Translocation, switching and gating: Potential roles for ATP in long-range communication on DNA by Type III restriction endonucleases

Biochemical Society Transactions

Volumn 39, Issue 2, 2011, Pages 589-594

  Szczelkun, Mark D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

ATP binding cassette transporter (ABC transporter); DNA sliding; Gyrase; Heat shock protein 90; Helicase; Histidine kinase and MutL ATPase (GHKL ATPase); Molecular switch

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; DNA; DNA TOPOISOMERASE; ESTERASE; HELICASE; PROTEIN MUTL; PROTEIN MUTS; RAD50 PROTEIN; TYPE III RESTRICTION ENDONUCLEASE; UNCLASSIFIED DRUG;

CELL COMMUNICATION; DNA CLEAVAGE; DNA SEQUENCE; DNA TRANSFER; GENE SWITCHING; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN HYDROLYSIS; REVIEW;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; DEOXYRIBONUCLEASES, TYPE III SITE-SPECIFIC; DNA; HUMANS; MODELS, BIOLOGICAL; MOVEMENT; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN TRANSPORT; SUBSTRATE SPECIFICITY;

EID: 79953191521     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390589     Document Type: Review

References (48)

1. Singleton, M.R., Dillingham, M.S. and Wigley, D.B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23-50
2. Dillingham, M.S., Wigley, D.B. and Webb, M.R. (2000) Demonstration of unidirectional single-stranded DNA translocation by PcrA helicase: measurement of step size and translocation speed. Biochemistry 39, 205-212 (Pubitemid 30033335)
3. Saikrishnan, K., Powell, B., Cook, N.J., Webb, M.R. and Wigley, D.B. (2009) Mechanistic basis of 5′-3′ translocation in SF1B helicases. Cell 137, 849-859
4. Velankar, S.S., Soultanas, P., Dillingham, M.S., Subramanya, H.S. and Wigley, D.B. (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97, 75-84 (Pubitemid 29165891)
5. Jankowsky, E. (2011) RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 36, 19-29
6. Stanley, L.K., Seidel, R., Van Der Scheer, C., Dekker, N.H., Szczelkun, M.D. and Dekker, C. (2006) When a helicase is not a helicase: dsDNA tracking by the motor protein EcoR124I. EMBO J. 25, 2230-2239
7. Sistla, S. and Rao, D.N. (2004) S-adenosyl-L-methionine-dependent restriction enzymes. Crit. Rev. Biochem. Mol. Biol. 39, 1-19
8. Szczelkun, M.D., Friedhoff, P. and Seidel, R. (2010) Maintaining a sense of direction during long-range communication on DNA. Biochem. Soc. Trans. 38, 404-409
9. Janscak, P., Sandmeier, U., Szczelkun, M.D. and Bickle, T.A. (2001) Subunit assembly and mode of DNA cleavage of the type III restriction endonucleases EcoP1I and EcoP15I. J. Mol. Biol. 306, 417-431
10. Sears, A. and Szczelkun, M.D. (2005) Subunit assembly modulates the activities of the Type III restriction-modification enzyme PstII in vitro. Nucleic Acids Res. 33, 4788-4796 (Pubitemid 41418879)
11. McClelland, S.E. and Szczelkun, M.D. (2004) The type I and III restriction endonucleases: structural elements in the molecular motors that process DNA. Nucleic Acids Mol. Biol. 14, 111-135
12. van Aelst, K., Toth, J., Ramanathan, S.P., Schwarz, F.W., Seidel, R. and Szczelkun, M.D. (2010) Type III restriction enzymes cleave DNA by long-range interaction between sites in both head-to-head and tail-to-tail inverted repeat. Proc. Natl. Acad. Sci. U.S.A. 107, 9123-9128
13. Saha, S. and Rao, D.N. (1995) ATP hydrolysis is required for DNA cleavage by EcoPI restriction enzyme. J. Mol. Biol. 247, 559-567
14. Saha, S. and Rao, D.N. (1997) Mutations in the Res subunit of the EcoPI restriction enzyme that affect ATP-dependent reactions. J. Mol. Biol. 269, 342-354
15. Meisel, A., Mackeldanz, P., Bickle, T.A., Kruger, D.H. and Schroeder, C. (1995) Type III restriction endonucleases translocate DNA in a reaction driven by recognition site-specific ATP hydrolysis. EMBO J. 14, 2958-2966
16. Crampton, N., Roes, S., Dryden, D.T., Rao, D.N., Edwardson, J.M. and Henderson, R.M. (2007) DNA looping and translocation provide an optimal cleavage mechanism for the type III restriction enzymes. EMBO J. 26, 3815-3825
17. Crampton, N., Yokokawa, M., Dryden, D.T., Edwardson, J.M., Rao, D.N., Takeyasu, K., Yoshimura, S.H. and Henderson, R.M. (2007) Fast-scan atomic force microscopy reveals that the type III restriction enzyme EcoP15I is capable of DNA translocation and looping. Proc. Natl. Acad. Sci. U.S.A. 104, 12755-12760
18. Raghavendra, N.K. and Rao, D.N. (2004) Unidirectional translocation from recognition site and a necessary interaction with DNA end for cleavage by Type III restriction enzyme. Nucleic Acids Res. 32, 5703-5711 (Pubitemid 39619153)
19. Ramanathan, S.P., van Aelst, K., Sears, A., Peakman, L.J., Diffin, F.M., Szczelkun, M.D. and Seidel, R. (2009) Type III restriction enzymes communicate in 1D without looping between their target sites. Proc. Natl. Acad. Sci. U.S.A. 106, 1748-1753
