Different activities of the conserved lysine residues in the double-stranded RNA binding domains of RNA helicase A in vitro and in the cell

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 7, 2014, Pages 2234-2243

  Xing, Li ^a   Niu, Meijuan ^b   Zhao, Xia ^b   Kleiman, Lawrence ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Double stranded RNA binding domain; Helicase activity; HIV 1; Lysine; RNA helicase A

Indexed keywords

LYSINE; MESSENGER RNA; RNA HELICASE; RNA HELICASE A; TRANSFER RNA; UNCLASSIFIED DRUG; VIRUS RNA;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME PURIFICATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA METABOLISM;

DOUBLE-STRANDED RNA BINDING DOMAIN; HELICASE ACTIVITY; HIV-1; LYSINE; RNA HELICASE A;

ALANINE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; DEAD-BOX RNA HELICASES; HEK293 CELLS; HIV-1; HUMANS; LYSINE; NEOPLASM PROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA, DOUBLE-STRANDED; RNA-BINDING PROTEINS; VIRUS REPLICATION;

EID: 84900036094     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.04.003     Document Type: Article

References (58)

1. Q.S. He, H. Tang, J. Zhang, K. Truong, F. Wong-Staal, and D. Zhou Comparisons of RNAi approaches for validation of human RNA helicase A as an essential factor in hepatitis C virus replication J. Virol. Methods 154 2008 216 219
2. O. Isken, M. Baroth, C.W. Grassmann, S. Weinlich, D.H. Ostareck, A. Ostareck-Lederer, and S.E. Behrens Nuclear factors are involved in hepatitis C virus RNA replication RNA 13 2007 1675 1692
3. P. Lawrence, and E. Rieder Identification of RNA helicase A as a new host factor in the replication cycle of foot-and-mouth disease virus J. Virol. 83 2009 11356 11366
4. L. Lin, Y. Li, H.M. Pyo, X. Lu, S.N. Raman, Q. Liu, E.G. Brown, and Y. Zhou Identification of RNA helicase A as a cellular factor that interacts with influenza A virus NS1 protein and its role in the virus life cycle J. Virol. 86 2012 1942 1954
5. R. Fujii, M. Okamoto, S. Aratani, T. Oishi, T. Ohshima, K. Taira, M. Baba, A. Fukamizu, and T. Nakajima A role of RNA helicase A in cis-acting transactivation response element-mediated transcriptional regulation of human immunodeficiency virus type 1 J. Biol. Chem. 276 2001 5445 5451
6. J. Li, H. Tang, T.M. Mullen, C. Westberg, T.R. Reddy, D.W. Rose, and F. Wong-Staal A role for RNA helicase A in post-transcriptional regulation of HIV type 1 Proc. Natl. Acad. Sci. U. S. A. 96 1999 709 714
7. C. Bolinger, A. Sharma, D. Singh, L. Yu, and K. Boris-Lawrie RNA helicase A modulates translation of HIV-1 and infectivity of progeny virions Nucleic Acids Res. 38 2010 1686 1696
8. Lys3 to HIV-1 RNA J. Virol. 85 2011 1847 1860
9. S. Aratani, T. Oishi, H. Fujita, M. Nakazawa, R. Fujii, N. Imamoto, Y. Yoneda, A. Fukamizu, and T. Nakajima The nuclear import of RNA helicase A is mediated by importin-alpha3 Biochem. Biophys. Res. Commun. 340 2006 125 133
10. H. Fujita, T. Ohshima, T. Oishi, S. Aratani, R. Fujii, A. Fukamizu, and T. Nakajima Relevance of nuclear localization and functions of RNA helicase A Int. J. Mol. Med. 15 2005 555 560
11. S.F. Anderson, B.P. Schlegel, T. Nakajima, E.S. Wolpin, and J.D. Parvin BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A Nat. Genet. 19 1998 254 256
12. S. Aratani, R. Fujii, T. Oishi, H. Fujita, T. Amano, T. Ohshima, M. Hagiwara, A. Fukamizu, and T. Nakajima Dual roles of RNA helicase A in CREB-dependent transcription Mol. Cell. Biol. 21 2001 4460 4469
13. T. Nakajima, C. Uchida, S.F. Anderson, C.G. Lee, J. Hurwitz, J.D. Parvin, and M. Montminy RNA helicase A mediates association of CBP with RNA polymerase II Cell 90 1997 1107 1112
14. J.A. Toretsky, V. Erkizan, A. Levenson, O.D. Abaan, J.D. Parvin, T.P. Cripe, A.M. Rice, S.B. Lee, and A. Uren Oncoprotein EWS-FLI1 activity is enhanced by RNA helicase A Cancer Res. 66 2006 5574 5581
