New Perspectives on DNA and RNA Triplexes As Effectors of Biological Activity

PLoS Genetics

Volumn 11, Issue 12, 2015, Pages

  Bacolla, Albino ^a   Wang, Guliang ^a   Vasquez, Karen M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEOPROTEIN; PROTEIN BINDING; TRIPLEX DNA; UNTRANSLATED RNA;

ANIMAL; CHEMISTRY; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM;

ANIMALS; DNA; EPIGENESIS, GENETIC; HUMANS; NUCLEOPROTEINS; PROTEIN BINDING; RNA, UNTRANSLATED;

EID: 84953302412     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005696     Document Type: Review

References (76)

1. Saenger W, Cantor CR, Principles of Nucleic Acid Structure. New York: Springer-Verlag; 1984. p. 556.
2. Soyfer VN, Potaman VN, Triple-Helical Nucleic Acids. New York: Springer-Verlag; 1996. p. 360.
3. Wells RD, Collier DA, Hanvey JC, Shimizu M, Wohlrab F, The chemistry and biology of unusual DNA structures adopted by oligopurine.oligopyrimidine sequences. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 1988;2(14):2939–2949. 3053307.
4. Frank-Kamenetskii MD, Mirkin SM, Triplex DNA structures. Annu Rev Biochem. 1995;64:65–95. 7574496.
5. Wells RD, Warren ST, Genetic Instabilities and Hereditary Neurological Diseases. San Diego: Academic Press; 1998. p. 829.
6. Wang G, Vasquez KM, Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells. Proc Natl Acad Sci U S A. 2004;101(37):13448–13453. 15342911.
7. Bacolla A, Jaworski A, Larson JE, Jakupciak JP, Chuzhanova N, Abeysinghe SS, et al. Breakpoints of gross deletions coincide with non-B DNA conformations. Proc Natl Acad Sci U S A. 2004;101(39):14162–14167. 15377784.
8. Bacolla A, Wells RD, Non-B DNA conformations, genomic rearrangements, and human disease. The Journal of biological chemistry. 2004;279(46):47411–47414. doi: 10.1074/jbc.R400028200 15326170.
9. Iyer RR, Pluciennik A, Napierala M, Wells RD, DNA Triplet Repeat Expansion and Mismatch Repair. Annual review of biochemistry. 2015. doi: 10.1146/annurev-biochem-060614-034010 25580529.
10. Wang G, Vasquez KM, Impact of alternative DNA structures on DNA damage, DNA repair, and genetic instability. DNA Repair (Amst). 2014;19:143–151. doi: 10.1016/j.dnarep.2014.03.017 24767258.
11. Aguilera A, Garcia-Muse T, Causes of genome instability. Annual review of genetics. 2013;47:1–32. doi: 10.1146/annurev-genet-111212-133232 23909437.
12. Mirkin SM, Expandable DNA repeats and human disease. Nature. 2007;447(7147):932–940. 17581576.
13. Javadekar SM, Raghavan SC, Snaps and Mends: DNA Breaks and Chromosomal Translocations. The FEBS journal. 2015. doi: 10.1111/febs.13311 25913527.
14. Rajeswari MR, DNA triplex structures in neurodegenerative disorder, Friedreich's ataxia. Journal of biosciences. 2012;37(3):519–532. 22750988.
15. Davis TL, Firulli AB, Kinniburgh AJ, Ribonucleoprotein and protein factors bind to an H-DNA-forming c-myc DNA element: possible regulators of the c-myc gene. Proc Natl Acad Sci U S A. 1989;86(24):9682–9686. 2690070.
16. Brahmachari SK, Sarkar PS, Raghavan S, Narayan M, Maiti AK, Polypurine/polypyrimidine sequences as cis-acting transcriptional regulators. Gene. 1997;190(1):17–26. 9185844.
17. Praseuth D, Guieysse AL, Helene C, Triple helix formation and the antigene strategy for sequence-specific control of gene expression. Biochim Biophys Acta. 1999;1489(1):181–206. 10807007.
