DEAD-box protein CYT-19 is activated by exposed helices in a group I intron RNA

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

Volumn 111, Issue 29, 2014, Pages

  Jarmoskaite, Inga ^a   Bhaskaran, Hari ^a,c   Seifert, Soenke ^b   Russell, Rick ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

RNA folding; RNA misfolding; RNA tertiary structure; RNA unwinding; Superfamily 2 helicase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; DEAD BOX PROTEIN; DEAD BOX PROTEIN CYT 19; MITOCHONDRIAL RNA; RIBOZYME; RNA; RNA HELICASE; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; INTRON; NEUROSPORA CRASSA; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING; RNA FOLDING; RNA STRUCTURE; TETRAHYMENA;

RNA FOLDING; RNA MISFOLDING; RNA TERTIARY STRUCTURE; RNA UNWINDING; SUPERFAMILY 2 HELICASE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; DEAD-BOX RNA HELICASES; ENZYME ACTIVATION; FUNGAL PROTEINS; HYDROLYSIS; INTRONS; MAGNESIUM; MODELS, MOLECULAR; NEUROSPORA CRASSA; NUCLEIC ACID CONFORMATION; PROTEIN FOLDING; RNA; RNA, CATALYTIC; TETRAHYMENA;

EID: 84904631841     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1404307111     Document Type: Article

References (65)

