Functions of Replication Protein A as a Sensor of R Loops and a Regulator of RNaseH1

Molecular Cell

Volumn 65, Issue 5, 2017, Pages 832-847.e4

  Nguyen, Hai Dang ^a   Yadav, Tribhuwan ^a   Giri, Sumanprava ^a   Saez, Borja ^a   Graubert, Timothy A ^a   Zou, Lee ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

genome instability; R loop; RNase H1; RPA; splicing inhibitor; splicing mutation; ssDNA

Indexed keywords

BIOTIN; ENZYME; MONOCLONAL ANTIBODY; REPLICATION FACTOR A; RNASEH1; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; DNA; PROTEIN BINDING; RIBONUCLEASE H; RIBONUCLEASE HI; RNA; RPA1 PROTEIN, HUMAN;

ARTICLE; CATALYSIS; DNA DAMAGE; DNA REPLICATION; DNA RNA HYBRIDIZATION; GENE REPRESSION; GENOMIC INSTABILITY; HUMAN; IN VITRO STUDY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA ANALYSIS; RNA STRUCTURE; STIMULATION; BINDING SITE; CHEMISTRY; CONFORMATION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PROTEIN DOMAIN; RNA INTERFERENCE; STRUCTURE ACTIVITY RELATION; TIME FACTOR;

BINDING SITES; DNA; GENOMIC INSTABILITY; HEK293 CELLS; HELA CELLS; HUMANS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; REPLICATION PROTEIN A; RIBONUCLEASE H; RNA; RNA INTERFERENCE; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 85014197809     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2017.01.029     Document Type: Article

References (62)