18. Hoyne PR, Maher LJ, 3rdFunctional studies of potential intrastrand triplex elements in the Escherichia coli genome. J Mol Biol. 2002;318(2):373–386. 12051844.
19. Hile SE, Eckert KA, Positive correlation between DNA polymerase alpha-primase pausing and mutagenesis within polypyrimidine/polypurine microsatellite sequences. J Mol Biol. 2004;335(3):745–759. 14687571.
20. Krasilnikova MM, Mirkin SM, Replication stalling at Friedreich's ataxia (GAA)n repeats in vivo. Mol Cell Biol. 2004;24(6):2286–2295. 14993268.
21. Raghavan SC, Chastain P, Lee JS, Hegde BG, Houston S, Langen R, et al. Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation. J Biol Chem. 2005;280(24):22749–22760. 15840562.
22. Wang G, Carbajal S, Vijg J, DiGiovanni J, Vasquez KM, DNA structure-induced genomic instability in vivo. J Natl Cancer Inst. 2008;100(24):1815–1817. 19066276. doi: 10.1093/jnci/djn385
23. Wang G, Vasquez KM, Models for chromosomal replication-independent non-B DNA structure-induced genetic instability. Mol Carcinog. 2009;48(4):286–298. 19123200. doi: 10.1002/mc.20508
24. Wang G, Vasquez KM, Non-B DNA structure-induced genetic instability. Mutat Res. 2006;598(1–2):103–119. 16516932.
25. Liu G, Myers S, Chen X, Bissler JJ, Sinden RR, Leffak M, Replication Fork Stalling and Checkpoint Activation by a PKD1 Locus Mirror Repeat Polypurine-Polypyrimidine (Pu-Py) Tract. The Journal of biological chemistry. 2012;287(40):33412–33423. Epub 2012/08/09. doi: 10.1074/jbc.M112.402503 22872635; PubMed Central PMCID: PMC3460443.
26. Pollard LM, Sharma R, Gomez M, Shah S, Delatycki MB, Pianese L, et al. Replication-mediated instability of the GAA triplet repeat mutation in Friedreich ataxia. Nucleic Acids Res. 2004;32(19):5962–5971. doi: 10.1093/nar/gkh933 15534367; PubMed Central PMCID: PMC528813.
27. Patel HP, Lu L, Blaszak RT, Bissler JJ, PKD1 intron 21: triplex DNA formation and effect on replication. Nucleic Acids Res. 2004;32(4):1460–1468. 14990751.
28. Diviacco S, Rapozzi V, Xodo L, Helene C, Quadrifoglio F, Giovannangeli C, Site-directed inhibition of DNA replication by triple helix formation. FASEB J. 2001;15(14):2660–2668. 11726542.
29. Betous R, Rey L, Wang G, Pillaire MJ, Puget N, Selves J, et al. Role of TLS DNA polymerases eta and kappa in processing naturally occurring structured DNA in human cells. Mol Carcinog. 2009;48(4):369–378. 19117014. doi: 10.1002/mc.20509
30. Ipsaro JJ, Joshua-Tor L, From guide to target: molecular insights into eukaryotic RNA-interference machinery. Nat Struct Mol Biol. 2015;22(1):20–28. doi: 10.1038/nsmb.2931 25565029.
31. Weiberg A, Bellinger M, Jin H, Conversations between kingdoms: small RNAs. Curr Opin Biotechnol. 2015;32C:207–215. doi: 10.1016/j.copbio.2014.12.025 25622136.
32. Consortium EP, An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489(7414):57–74. doi: 10.1038/nature11247 22955616; PubMed Central PMCID: PMCPMC3439153.
33. Khandelwal A, Bacolla A, Vasquez KM, Jain A, Long non-coding RNA: A new paradigm for lung cancer. Mol Carcinog. 2015;54(11):1235–1251. doi: 10.1002/mc.22362 26332907.
