A flexible brace maintains the assembly of a hexameric replicative helicase during DNA unwinding

Nucleic Acids Research

Volumn 40, Issue 5, 2012, Pages 2271-2283

  Whelan, Fiona ^a   Stead, Jonathan A ^b   Shkumatov, Alexander V ^c   Svergun, Dmitri I ^c   Sanders, Cyril M ^b   Antson, Alfred A ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; E1 HELICASE; HELICASE; OLIGOMER; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTALLOGRAPHY; DNA DENATURATION; DNA SEQUENCE; ELECTRIC POTENTIAL; ENZYME CONFORMATION; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA INTERACTION; PROTEIN HYDROLYSIS; RADIATION SCATTERING; STATIC ELECTRICITY;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; DNA HELICASES; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SCATTERING, SMALL ANGLE; SEQUENCE DELETION; STATIC ELECTRICITY; VIRAL PROTEINS; X-RAY DIFFRACTION;

PAPILLOMAVIRIDAE; POLYOMAVIRUS;

EID: 84858405982     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr906     Document Type: Article

References (57)

1. Neuwald, A. F., Aravind, L., Spouge, J. L. and Koonin, E. V. (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res., 9, 27-43.
2. Saraste, M., Sibbald, P. R. and Wittinghofer, A. (1990) The P-loop-a common motif in ATP-and GTP-binding proteins. Trends Biochem. Sci., 15, 430-434.
3. Iyer, L. M., Leipe, D. D., Koonin, E. V. and Aravind, L. (2004) Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol., 146, 11-31.
4. Vetter, I. R. and Wittinghofer, A. (1999) Nucleoside triphosphate-binding proteins: different scaffolds to achieve phosphoryl transfer. Q. Rev. Biophys., 32, 1-56.
5. Ogura, T., Whiteheart, S. W. and Wilkinson, A. J. (2004) Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ATPases. J. Struct. Biol., 146, 106-112.
6. Erzberger, J. P. and Berger, J. M. (2006) Evolutionary relationships and structural mechanisms of AAA+proteins. Annu. Rev. Biophys. Biomol. Struct., 35, 93-114.
7. Singleton, M. R., Sawaya, M. R., Ellenberger, T. and Wigley, D. B. (2000) Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell, 101, 589-600.
8. Martin, A., Baker, T. A. and Sauer, R. T. (2005) Rebuilt AAA+ motors reveal operating principles for ATP-fuelled machines. Nature, 437, 1115-1120.
9. Sanders, C. M., Kovalevskiy, O. V., Sizov, D., Lebedev, A. A., Isupov, M. N. and Antson, A. A. (2007) Papillomavirus E1 helicase assembly maintains an asymmetric state in the absence of DNA and nucleotide cofactors. Nucleic Acids Res., 35, 6451-6457.
10. Castella, S., Burgin, D. and Sanders, C. M. (2006) Role of ATP hydrolysis in the DNA translocase activity of the bovine papillomavirus (BPV-1) E1 helicase. Nucleic Acids Res., 34, 3731-3741.
11. Enemark, E. J. and Joshua-Tor, L. (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature, 442, 270-275.
12. Mertens, H. D. and Svergun, D. I. (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J. Struct. Biol., 172, 128-141.
13. Bielnicki, J. A., Shkumatov, A. V., Derewenda, U., Somlyo, A. V., Svergun, D. I. and Derewenda, Z. S. (in press) Insights into the molecular activation mechanism of the RhoA-specific guanine nucleotide exchange factor, PDZRhoGEF. J. Biol. Chem, 286, 35163-35175.
14. Verstraete, K., Vandriessche, G., Januar, M., Elegheert, J., Shkumatov, A. V., Desfosses, A., Van Craenenbroeck, K., Svergun, D. I., Gutsche, I., Vergauwen, B. et al. (2011) Structural insights into the extracellular assembly of the hematopoietic Flt3 signaling complex. Blood, 118, 60-68.
15. Mylonas, E., Hascher, A., Bernado, P., Blackledge, M., Mandelkow, E. and Svergun, D. I. (2008) Domain conformation of tau protein studied by solution small-angle X-ray scattering. Biochemistry, 47, 10345-10353.
16. Shkumatov, A. V., Chinnathambi, S., Mandelkow, E. and Svergun, D. I. (2011) Structural memory of natively unfolded tau protein detected by small-angle X-ray scattering. Proteins, 79, 2122-2131.
17. Iggo, R. D. and Lane, D. P. (1989) Nuclear protein p68 is an RNA-dependent ATPase. EMBO J., 8, 1827-1831.
18. Roessle, M. W., Klaering, R., Ristau, U., Robrahn, B., Jahn, D., Gehrmann, T., Konarev, P., Round, A., Fiedler, S., Hermes, C. et al. (2007) Upgrade of the small-angle X-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg. J. Appl. Crystallogr., 40, s190-s194.
19. Round, A. R., Franke, D., Moritz, S., Huchler, R., Fritsche, M., Malthan, D., Klaering, R., Svergun, D. I. and Roessle, M. (2008) Automated sample-changing robot for solution scattering experiments at the EMBL Hamburg SAXS station X33. J. Appl. Crystallogr., 41, 913-917.
20. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr., 36, 1277-1282.
21. Guinier, A. (1939) La diffraction des rayons X aux tres petits angles: application a l'etude de phenomenes ultramicroscopiques. Ann. Phys., 12, 161-237.
22. Svergun, D. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr., 25, 495-503.
23. Fischer, F., de Oliveira Neto, M., Napolitano, H. B., Craievich, A. F. and Polikarpov, I. (2010) The molecular weight of proteins in solution can be determined from a single SAXS measurement on a relative scale. J. Appl. Cryst., 43, 101-109.