1. Alzu, A., Bermejo, R., Begnis, M., Lucca, C., Piccini, D., Carotenuto, W., Saponaro, M., Brambati, A., Cocito, A., Foiani, M., Liberi, G., Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 151 (2012), 835–846.
2. Arora, R., Lee, Y., Wischnewski, H., Brun, C.M., Schwarz, T., Azzalin, C.M., RNaseH1 regulates TERRA-telomeric DNA hybrids and telomere maintenance in ALT tumour cells. Nat. Commun., 5, 2014, 5220.
3. Bhatia, V., Barroso, S.I., García-Rubio, M.L., Tumini, E., Herrera-Moyano, E., Aguilera, A., BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 511 (2014), 362–365.
4. Boguslawski, S.J., Smith, D.E., Michalak, M.A., Mickelson, K.E., Yehle, C.O., Patterson, W.L., Carrico, R.J., Characterization of monoclonal antibody to DNA.RNA and its application to immunodetection of hybrids. J. Immunol. Methods 89 (1986), 123–130.
5. Bubeck, D., Reijns, M.A.M., Graham, S.C., Astell, K.R., Jones, E.Y., Jackson, A.P., PCNA directs type 2 RNase H activity on DNA replication and repair substrates. Nucleic Acids Res. 39 (2011), 3652–3666.
6. Cerritelli, S.M., Crouch, R.J., Ribonuclease H: the enzymes in eukaryotes. FEBS J. 276 (2009), 1494–1505.
7. Chan, Y.A., Aristizabal, M.J., Lu, P.Y.T., Luo, Z., Hamza, A., Kobor, M.S., Stirling, P.C., Hieter, P., Genome-wide profiling of yeast DNA:RNA hybrid prone sites with DRIP-chip. PLoS Genet., 10, 2014, e1004288.
8. Chaudhuri, J., Khuong, C., Alt, F.W., Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature 430 (2004), 992–998.
9. Chiarle, R., Zhang, Y., Frock, R.L., Lewis, S.M., Molinie, B., Ho, Y.-J., Myers, D.R., Choi, V.W., Compagno, M., Malkin, D.J., et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147 (2011), 107–119.
10. De, I., Bessonov, S., Hofele, R., dos Santos, K., Will, C.L., Urlaub, H., Lührmann, R., Pena, V., The RNA helicase Aquarius exhibits structural adaptations mediating its recruitment to spliceosomes. Nat. Struct. Mol. Biol. 22 (2015), 138–144.
11. El Hage, A., Webb, S., Kerr, A., Tollervey, D., Genome-wide distribution of RNA-DNA hybrids identifies RNase H targets in tRNA genes, retrotransposons and mitochondria. PLoS Genet., 10, 2014, e1004716.
12. Flynn, R.L., Zou, L., Oligonucleotide/oligosaccharide-binding fold proteins: a growing family of genome guardians. Crit. Rev. Biochem. Mol. Biol. 45 (2010), 266–275.
13. Gan, W., Guan, Z., Liu, J., Gui, T., Shen, K., Manley, J.L., Li, X., R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev. 25 (2011), 2041–2056.
14. García-Rubio, M.L., Pérez-Calero, C., Barroso, S.I., Tumini, E., Herrera-Moyano, E., Rosado, I.V., Aguilera, A., The Fanconi Anemia Pathway Protects Genome Integrity from R-loops. PLoS Genet., 11, 2015, e1005674.
15. Ginno, P.A., Lott, P.L., Christensen, H.C., Korf, I., Chédin, F., R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol. Cell 45 (2012), 814–825.
16. Giri, S., Aggarwal, V., Pontis, J., Shen, Z., Chakraborty, A., Khan, A., Mizzen, C., Prasanth, K.V., Ait-Si-Ali, S., Ha, T., Prasanth, S.G., The preRC protein ORCA organizes heterochromatin by assembling histone H3 lysine 9 methyltransferases on chromatin. eLife, 4, 2015.
17. Graubert, T.A., Shen, D., Ding, L., Okeyo-Owuor, T., Lunn, C.L., Shao, J., Krysiak, K., Harris, C.C., Koboldt, D.C., Larson, D.E., et al. Recurrent mutations in the U2AF1 splicing factor in myelodysplastic syndromes. Nat. Genet. 44 (2011), 53–57.
18. Groh, M., Gromak, N., Out of balance: R-loops in human disease. PLoS Genet., 10, 2014, e1004630.
19. Hatchi, E., Skourti-Stathaki, K., Ventz, S., Pinello, L., Yen, A., Kamieniarz-Gdula, K., Dimitrov, S., Pathania, S., McKinney, K.M., Eaton, M.L., et al. BRCA1 recruitment to transcriptional pause sites is required for R-loop-driven DNA damage repair. Mol. Cell 57 (2015), 636–647.
20. Helmrich, A., Ballarino, M., Tora, L., Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 44 (2011), 966–977.
