One-Dimensional Sliding of p53 Along DNA Is Accelerated in the Presence of Ca2 + or Mg2 + at Millimolar Concentrations

Journal of Molecular Biology

Volumn 427, Issue 16, 2015, Pages 2663-2678

  Murata, Agato ^a   Ito, Yuji ^a   Kashima, Risa ^b,c   Kanbayashi, Saori ^a   Nanatani, Kei ^a   Igarashi, Chihiro ^a   Okumura, Masaki ^a   Inaba, Kenji ^a   Tokino, Takashi ^b   Takahashi, Satoshi ^a   Kamagata, Kiyoto ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b SAPPORO MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

divalent cation; DNA; p53; single molecule; sliding

Indexed keywords

CALCIUM ION; CYSTEINE; DNA; MAGNESIUM ION; MUTANT PROTEIN; PROTEIN P53; CALCIUM; DNA BINDING PROTEIN; MAGNESIUM; PROTEIN BINDING; TP53 PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ANISOTROPY; APPARENT DISSOCIATION CONSTANT; ARTICLE; BINDING AFFINITY; BINDING SITE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIFFUSION COEFFICIENT; DISSOCIATION RATE CONSTANT; DNA SEQUENCE; FLUORESCENCE MICROSCOPY; MOLECULAR DYNAMICS; MUTATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN STABILITY; CHEMISTRY; CONFORMATION; DIFFUSION; DRUG EFFECTS; FLUORESCENCE POLARIZATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; CALCIUM; DIFFUSION; DNA; DNA-BINDING PROTEINS; FLUORESCENCE POLARIZATION; HUMANS; MAGNESIUM; MICROSCOPY, FLUORESCENCE; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84938211900     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.06.016     Document Type: Article

References (54)

