Insights into G-quadruplex specific recognition by the DEAH-box helicase RHAU: Solution structure of a peptide-quadruplex complex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 31, 2015, Pages 9608-9613

  Heddi, Brahim ^a   Cheong, Vee Vee ^a   Martadinata, Herry ^a   Phan, Anh Tuân ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

DEAH box family; DHX36; G quadruplex; NMR; Rhau helicase

Indexed keywords

DEAH BOX HELICASE RHAU; DOUBLE STRANDED DNA; GUANINE QUADRUPLEX; LIGAND; MULTIPROTEIN COMPLEX; RNA HELICASE; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; MUTANT PROTEIN; PEPTIDE; PROTEIN BINDING; SOLUTION AND SOLUBILITY;

ARTICLE; AU RICH ELEMENT; BINDING ASSAY; CONFORMATION; DNA SEQUENCE; GEL ELECTROPHORESIS; HUMAN; MOLECULAR CROWDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN STRUCTURE; RNA SEQUENCE; STATIC ELECTRICITY; AGAR GEL ELECTROPHORESIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY;

AMINO ACID SEQUENCE; DEAD-BOX RNA HELICASES; ELECTROPHORESIS, AGAR GEL; G-QUADRUPLEXES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS;

EID: 84938717683     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422605112     Document Type: Article

References (44)