20. Peakman, L.J. and Szczelkun, M.D. (2004) DNA communications by Type III restriction endonucleases-confirmation of 1D translocation over 3D looping. Nucleic Acids Res. 32, 4166-4174 (Pubitemid 39232289)
21. Sears, A., Peakman, L.J., Wilson, G.G. and Szczelkun, M.D. (2005) Characterization of the type III restriction endonuclease PstII from Providencia stuartii. Nucleic Acids Res. 33, 4775-4787 (Pubitemid 41418878)
22. Seidel, R., Bloom, J.G., Dekker, C. and Szczelkun, M.D. (2008) Motor step size and ATP coupling efficiency of the dsDNA translocase EcoR124I. EMBO J. 27, 1388-1398 (Pubitemid 351655181)
23. Kingston, I.J., Gormley, N.A. and Halford, S.E. (2003) DNA supercoiling enables the type IIS restriction enzyme BspMI to recognise the relative orientation of two DNA sequences. Nucleic Acids Res. 31, 5221-5228 (Pubitemid 37441889)
24. Watson, M.A., Gowers, D.M. and Halford, S.E. (2000) Alternative geometries of DNA looping: an analysis using the SfiI endonuclease. J. Mol. Biol. 298, 461-475
25. Adzuma, K. and Mizuuchi, K. (1989) Interaction of proteins located at a distance along DNA: mechanism of target immunity in the Mu DNA strand-transfer reaction. Cell 57, 41-47 (Pubitemid 19098867)
26. Gowers, D.M., Bellamy, S.R. and Halford, S.E. (2004) One recognition sequence, seven restriction enzymes, five reaction mechanisms. Nucleic Acids Res. 32, 3469-3479 (Pubitemid 39117464)
27. Marshall, J.J., Gowers, D.M. and Halford, S.E. (2007) Restriction endonucleases that bridge and excise two recognition sites from DNA. J. Mol. Biol. 367, 419-431
28. Wood, K.M., Daniels, L.E. and Halford, S.E. (2005) Long-range communications between DNA sites by the dimeric restriction endonuclease SgrAI. J. Mol. Biol. 350, 240-253
29. Blackwell, L.J., Martik, D., Bjornson, K.P., Bjornson, E.S. and Modrich, P. (1998) Nucleotide-promoted release of hMutSα from heteroduplex DNA is consistent with an ATP-dependent translocation mechanism. J. Biol. Chem. 273, 32055-32062
30. Rudolph, M.G. and Klostermeier, D. (2009) The Thermus thermophilus DEAD box helicase Hera contains a modified RNA recognition motif domain loosely connected to the helicase core. RNA 15, 1993-2001
31. Smith, A.J., Szczelkun, M.D. and Savery, N.J. (2007) Controlling the motor activity of a transcription-repair coupling factor: autoinhibition and the role of RNA polymerase. Nucleic Acids Res. 35, 1802-1811 (Pubitemid 47061651)
32. Wittinghofer, A. and Pai, E.F. (1991) The structure of Ras protein: a model for a universal molecular switch. Trends Biochem. Sci. 16, 382-387
33. Dutta, R. and Inouye, M. (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci. 25, 24-28 (Pubitemid 30060426)
34. Ban, C., Junop, M. and Yang, W. (1999) Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell 97, 85-97 (Pubitemid 29165892)
35. Pearl, L.H., Prodromou, C. and Workman, P. (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J. 410, 439-453 (Pubitemid 351429015)
36. Polosina, Y.Y. and Cupples, C.G. (2010) Wot the 'L-Does MutL do? Mutat. Res. 705, 228-238
37. Schoeffler, A.J. and Berger, J.M. (2008) DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys. 41, 41-101
38. Bates, A.D. and Maxwell, A. (2010) The role of ATP in the reactions of type II DNA topoisomerases. Biochem. Soc. Trans. 38, 438-442
39. Hopfner, K.P. and Tainer, J.A. (2003) Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr. Opin. Struct. Biol. 13, 249-255
40. Ye, J., Osborne, A.R., Groll, M. and Rapoport, T.A. (2004) RecA-like motor ATPases: lessons from structures. Biochim. Biophys. Acta 1659, 1-18
41. Hopfner, K.P., Karcher, A., Shin, D.S., Craig, L., Arthur, L.M., Carney, J.P. and Tainer, J.A. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800
42. Kunkel, T.A. and Erie, D.A. (2005) DNA mismatch repair. Annu. Rev. Biochem. 74, 681-710
43. Iyer, R.R., Pluciennik, A., Burdett, V. and Modrich, P.L. (2006) DNA mismatch repair: functions and mechanisms. Chem. Rev. 106, 302-323
44. Locher, K.P. (2009) Structure and mechanism of ATP-binding cassette transporters. Philos. Trans. R. Soc. London Ser. B 364, 239-245
45. Patzlaff, J.S., Van Der Heide, T. and Poolman, B. (2003) The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J. Biol. Chem. 278, 29546-29551
46. Jones, P.M., O'Mara, M.L. and Georg, A.M. (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34, 520-531
47. Savery, N.J. (2007) The molecular mechanism of transcription-coupled DNA repair. Trends Microbiol. 15, 326-333
48. Selby, C.P. and Sancar, A. (1993) Molecular mechanism of transcription-repair coupling. Science 260, 53-58 (Pubitemid 23122744)