21. Huertas, P., Aguilera, A., Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 12 (2003), 711–721.
22. Ilagan, J.O., Ramakrishnan, A., Hayes, B., Murphy, M.E., Zebari, A.S., Bradley, P., Bradley, R.K., U2AF1 mutations alter splice site recognition in hematological malignancies. Genome Res. 25 (2015), 14–26.
23. Kashyap, M.K., Kumar, D., Villa, R., La Clair, J.J., Benner, C., Sasik, R., Jones, H., Ghia, E.M., Rassenti, L.Z., Kipps, T.J., et al. Targeting the spliceosome in chronic lymphocytic leukemia with the macrolides FD-895 and pladienolide-B. Haematologica 100 (2015), 945–954.
24. Kotake, Y., Sagane, K., Owa, T., Mimori-Kiyosue, Y., Shimizu, H., Uesugi, M., Ishihama, Y., Iwata, M., Mizui, Y., Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat. Chem. Biol. 3 (2007), 570–575.
25. Lagisetti, C., Pourpak, A., Goronga, T., Jiang, Q., Cui, X., Hyle, J., Lahti, J.M., Morris, S.W., Webb, T.R., Synthetic mRNA splicing modulator compounds with in vivo antitumor activity. J. Med. Chem. 52 (2009), 6979–6990.
26. Li, X., Manley, J.L., Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122 (2005), 365–378.
27. Li, M., Pokharel, S., Wang, J.-T., Xu, X., Liu, Y., RECQ5-dependent SUMOylation of DNA topoisomerase I prevents transcription-associated genome instability. Nat. Commun., 6, 2015, 6720.
28. Lim, Y.W., Sanz, L.A., Xu, X., Hartono, S.R., Chédin, F., Genome-wide DNA hypomethylation and RNA:DNA hybrid accumulation in Aicardi-Goutières syndrome. eLife, 4, 2015.
29. Maizels, N., Gray, L.T., The G4 genome. PLoS Genet., 9, 2013, e1003468.
30. Maréchal, A., Zou, L., RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response. Cell Res. 25 (2015), 9–23.
31. Maréchal, A., Li, J.-M., Ji, X.Y., Wu, C.-S., Yazinski, S.A., Nguyen, H.D., Liu, S., Jiménez, A.E., Jin, J., Zou, L., PRP19 transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol. Cell 53 (2014), 235–246.
32. Mischo, H.E., Gómez-González, B., Grzechnik, P., Rondón, A.G., Wei, W., Steinmetz, L., Aguilera, A., Proudfoot, N.J., Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell 41 (2011), 21–32.
33. Moreira, M.-C., Klur, S., Watanabe, M., Németh, A.H., Le Ber, I., Moniz, J.-C., Tranchant, C., Aubourg, P., Tazir, M., Schöls, L., et al. Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat. Genet. 36 (2004), 225–227.
34. Nowotny, M., Cerritelli, S.M., Ghirlando, R., Gaidamakov, S.A., Crouch, R.J., Yang, W., Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD. EMBO J. 27 (2008), 1172–1181.
35. Paulsen, R.D., Soni, D.V., Wollman, R., Hahn, A.T., Yee, M.-C., Guan, A., Hesley, J.A., Miller, S.C., Cromwell, E.F., Solow-Cordero, D.E., et al. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell 35 (2009), 228–239.
36. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612.
37. Petzold, C., Marceau, A.H., Miller, K.H., Marqusee, S., Keck, J.L., Interaction with Single-stranded DNA-binding Protein Stimulates Escherichia coli Ribonuclease HI Enzymatic Activity. J. Biol. Chem. 290 (2015), 14626–14636.
38. Polak, P., Arndt, P.F., Transcription induces strand-specific mutations at the 5′ end of human genes. Genome Res. 18 (2008), 1216–1223.
39. Santos-Pereira, J.M., Aguilera, A., R loops: new modulators of genome dynamics and function. Nat. Rev. Genet. 16 (2015), 583–597.
40. Sanz, L.A., Hartono, S.R., Lim, Y.W., Steyaert, S., Rajpurkar, A., Ginno, P.A., Xu, X., Chédin, F., Prevalent, Dynamic, and Conserved R-Loop Structures Associate with Specific Epigenomic Signatures in Mammals. Mol. Cell 63 (2016), 167–178.
41. Schwab, R.A., Nieminuszczy, J., Shah, F., Langton, J., Lopez Martinez, D., Liang, C.-C., Cohn, M.A., Gibbons, R.J., Deans, A.J., Niedzwiedz, W., The Fanconi Anemia Pathway Maintains Genome Stability by Coordinating Replication and Transcription. Mol. Cell 60 (2015), 351–361.
