Human DHX9 helicase unwinds triple-helical DNA structures

Biochemistry

Volumn 49, Issue 33, 2010, Pages 6992-6999

  Jain, Aklank ^a   Bacolla, Albino ^a   Chakraborty, Prasun ^b   Grosse, Frank ^b   Vasquez, Karen M ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATP HYDROLYSIS; DNA STRUCTURE; DOUBLE-STRAND BREAKS; FORKED DUPLEX SUBSTRATES; FORMING SEQUENCES; GENE STRUCTURE; GENOME STABILITY; HELICASE ACTIVITIES; HELICASES; HUMAN GENOMES; IMMUNOPRECIPITATES; IN-VITRO; INTRAMOLECULAR TRIPLEXES; MAMMALIAN CELLS; NATURALLY OCCURRING; ORDER REACTIONS; SINGLE-STRANDED OVERHANGS; TRIPLEX DNA; TRIPLEX-FORMING OLIGONUCLEOTIDES;

GENE EXPRESSION; GENE THERAPY; GENETIC ENGINEERING; MAMMALS; OLIGONUCLEOTIDES; REACTION KINETICS;

DNA;

ADENOSINE TRIPHOSPHATE; DHX9 HELICASE; HELICASE; UNCLASSIFIED DRUG; DEAD BOX PROTEIN; DHX9 PROTEIN, HUMAN; DNA; RECOMBINANT PROTEIN; TRIPLEX DNA; TUMOR PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; GENOMIC INSTABILITY; HYDROGEN BOND; HYDROLYSIS; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; CHEMISTRY; CONFORMATION; HUMAN; ISOLATION AND PURIFICATION; METABOLISM;

ADENOSINE TRIPHOSPHATE; DEAD-BOX RNA HELICASES; DNA; HUMANS; NEOPLASM PROTEINS; NUCLEIC ACID CONFORMATION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

MAMMALIA;

EID: 77955686716     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100795m     Document Type: Article

References (69)