1. B. Vogelstein, D. Lane, and A.J. Levine Surfing the p53 network Nature 408 2000 307 310
2. C.J. Brown, S. Lain, C.S. Verma, A.R. Fersht, and D.P. Lane Awakening guardian angels: drugging the p53 pathway Nat. Rev. Cancer 9 2009 862 873
3. A.C. Joerger, and A.R. Fersht The tumor suppressor p53: from structures to drug discovery Cold Spring Harb. Perspect. Biol. 2 2010 a000919
4. Y. Jiao, D.I. Cherny, G. Heim, T.M. Jovin, and T.E. Schäffer Dynamic interactions of p53 with DNA in solution by time-lapse atomic force microscopy J. Mol. Biol. 314 2001 233 243
5. A. Tafvizi, F. Huang, A.R. Fersht, L.A. Mirny, and A.M. van Oijen A single-molecule characterization of p53 search on DNA Proc. Natl. Acad. Sci. U. S. A. 108 2011 563 568
6. A. Tafvizi, F. Huang, J.S. Leith, A.R. Fersht, L.A. Mirny, and A.M. van Oijen Tumor suppressor p53 slides on DNA with low friction and high stability Biophys. J. 95 2008 L01 L03
7. J.S. Leith, A. Tafvizi, F. Huang, W.E. Uspal, P.S. Doyle, A.R. Fersht, L.A. Mirny, and A.M. van Oijen Sequence-dependent sliding kinetics of p53 Proc. Natl. Acad. Sci. U. S. A. 109 2012 16552 16557
8. T. Terakawa, H. Kenzaki, and S. Takada p53 searches on DNA by rotation-uncoupled sliding at C-terminal tails and restricted hopping of core domains J. Am. Chem. Soc. 134 2012 14555 14562
9. P. Nicotera, B. Zhivotovsky, and S. Orrenius Nuclear calcium transport and the role of calcium in apoptosis Cell Calcium 16 1994 279 288
10. M.J. Berridge, M.D. Bootman, and P. Lipp Calcium - a life and death signal Nature 395 1998 645 648
11. Q.L. Zhao, T. Kondo, A. Noda, and Y. Fujiwara Mitochondrial and intracellular free-calcium regulation of radiation-induced apoptosis in human leukemic cells Int. J. Radiat. Biol. 75 1999 493 504
12. R. Gogna, E. Madan, B. Keppler, and U. Pati Gallium compound GaQ(3)-induced Ca(2 +) signalling triggers p53-dependent and -independent apoptosis in cancer cells Br. J. Pharmacol. 166 2012 617 636
13. A. Ikari, H. Sawada, A. Sanada, C. Tonegawa, Y. Yamazaki, and J. Sugatani Magnesium deficiency suppresses cell cycle progression mediated by increase in transcriptional activity of p21(Cip1) and p27(Kip1) in renal epithelial NRK-52E cells J. Cell. Biochem. 112 2011 3563 3572
14. A.Z. Li, H. Huang, X. Re, L.J. Qi, and K.A. Marx A gel electrophoresis study of the competitive effects of monovalent counterion on the extent of divalent counterions binding to DNA Biophys. J. 74 1998 964 973
15. V. Tereshko, G. Minasov, and M. Egli The Dickerson-Drew B-DNA dodecamer revisited at atomic resolution J. Am. Chem. Soc. 121 1999 470 471
16. G. Minasov, V. Tereshko, and M. Egli Atomic-resolution crystal structures of B-DNA reveal specific influences of divalent metal ions on conformation and packing J. Mol. Biol. 291 1999 83 99
17. T.K. Chiu, and R.E. Dickerson 1 Å crystal structures of B-DNA reveal sequence-specific binding and groove-specific bending of DNA by magnesium and calcium J. Mol. Biol. 301 2000 915 945
18. N.V. Hud, and M. Polak DNA-cation interactions: the major and minor grooves are flexible ionophores Curr. Opin. Struct. Biol. 11 2001 293 301
19. R. Ahmad, H. Arakawa, and H.A. Tajmir-Riahi A comparative study of DNA complexation with Mg(II) and Ca(II) in aqueous solution: major and minor grooves bindings Biophys. J. 84 2003 2460 2466
20. O.G. Berg, and C. Blomberg Association kinetics with coupled diffusion III. Ionic-strength dependence of the lac repressor-operator association Biophys. Chem. 8 1978 271 280
21. M.D. Barkley Salt dependence of the kinetics of the lac repressor-operator interaction: role of nonoperator deoxyribonucleic acid in the association reaction Biochemistry 20 1981 3833 3842
22. A.N. Bullock, J. Henckel, B.S. DeDecker, C.M. Johnson, P.V. Nikolova, M.R. Proctor, D.P. Lane, and A.R. Fersht Thermodynamic stability of wild-type and mutant p53 core domain Proc. Natl. Acad. Sci. U. S. A. 94 1997 14338 14342
23. T.J. Petty, S. Emamzadah, L. Costantino, I. Petkova, E.S. Stavridi, J.G. Saven, E. Vauthey, and T.D. Halazonetis An induced fit mechanism regulates p53 DNA binding kinetics to confer sequence specificity EMBO J. 30 2011 2167 2176
24. S. Bell, S. Hansen, and J. Buchner Refolding and structural characterization of the human p53 tumor suppressor protein Biophys. Chem. 96 2002 243 257
25. M.E. Anderson, B. Woelker, M. Reed, P. Wang, and P. Tegtmeyer Reciprocal interference between the sequence-specific core and nonspecific C-terminal DNA binding domains of p53: implications for regulation Mol. Cell. Biol. 17 1997 6255 6264
26. R.L. Weinberg, S.M. Freund, D.B. Veprintsev, M. Bycroft, and A.R. Fersht Regulation of DNA binding of p53 by its C-terminal domain J. Mol. Biol. 342 2004 801 811
27. S. Rajagopalan, F. Huang, and A.R. Fersht Single-molecule characterization of oligomerization kinetics and equilibria of the tumor suppressor p53 Nucleic Acids Res. 39 2011 2294 2303
