ATP-dependent G-quadruplex unfolding by Bloom helicase exhibits low processivity

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages 5961-5970

  Budhathoki, Jagat B ^a   Stafford, Edward J ^a   Yodh, Jaya G ^b   Balci, Hamza ^a  

^a KENT STATE UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BLOOM SYNDROME HELICASE; DOUBLE STRANDED DNA; GUANINE QUADRUPLEX; HELICASE; PIF1 HELICASE; SINGLE STRANDED DNA BINDING PROTEIN; UNCLASSIFIED DRUG; DNA; POLYTHYMIDYLIC ACID; RECQ HELICASE; SINGLE STRANDED DNA;

AMINO ACID SEQUENCE; ARTICLE; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME LOCALIZATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN UNFOLDING; CHEMISTRY; KINETICS; METABOLISM; TELOMERE;

ADENOSINE TRIPHOSPHATE; DNA; DNA, SINGLE-STRANDED; G-QUADRUPLEXES; HUMANS; KINETICS; POLY T; RECQ HELICASES; TELOMERE;

EID: 84942163137     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv531     Document Type: Article

References (68)

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2. Karow, J.K., Chakraverty, R.K. and Hickson, I.D. (1997) The Bloom's syndrome gene product is a 3'-5' DNA helicase. J. Biol. Chem., 272, 30611-30614.
3. Chakraverty, R.K. and Hickson, I.D. (1999) Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays, 21, 286-294.
4. Ellis, NA, Groden, J., Ye, T.Z., Straughen, J., Lennon, DJ., Ciocci, S., Proytcheva, M. and German, J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83, 655-666.
5. Yodh, J.G., Stevens, B.C, Kanagaraj, R., Janscak, P. and Ha, T (2009) BLM helicase measures DNA unwound before switching strands and hRPA promotes unwinding reinitiation. EMBO J., 28, 405-416.
6. Johnson, J.E., Cao, K., Ryvkin, P., Wang, L.S. and Johnson, F.B. (2010) Altered gene expression in the Werner and Bloom syndromes is associated with sequences having G-quadruplex forming potential. Nucleic Acids Res., 38, 1114-1122.
7. Kamath-Loeb, A., Loeb, L.A. and Fry, M. (2012) The Werner syndrome protein is distinguished from the Bloom syndrome protein by its capacity to tightly bind diverse DNA structures. PloS One, 7, e30189.
8. Liu, J.Q., Chen, C.Y, Xue, Y, Hao Y.H. and Tan, Z. (2010) G-quadruplex hinders translocation of BLM helicase on DNA: a real-time fluorescence spectroscopic unwinding study and comparison with duplex substrates. J. Am. Chem. Soc, 132, 10521-10527.
9. Sun, H., Karow, J.K., Hickson, I.D. and Maizels, N (1998) The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem., 273, 27587-27592.
10. Blackburn, E.H. (1991) Structure and function of telomeres. Nature, 350, 569-573.
11. Chaires, J.B. (2010) Human telomeric G-quadruplex: thermodynamic and kinetic studies of telomeric quadruplex stability. FEBS J., 277, 1098-1106.
12. Gellert, M., Lipsett, MN. and Davies, DR. (1962) Helix formation by guanylic acid. Proc. Natl. Acad. Sci. U.S.A., 48, 2013-2018.
13. Tran, PL, Mergny, J.L. and Alberti, P (2011) Stability of telomeric G-quadruplexes. Nucleic Acids Res., 39, 3282-3294.
14. Biffi, G, Tannahill, D., McCafferty, J. and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem., 5, 182-186.
15. Bachrati, C.Z. and Hickson, I.D (2003) RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J., 374, 577-606.
16. Opresko, PL, Cheng, W.H. and Bohr, V.A. (2004) Junction of RecQ helicase biochemistry and human disease. J. Biol. Chem., 279, 18099-18102.
17. Fry, M. and Loeb, L.A. (1999) Human werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n. J. Biol. Chem., 274, 12797-12802.
18. Huber, M.D., Lee, D.C. and Maizels, N (2002) G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucleic Acids Res., 30, 3954-3961.
19. Mohaghegh, P, Karow, J.K., Brosh, R.M. Jr, Bohr, V.A. and Hickson, I.D (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res., 29, 2843-2849.
20. Budhathoki, J.B., Ray, S., Urban, V., Janscak, P, Yodh, J.G. and Balci, H. (2015) RecQ-core of BLM unfolds telomeric G-quadruplex in the absence of ATP. Nucleic Acids Res, 42, 11528-11545.
21. Chatterjee, S., Zagelbaum, J., Savitsky, P, Sturzenegger, A., Huttner, D, Janscak, P, Hickson, I.D., Gileadi, O. and Rothenberg, E. (2014) Mechanistic insight into the interaction of BLM helicase with intra-strand G-quadruplex structures. Nat. Commun., 5, 5556.