1. Mirkin, S. M. (2008) Discovery of alternative DNA structures: A heroic decade (1979-1989) Front. Biosci. 13, 1064-1071
2. Patel, D. J., Phan, A. T., and 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, 7429-7455
3. Rich, A. and Zhang, S. (2003) Timeline: Z-DNA: The long road to biological function Nat. Rev. Genet. 4, 566-572
4. Neidle, S. (2009) The structures of quadruplex nucleic acids and their drug complexes Curr. Opin. Struct. Biol. 19, 239-250
5. Zhao, J., Bacolla, A., Wang, G., and Vasquez, K. M. (2010) Non-B DNA structure-induced genetic instability and evolution Cell. Mol. Life Sci. 67, 43-62
6. Bacolla, A. and Wells, R. D. (2004) Non-B DNA conformations, genomic rearrangements, and human disease J. Biol. Chem. 279, 47411-47414
7. Wong, H. M., Payet, L., and Huppert, J. L. (2009) Function and targeting of G-quadruplexes Curr. Opin. Mol. Ther. 11, 146-155
8. Du, Z., Zhao, Y., and Li, N. (2008) Genome-wide analysis reveals regulatory role of G4 DNA in gene transcription Genome Res. 18, 233-241
9. Eddy, J. and Maizels, N. (2008) Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes Nucleic Acids Res. 36, 1321-1333
10. Bacolla, A., Collins, J. R., Gold, B., Chuzhanova, N., Yi, M., Stephens, R. M., Stefanov, S., Olsh, A., Jakupciak, J. P., Dean, M., Lempicki, R. A., Cooper, D. N., and Wells, R. D. (2006) Long homopurine*homopyrimidine sequences are characteristic of genes expressed in brain and the pseudoautosomal region Nucleic Acids Res. 34, 2663-2675
11. Hughes, J. F., Skaletsky, H., Pyntikova, T., Minx, P. J., Graves, T., Rozen, S., Wilson, R. K., and Page, D. C. (2005) Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee Nature 437, 100-103
12. Locke, D. P., Segraves, R., Carbone, L., Archidiacono, N., Albertson, D. G., Pinkel, D., and Eichler, E. E. (2003) Large-scale variation among human and great ape genomes determined by array comparative genomic hybridization Genome Res. 13, 347-357
13. Marques-Bonet, T., Girirajan, S., and Eichler, E. E. (2009) The origins and impact of primate segmental duplications Trends Genet. 25, 443-454
14. Fernando, H., Sewitz, S., Darot, J., Tavare, S., Huppert, J. L., and Balasubramanian, S. (2009) Genome-wide analysis of a G-quadruplex-specific single-chain antibody that regulates gene expression Nucleic Acids Res. 37, 6716-6722
15. Li, H., Xiao, J., Li, J., Lu, L., Feng, S., and Droge, P. (2009) Human genomic Z-DNA segments probed by the Zα domain of ADAR1 Nucleic Acids Res. 37, 2737-2746
16. Goidts, V., Szamalek, J. M., de Jong, P. J., Cooper, D. N., Chuzhanova, N., Hameister, H., and Kehrer-Sawatzki, H. (2005) Independent intrachromosomal recombination events underlie the pericentric inversions of chimpanzee and gorilla chromosomes homologous to human chromosome 16 Genome Res. 15, 1232-1242
17. Kolb, J., Chuzhanova, N. A., Hogel, J., Vasquez, K. M., Cooper, D. N., Bacolla, A., and Kehrer-Sawatzki, H. (2009) Cruciform-forming inverted repeats appear to have mediated many of the microinversions that distinguish the human and chimpanzee genomes Chromosome Res. 17, 469-483
18. Perry, G. H., Ben-Dor, A., Tsalenko, A., Sampas, N., Rodriguez-Revenga, L., Tran, C. W., Scheffer, A., Steinfeld, I., Tsang, P., Yamada, N. A., Park, H. S., Kim, J. I., Seo, J. S., Yakhini, Z., Laderman, S., Bruhn, L., and Lee, C. (2008) The fine-scale and complex architecture of human copy-number variation Am. J. Hum. Genet. 82, 685-695
19. Hastings, P. J., Lupski, J. R., Rosenberg, S. M., and Ira, G. (2009) Mechanisms of change in gene copy number Nat. Rev. Genet. 10, 551-564
20. Lupski, J. R. (2009) Genomic disorders ten years on Genome Med. 1, 42
21. Bacolla, A., Jaworski, A., Larson, J. E., Jakupciak, J. P., Chuzhanova, N., Abeysinghe, S. S., O'Connell, C. D., Cooper, D. N., and Wells, R. D. (2004) Breakpoints of gross deletions coincide with non-B DNA conformations Proc. Natl. Acad. Sci. U.S.A. 101, 14162-14167