34. Toscano-Garibay JD, Aquino-Jarquin G, Transcriptional regulation mechanism mediated by miRNA-DNA*DNA triplex structure stabilized by Argonaute. Biochim Biophys Acta. 2014;1839(11):1079–1083. doi: 10.1016/j.bbagrm.2014.07.016 25086339.
35. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010;464(7291):1071–1076. doi: 10.1038/nature08975 20393566; PubMed Central PMCID: PMC3049919.
36. Yan TH, Lu SW, Huang YQ, Que GB, Chen JH, Chen YP, et al. Upregulation of the long noncoding RNA HOTAIR predicts recurrence in stage Ta/T1 bladder cancer. Tumour Biol. 2014;35(10):10249–10257. doi: 10.1007/s13277-014-2344-8 25030736.
37. Schmitz KM, Mayer C, Postepska A, Grummt I, Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 2010;24(20):2264–2269. doi: 10.1101/gad.590910 20952535; PubMed Central PMCID: PMC2956204.
38. Bierhoff H, Schmitz K, Maass F, Ye J, Grummt I, Noncoding transcripts in sense and antisense orientation regulate the epigenetic state of ribosomal RNA genes. Cold Spring Harb Symp Quant Biol. 2010;75:357–364. doi: 10.1101/sqb.2010.75.060 21502405.
39. Bagasra O, Stir AE, Pirisi-Creek L, Creek KE, Bagasra AU, Glenn N, et al. Role of micro-RNAs in regulation of lentiviral latency and persistence. Appl Immunohistochem Mol Morphol. 2006;14(3):276–290. 16932018.
40. Kanak M, Alseiari M, Balasubramanian P, Addanki K, Aggarwal M, Noorali S, et al. Triplex-forming MicroRNAs form stable complexes with HIV-1 provirus and inhibit its replication. Appl Immunohistochem Mol Morphol. 2010;18(6):532–545. doi: 10.1097/PAI.0b013e3181e1ef6a 20502318.
41. Holbrook SR, Sussman JL, Warrant RW, Kim SH, Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. J Mol Biol. 1978;123(4):631–660. 357743.
42. Wilusz JE, JnBaptiste CK, Lu LY, Kuhn CD, Joshua-Tor L, Sharp PA, A triple helix stabilizes the 3' ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 2012;26(21):2392–2407. doi: 10.1101/gad.204438.112 23073843; PubMed Central PMCID: PMC3489998.
43. Brown JA, Valenstein ML, Yario TA, Tycowski KT, Steitz JA, Formation of triple-helical structures by the 3'-end sequences of MALAT1 and MENbeta noncoding RNAs. Proc Natl Acad Sci U S A. 2012;109(47):19202–19207. doi: 10.1073/pnas.1217338109 23129630; PubMed Central PMCID: PMC3511071.
44. Mitton-Fry RM, DeGregorio SJ, Wang J, Steitz TA, Steitz JA, Poly(A) tail recognition by a viral RNA element through assembly of a triple helix. Science. 2010;330(6008):1244–1247. doi: 10.1126/science.1195858 21109672; PubMed Central PMCID: PMC3074936.
45. Conrad NK, The emerging role of triple helices in RNA biology. Wiley Interdiscip Rev RNA. 2014;5(1):15–29. doi: 10.1002/wrna.1194 24115594.
46. Devi G, Zhou Y, Zhong Z, Toh DF, Chen G, RNA triplexes: from structural principles to biological and biotech applications. Wiley Interdiscip Rev RNA. 2015;6(1):111–128. doi: 10.1002/wrna.1261 25146348.
47. Garst AD, Edwards AL, Batey RT, Riboswitches: structures and mechanisms. Cold Spring Harb Perspect Biol. 2011;3(6). doi: 10.1101/cshperspect.a003533 20943759; PubMed Central PMCID: PMC3098680.