22. Ray, S., Bandaria, J.N, Qureshi, M.H, Yildiz, A. and Balci, H. (2014) G-quadruplex formation in telomeres enhances POT1/TPP1 protection against RPA binding. Proc. Natl. Acad. Sci. U.S.A., 111, 2990-2995.
23. Ray, S., Qureshi, M.H., Malcolm, D.W., Budhathoki, J.B., Celik, U. and Balci, H. (2013) RPA-mediated unfolding of systematically varying G-quadruplex structures. Biophys. J., 104, 2235-2245.
24. Zhou, R., Zhang, J., Bochman, M.L., Zakian, V.A. and Ha, T. (2014) Periodic DNA patrolling underlies diverse functions of Pif1 on R-loops and G-rich DNA. eLife, 3, e02190.
25. Janscak, P., Garcia, P.L., Hamburger, F., Makuta, Y., Shiraishi, K., Imai, Y., Ikeda, H. and Bickle, T.A. (2003) Characterization and mutational analysis of the RecQ core of the bloom syndrome protein. J. Mol. Biol., 330, 29-42.
26. Viglasky, V., Bauer, L., Tluckova, K. and Javorsky, P. (2010) Evaluation of human telomeric g-quadruplexes: the influence of overhanging sequences on quadruplex stability and folding. J. Nucleic Acids, 2010, 82035.
27. Park, J., Myong, S., Niedziela-Majka, A., Lee, K.S., Yu, J., Lohman, T.M. and Ha, T. (2010) PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell, 142, 544-555.
28. Gyimesi, M., Sarlos, K. and Kovacs, M. (2010) Processive translocation mechanism of the human Bloom's syndrome helicase along single-stranded DNA. Nucleic Acids Res., 38, 4404-4414.
29. Yang, Y., Dou, S.X., Xu, Y.N., Bazeille, N., Wang, P.Y., Rigolet, P., Xu, H.Q. and Xi, X.G. (2010) Kinetic mechanism of DNA unwinding by the BLM helicase core and molecular basis for its low processivity. Biochemistry, 49, 656-668.
30. Hwang, H., Buncher, N., Opresko, P.L. and Myong, S. (2012) POT1-TPP1 regulates telomeric overhang structural dynamics. Structure, 20, 1872-1880.
31. Xu, Y.N., Bazeille, N., Ding, X.Y., Lu, X.M., Wang, P.Y., Bugnard, E., Grondin, V., Dou, S.X. and Xi, X.G. (2012) Multimeric BLM is dissociated upon ATP hydrolysis and functions as monomers in resolving DNA structures. Nucleic Acids Res., 40, 9802-9814.
32. Gyimesi, M., Pires, R.H., Billington, N., Sarlos, K., Kocsis, Z.S., Modos, K., Kellermayer, M.S. and Kovacs, M. (2013) Visualization of human Bloom's syndrome helicase molecules bound to homologous recombination intermediates. FA S E B J., 27, 4954-4964.
33. Byrd, A.K. and Raney, K.D. (2015) A parallel quadruplex DNA is bound tightly but unfolded slowly by pif1 helicase. J. Biol. Chem., 290, 6482-6494.
34. Chistol, G. and Walter, J. (2014) Molecular watchdogs on genome patrol. eLife, 3, e02854.
35. German, J. (1993) Bloom syndrome: amendelian prototype of somatic mutational disease. Medicine (Baltimore), 72, 393-406.
36. Karow, J.K., Chakraverty, R.K. and Hickson, I.D. (1997) The Bloom's syndrome gene product is a 3'-5' DNA helicase. J. Biol. Chem., 272, 30611-30614.
37. Chakraverty, R.K. and Hickson, I.D. (1999) Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays, 21, 286-294.
38. Ellis, NA, Groden, J., Ye, T.Z., Straughen, J., Lennon, DJ., Ciocci, S., Proytcheva, M. and German, J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83, 655-666.
39. Yodh, J.G., Stevens, B.C, Kanagaraj, R., Janscak, P. and Ha, T (2009) BLM helicase measures DNA unwound before switching strands and hRPA promotes unwinding reinitiation. EMBO J., 28, 405-416.
40. Johnson, J.E., Cao, K., Ryvkin, P., Wang, L.S. and Johnson, F.B. (2010) Altered gene expression in the Werner and Bloom syndromes is associated with sequences having G-quadruplex forming potential. Nucleic Acids Res., 38, 1114-1122.
41. Kamath-Loeb, A., Loeb, L.A. and Fry, M. (2012) The Werner syndrome protein is distinguished from the Bloom syndrome protein by its capacity to tightly bind diverse DNA structures. PloS One, 7, e30189.
42. Liu, J.Q., Chen, C.Y, Xue, Y, Hao Y.H. and Tan, Z. (2010) G-quadruplex hinders translocation of BLM helicase on DNA: a real-time fluorescence spectroscopic unwinding study and comparison with duplex substrates. J. Am. Chem. Soc, 132, 10521-10527.
43. Sun, H., Karow, J.K., Hickson, I.D. and Maizels, N (1998) The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem., 273, 27587-27592.
44. Blackburn, E.H. (1991) Structure and function of telomeres. Nature, 350, 569-573.