24. Svergun, D., Barberato, C. and Koch, M. H. J. . (1995) CRYSOL-a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates. J. Appl. Crystallogr., 28, 768-773.
25. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J., 76, 2879-2886.
26. Svergun, D. I., Petoukhov, M. V. and Koch, M. H. (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys. J., 80, 2946-2953.
27. Volkov, V. V. and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr., 36, 860-864.
28. Kozin, M. B. and Svergun, D. I. (2001) Automated matching of high-and low-resolution structural models. J. Appl. Crystallogr., 34, 33-41.
29. Petoukhov, M. V. and Svergun, D. I. (2005) Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys. J., 89, 1237-1250.
30. McNicholas, S., Potterton, E., Wilson, K. S. and Noble, M. E. M. (2011) Presenting your structures: the CCP4mg molecular-graphics software. Acta Crystallogr. D, 67, 386-394.
31. Jo, S., Vargyas, M., Vasko-Szedlar, J., Roux, B. and Im, W. (2008) PBEQ-Solver for online visualization of electrostatic potential of biomolecules. Nucleic Acids Res., 36, W270-W275.
32. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797.
33. Lassmann, T. and Sonnhammer, E. L. (2005) Kalign-an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics, 6, 298.
34. Yang, Z. R., Thomson, R., McNeil, P. and Esnouf, R. M. (2005) RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics, 21, 3369-3376.
35. Linding, R., Jensen, L. J., Diella, F., Bork, P., Gibson, T. J. and Russell, R. B. (2003) Protein disorder prediction: implications for structural proteomics. Structure, 11, 1453-1459.
36. Ward, J. J., McGuffin, L. J., Bryson, K., Buxton, B. F. and Jones, D. T. (2004) The DISOPRED server for the prediction of protein disorder. Bioinformatics, 20, 2138-2139.
37. Li, X., Romero, P., Rani, M., Dunker, A. K. and Obradovic, Z. (1999) Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform., 10, 30-40.
38. Romero, P., Obradovic, Z. and Dunker, K. (1997) Sequence data analysis for long disordered regions prediction in the Calcineurin Family. Genome Inform. Ser. Workshop Genome Inform., 8, 110-124.
39. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J. and Dunker, A. K. (2001) Sequence complexity of disordered protein. Proteins, 42, 38-48.
40. Enemark, E. J., Stenlund, A. and Joshua-Tor, L. (2002) Crystal structures of two intermediates in the assembly of the papillomavirus replication initiation complex. EMBO J., 21, 1487-1496.
41. Schuck, S. and Stenlund, A. (2007) ATP-dependent minor groove recognition of TA base pairs is required for template melting by the E1 initiator protein. J. Virol., 81, 3293-3302.
42. DeLano, W. L. T. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA. USA.
43. Lindahl, E., Azuara, C., Koehl, P. and Delarue, M. (2006) NOMAD-Ref: visualization, deformation and refinement of macromolecular structures based on all-atom normal mode analysis. Nucleic Acids Res., 34, W52-W56.
44. Dyson, H. J. and Wright, P. E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol., 6, 197-208.
45. Schneider, T. D. and Stephens, R. M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res., 18, 6097-6100.
46. Im, W., Beglov, D. and Roux, B. (1998) Continuum solvation model: computation of electrostatic forces from numerical solutions to the Poisson-Boltzmann equation. Comp. Phys. Commun., 111, 59-75.
47. Gai, D., Zhao, R., Li, D., Finkielstein, C. V. and Chen, X. S. (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell, 119, 47-60.
48. Montenarh, M., Vesco, C., Kemmerling, G., Mu?ller, D. and Henning, R. (1986) Regions of SV40 large T antigen necessary for oligomerization and complex formation with the cellular oncoprotein p53. FEBS Lett., 204, 51-55.
49. Cuesta, I., Nunez-Ramirez, R., Scheres, S. H., Gai, D., Chen, X. S., Fanning, E. and Carazo, J. M. (2010) Conformational rearrangements of SV40 large T antigen during early replication events. J. Mol. Biol., 397, 1276-1286.
50. Mancini, E. J., Kainov, D. E., Grimes, J. M., Tuma, R., Bamford, D. H. and Stuart, D. I. (2004) Atomic snapshots of an RNA packaging motor reveal conformational changes linking ATP hydrolysis to RNA translocation. Cell, 118, 743-755.
51. Niedenzu, T., Roleke, D., Bains, G., Scherzinger, E. and Saenger, W. (2001) Crystal structure of the hexameric replicative helicase RepA of plasmid RSF1010. J. Mol. Biol., 306, 479-487.
52. Tompa, P. (2002) Intrinsically unstructured proteins. Trends Biochem. Sci., 27, 527-533.
53. Fuxreiter, M., Tompa, P. and Simon, I. (2007) Local structural disorder imparts plasticity on linear motifs. Bioinformatics, 23, 950-956.
54. Triezenberg, S. J. (1995) Structure and function of transcriptional activation domains. Curr. Opin. Genet. Dev., 5, 190-196.
55. Tompa, P., Szasz, C. and Buday, L. (2005) Structural disorder throws new light on moonlighting. Trends Biochem. Sci., 30, 484-489.
56. Demchenko, A. P. (2001) Recognition between flexible protein molecules: induced and assisted folding. J. Mol. Recognit., 14, 42-61.
57. Hegyi, H., Schad, E. and Tompa, P. (2007) Structural disorder promotes assembly of protein complexes. BMC Struct. Biol., 7, 65.