15. T.R. Hartman, S. Qian, C. Bolinger, S. Fernandez, D.R. Schoenberg, and K. Boris-Lawrie RNA helicase A is necessary for translation of selected messenger RNAs Nat. Struct. Mol. Biol. 13 2006 509 516
16. L. Xing, M. Niu, and L. Kleiman In vitro and in vivo analysis of the interaction between RNA helicase A and HIV-1 RNA J. Virol. 86 2012 13272 13280
17. B.B. Roy, J. Hu, X. Guo, R.S. Russell, F. Guo, L. Kleiman, and C. Liang Association of RNA helicase A with human immunodeficiency virus type 1 particles J. Biol. Chem. 281 2006 12625 12635
18. C.G. Lee, and J. Hurwitz A new RNA helicase isolated from HeLa cells that catalytically translocates in the 3′ to 5′ direction J. Biol. Chem. 267 1992 4398 4407
19. S. Zhang, and F. Grosse Molecular characterization of nuclear DNA helicase II (RNA helicase A) Methods Mol. Biol. 587 2010 291 302
20. T.J. Gibson, and J.D. Thompson Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: implications for monomeric RNA helicases Nucleic Acids Res. 22 1994 2552 2556
21. A. Marchler-Bauer, S. Lu, J.B. Anderson, F. Chitsaz, M.K. Derbyshire, C. DeWeese-Scott, J.H. Fong, L.Y. Geer, R.C. Geer, N.R. Gonzales, M. Gwadz, D.I. Hurwitz, J.D. Jackson, Z. Ke, C.J. Lanczycki, F. Lu, G.H. Marchler, M. Mullokandov, M.V. Omelchenko, C.L. Robertson, J.S. Song, N. Thanki, R.A. Yamashita, D. Zhang, N. Zhang, C. Zheng, and S.H. Bryant CDD: a conserved domain database for the functional annotation of proteins Nucleic Acids Res. 39 2010 D225 D229
22. O. Cordin, J. Banroques, N.K. Tanner, and P. Linder The DEAD-box protein family of RNA helicases Gene 367 2006 17 37
23. C.G. Burd, and G. Dreyfuss Conserved structures and diversity of functions of RNA-binding proteins Science 265 1994 615 621
24. S. Zhang, and F. Grosse Domain structure of human nuclear DNA helicase II (RNA helicase A) J. Biol. Chem. 272 1997 11487 11494
25. A. Ranji, N. Shkriabai, M. Kvaratskhelia, K. Musier-Forsyth, and K. Boris-Lawrie Features of double-stranded RNA-binding domains of RNA helicase A are necessary for selective recognition and translation of complex mRNAs J. Biol. Chem. 286 2011 5328 5337
26. H. Walbott, S. Mouffok, R. Capeyrou, S. Lebaron, O. Humbert, H. van Tilbeurgh, Y. Henry, and N. Leulliot Prp43p contains a processive helicase structural architecture with a specific regulatory domain EMBO J. 29 2010 2194 2204
27. B. Tian, P.C. Bevilacqua, A. Diegelman-Parente, and M.B. Mathews The double-stranded-RNA-binding motif: interference and much more Nat. Rev. Mol. Cell Biol. 5 2004 1013 1023
28. U. Kim, Y. Wang, T. Sanford, Y. Zeng, and K. Nishikura Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing Proc. Natl. Acad. Sci. U. S. A. 91 1994 11457 11461
29. P.E. March, J. Ahnn, and M. Inouye The DNA sequence of the gene (rnc) encoding ribonuclease III of Escherichia coli Nucleic Acids Res. 13 1985 4677 4685
30. E. Meurs, K. Chong, J. Galabru, N.S. Thomas, I.M. Kerr, B.R. Williams, and A.G. Hovanessian Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon Cell 62 1990 379 390
31. A. Kharrat, M.J. Macias, T.J. Gibson, M. Nilges, and A. Pastore Structure of the dsRNA binding domain of E. coli RNase III EMBO J. 14 1995 3572 3584
32. M. Bycroft, S. Grunert, A.G. Murzin, M. Proctor, and D. St Johnston NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5 EMBO J. 14 1995 3563 3571
33. A. Ramos, S. Grunert, J. Adams, D.R. Micklem, M.R. Proctor, S. Freund, M. Bycroft, D. St Johnston, and G. Varani RNA recognition by a Staufen double-stranded RNA-binding domain EMBO J. 19 2000 997 1009
34. S. Nanduri, B.W. Carpick, Y. Yang, B.R. Williams, and J. Qin Structure of the double-stranded RNA-binding domain of the protein kinase PKR reveals the molecular basis of its dsRNA-mediated activation EMBO J. 17 1998 5458 5465