1. Cordin O, Banroques J, Tanner NK, Linder P (2006) The DEAD-box protein family of RNA helicases. Gene 367:17-37. (Pubitemid 43286737)
2. Jankowsky E, Fairman ME (2007) RNA helicases - one fold for many functions. Curr Opin Struct Biol 17(3):316-324. (Pubitemid 47021361)
3. Linder P, Jankowsky E (2011) From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12(8):505-516.
4. Liu F, Putnam A, Jankowsky E (2008) ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc Natl Acad Sci USA 105(51):20209-20214.
5. Hilbert M, Karow AR, Klostermeier D (2009) The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biol Chem 390(12):1237-1250.
6. Mallam AL, Del Campo M, Gilman B, Sidote DJ, Lambowitz AM (2012) Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 490(7418):121-125.
7. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S (2006) Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125(2):287-300.
8. Chen Y, et al. (2008) DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc Natl Acad Sci USA 105(51):20203-20208.
9. Henn A, Cao W, Hackney DD, De La Cruz EM (2008) The ATPase cycle mechanism of the DEAD-box rRNA helicase, DbpA. J Mol Biol 377(1):193-205.
10. Henn A, Bradley MJ, De La Cruz EM (2012) ATP utilization and RNA conformational rearrangement by DEAD-box proteins. Annu Rev Biophys 41:247-267.
11. Jarmoskaite I, Russell R (2011) DEAD-box proteins as RNA helicases and chaperones. Wiley Interdiscip Rev RNA 2(1):135-152.
12. Fairman-Williams ME, Guenther UP, Jankowsky E (2010) SF1 and SF2 helicases: Family matters. Curr Opin Struct Biol 20(3):313-324.
13. Cao W, et al. (2011) Mechanism of Mss116 ATPase reveals functional diversity of DEAD-Box proteins. J Mol Biol 409(3):399-414.
14. Rogers GW, Jr, Richter NJ, Merrick WC (1999) Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J Biol Chem 274(18): 12236-12244.
15. Bizebard T, Ferlenghi I, Iost I, Dreyfus M (2004) Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases. Biochemistry 43(24):7857-7866. (Pubitemid 38787694)
16. Uhlmann-Schiffler H, Jalal C, Stahl H (2006) Ddx42p-a human DEAD box protein with RNA chaperone activities. Nucleic Acids Res 34(1):10-22. (Pubitemid 43167916)
17. Mohr S, Stryker JM, Lambowitz AM (2002) A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109(6):769-779. (Pubitemid 34722271)
18. Huang HR, et al. (2005) The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function. Proc Natl Acad Sci USA 102(1):163-168.
19. Halls C, et al. (2007) Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J Mol Biol 365(3): 835-855. (Pubitemid 46001664)
20. Potratz JP, Del Campo M, Wolf RZ, Lambowitz AM, Russell R (2011) ATP-dependent roles of the DEAD-box protein Mss116p in group II intron splicing in vitro and in vivo. J Mol Biol 411(3):661-679.
21. Zingler N, Solem A, Pyle AM (2010) Dual roles for the Mss116 cofactor during splicing of the ai5γ group II intron. Nucleic Acids Res 38(19):6602-6609.
22. Karunatilaka KS, Solem A, Pyle AM, Rueda D (2010) Single-molecule analysis of Mss116-mediated group II intron folding. Nature 467(7318):935-939.
23. Russell R, Jarmoskaite I, Lambowitz AM (2013) Toward a molecular understanding of RNA remodeling by DEAD-box proteins. RNA Biol 10(1):44-55.
24. Del Campo M, et al. (2007) Do DEAD-box proteins promote group II intron splicing without unwinding RNA? Mol Cell 28(1):159-166. (Pubitemid 47531967)
25. Del Campo M, et al. (2009) Unwinding by local strand separation is critical for the function of DEAD-box proteins as RNA chaperones. J Mol Biol 389(4):674-693.
26. Tijerina P, Bhaskaran H, Russell R (2006) Nonspecific binding to structured RNA and preferential unwinding of an exposed helix by the CYT-19 protein, a DEAD-box RNA chaperone. Proc Natl Acad Sci USA 103(45):16698-16703. (Pubitemid 44737316)
27. Grohman JK, et al. (2007) Probing the mechanisms of DEAD-box proteins as general RNA chaperones: The C-terminal domain of CYT-19 mediates general recognition of RNA. Biochemistry 46(11):3013-3022. (Pubitemid 46449125)
28. Bhaskaran H, Russell R (2007) Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 449(7165):1014-1018. (Pubitemid 350014602)
29. Cate JH, et al. (1996) Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 273(5282):1678-1685. (Pubitemid 26317777)
30. Golden BL, Gooding AR, Podell ER, Cech TR (1998) A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science 282(5387):259-264. (Pubitemid 28487190)
31. Lehnert V, Jaeger L, Michel F, Westhof E (1996) New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: A complete 3D model of the Tetrahymena thermophila ribozyme. Chem Biol 3(12):993-1009. (Pubitemid 27058823)
32. Russell R, Herschlag D (2001) Probing the folding landscape of the Tetrahymena ribozyme: Commitment to form the native conformation is late in the folding pathway. J Mol Biol 308(5):839-851. (Pubitemid 32574363)
33. Russell R, et al. (2006) The paradoxical behavior of a highly structured misfolded intermediate in RNA folding. J Mol Biol 363(2):531-544. (Pubitemid 44436255)