28. A.M. van Oijen, P.C. Blainey, D.J. Crampton, C.C. Richardson, T. Ellenberger, and X.S. Xie Single-molecule kinetics of lambda exonuclease reveal base dependence and dynamic disorder Science 301 2003 1235 1238
29. J.B. Lee, R.K. Hite, S.M. Hamdan, X.S. Xie, C.C. Richardson, and A.M. van Oijen DNA primase acts as a molecular brake in DNA replication Nature 439 2006 621 624
30. A.L. Forget, and S.C. Kowalczykowski Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search Nature 482 2012 423 427
31. P.S. Doyle, B. Ladoux, and J.L. Viovy Dynamics of a tethered polymer in shear flow Phys. Rev. Lett. 84 2000 4769 4772
32. P.C. Blainey, A.M. van Oijen, A. Banerjee, G.L. Verdine, and X.S. Xie A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA Proc. Natl. Acad. Sci. U. S. A. 103 2006 5752 5757
33. G. Komazin-Meredith, R. Mirchev, D.E. Golan, A.M. van Oijen, and D.M. Coen Hopping of a processivity factor on DNA revealed by single-molecule assays of diffusion Proc. Natl. Acad. Sci. U. S. A. 105 2008 10721 10726
34. S.E. Halford, and J.F. Marko How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res. 32 2004 3040 3052
35. M. Slutsky, and L.A. Mirny Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential Biophys. J. 87 2004 4021 4035
36. Y. Xue, S. Wang, and X. Feng Influence of magnesium ion on the binding of p53 DNA-binding domain to DNA-response elements J. Biochem. 146 2009 77 85
37. E. Paleček, V. Ostatná, H. Černocká, A.C. Joerger, and A.R. Fersht Electrocatalytic monitoring of metal binding and mutation-induced conformational changes in p53 at picomole level J. Am. Chem. Soc. 133 2011 7190 7196
38. T.M. Lohman Kinetics of protein-nucleic acid interactions: use of salt effects to probe mechanisms of interaction CRC Crit. Rev. Biochem. 19 1986 191 245
39. J. Duguid, V.A. Bloomfield, J. Benevides, and G.J. Thomas Raman spectroscopy of DNA-metal complexes. I. Interactions and conformational effects of the divalent cations: Mg, Ca, Sr, Ba, Mn, Co, Ni, Cu, Pd, and Cd Biophys. J. 65 1993 1916 1928
40. L. McFail-Isom, X. Shui, and L.D. Williams Divalent cations stabilize unstacked conformations of DNA and RNA by interacting with base pi systems Biochemistry 37 1998 17105 17111
41. R. Melero, S. Rajagopalan, M. Lázaro, A.C. Joerger, T. Brandt, D.B. Veprintsev, G. Lasso, D. Gil, S.H. Scheres, J.M. Carazo, A.R. Fersht, and M. Valle Electron microscopy studies on the quaternary structure of p53 reveal different binding modes for p53 tetramers in complex with DNA Proc. Natl. Acad. Sci. U. S. A. 108 2011 557 562
42. R. Aramayo, M.B. Sherman, K. Brownless, R. Lurz, A.L. Okorokov, and E.V. Orlova Quaternary structure of the specific p53-DNA complex reveals the mechanism of p53 mutant dominance Nucleic Acids Res. 39 2011 8960 8971
43. D.B. Veprintsev, S.M. Freund, A. Andreeva, S.E. Rutledge, H. Tidow, J.M. Cañadillas, C.M. Blair, and A.R. Fersht Core domain interactions in full-length p53 in solution Proc. Natl. Acad. Sci. U. S. A. 103 2006 2115 2119
44. F. Huang, S. Rajagopalan, G. Settanni, R.J. Marsh, D.A. Armoogum, N. Nicolaou, A.J. Bain, E. Lerner, E. Haas, L. Ying, and A.R. Fersht Multiple conformations of full-length p53 detected with single-molecule fluorescence resonance energy transfer Proc. Natl. Acad. Sci. U. S. A. 106 2009 20758 20763
45. M. Bista, S.M. Freund, and A.R. Fersht Domain-domain interactions in full-length p53 and a specific DNA complex probed by methyl NMR spectroscopy Proc. Natl. Acad. Sci. U. S. A. 109 2012 15752 15756
46. Y.M. Wang, R.H. Austin, and E.C. Cox Single molecule measurements of repressor protein 1D diffusion on DNA Phys. Rev. Lett. 97 2006 048302
47. N.Y. Yao, R.E. Georgescu, J. Finkelstein, and M.E. O'Donnell Single-molecule analysis reveals that the lagging strand increases replisome processivity but slows replication fork progression Proc. Natl. Acad. Sci. U. S. A. 106 2009 13236 13241
48. A.R. Dunn, N.M. Kad, S.R. Nelson, D.M. Warshaw, and S.S. Wallace Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA Nucleic Acids Res. 9 2011 7487 7498
49. N.M. Kad, H. Wang, G.G. Kennedy, D.M. Warshaw, B.V. Houten, and D.N.A. Collaborative Dynamic Scanning by nucleotide excision repair proteins investigated by single-molecule imaging of quantum-dot-labeled proteins Mol. Cell 37 2010 702 713
50. S.R. Nelson, A.R. Dunn, S.D. Kathe, D.M. Warshaw, and S.S. Wallace Two glycosylase families diffusively scan DNA using a wedge residue to probe for and identify oxidatively damaged bases Proc. Natl. Acad. Sci. U. S. A. 111 2014 E2091 E2099
51. R. Strick, P.L. Strissel, K. Gavrilov, and R. Levi-Setti Cation-chromatin binding as shown by ion microscopy is essential for the structural integrity of chromosomes J. Cell Biol. 155 2001 899 910
52. A. Romani Regulation of magnesium homeostasis and transport in mammalian cells Arch. Biochem. Biophys. 458 2007 90 102
53. 2 +] changes in nucleus and cytosol Cell Calcium 16 1994 239 246
54. A.I. Coffer, and P.P. Knowles Divalent metal ions induce conformational change in pure, human wild-type p53 tumor suppressor protein Biochim. Biophys. Acta 1209 1994 279 285