Single-molecule imaging reveals a common mechanism shared by G-quadruplex-resolving helicases

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

Volumn 113, Issue 30, 2016, Pages 8448-8453

  Tippana, Ramreddy ^a   Hwang, Helen ^b,c   Opresko, Patricia L ^d   Bohr, Vilhelm A ^e   Myong, Sua ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e Biomedical Research Center   (United States)

Author keywords

BLM; G Quadruplex; Resolving activity; RHAU; WRN

Indexed keywords

BLOOM SYNDROME HELICASE; BRACO 19; DNA; G4 RESOLVASE 1; GUANINE QUADRUPLEX; HELICASE; LIGAND; NMM; PHEN DC3; RESOLVASE; RNA HELICASE; RNA HELICASE AU RICH ELEMENT; UNCLASSIFIED DRUG; WERNER HELICASE; WERNER SYNDROME PROTEIN; DEAD BOX PROTEIN; DHX36 PROTEIN, HUMAN; PROTEIN BINDING; RECQ HELICASE; WERNER SYNDROME ATP DEPENDENT HELICASE; WRN PROTEIN, HUMAN;

ARTICLE; ENZYME ACTIVITY; ENZYME SPECIFICITY; MOLECULAR BIOLOGY; MOLECULAR IMAGING; MOLECULE; OPTICAL RESOLUTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN UNFOLDING; CHEMISTRY; CIRCULAR DICHROISM; CONFORMATION; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; NUCLEOTIDE SEQUENCE; PROCEDURES; SINGLE MOLECULE IMAGING; TELOMERE;

BASE SEQUENCE; CIRCULAR DICHROISM; DEAD-BOX RNA HELICASES; DNA; G-QUADRUPLEXES; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; RECQ HELICASES; SINGLE MOLECULE IMAGING; SUBSTRATE SPECIFICITY; TELOMERE; WERNER SYNDROME HELICASE;

EID: 84979529912     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1603724113     Document Type: Article

References (47)

