-18476.
69. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553-563.
70. Nourani, A., Robert, F., and Winston, F. 2006. Evidence that Spt2/Sin1, an HMG-like factor, plays roles in transcription elongation, chromatin structure, and genome stability in Saccharomyces cerevisiae. Mol. Cell. Biol. 26: 1496-1509.
71. Nudler, E. and Gottesman, M.E. 2002. Transcription termination and anti-termination in E. coli genes. Cells 7: 755-768.
72. Okazaki, I.M., Kinoshita, K., Muramatsu, M., Yoshikawa, K., and Honjo, T. 2002. The AID enzyme induces class switch recombination in fibroblasts. Nature 416: 340-345.
73. Petersen-Mahrt, S.K., Harris, R.S., and Neuberger, M.S. 2002. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418: 99-103.
74. Phoenix, P., Raymond, M.A., Masse, E., and Drolet, M. 1997. Roles of DNA topoisomerases in the regulation of R-loop formation in vitro. J. Biol. Chem. 272: 1473-1479.
75. Piruat, J.I. and Aguilera, A. 1998. A novel yeast gene, THO2, is involved in RNA pol II transcription and provides new evidence for transcriptional elongation-associated recombination. EMBO J. 17: 4859-4872.
76. Prado, F. and Aguilera, A. 2005. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 24: 1267-1276.
77. Prado, F., Piruat, J.I., and Aguilera, A. 1997. Recombination between DNA repeats in yeast hpr1Δ cells is linked to transcription elongation. EMBO J. 16: 2826-2835.
78. Proudfoot, N.J., Furger, A., and Dye, M.J. 2002. Integrating mRNA processing with transcription. Cell 108: 501-512.
79. Rada, C., Williams, G.T., Nilsen, H., Barnes, D.E., Lindahl, T., and Neuberger, M.S. 2002. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12: 1748-1755.
80. Ramiro, A.R., Stavropoulos, P., Jankovic, M., and Nussenzweig, M.C. 2003. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the non-template strand. Nat. Immunol. 4: 452-456.
81. Reaban, M.E., Lebowitz, J., and Griffin, J.A. 1994. Transcription induces the formation of a stable RNA.DNA hybrid in the immunoglobulin α switch region. J. Biol. Chem. 269: 21850-21857.
82. Reed, R. and Cheng, H. 2005. TREX, SR proteins and export of mRNA. Curr. Opin. Cell Biol. 17: 269-273.
83. Rehwinkel, J., Herold, A., Gari, K., Kocher, T., Rode, M., Ciccarelli, F.L., Wilm, M., and Izaurralde, E. 2004. Genomewide analysis of mRNAs regulated by the THO complex in Drosophila melanogaster. Nat. Struct. Mol. Biol. 11: 558-566.
84. Richardson, J.P. 2002. Rho-dependent termination and ATPases in transcript termination. Biochim. Biophys. Acta 1577: 251-260.
85. Roberts, J.W. 1969. Termination factor for RNA synthesis. Nature 224: 1168-1174.
86. Rondon, A.G., Jimeno, S., Garcia-Rubio, M., and Aguilera, A. 2003. Molecular evidence that the eukaryotic THO/TREX complex is required for efficient transcription elongation. J. Biol. Chem. 278: 39037-39043.
87. Sanford, J.R., Gray, N.K., Beckmann, K., and Caceres, J.F. 2004. A novel role for shuttling SR proteins in mRNA translation. Genes & Dev. 18: 755-768.
88. Shinkura, R., Tian, M., Smith, M., Chua, K., Fujiwara, Y., and Alt, F.W. 2003. The influence of transcriptional orientation on endogenous switch region function. Nat. Immunol. 4: 435-441.
89. Sohail, A., Klapacz, J., Samaranayake, M., Ullah, A., and Bhagwat, A.S. 2003. Human activation-induced cytidine deaminase causes transcription- dependent, strand-biased C to U deaminations. Nucleic Acids Res. 31: 2990-2994.
90. Stavnezer, J. and Schrader, C.E. 2006. Mismatch repair converts AID-instigated nicks to double-strand breaks for antibody class-switch recombination. Trends Genet. 22: 23-28.
91. Strasser, K., Masuda, S., Mason, P., Pfannstiel, J., Oppizzi, M., Rodriguez-Navarro, S., Rondon, A.G., Aguilera, A., Struhl, K., Reed, R., et al. 2002. TREX is a conserved complex coupling transcription with messenger RNA export. Nature 417: 304-308.
92. Sugimoto, N., Nakano, S., Katoh, M., Matsumura, A., Nakamuta, H., Ohmichi, T., Yoneyama, M., and Sasaki, M. 1995. Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry 34: 11211-11216.
93. Sun, H., Yabuki, A., and Maizels, N. 2001. A human nuclease specific for G4 DNA. Proc. Natl. Acad. Sci. 98: 12444-12449.
94. Takeuchi, Y., Horiuchi, T., and Kobayashi, T. 2003. Transcription- dependent recombination and the role of fork collision in yeast rDNA. Genes & Dev. 17: 1497-1506.
95. Tian, M. and Alt, F.W. 2000. Transcription-induced cleavage of immunoglobulin switch regions by nucleotide excision repair nucleases in vitro. J. Biol. Chem. 275: 24163-24172.
96. Ujvari, A. and Luse, D.S. 2004. Newly Initiated RNA encounters a factor involved in splicing immediately upon emerging from within RNA polymerase II. J. Biol. Chem. 279: 49773-49779.
97. Wang, J., Takagaki, Y., and Manley, J.L. 1996. Targeted disruption of an essential vertebrate gene: ASF/SF2 is required for cell viability. Genes & Dev. 10: 2588-2599.
98. Westover, K.D., Bushnell, D.A., and Kornberg, R.D. 2004. Structural basis of transcription: Separation of RNA from DNA by RNA polymerase II. Science 303: 1014-1016.
99. Yu, K. and Lieber, M.R. 2003. Nucleic acid structures and enzymes in the immunoglobulin class switch recombination mechanism. DNA Repair (Amst.) 2: 1163-1174.
100. Yu, K., Chedin, F., Hsieh, C.L., Wilson, T.E., and Lieber, M.R. 2003. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4: 442-451.
101. Zarrin, A.A., Alt, F.W., Chaudhuri, J., Stokes, N., Kaushal, D., Du Pasquier, L., and Tian, M. 2004. An evolutionarily conserved target motif for immunoglobulin class-switch recombination. Nat. Immunol. 5: 1275-1281.
102. Zhang, J., Bottaro, A., Li, S., Stewart, V., and Alt, F.W. 1993. A selective defect in IgG2b switching as a result of targeted mutation of the I γ 2b promoter and exon. EMBO J. 12: 3529-3537.
103. Zorio, D.A. and Bentley, D.L. 2004. The link between mRNA processing and transcription: Communication works both ways. Exp. Cell Res. 296: 91-97.