42. Shiotani, B., Nguyen, H.D., Håkansson, P., Maréchal, A., Tse, A., Tahara, H., Zou, L., Two distinct modes of ATR activation orchestrated by Rad17 and Nbs1. Cell Rep. 3 (2013), 1651–1662.
43. Sikorski, T.W., Ficarro, S.B., Holik, J., Kim, T., Rando, O.J., Marto, J.A., Buratowski, S., Sub1 and RPA associate with RNA polymerase II at different stages of transcription. Mol. Cell 44 (2011), 397–409.
44. Skourti-Stathaki, K., Proudfoot, N.J., A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev. 28 (2014), 1384–1396.
45. Skourti-Stathaki, K., Proudfoot, N.J., Gromak, N., Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol. Cell 42 (2011), 794–805.
46. Skourti-Stathaki, K., Kamieniarz-Gdula, K., Proudfoot, N.J., R-loops induce repressive chromatin marks over mammalian gene terminators. Nature 516 (2014), 436–439.
47. Sollier, J., Cimprich, K.A., Breaking bad: R-loops and genome integrity. Trends Cell Biol. 25 (2015), 514–522.
48. Sollier, J., Stork, C.T., García-Rubio, M.L., Paulsen, R.D., Aguilera, A., Cimprich, K.A., Transcription-coupled nucleotide excision repair factors promote R-loop-induced genome instability. Mol. Cell 56 (2014), 777–785.
49. Stirling, P.C., Chan, Y.A., Minaker, S.W., Aristizabal, M.J., Barrett, I., Sipahimalani, P., Kobor, M.S., Hieter, P., R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev. 26 (2012), 163–175.
50. Sun, Q., Csorba, T., Skourti-Stathaki, K., Proudfoot, N.J., Dean, C., R-Loop Stabilization Represses Antisense Transcription at the Arabidopsis FLC Locus. Science 340 (2013), 619–621.
51. Suzuki, Y., Holmes, J.B., Cerritelli, S.M., Sakhuja, K., Minczuk, M., Holt, I.J., Crouch, R.J., An upstream open reading frame and the context of the two AUG codons affect the abundance of mitochondrial and nuclear RNase H1. Mol. Cell. Biol. 30 (2010), 5123–5134.
52. Tuduri, S., Crabbé, L., Conti, C., Tourrière, H., Holtgreve-Grez, H., Jauch, A., Pantesco, V., De Vos, J., Thomas, A., Theillet, C., et al. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat. Cell Biol. 11 (2009), 1315–1324.
53. Wahba, L., Amon, J.D., Koshland, D., Vuica-Ross, M., RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol. Cell 44 (2011), 978–988.
54. Wan, Y., Zheng, X., Chen, H., Guo, Y., Jiang, H., He, X., Zhu, X., Zheng, Y., Splicing function of mitotic regulators links R-loop-mediated DNA damage to tumor cell killing. J. Cell Biol. 209 (2015), 235–246.
55. Wellinger, R.E., Prado, F., Aguilera, A., Replication fork progression is impaired by transcription in hyperrecombinant yeast cells lacking a functional THO complex. Mol. Cell. Biol. 26 (2006), 3327–3334.
56. Wu, H., Lima, W.F., Crooke, S.T., Investigating the structure of human RNase H1 by site-directed mutagenesis. J. Biol. Chem. 276 (2001), 23547–23553.
57. Yadav, T., Carrasco, B., Myers, A.R., George, N.P., Keck, J.L., Alonso, J.C., Genetic recombination in Bacillus subtilis: a division of labor between two single-strand DNA-binding proteins. Nucleic Acids Res. 40 (2012), 5546–5559.
58. Yokoi, A., Kotake, Y., Takahashi, K., Kadowaki, T., Matsumoto, Y., Minoshima, Y., Sugi, N.H., Sagane, K., Hamaguchi, M., Iwata, M., Mizui, Y., Biological validation that SF3b is a target of the antitumor macrolide pladienolide. FEBS J. 278 (2011), 4870–4880.
59. Yu, K., Chedin, F., Hsieh, C.-L., Wilson, T.E., Lieber, M.R., R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4 (2003), 442–451.
60. Zeman, M.K., Cimprich, K.A., Causes and consequences of replication stress. Nat. Cell Biol. 16 (2014), 2–9.
61. Zhao, D.Y., Gish, G., Braunschweig, U., Li, Y., Ni, Z., Schmitges, F.W., Zhong, G., Liu, K., Li, W., Moffat, J., et al. SMN and symmetric arginine dimethylation of RNA polymerase II C-terminal domain control termination. Nature 529 (2016), 48–53.
62. Zou, L., Elledge, S.J., Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003), 1542–1548.