22. Bacolla, A., Jaworski, A., Connors, T. D., and Wells, R. D. (2001) Pkd1 unusual DNA conformations are recognized by nucleotide excision repair J. Biol. Chem. 276, 18597-18604
23. Wang, G., Christensen, L. A., and Vasquez, K. M. (2006) Z-DNA-forming sequences generate large-scale deletions in mammalian cells Proc. Natl. Acad. Sci. U.S.A. 103, 2677-2682
24. Wang, G. and Vasquez, K. M. (2004) Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells Proc. Natl. Acad. Sci. U.S.A. 101, 13448-13453
25. Wang, G., Carbajal, S., Vijg, J., DiGiovanni, J., and Vasquez, K. M. (2008) DNA structure-induced genomic instability in vivo J. Natl. Cancer Inst. 100, 1815-1817
26. Christensen, L. A., Finch, R. A., Booker, A. J., and Vasquez, K. M. (2006) Targeting oncogenes to improve breast cancer chemotherapy Cancer Res. 66, 4089-4094
27. Kim, E. and Deppert, W. (2006) The versatile interactions of p53 with DNA: When flexibility serves specificity Cell Death Differ. 13, 885-889
28. Brosh, R. M., Jr. (2008) Molecular biology: The Bloom's complex mousetrap Nature 456, 453-454
29. Wu, Y., Shin-ya, K., and Brosh, R. M., Jr. (2008) FANCJ helicase defective in Fanconia anemia and breast cancer unwinds G-quadruplex DNA to defend genomic stability Mol. Cell. Biol. 28, 4116-4128
30. Thompson, L. H. and Hinz, J. M. (2009) Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: Mechanistic insights Mutat. Res. 668, 54-72
31. Zhang, S. S. and Grosse, F. (1991) Purification and characterization of two DNA helicases from calf thymus nuclei J. Biol. Chem. 266, 20483-20490
32. Zhang, S. and Grosse, F. (1997) Domain structure of human nuclear DNA helicase II (RNA helicase A) J. Biol. Chem. 272, 11487-11494
33. Fuller-Pace, F. V. (2006) DExD/H box RNA helicases: Multifunctional proteins with important roles in transcriptional regulation Nucleic Acids Res. 34, 4206-4215
34. Zhang, S. and Grosse, F. (1994) Nuclear DNA helicase II unwinds both DNA and RNA Biochemistry 33, 3906-3912
35. Lee, C. G., da Costa Soares, V., Newberger, C., Manova, K., Lacy, E., and Hurwitz, J. (1998) RNA helicase A is essential for normal gastrulation Proc. Natl. Acad. Sci. U.S.A. 95, 13709-13713
36. Zhang, S. and Grosse, F. (2004) Multiple functions of nuclear DNA helicase II (RNA helicase A) in nucleic acid metabolism Acta Biochim. Biophys. Sin. 36, 177-183
37. Perkins, B. D., Wilson, J. H., Wensel, T. G., and Vasquez, K. M. (1998) Triplex targets in the human rhodopsin gene Biochemistry 37, 11315-11322
38. Brosh, R. M., Jr., Majumdar, A., Desai, S., Hickson, I. D., Bohr, V. A., and Seidman, M. M. (2001) Unwinding of a DNA triple helix by the Werner and Bloom syndrome helicases J. Biol. Chem. 276, 3024-3030
39. Sommers, J. A., Rawtani, N., Gupta, R., Bugreev, D. V., Mazin, A. V., Cantor, S. B., and Brosh, R. M., Jr. (2009) FANCJ uses its motor ATPase to destabilize protein-DNA complexes, unwind triplexes, and inhibit RAD51 strand exchange J. Biol. Chem. 284, 7505-7517
40. Patel, S. S. and Donmez, I. (2006) Mechanisms of helicases J. Biol. Chem. 281, 18265-18268
41. Nakajima, T., Uchida, C., Anderson, S. F., Lee, C. G., Hurwitz, J., Parvin, J. D., and Montminy, M. (1997) RNA helicase A mediates association of CBP with RNA polymerase II Cell 90, 1107-1112
42. Chakraborty, P. and Grosse, F. (2010) WRN helicase unwinds Okazaki fragment-like hybrids in a reaction stimulated by the human DHX9 helicase Nucleic Acids Res. (in press)
43. Lohman, T. M. and Bjornson, K. P. (1996) Mechanisms of helicase-catalyzed DNA unwinding Annu. Rev. Biochem. 65, 169-214
44. Martin, G. M. (1997) The Werner mutation: Does it lead to a "public" or "private" mechanism of aging? Mol. Med. 3, 356-358
45. Kennedy, R. D. and D'Andrea, A. D. (2005) The Fanconi Anemia/BRCA pathway: New faces in the crowd Genes Dev. 19, 2925-2940
