RNA remodeling by hexameric RNA helicases

RNA Biology

Volumn 7, Issue 6, 2010, Pages 655-666

  Rabhi, Makhlouf ^a,b   Tuma, Roman ^c   Boudvillain, Marc ^a  

^a CENTRE DE BIOPHYSIQUE MOLÉCULAIRE   (France)

^b UNIVERSITÉ D'ORLÉANS   (France)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Molecular motor; P4; Packaging; Rho; Transcription termination; Translocation; Virus

Indexed keywords

HOLOENZYME; RNA HELICASE; RNA POLYMERASE; TRANSCRIPTION TERMINATION FACTOR RHO;

BACTERIAL GENOME; BACTERIOPHAGE; BIOCHEMISTRY; DENATURATION; DNA RNA HYBRIDIZATION; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME STRUCTURE; ESCHERICHIA COLI; HYDROLYSIS; MOLECULAR MODEL; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; REVIEW; RNA BINDING; RNA STRUCTURE; RNA TRANSCRIPTION; TRANSCRIPTION TERMINATION;

BACTERIOPHAGE PHI-8; ESCHERICHIA COLI;

EID: 78751675312     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.7.6.13570     Document Type: Review

References (85)

1. Jankowsky E, Fairman ME. RNA helicases - one fold for many functions. Curr Opin Struct Biol 2007; 17:316-24. (Pubitemid 47021361)
2. Patel SS, Picha KM. Structure and function of hexameric helicases. Annu Rev Biochem 2000; 69:651-97.
3. Pyle AM. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu Rev Biophys 2008; 37:317-36.
4. Singleton MR, Dillingham MS, Wigley DB. Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem 2007; 76:23-50.
5. Byrd AK, Raney KD. Protein displacement by an assembly of helicase molecules aligned along single-stranded DNA. Nat Struct Mol Biol 2004; 11:531-8.
6. Sun B, Wei KJ, Zhang B, Zhang XH, Dou SX, Li M, et al. Impediment of E. coli UvrD by DNA-destabilizing force reveals a strained-inchworm mechanism of DNA unwinding. EMBO J 2008; 27:3279-87.
7. Berger JM. SnapShot: nucleic acid helicases and translocases. Cell 2008; 134:888.
8. Chemla YR, Aathavan K, Michaelis J, Grimes S, Jardine PJ, Anderson DL, et al. Mechanism of force generation of a viral DNA packaging motor. Cell 2005; 122:683-92. (Pubitemid 41242634)
9. Sclafani RA, Fletcher RJ, Chen XS. Two heads are better than one: regulation of DNA replication by hexameric helicases. Genes Dev 2004; 18:2039-45.
10. Michel B, Boubakri H, Baharoglu Z, LeMasson M, Lestini R. Recombination proteins and rescue of arrested replication forks. DNA Repair (Amst) 2007; 6:967-80.
11. Rabhi M, Rahmouni AR, Boudvillain M. Transcription termination factor Rho: a ring-shaped RNA helicase from bacteria. In: Jankowsky E, Ed. RNA helicases. Cambridge (UK): RSC Publishing 2010; 243-71.
12. Scheffner M, Knippers R, Stahl H. RNA unwinding activity of SV40 large T antigen. Cell 1989; 57:955-63.
13. Eichman BF, Fanning E. The power of pumping together; deconstructing the engine of a DNA replication machine. Cell 2004; 119:3-4. (Pubitemid 39349313)
14. Kainov DE, Pirttimaa M, Tuma R, Butcher SJ, Thomas GJ Jr, Bamford DH, et al. RNA packaging device of double-stranded RNA bacteriophages, possibly as simple as hexamer of P4 protein. J Biol Chem 2003; 278:48084-91.
15. Kainov DE, Tuma R, Mancini EJ. Hexameric molecular motors: P4 packaging ATPase unravels the mechanism. Cell Mol Life Sci 2006; 63:1095-105.
16. Brennan CA, Dombroski AJ, Platt T. Transcription termination factor rho is an RNA-DNA helicase. Cell 1987; 48:945-52.
17. Brennan CA, Steinmetz EJ, Spear P, Platt T. Specificity and efficiency of rho-factor helicase activity depends on magnesium concentration and energy coupling to NTP hydrolysis. J Biol Chem 1990; 265:5440-7. (Pubitemid 120012839)
18. Walmacq C, Rahmouni AR, Boudvillain M. Influence of substrate composition on the helicase activity of transcription termination factor Rho: reduced processivity of Rho hexamers during unwinding of RNADNA hybrid regions. J Mol Biol 2004; 342:403-20. (Pubitemid 39149747)