35. H. Wu, A. Henras, G. Chanfreau, and J. Feigon Structural basis for recognition of the AGNN tetraloop RNA fold by the double-stranded RNA-binding domain of Rnt1p RNase III Proc. Natl. Acad. Sci. U. S. A. 101 2004 8307 8312
36. Z. Wang, E. Hartman, K. Roy, G. Chanfreau, and J. Feigon Structure of a yeast RNase III dsRBD complex with a noncanonical RNA substrate provides new insights into binding specificity of dsRBDs Structure 19 2011 999 1010
37. J.M. Ryter, and S.C. Schultz Molecular basis of double-stranded RNA-protein interactions: structure of a dsRNA-binding domain complexed with dsRNA EMBO J. 17 1998 7505 7513
38. Q. Fu, and Y.A. Yuan Structural insights into RISC assembly facilitated by dsRNA-binding domains of human RNA helicase A (DHX9) Nucleic Acids Res. 41 2013 3457 3470
39. J. Blaszczyk, J. Gan, J.E. Tropea, D.L. Court, D.S. Waugh, and X. Ji Noncatalytic assembly of ribonuclease III with double-stranded RNA Structure 12 2004 457 466
40. K.T. Jeang, and V. Yedavalli Role of RNA helicases in HIV-1 replication Nucleic Acids Res. 34 2006 4198 4205
41. A. Ranji, and K. Boris-Lawrie RNA helicases: emerging roles in viral replication and the host innate response RNA Biol. 7 2010 775 787
42. G. Cachianes, C. Ho, R.F. Weber, S.R. Williams, D.V. Goeddel, and D.W. Leung Epstein-Barr virus-derived vectors for transient and stable expression of recombinant proteins Biotechniques 15 1993 255 259
43. E.F. Terwilliger, E.A. Cohen, Y.C. Lu, J.G. Sodroski, and W.A. Haseltine Functional role of human immunodeficiency virus type 1 vpu Proc. Natl. Acad. Sci. U. S. A. 86 1989 5163 5167
44. P.L. Pham, A. Kamen, and Y. Durocher Large-scale transfection of mammalian cells for the fast production of recombinant protein Mol. Biotechnol. 34 2006 225 237
45. M.K. Gorny, V. Gianakakos, S. Sharpe, and S. Zolla-Pazner Generation of human monoclonal antibodies to human immunodeficiency virus Proc. Natl. Acad. Sci. U. S. A. 86 1989 1624 1628
46. Lys3 annealing to viral RNA in human immunodeficiency virus type 1 J. Virol. 83 2009 8099 8107
47. L. Xing, M. Niu, X. Zhao, and L. Kleiman Roles of the linker region of RNA helicase A in HIV-1 RNA metabolism PLoS ONE 8 2013 e78596
48. L. Xing, and E. Kieff Epstein-Barr virus BHRF1 micro- and stable RNAs during latency III and after induction of replication J. Virol. 81 2007 9967 9975
49. I. Wong, and T.M. Lohman A double-filter method for nitrocellulose-filter binding: application to protein-nucleic acid interactions Proc. Natl. Acad. Sci. U. S. A. 90 1993 5428 5432
50. R.S. Russell, C. Liang, and M.A. Wainberg Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably? Retrovirology 1 2004 23
51. J.M. Caruthers, and D.B. McKay Helicase structure and mechanism Curr. Opin. Struct. Biol. 12 2002 123 133
52. S. Granneman, C. Lin, E.A. Champion, M.R. Nandineni, C. Zorca, and S.J. Baserga The nucleolar protein Esf2 interacts directly with the DExD/H box RNA helicase, Dbp8, to stimulate ATP hydrolysis Nucleic Acids Res. 34 2006 3189 3199
53. B. Schwer, and T. Meszaros RNA helicase dynamics in pre-mRNA splicing EMBO J. 19 2000 6582 6591
54. A.J. Sadler, O. Latchoumanin, D. Hawkes, J. Mak, and B.R. Williams An antiviral response directed by PKR phosphorylation of the RNA helicase A PLoS Pathog. 5 2009 e1000311
55. Z. Manojlovic, and B. Stefanovic A novel role of RNA helicase A in regulation of translation of type I collagen mRNAs RNA 18 2012 321 334
56. J. Jin, W. Jing, X.X. Lei, C. Feng, S. Peng, K. Boris-Lawrie, and Y. Huang Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes Nucleic Acids Res. 39 2011 3724 3734
57. A. Izzo, C. Regnard, V. Morales, E. Kremmer, and P.B. Becker Structure-function analysis of the RNA helicase maleless Nucleic Acids Res. 36 2008 950 962
58. R. Chenna, H. Sugawara, T. Koike, R. Lopez, T.J. Gibson, D.G. Higgins, and J.D. Thompson Multiple sequence alignment with the Clustal series of programs Nucleic Acids Res. 31 2003 3497 3500