1. Gellert M, Lipsett MN, Davies DR (1962) Helix formation by guanylic acid. Proc Natl Acad Sci USA 48(12):2013-2018.
2. Sen D, Gilbert W (1988) Formation of parallel four-stranded complexes by guaninerich motifs in DNA and its implications for meiosis. Nature 334(6180):364-366.
3. Smith FW, Feigon J (1992) Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature 356(6365):164-168.
4. Laughlan G, et al. (1994) The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science 265(5171):520-524.
5. Parkinson GN, Lee MP, Neidle S (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417(6891):876-880.
6. Patel DJ, Phan AT, Kuryavyi V (2007) Human telomere, oncogenic promoter and 5'-UTR G-quadruplexes: Diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res 35(22):7429-7455.
7. Maizels N, Gray LT (2013) The G4 genome. PLoS Genet 9(4):e1003468.
8. Biffi G, Tannahill D, McCafferty J, Balasubramanian S (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 5(3):182-186.
9. Henderson A, et al. (2014) Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res 42(2):860-869.
10. Cahoon LA, Seifert HS (2009) An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325(5941):764-767.
11. Kumari S, Bugaut A, Huppert JL, Balasubramanian S (2007) An RNA G-quadruplex in the 5' UTR of the NRAS proto-oncogene modulates translation. Nat Chem Biol 3(4): 218-221.
12. Oganesian L, Bryan TM (2007) Physiological relevance of telomeric G-quadruplex formation: A potential drug target. BioEssays 29(2):155-165.
13. Sun H, Karow JK, Hickson ID, Maizels N (1998) The Bloom's syndrome helicase unwinds G4 DNA. J Biol Chem 273(42):27587-27592.
14. Wu Y, Shin-ya K, Brosh RM, Jr (2008) FANCJ helicase defective in Fanconia anemia and breast cancer unwinds G-quadruplex DNA to defend genomic stability. Mol Cell Biol 28(12):4116-4128.
15. Ribeyre C, et al. (2009) The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet 5(5):e1000475.
16. Vaughn JP, et al. (2005) The DEXH protein product of the DHX36 gene is the major source of tetramolecular quadruplex G4-DNA resolving activity in HeLa cell lysates. J Biol Chem 280(46):38117-38120.
17. Phan AT, et al. (2005) An interlocked dimeric parallel-stranded DNA quadruplex: A potent inhibitor of HIV-1 integrase. Proc Natl Acad Sci USA 102(3):634-639.
18. Kuryavyi V, Cahoon LA, Seifert HS, Patel DJ (2012) RecA-binding pilE G4 sequence essential for pilin antigenic variation forms monomeric and 5' end-stacked dimeric parallel G-quadruplexes. Structure 20(12):2090-2102.
19. Gallo A, et al. (2012) Structure of nucleophosmin DNA-binding domain and analysis of its complex with a G-quadruplex sequence from the c-MYC promoter. J Biol Chem 287(32):26539-26548.
20. Horvath MP, Schultz SC (2001) DNA G-quartets in a 1.86 Å resolution structure of an Oxytricha nova telomeric protein-DNA complex. J Mol Biol 310(2):367-377.
21. Russo Krauss I, Pica A, Merlino A, Mazzarella L, Sica F (2013) Duplex-quadruplex motifs in a peculiar structural organization cooperatively contribute to thrombin binding of a DNA aptamer. Acta Crystallogr D Biol Crystallogr 69(Pt 12):2403-2411.
22. Phan AT, et al. (2011) Structure-function studies of FMRP RGG peptide recognition of an RNA duplex-quadruplex junction. Nat Struct Mol Biol 18(7):796-804.
23. Hayashi T, et al. (2014) Binding of an RNA aptamer and a partial peptide of a prion protein: Crucial importance of water entropy in molecular recognition. Nucleic Acids Res 42(11):6861-6875.
24. Chalupníková K, et al. (2008) Recruitment of the RNA helicase RHAU to stress granules via a unique RNA-binding domain. J Biol Chem 283(50):35186-35198.
25. Lattmann S, Stadler MB, Vaughn JP, Akman SA, Nagamine Y (2011) The DEAH-box RNA helicase RHAU binds an intramolecular RNA G-quadruplex in TERC and associates with telomerase holoenzyme. Nucleic Acids Res 39(21):9390-9404.
26. Lattmann S, Giri B, Vaughn JP, Akman SA, Nagamine Y (2010) Role of the amino terminal RHAU-specific motif in the recognition and resolution of guanine quadruplex- RNA by the DEAH-box RNA helicase RHAU. Nucleic Acids Res 38(18):6219-6233.
27. Meier M, et al. (2013) Binding of G-quadruplexes to the N-terminal recognition domain of the RNA helicase associated with AU-rich element (RHAU). J Biol Chem 288(49):35014-35027.
28. Do NQ, Phan AT (2012) Monomer-dimer equilibrium for the 5'-5' stacking of propeller- type parallel-stranded G-quadruplexes: NMR structural study. Chemistry 18(46): 14752-14759.
29. + solution. Nucleic Acids Res 35(19):6517-6525.
30. Heddi B, Phan AT (2011) Structure of human telomeric DNA in crowded solution. J Am Chem Soc 133(25):9824-9833.
31. + solution under molecular crowding condition. J Am Chem Soc 129(36):11185-11191.
32. Lech CJ, Heddi B, Phan AT (2013) Guanine base stacking in G-quadruplex nucleic acids. Nucleic Acids Res 41(3):2034-2046.
33. Chung WJ, et al. (2015) Structure of a left-handed DNA G-quadruplex. Proc Natl Acad Sci USA 112(9):2729-2733.
34. Balasubramanian S, Hurley LH, Neidle S (2011) Targeting G-quadruplexes in gene promoters: A novel anticancer strategy? Nat Rev Drug Discov 10(4):261-275.
35. Martadinata H, Phan AT (2014) Formation of a stacked dimeric G-quadruplex containing bulges by the 5'-terminal region of human telomerase RNA (hTERC). Biochemistry 53(10):1595-1600.
36. Phan AT, Kuryavyi V, Gaw HY, Patel DJ (2005) Small-molecule interaction with a fiveguanine- tract G-quadruplex structure from the human MYC promoter. Nat Chem Biol 1(3):167-173.
37. Adrian M, et al. (2014) Structure and conformational dynamics of a stacked dimeric G-quadruplex formed by the human CEB1 minisatellite. J Am Chem Soc 136(17):6297-6305.
38. Amrane S, et al. (2012) Formation of pearl-necklace monomorphic G-quadruplexes in the human CEB25 minisatellite. J Am Chem Soc 134(13):5807-5816.
39. + solution: An intramolecular (3 + 1) G-quadruplex scaffold. J Am Chem Soc 128(30):9963-9970.
40. + solution. Nucleic Acids Res 34(19):5715-5719.
41. + solution: A stable baskettype G-quadruplex with only two G-tetrad layers. J Am Chem Soc 131(12):4301-4309.
42. n in the human telomere favors a G-quadruplex structure containing a G·C·G·C tetrad. Nucleic Acids Res 37(18):6239-6248.
43. Drew HR, et al. (1981) Structure of a B-DNA dodecamer: Conformation and dynamics. Proc Natl Acad Sci USA 78(4):2179-2183.
44. Lim KW, Phan AT (2013) Structural basis of DNA quadruplex-duplex junction formation. Angew Chem Int Ed Engl 52(33):8566-8569.