19. Walmacq C, Rahmouni AR, Boudvillain M. Testing the steric exclusion model for hexameric helicases: substrate features that alter RNA-DNA unwinding by the transcription termination factor Rho. Biochemistry 2006; 45:5885-95.
20. Walstrom KM, Dozono JM, Robic S, von Hippel PH. Kinetics of the RNA-DNA helicase activity of Escherichia coli transcription termination factor rho. 1. Characterization and analysis of the reaction. Biochemistry 1997; 36:7980-92.
21. Walstrom KM, Dozono JM, von Hippel PH. Kinetics of the RNA-DNA helicase activity of Escherichia coli transcription termination factor rho. 2. Processivity, ATP consumption and RNA binding. Biochemistry 1997; 36:7993-8004.
22. Walstrom KM, Dozono JM, von Hippel PH. Effects of reaction conditions on RNA secondary structure and on the helicase activity of Escherichia coli transcription termination factor Rho. J Mol Biol 1998; 279:713-26.
23. Schwartz A, Walmacq C, Rahmouni AR, Boudvillain M. Noncanonical interactions in the management of RNA structural blocks by the transcription termination rho helicase. Biochemistry 2007; 46:9366-79.
24. Harinarayanan R, Gowrishankar J. Host factor titration by chromosomal R-loops as a mechanism for run-away plasmid replication in transcription termination-defective mutants of Escherichia coli. J Mol Biol 2003; 332:31-46.
25. Drolet M. Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 2006; 59:723-30.
26. Gowrishankar J, Harinarayanan R. Why is transcription coupled to translation in bacteria? Mol Microbiol 2004; 54:598-603.
27. Ciampi MS. Rho-dependent terminators and transcription termination. Microbiology 2006; 152:2515-28.
28. Banerjee S, Chalissery J, Bandey I, Sen R. Rho-dependent transcription termination: more questions than answers. J Microbiol 2006; 44:11-22.
29. Donmez I, Patel SS. Mechanisms of a ring shaped helicase. Nucleic Acids Res 2006; 34:4216-24.
30. Jeong YJ, Levin MK, Patel SS. The DNA-unwinding mechanism of the ring helicase of bacteriophage T7. Proc Natl Acad Sci USA 2004; 101:7264-9.
31. Lisal J, Tuma R. Cooperative mechanism of RNA packaging motor. J Biol Chem 2005; 280:23157-64.
32. Lisal J, Kainov DE, Lam TT, Emmett MR, Wei H, Gottlieb P, et al. Interaction of packaging motor with the polymerase complex of dsRNA bacteriophage. Virology 2006; 351:73-9.
33. Schwartz A, Margeat E, Rahmouni AR, Boudvillain M. Transcription termination factor Rho can displace streptavidin from biotinylated RNA. J Biol Chem 2007; 282:31469-76.
34. Burgess BR, Richardson JP. Transcription factor Rho does not require a free end to act as an RNA-DNA helicase on an RNA. J Biol Chem 2001; 276:17106-10.
35. Yu X, Horiguchi T, Shigesada K, Egelman EH. Three-dimensional reconstruction of transcription termination factor rho: orientation of the N-terminal domain and visualization of an RNA-binding site. J Mol Biol 2000; 299:1279-87.
36. Gogol EP, Seifried SE, von Hippel PH. Structure and assembly of the Escherichia coli transcription termination factor rho and its interaction with RNA I. Cryoelectron microscopic studies. J Mol Biol 1991; 221:1127-38.
37. Oda T, Takanami M. Observations on the structure of the termination factor rho and its attachment to DNA. J Mol Biol 1972; 71:799-802.
38. Bear DG, Hicks PS, Escudero KW, Andrews CL, McSwiggen JA, von Hippel PH. Escherichia coli transcription termination factor rho with RNA II. Electron microscopy and nuclease protection experiments. J Mol Biol 1988; 199:623-35.
39. Skordalakes E, Berger JM. Structure of the rho transcription terminator. Mechanism of mRNA recognition and helicase loading. Cell 2003; 114:135-46.
40. Skordalakes E, Brogan AP, Park BS, Kohn H, Berger JM. Structural mechanism of inhibition of the Rho transcription termination factor by the antibiotic bicyclomycin. Structure 2005; 13:99-109. (Pubitemid 40092478)