45. Chaires, J.B. (2010) Human telomeric G-quadruplex: thermodynamic and kinetic studies of telomeric quadruplex stability. FEBS J., 277, 1098-1106.
46. Gellert, M., Lipsett, MN. and Davies, DR. (1962) Helix formation by guanylic acid. Proc. Natl. Acad. Sci. U.S.A., 48, 2013-2018.
47. Tran, PL, Mergny, J.L. and Alberti, P (2011) Stability of telomeric G-quadruplexes. Nucleic Acids Res., 39, 3282-3294.
48. Biffi, G, Tannahill, D., McCafferty, J. and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat. Chem., 5, 182-186.
49. Bachrati, C.Z. and Hickson, I.D (2003) RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J., 374, 577-606.
50. Opresko, PL, Cheng, W.H. and Bohr, V.A. (2004) Junction of RecQ helicase biochemistry and human disease. J. Biol. Chem., 279, 18099-18102.
51. Fry, M. and Loeb, L.A. (1999) Human werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n. J. Biol. Chem., 274, 12797-12802.
52. Huber, M.D., Lee, D.C. and Maizels, N (2002) G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucleic Acids Res., 30, 3954-3961.
53. Mohaghegh, P, Karow, J.K., Brosh, R.M. Jr, Bohr, V.A. and Hickson, I.D (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res., 29, 2843-2849.
54. Budhathoki, J.B., Ray, S., Urban, V., Janscak, P, Yodh, J.G. and Balci, H. (2015) RecQ-core of BLM unfolds telomeric G-quadruplex in the absence of ATP. Nucleic Acids Res, 42, 11528-11545.
55. Chatterjee, S., Zagelbaum, J., Savitsky, P, Sturzenegger, A., Huttner, D, Janscak, P, Hickson, I.D., Gileadi, O. and Rothenberg, E. (2014) Mechanistic insight into the interaction of BLM helicase with intra-strand G-quadruplex structures. Nat. Commun., 5, 5556.
56. Ray, S., Bandaria, J.N, Qureshi, M.H, Yildiz, A. and Balci, H. (2014) G-quadruplex formation in telomeres enhances POT1/TPP1 protection against RPA binding. Proc. Natl. Acad. Sci. U.S.A., 111, 2990-2995.
57. Ray, S., Qureshi, M.H., Malcolm, D.W., Budhathoki, J.B., Celik, U. and Balci, H. (2013) RPA-mediated unfolding of systematically varying G-quadruplex structures. Biophys. J., 104, 2235-2245.
58. Zhou, R., Zhang, J., Bochman, M.L., Zakian, V.A. and Ha, T. (2014) Periodic DNA patrolling underlies diverse functions of Pif1 on R-loops and G-rich DNA. eLife, 3, e02190.
59. Janscak, P., Garcia, P.L., Hamburger, F., Makuta, Y., Shiraishi, K., Imai, Y., Ikeda, H. and Bickle, T.A. (2003) Characterization and mutational analysis of the RecQ core of the bloom syndrome protein. J. Mol. Biol., 330, 29-42.
60. Viglasky, V., Bauer, L., Tluckova, K. and Javorsky, P. (2010) Evaluation of human telomeric g-quadruplexes: the influence of overhanging sequences on quadruplex stability and folding. J. Nucleic Acids, 2010, 82035.
61. Park, J., Myong, S., Niedziela-Majka, A., Lee, K.S., Yu, J., Lohman, T.M. and Ha, T. (2010) PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell, 142, 544-555.
62. Gyimesi, M., Sarlos, K. and Kovacs, M. (2010) Processive translocation mechanism of the human Bloom's syndrome helicase along single-stranded DNA. Nucleic Acids Res., 38, 4404-4414.
63. Yang, Y., Dou, S.X., Xu, Y.N., Bazeille, N., Wang, P.Y., Rigolet, P., Xu, H.Q. and Xi, X.G. (2010) Kinetic mechanism of DNA unwinding by the BLM helicase core and molecular basis for its low processivity. Biochemistry, 49, 656-668.
64. Hwang, H., Buncher, N., Opresko, P.L. and Myong, S. (2012) POT1-TPP1 regulates telomeric overhang structural dynamics. Structure, 20, 1872-1880.
65. Xu, Y.N., Bazeille, N., Ding, X.Y., Lu, X.M., Wang, P.Y., Bugnard, E., Grondin, V., Dou, S.X. and Xi, X.G. (2012) Multimeric BLM is dissociated upon ATP hydrolysis and functions as monomers in resolving DNA structures. Nucleic Acids Res., 40, 9802-9814.
66. Gyimesi, M., Pires, R.H., Billington, N., Sarlos, K., Kocsis, Z.S., Modos, K., Kellermayer, M.S. and Kovacs, M. (2013) Visualization of human Bloom's syndrome helicase molecules bound to homologous recombination intermediates. FA S E B J., 27, 4954-4964.
67. Byrd, A.K. and Raney, K.D. (2015) A parallel quadruplex DNA is bound tightly but unfolded slowly by pif1 helicase. J. Biol. Chem., 290, 6482-6494.
68. Chistol, G. and Walter, J. (2014) Molecular watchdogs on genome patrol. eLife, 3, e02854.