46. n J. Biol. Chem. 274, 12797-12802
47. 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
48. 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
49. Owczarzy, R., Moreira, B. G., You, Y., Behlke, M. A., and Walder, J. A. (2008) Predicting stability of DNA duplexes in solutions containing magnesium and monovalent cations Biochemistry 47, 5336-5353
50. Wu, P., Kawamoto, Y., Hara, H., and Sugimoto, N. (2002) Effect of divalent cations and cytosine protonation on thermodynamic properties of intermolecular DNA double and triple helices J. Inorg. Biochem. 91, 277-285
51. Plum, G. E. and Breslauer, K. J. (1995) Thermodynamics of an intramolecular DNA triple helix: A calorimetric and spectroscopic study of the pH and salt dependence of thermally induced structural transitions J. Mol. Biol. 248, 679-695
52. Schroth, G. P. and Ho, P. S. (1995) Occurrence of potential cruciform and H-DNA forming sequences in genomic DNA Nucleic Acids Res. 23, 1977-1983
53. Jain, A., Wang, G., and Vasquez, K. M. (2008) DNA triple helices: Biological consequences and therapeutic potential Biochimie 90, 1117-1130
54. Raghavan, S. C. and Lieber, M. R. (2004) Chromosomal translocations and non-B DNA structures in the human genome Cell Cycle 3, 762-768
55. Lieber, M. R., Ma, Y., Pannicke, U., and Schwarz, K. (2004) The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination DNA Repair 3, 817-826
56. Walker, J. R., Corpina, R. A., and Goldberg, J. (2001) Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair Nature 412, 607-614
57. Smith, G. C. and Jackson, S. P. (1999) The DNA-dependent protein kinase Genes Dev. 13, 916-934
58. Zhang, S., Schlott, B., Gorlach, M., and Grosse, F. (2004) DNA-dependent protein kinase (DNA-PK) phosphorylates nuclear DNA helicase II/RNA helicase A and hnRNP proteins in an RNA-dependent manner Nucleic Acids Res. 32, 1-10
59. Mischo, H. E., Hemmerich, P., Grosse, F., and Zhang, S. (2005) Actinomycin D induces histone γ-H2AX foci and complex formation of γ-H2AX with Ku70 and nuclear DNA helicase II J. Biol. Chem. 280, 9586-9594
60. Friedemann, J., Grosse, F., and Zhang, S. (2005) Nuclear DNA helicase II (RNA helicase A) interacts with Werner syndrome helicase and stimulates its exonuclease activity J. Biol. Chem. 280, 31303-31313
61. Schlegel, B. P., Starita, L. M., and Parvin, J. D. (2003) Overexpression of a protein fragment of RNA helicase A causes inhibition of endogenous BRCA1 function and defects in ploidy and cytokinesis in mammary epithelial cells Oncogene 22, 983-991
62. Anderson, S. F., Schlegel, B. P., Nakajima, T., Wolpin, E. S., and Parvin, J. D. (1998) BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A Nat. Genet. 19, 254-256
63. Bau, D. T., Mau, Y. C., and Shen, C. Y. (2006) The role of BRCA1 in non-homologous end-joining Cancer Lett. 240, 1-8
64. Wei, L., Lan, L., Hong, Z., Yasui, A., Ishioka, C., and Chiba, N. (2008) Rapid recruitment of BRCA1 to DNA double-strand breaks is dependent on its association with Ku80 Mol. Cell. Biol. 28, 7380-7393
65. Patel, H. P., Lu, L., Blaszak, R. T., and Bissler, J. J. (2004) PKD1 intron 21: Triplex DNA formation and effect on replication Nucleic Acids Res. 32, 1460-1468
66. n tracts Proc. Natl. Acad. Sci. U.S.A. 88, 507-511
67. Ohshima, K., Montermini, L., Wells, R. D., and Pandolfo, M. (1998) Inhibitory effects of expanded GAA·TTC triplet repeats from intron I of the Friedreich ataxia gene on transcription and replication in vivo J. Biol. Chem. 273, 14588-14595
68. n repeats in vivo Mol. Cell. Biol. 24, 2286-2295
69. Belotserkovskii, B. P., De Silva, E., Tornaletti, S., Wang, G., Vasquez, K. M., and Hanawalt, P. C. (2007) A triplex-forming sequence from the human c-MYC promoter interferes with DNA transcription J. Biol. Chem. 282, 32433-32441