41. Kim DE, Patel SS. The kinetic pathway of RNA binding to the Escherichia coli transcription termination factor Rho. J Biol Chem 2001; 276:13902-10.
42. Lisal J, Lam TT, Kainov DE, Emmett MR, Marshall AG, Tuma R. Functional visualization of viral molecular motor by hydrogen-deuterium exchange reveals transient states. Nat Struct Mol Biol 2005; 12:460-6. (Pubitemid 43085908)
43. Link TM, Valentin-Hansen P, Brennan RG. Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci USA 2009; 106:19292-7.
44. + enhancer binding proteins in transcriptional activation. J Struct Biol 2006; 156:190-9.
45. Pani B, Ranjan A, Sen R. Interaction surface of bacteriophage P4 protein Psu required for complex formation with the transcription terminator Rho. J Mol Biol 2009; 389:647-60.
46. Pichoff S, Alibaud L, Guedant A, Castanie MP, Bouche JP. An Escherichia coli gene (yaeO) suppresses temperature-sensitive mutations in essential genes by modulating Rho-dependent transcription termination. Mol Microbiol 1998; 29:859-69.
47. Epshtein V, Cardinale CJ, Ruckenstein AE, Borukhov S, Nudler E. An allosteric path to transcription termination. Mol Cell 2007; 28:991-1001.
48. Mooney RA, Davis SE, Peters JM, Rowland JL, Ansari AZ, Landick R. Regulator trafficking on bacterial transcription units in vivo. Mol Cell 2009; 33:97-108.
49. Pirttimaa MJ, Bamford DH. RNA secondary structures of the bacteriophage phi6 packaging regions. RNA 2000; 6:880-9.
50. Thomsen ND, Berger JM. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 2009; 139:523-34.
51. Chen X, Stitt BL. ADP but not P(i) dissociation contributes to rate limitation for Escherichia coli Rho. J Biol Chem 2009; 284:33773-80.
52. Adelman JL, Jeong YJ, Liao JC, Patel G, Kim DE, Oster G, et al. Mechanochemistry of transcription termination factor Rho. Mol Cell 2006; 22:611-21.
53. O I, Stitt BL. 8-Azido-ATP inactivation of Escherichia coli transcription termination factor Rho. Modification of one subunit inactivates the hexamer. J Biol Chem 1994; 269:5009-15.
54. Kainov DE, Mancini EJ, Telenius J, Lisal J, Grimes JM, Bamford DH, et al. Structural basis of mechanochemical coupling in a hexameric molecular motor. J Biol Chem 2008; 283:3607-17.
55. Mancini EJ, Kainov DE, Grimes JM, Tuma R, Bamford DH, Stuart DI. Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell 2004; 118:743-55.
56. Telenius J, Wallin AE, Straka M, Zhang H, Mancini EJ, Tuma R. RNA packaging motor: From structure to quantum mechanical modelling and sequential-stochastic mechanism. Comput Math Methods Med 2008; 9:351-69.
57. Browne RJ, Barr EW, Stitt BL. Catalytic cooperativity among subunits of Escherichia coli transcription termination factor Rho. Kinetics and substrate structural requirements. J Biol Chem 2005; 280:13292-9.
58. Jeong YJ, Kim DE, Patel SS. Nucleotide binding induces conformational changes in Escherichia coli transcription termination factor Rho. J Biol Chem 2004; 279:18370-6.
59. Lowery-Goldhammer C, Richardson JP. An RNA-dependent nucleoside triphosphate phosphohydrolase (ATPase) associated with rho termination factor. Proc Natl Acad Sci USA 1974; 71:2003-7.
60. Frilander M, Bamford DH. In vitro packaging of the single-stranded RNA genomic precursors of the segmented double-stranded RNA bacteriophage phi 6: the three segments modulate each other's packaging efficiency. J Mol Biol 1995; 246:418-28.
61. Bogden CE, Fass D, Bergman N, Nichols MD, Berger JM. The structural basis for terminator recognition by the Rho transcription termination factor. Mol Cell 1999; 3:487-93.
62. Richardson LV, Richardson JP. Cytosine nucleoside inhibition of the ATPase of Escherichia coli termination factor rho: evidence for a base specific interaction between rho and RNA. Nucleic Acids Res 1992; 20:5383-7.