48. Butcher SE, Pyle AM, The molecular interactions that stabilize RNA tertiary structure: RNA motifs, patterns, and networks. Acc Chem Res. 2011;44(12):1302–1311. doi: 10.1021/ar200098t 21899297.
49. Fica SM, Mefford MA, Piccirilli JA, Staley JP, Evidence for a group II intron-like catalytic triplex in the spliceosome. Nat Struct Mol Biol. 2014;21(5):464–471. doi: 10.1038/nsmb.2815 24747940; PubMed Central PMCID: PMC4257784.
50. Wahl MC, Will CL, Luhrmann R, The spliceosome: design principles of a dynamic RNP machine. Cell. 2009;136(4):701–718. doi: 10.1016/j.cell.2009.02.009 19239890.
51. Keating KS, Toor N, Perlman PS, Pyle AM, A structural analysis of the group II intron active site and implications for the spliceosome. RNA. 2010;16(1):1–9. doi: 10.1261/rna.1791310 19948765; PubMed Central PMCID: PMC2802019.
52. Steitz TA, Steitz JA, A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci U S A. 1993;90(14):6498–6502. 8341661; PubMed Central PMCID: PMC46959.
53. Sharp PA, On the origin of RNA splicing and introns. Cell. 1985;42(2):397–400. 2411416.
54. Cech TR, The generality of self-splicing RNA: relationship to nuclear mRNA splicing. Cell. 1986;44(2):207–210. 2417724.
55. Toor N, Keating KS, Taylor SD, Pyle AM, Crystal structure of a self-spliced group II intron. Science. 2008;320(5872):77–82. doi: 10.1126/science.1153803 18388288.
56. Fica SM, Tuttle N, Novak T, Li NS, Lu J, Koodathingal P, et al. RNA catalyses nuclear pre-mRNA splicing. Nature. 2013;503(7475):229–234. doi: 10.1038/nature12734 24196718.
57. Fica SM, Mefford MA, Piccirilli JA, Staley JP, Evidence for a group II intron-like catalytic triplex in the spliceosome. Nat Struct Mol Biol. 2014;21(5):464–471. doi: 10.1038/nsmb.2815 24747940.
58. Stahley MR, Strobel SA, Structural evidence for a two-metal-ion mechanism of group I intron splicing. Science. 2005;309(5740):1587–1590. doi: 10.1126/science.1114994 16141079.
59. Wlodaver AM, Staley JP, The DExD/H-box ATPase Prp2p destabilizes and proofreads the catalytic RNA core of the spliceosome. RNA. 2014;20(3):282–294. doi: 10.1261/rna.042598.113 24442613; PubMed Central PMCID: PMC3923124.
60. Galej WP, Nguyen TH, Newman AJ, Nagai K, Structural studies of the spliceosome: zooming into the heart of the machine. Curr Opin Struct Biol. 2014;25:57–66. doi: 10.1016/j.sbi.2013.12.002 24480332; PubMed Central PMCID: PMC4045393.
61. Anokhina M, Bessonov S, Miao Z, Westhof E, Hartmuth K, Luhrmann R, RNA structure analysis of human spliceosomes reveals a compact 3D arrangement of snRNAs at the catalytic core. EMBO J. 2013;32(21):2804–2818. doi: 10.1038/emboj.2013.198 24002212; PubMed Central PMCID: PMC3817461.
62. Hukezalie KR, Wong JM, Structure-function relationship and biogenesis regulation of the human telomerase holoenzyme. FEBS J. 2013;280(14):3194–3204. doi: 10.1111/febs.12272 23551398.
63. Ulyanov NB, Shefer K, James TL, Tzfati Y, Pseudoknot structures with conserved base triples in telomerase RNAs of ciliates. Nucleic Acids Res. 2007;35(18):6150–6160. doi: 10.1093/nar/gkm660 17827211; PubMed Central PMCID: PMC2094054.