1. Parkinson GN, Lee MP, Neidle S (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417(6891):876-880.
2. 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.
3. Biffi G, Di Antonio M, Tannahill D, Balasubramanian S (2014) Visualization and selective chemical targeting of RNA G-quadruplex structures in the cytoplasm of human cells. Nat Chem 6(1):75-80.
4. 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.
5. Maizels N (2015) G4- Associated human diseases. EMBO Rep 16(8):910-922.
6. 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.
7. 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.
8. Phan AT, Kuryavyi V, Gaw HY, Patel DJ (2005) Small-molecule interaction with a five-guanine- Tract G-quadruplex structure from the human MYC promoter. Nat Chem Biol 1(3):167-173.
9. Budhathoki JB, et al. (2014) RecQ-core of BLM unfolds telomeric G-quadruplex in the absence of ATP. Nucleic Acids Res 42(18):11528-11545.
10. Paeschke K, et al. (2013) Pif1 family helicases suppress genome instability at G-quadruplex motifs. Nature 497(7450):458-462.
11. Giri B, et al. (2011) G4 resolvase 1 tightly binds and unwinds unimolecular G4-DNA. Nucleic Acids Res 39(16):7161-7178.
12. Chen MC, Murat P, Abecassis K, Ferré-D'Amaré AR, Balasubramanian S (2015) Insights into the mechanism of a G-quadruplex-unwinding DEAH-box helicase. Nucleic Acids Res 43(4):2223-2231.
13. Gao X, et al. (2015) A G-quadruplex DNA structure resolvase, RHAU, is essential for spermatogonia differentiation. Cell Death Dis 6:e1610.
14. Heddi B, Cheong VV, Martadinata H, Phan AT (2015) Insights into G-quadruplex specific recognition by the DEAH-box helicase RHAU: Solution structure of a peptidequadruplex complex. Proc Natl Acad Sci USA 112(31):9608-9613.
15. Tippana R, Xiao W, Myong S (2014) G-quadruplex conformation and dynamics are determined by loop length and sequence. Nucleic Acids Res 42(12):8106-8114.
16. Creacy SD, et al. (2008) G4 resolvase 1 binds both DNA and RNA tetramolecular quadruplex with high affinity and is the major source of tetramolecular quadruplex G4-DNA and G4-RNA resolving activity in HeLa cell lysates. J Biol Chem 283(50):34626-34634.
17. Miyoshi D, Nakao A, Sugimoto N (2003) Structural transition from antiparallel to parallel G-quadruplex of d(G4T4G4) induced by Ca2+. Nucleic Acids Res 31(4):1156-1163.
18. Dai J, Carver M, Hurley LH, Yang D (2011) Solution structure of a 2:1 quindolinec- MYC G-quadruplex: Insights into G-quadruplex-interactive small molecule drug design. J Am Chem Soc 133(44):17673-17680.
19. Mathad RI, Hatzakis E, Dai J, Yang D (2011) c-MYC promoter G-quadruplex formed at the 5′-end of NHE III1 element: Insights into biological relevance and parallel-stranded G-quadruplex stability. Nucleic Acids Res 39(20):9023-9033.
20. Ambrus A, et al. (2006) Human telomeric sequence forms a hybrid- Type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution. Nucleic Acids Res 34(9):2723-2735.
21. Roy R, Hohng S, Ha T (2008) A practical guide to single-molecule FRET. Nat Methods 5(6): 507-516.
22. Qiu Y, et al. (2013) Srs2 prevents Rad51 filament formation by repetitive motion on DNA. Nat Commun 4:2281.
23. Hwang H, et al. (2014) Telomeric overhang length determines structural dynamics and accessibility to telomerase and ALT- Associated proteins. Structure 22(6):842-853.
24. Pandey S, Agarwala P, Maiti S (2013) Effect of loops and G-quartets on the stability of RNA G-quadruplexes. J Phys Chem B 117(23):6896-6905.
25. Damerla RR, et al. (2012) Werner syndrome protein suppresses the formation of large deletions during the replication of human telomeric sequences. Cell Cycle 11(16): 3036-3044.
26. Hazel P, Huppert J, Balasubramanian S, Neidle S (2004) Loop-length-dependent folding of G-quadruplexes. J Am Chem Soc 126(50):16405-16415.
27. Budhathoki JB, Stafford EJ, Yodh JG, Balci H (2015) ATP-dependent G-quadruplex unfolding by Bloom helicase exhibits low processivity. Nucleic Acids Res 43(12): 5961-5970.
28. Chatterjee S, et al. (2014) Mechanistic insight into the interaction of BLM helicase with intra-strand G-quadruplex structures. Nat Commun 5:5556.
29. Wu WQ, Hou XM, Li M, Dou SX, Xi XG (2015) BLM unfolds G-quadruplexes in different structural environments through different mechanisms. Nucleic Acids Res 43(9):4614-4626.
30. McMurray CT (2010) Mechanisms of trinucleotide repeat instability during human development. Nat Rev Genet 11(11):786-799.
31. Lemmens B, van Schendel R, Tijsterman M (2015) Mutagenic consequences of a single G-quadruplex demonstrate mitotic inheritance of DNA replication fork barriers. Nat Commun 6:8909.
32. Piazza A, et al. (2015) Short loop length and high thermal stability determine genomic instability induced by G-quadruplex-forming minisatellites. EMBO J 34(12):1718-1734.
33. Bharti SK, et al. (2013) Specialization among iron-sulfur cluster helicases to resolve G-quadruplex DNA structures that threaten genomic stability. J Biol Chem 288(39):28217-28229.
34. Kreig A, et al. (2015) G-quadruplex formation in double strand DNA probed by NMM and CV fluorescence. Nucleic Acids Res 43(16):7961-7970.
35. Brázda V, Hároníková L, Liao JC, Fojta M (2014) DNA and RNA quadruplex-binding proteins. Int J Mol Sci 15(10):17493-17517.
36. Drosopoulos WC, Kosiyatrakul ST, Schildkraut CL (2015) BLM helicase facilitates telomere replication during leading strand synthesis of telomeres. J Cell Biol 210(2):191-208.
37. Zhou R, Zhang J, Bochman ML, Zakian VA, Ha T (2014) Periodic DNA patrolling underlies diverse functions of Pif1 on R-loops and G-rich DNA. eLife 3:e02190.
38. Reddy S, Li B, Comai L (2010) Processing of human telomeres by the Werner syndrome protein. Cell Cycle 9(16):3137-3138.
39. Edwards DN, Machwe A, Chen L, Bohr VA, Orren DK (2015) The DNA structure and sequence preferences of WRN underlie its function in telomeric recombination events. Nat Commun 6:8331.
40. Myong S, Rasnik I, Joo C, Lohman TM, Ha T (2005) Repetitive shuttling of a motor protein on DNA. Nature 437(7063):1321-1325.
41. Park J, et al. (2010) PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell 142(4):544-555.
42. Myong S, et al. (2009) Cytosolic viral sensor RIG-I is a 5′- Triphosphate-dependent translocase on double-stranded RNA. Science 323(5917):1070-1074.
43. Yodh JG, Stevens BC, Kanagaraj R, Janscak P, Ha T (2009) BLM helicase measures DNA unwound before switching strands and hRPA promotes unwinding reinitiation. EMBO J 28(4):405-416.
44. Koh HR, Xing L, Kleiman L, Myong S (2014) Repetitive RNA unwinding by RNA helicase A facilitates RNA annealing. Nucleic Acids Res 42(13):8556-8564.
45. Jena PV, et al. (2009) G-quadruplex DNA bound by a synthetic ligand is highly dynamic. J Am Chem Soc 131(35):12522-12523.
46. Opresko PL, Sowd G, Wang H (2009) The Werner syndrome helicase/exonuclease processes mobile D-loops through branch migration and degradation. PloS One 4(3): E4825.
47. Karow JK, Chakraverty RK, Hickson ID (1997) The Bloom's syndrome gene product is a 3'-5' DNA helicase. J Biol Chem 272(49):30611-30614.