63. Briercheck DM, Allison TJ, Richardson JP, Ellena JF, Wood TC, Rule GS. 1H, 15N and 13C resonance assignments and secondary structure determination of the RNA-binding domain of E.coli rho protein. J Biomol NMR 1996; 8:429-44.
64. McSwiggen JA, Bear DG, von Hippel PH. Interactions of Escherichia coli transcription termination factor rho with RNA I. Binding stoichiometries and free energies. J Mol Biol 1988; 199:609-22.
65. Richardson JP. Activation of rho protein ATPase requires simultaneous interaction at two kinds of nucleic acid-binding sites. J Biol Chem 1982; 257:5760-6.
66. Skordalakes E, Berger JM. Structural insights into RNA-dependent ring closure and ATPase activation by the Rho termination factor. Cell 2006; 127:553-64.
67. Paatero AO, Mindich L, Bamford DH. Mutational analysis of the role of nucleoside triphosphatase P4 in the assembly of the RNA polymerase complex of bacteriophage phi6. J Virol 1998; 72:10058-65.
68. Gutierrez P, Kozlov G, Gabrielli L, Elias D, Osborne MJ, Gallouzi IE, et al. Solution structure of YaeO, a Rho-specific inhibitor of transcription termination. J Biol Chem 2007; 282:23348-53. (Pubitemid 47311918)
69. Enemark EJ, Joshua-Tor L. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 2006; 442:270-5.
70. Peters JM, Mooney RA, Kuan PF, Rowland JL, Keles S, Landick R. Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci USA 2009; 106:15406-11.
71. Richardson JP. Rho-dependent termination and ATPases in transcript termination. Biochim Biophys Acta 2002; 1577:251-60.
72. Wei RR, Richardson JP. Mutational changes of conserved residues in the Q-loop region of transcription factor Rho greatly reduce secondary site RNA-binding. J Mol Biol 2001; 314:1007-15.
73. Wei RR, Richardson JP. Identification of an RNA-binding site in the ATP binding domain of Escherichia coli Rho by H2O2/Fe-EDTA cleavage protection studies. J Biol Chem 2001; 276:28380-7.
74. Burgess BR, Richardson JP. RNA passes through the hole of the protein hexamer in the complex with the Escherichia coli Rho factor. J Biol Chem 2001; 276:4182-9.
75. Galluppi GR, Richardson JP. ATP-induced changes in the binding of RNA synthesis termination protein Rho to RNA. J Mol Biol 1980; 138:513-39.
76. Schwartz A, Rabhi M, Jacquinot F, Margeat E, Rahmouni AR, Boudvillain M. A stepwise 2′-hydroxyl activation mechanism for the ring-shaped transcription termination Rho helicase. Nat Struct Mol Biol 2009; 16:1309-16.
77. Fedorova O, Boudvillain M, Kawaoka J, Pyle AM. Nucleotide analog interference mapping and suppression: specific applications in studies of RNA tertiary structure, dynamic helicase mechanism and RNA-protein interactions. In: Hartmann RK, Bindereif A, Schön A, Westhof E, Eds. Handbook of RNA Biochemistry. Weinheim: Wiley-VCH 2005; 259-93.
78. Boudvillain M, Nollmann M, Rahmouni AR, Margeat E. Keeping up to speed with the transcription termination factor Rho motor. Transcription; In press.
79. Patel SS. Structural biology: Steps in the right direction. Nature 2009; 462:581-3.
80. Pruijn GJ. Doughnuts dealing with RNA. Nat Struct Mol Biol 2005; 12:562-4.
81. Carpousis AJ. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol 2007; 61:71-87.
82. Jager S, Fuhrmann O, Heck C, Hebermehl M, Schiltz E, Rauhut R, et al. An mRNA degrading complex in Rhodobacter capsulatus. Nucleic Acids Res 2001; 29:4581-8.
83. Epshtein V, Dutta D, Wade J, Nudler E. An allosteric mechanism of Rho-dependent transcription termination. Nature 2010; 463:245-9.
84. Marquis KA, Burton BM, Nollmann M, Ptacin JL, Bustamante C, Ben-Yehuda S, et al. SpoIIIE strips proteins off the DNA during chromosome translocation. Genes Dev 2008; 22:1786-95.
85. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 1988; 16:10881-90.