64. Cash DD, Cohen-Zontag O, Kim NK, Shefer K, Brown Y, Ulyanov NB, et al. Pyrimidine motif triple helix in the Kluyveromyces lactis telomerase RNA pseudoknot is essential for function in vivo. Proc Natl Acad Sci U S A. 2013;110(27):10970–10975. doi: 10.1073/pnas.1309590110 23776224; PubMed Central PMCID: PMC3704002.
65. Huang J, Brown AF, Wu J, Xue J, Bley CJ, Rand DP, et al. Structural basis for protein-RNA recognition in telomerase. Nat Struct Mol Biol. 2014;21(6):507–512. doi: 10.1038/nsmb.2819 24793650.
66. Kim NK, Zhang Q, Feigon J, Structure and sequence elements of the CR4/5 domain of medaka telomerase RNA important for telomerase function. Nucleic Acids Res. 2014;42(5):3395–3408. doi: 10.1093/nar/gkt1276 24335084; PubMed Central PMCID: PMC3950677.
67. Dinman JD, Mechanisms and implications of programmed translational frameshifting. Wiley Interdiscip Rev RNA. 2012;3(5):661–673. doi: 10.1002/wrna.1126 22715123; PubMed Central PMCID: PMC3419312.
68. Yu CH, Noteborn MH, Pleij CW, Olsthoorn RC, Stem-loop structures can effectively substitute for an RNA pseudoknot in -1 ribosomal frameshifting. Nucleic Acids Res. 2011;39(20):8952–8959. doi: 10.1093/nar/gkr579 21803791; PubMed Central PMCID: PMC3203594.
69. Olsthoorn RC, Reumerman R, Hilbers CW, Pleij CW, Heus HA, Functional analysis of the SRV-1 RNA frameshifting pseudoknot. Nucleic Acids Res. 2010;38(21):7665–7672. doi: 10.1093/nar/gkq629 20639537; PubMed Central PMCID: PMC2995055.
70. Chen G, Chang KY, Chou MY, Bustamante C, Tinoco I, JrTriplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of -1 ribosomal frameshifting. Proc Natl Acad Sci U S A. 2009;106(31):12706–12711. doi: 10.1073/pnas.0905046106 19628688; PubMed Central PMCID: PMC2722267.
71. Advani VM, Belew AT, Dinman JD, Yeast telomere maintenance is globally controlled by programmed ribosomal frameshifting and the nonsense-mediated mRNA decay pathway. Translation 2013;1(1):e24418. doi: 10.4161/trla.24418 24563826; PubMed Central PMCID: PMC3908577.
72. Belew AT, Meskauskas A, Musalgaonkar S, Advani VM, Sulima SO, Kasprzak WK, et al. Ribosomal frameshifting in the CCR5 mRNA is regulated by miRNAs and the NMD pathway. Nature. 2014;512(7514):265–269. doi: 10.1038/nature13429 25043019.
73. Grote P, Herrmann BG, The long non-coding RNA Fendrr links epigenetic control mechanisms to gene regulatory networks in mammalian embryogenesis. RNA Biol. 2013;10(10):1579–1585. doi: 10.4161/rna.26165 24036695; PubMed Central PMCID: PMC3866236.
74. Schmitz U, Lai X, Winter F, Wolkenhauer O, Vera J, Gupta SK, Cooperative gene regulation by microRNA pairs and their identification using a computational workflow. Nucleic Acids Res. 2014;42(12):7539–7552. doi: 10.1093/nar/gku465 24875477; PubMed Central PMCID: PMC4081082.
75. Bochman ML, Paeschke K, Zakian VA, DNA secondary structures: stability and function of G-quadruplex structures. Nat Rev Genet. 2012;13(11):770–780. doi: 10.1038/nrg3296 23032257; PubMed Central PMCID: PMCPMC3725559.
76. Lu S, Wang G, Bacolla A, Zhao J, Spitser S, Vasquez KM, Short Inverted Repeats Are Hotspots for Genetic Instability: Relevance to Cancer Genomes. Cell Rep. 2015. doi: 10.1016/j.celrep.2015.02.039 25772355.