34. Russell R, Millett IS, Doniach S, Herschlag D (2000) Small angle X-ray scattering reveals a compact intermediate in RNA folding. Nat Struct Biol 7(5):367-370. (Pubitemid 30249997)
35. Mitchell D, 3rd, Jarmoskaite I, Seval N, Seifert S, Russell R (2013) The long-range P3 helix of the Tetrahymena ribozyme is disrupted during folding between the native and misfolded conformations. J Mol Biol 425(15):2670-2686.
36. Wan Y, Suh H, Russell R, Herschlag D (2010) Multiple unfolding events during native folding of the Tetrahymena group I ribozyme. J Mol Biol 400(5):1067-1077.
37. Benz-Moy TL, Herschlag D (2011) Structure-function analysis from the outside in: Long-range tertiary contacts in RNA exhibit distinct catalytic roles. Biochemistry 50(40):8733-8755.
38. Shcherbakova I, Brenowitz M (2005) Perturbation of the hierarchical folding of a large RNA by the destabilization of its Scaffold's tertiary structure. J Mol Biol 354(2): 483-496. (Pubitemid 41579860)
39. Treiber DK, Williamson JR (2001) Concerted kinetic folding of a multidomain ribozyme with a disrupted loop-receptor interaction. J Mol Biol 305(1):11-21. (Pubitemid 32039741)
40. Wan Y, Mitchell D, 3rd, Russell R (2009) Catalytic activity as a probe of native RNA folding. Methods Enzymol 468:195-218.
41. Russell R, Tijerina P, Chadee AB, Bhaskaran H (2007) Deletion of the P5abc peripheral element accelerates early and late folding steps of the Tetrahymena group I ribozyme. Biochemistry 46(17):4951-4961. (Pubitemid 46682994)
42. Pan J, Woodson SA (1999) The effect of long-range loop-loop interactions on folding of the Tetrahymena self-splicing RNA. J Mol Biol 294(4):955-965. (Pubitemid 30000387)
43. Celander DW, Cech TR (1991) Visualizing the higher order folding of a catalytic RNA molecule. Science 251(4992):401-407.
44. Sattin BD, Zhao W, Travers K, Chu S, Herschlag D (2008) Direct measurement of tertiary contact cooperativity in RNA folding. J Am Chem Soc 130(19):6085-6087. (Pubitemid 351657284)
45. Das R, et al. (2003) The fastest global events in RNA folding: electrostatic relaxation and tertiary collapse of the Tetrahymena ribozyme. J Mol Biol 332(2):311-319. (Pubitemid 37013501)
46. Liu F, Putnam AA, Jankowsky E (2013) DEAD-box helicases form nucleotidedependent long-lived complexes with RNA. Biochemistry 53(2):423-433.
47. Doniach S (2001) Changes in biomolecular conformation seen by small angle X-ray scattering. Chem Rev 101(6):1763-1778.
48. Shi H, O'Brien CA, Van Horn DJ, Wolin SL (1996) A misfolded form of 5S rRNA is complexed with the Ro and La autoantigens. RNA 2(8):769-784. (Pubitemid 26374208)
49. Fuchs G, Stein AJ, Fu C, Reinisch KM, Wolin SL (2006) Structural and biochemical basis for misfolded RNA recognition by the Ro autoantigen. Nat Struct Mol Biol 13(11): 1002-1009. (Pubitemid 44684852)
50. Reinisch KM, Wolin SL (2007) Emerging themes in non-coding RNA quality control. Curr Opin Struct Biol 17(2):209-214. (Pubitemid 46575257)
51. Staley JP, Guthrie C (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92(3):315-326. (Pubitemid 28093010)
52. Strunk BS, Karbstein K (2009) Powering through ribosome assembly. RNA 15(12): 2083-2104.
53. Rajkowitsch L, et al. (2007) RNA chaperones, RNA annealers and RNA helicases. RNA Biol 4(3):118-130. (Pubitemid 351237913)
54. Russell R (2008) RNA misfolding and the action of chaperones. Front Biosci 13:1-20.
55. Grohman JK, et al. (2013) A guanosine-centric mechanism for RNA chaperone function. Science 340(6129):190-195.
56. Grossberger R, et al. (2005) Influence of RNA structural stability on the RNA chaperone activity of the Escherichia coli protein StpA. Nucleic Acids Res 33(7): 2280-2289. (Pubitemid 41439895)
57. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475(7356):324-332.
58. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: Emerging mechanistic insights. Nat Rev Mol Cell Biol 11(7):515-528.
59. Böcking T, Aguet F, Harrison SC, Kirchhausen T (2011) Single-molecule analysis of a molecular disassemblase reveals the mechanism of Hsc70-driven clathrin uncoating. Nat Struct Mol Biol 18(3):295-301.
60. Taipale M, et al. (2012) Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150(5):987-1001.
61. Russell R, Herschlag D (1999) New pathways in folding of the Tetrahymena group I RNA enzyme. J Mol Biol 291(5):1155-1167. (Pubitemid 29423778)
62. Zaug AJ, Grosshans CA, Cech TR (1988) Sequence-specific endoribonuclease activity of the Tetrahymena ribozyme: Enhanced cleavage of certain oligonucleotide substrates that form mismatched ribozyme-substrate complexes. Biochemistry 27(25):8924-8931.
63. Bai Y, et al. (2007) Quantitative and comprehensive decomposition of the ion atmosphere around nucleic acids. J Am Chem Soc 129(48):14981-14988. (Pubitemid 350230720)
64. Pabit SA, et al. (2010) Counting ions around DNA with anomalous small-angle X-ray scattering. J Am Chem Soc 132(46):16334-16336.
65. Svergun DI (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25:495-503.