A small molecule directly inhibits the p53 transactivation domain from binding to replication protein A

Nucleic Acids Research

Volumn 41, Issue 3, 2013, Pages 2047-2059

  Glanzer, Jason G ^a   Carnes, Katie A ^b   Soto, Patricia ^c   Liu, Shengqin ^a   Parkhurst, Lawrence J ^b   Oakley, Gregory G ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c CREIGHTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; FUMAROPIMARIC ACID; PROTEIN INHIBITOR; PROTEIN P53; REPLICATION FACTOR A; SINGLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN; SINGLE STRANDED DNA BINDING PROTEIN F; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA HELIX; FLUORESCENCE ANALYSIS; INHIBITION KINETICS; MOLECULAR DOCKING; MOLECULAR INTERACTION; MOLECULAR MODEL; MUTATIONAL ANALYSIS; PHASE SEPARATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; STRUCTURE ANALYSIS; TRANSACTIVATION;

AMINO ACID SUBSTITUTION; BINDING SITES; BINDING, COMPETITIVE; DITERPENES; DNA, SINGLE-STRANDED; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; REPLICATION PROTEIN A; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84873690922     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1291     Document Type: Article

References (63)

1. Oakley,G.G. and Patrick,S.M. (2010) Replication protein A: directing traffic at the intersection of replication and repair. Front. Biosci., 15, 883-900.
2. Wold,M.S. (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem., 66, 61-92.
3. Patrick,S.M. and Turchi,J.J. (1999) Replication protein A (RPA) binding to duplex cisplatin-damaged DNA is mediated through the generation of single-stranded DNA. J. Biol. Chem., 274, 14972-14978.
4. Lao,Y., Lee,C.G. and Wold,M.S. (1999) Replication protein A interactions with DNA. 2. Characterization of double-stranded DNA-binding/helix- destabilization activities and the role of the zinc-finger domain in DNA interactions. Biochemistry, 38, 3974-3984.
5. Treuner,K., Ramsperger,U. and Knippers,R. (1996) Replication protein A induces the unwinding of long double-stranded DNA regions. J. Mol. Biol, 259, 104-112.
6. Daughdrill,G.W., Ackerman,J., Isern,N.G., Botuyan,M.V., Arrowsmith,C., Wold,M.S. and Lowry,D.F. (2001) The weak interdomain coupling observed in the 70 kDa subunit of human replication protein A is unaffected by ssDNA binding. Nucleic Acids Res., 29, 3270-3276.
7. Kantake,N., Sugiyama,T., Kolodner,R.D. and Kowalczykowski,S.C. (2003) The recombination-deficient mutant RPA (rfa1-t11) is displaced slowly from single-stranded DNA by Rad51 protein. J. Biol. Chem., 278, 23410-23417.
8. Kim,H.S. and Brill,S.J. (2001) Rfc4 interacts with Rpa1 and is required for both DNA replication and DNA damage checkpoints in Saccharomyces cerevisiae. Mol. Cell. Biol., 21, 3725-3737.
9. Haring,S.J., Mason,A.C., Binz,S.K. and Wold,M.S. (2008) Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J. Biol. Chem., 283, 19095-19111.
10. Oakley,G.G., Tillison,K., Opiyo,S.A., Glanzer,J.G., Horn,J.M. and Patrick,S.M. (2009) Physical interaction between replication protein A (RPA) and MRN: involvement of RPA2 phosphorylation and the N-terminus of RPA1. Biochemistry, 48, 7473-7481.
11. Li,R. and Botchan,M.R. (1993) The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell, 73, 1207-1221.
12. He,Z., Brinton,B.T., Greenblatt,J., Hassell,J.A. and Ingles,C.J. (1993) The transactivator proteins VP16 and GAL4 bind replication factor A. Cell, 73, 1223-1232.
13. Dutta,A., Ruppert,J.M., Aster,J.C. and Winchester,E. (1993) Inhibition of DNA replication factor RPA by p53. Nature, 365, 79-82.
14. Olson,E., Nievera,C.J., Liu,E., Lee,A.Y., Chen,L. and Wu,X. (2007) The Mre11 complex mediates the S-phase checkpoint through an interaction with replication protein A. Mol. Cell. Biol., 27, 6053-6067.
15. Xu,X., Vaithiyalingam,S., Glick,G.G., Mordes,D.A., Chazin,W.J. and Cortez,D. (2008) The basic cleft of RPA70N binds multiple checkpoint proteins, including RAD9, to regulate ATR signaling. Mol. Cell. Biol., 28, 7345-7353.
16. Ball,H.L., Ehrhardt,M.R., Mordes,D.A., Glick,G.G., Chazin,W.J. and Cortez,D. (2007) Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol., 27, 3367-3377.
17. Glanzer,J.G., Liu,S. and Oakley,G.G. (2011) Small molecule inhibitor of the RPA70 N-terminal protein interaction domain discovered using in silico and in vitro methods. Bioorg. Med. Chem., 19, 2589-2595.
18. Vogelstein,B., Lane,D. and Levine,A.J. (2000) Surfing the p53 network. Nature, 408, 307-310.
19. Levine,A.J. (1997) p53, the cellular gatekeeper for growth and division. Cell, 88, 323-331.
20. Joerger,A.C. and Fersht,A.R. (2010) The tumor suppressor p53: from structures to drug discovery. Cold Spring Harb. Perspect. Biol., 2, a000919.
21. Candau,R., Scolnick,D.M., Darpino,P., Ying,C.Y., Halazonetis,T.D. and Berger,S.L. (1997) Two tandem and independent sub-activation domains in the amino terminus of p53 require the adaptor complex for activity. Oncogene, 15, 807-816.
22. Vise,P.D., Baral,B., Latos,A.J. and Daughdrill,G.W. (2005) NMR chemical shift and relaxation measurements provide evidence for the coupled folding and binding of the p53 transactivation domain. Nucleic Acids Res., 33, 2061-2077.
23. Rajagopalan,S., Andreeva,A., Teufel,D.P., Freund,S.M. and Fersht,A.R. (2009) Interaction between the transactivation domain of p53 and PC4 exemplifies acidic activation domains as single-stranded DNA mimics. J. Biol. Chem., 284, 21728-21737.
24. Bochkareva,E., Kaustov,L., Ayed,A., Yi,G.S., Lu,Y., Pineda-Lucena,A., Liao,J.C., Okorokov,A.L., Milner,J., Arrowsmith,C.H. et al. (2005) Single-stranded DNA mimicry in the p53 transactivation domain interaction with replication protein A. Proc. Natl Acad. Sci. USA, 102, 15412-15417.
25. Rajagopalan,S., Andreeva,A., Rutherford,T.J. and Fersht,A.R. (2010) Mapping the physical and functional interactions between the tumor suppressors p53 and BRCA2. Proc. Natl Acad. Sci. USA, 107, 8587-8592.
26. Kaustov,L., Yi,G.S., Ayed,A., Bochkareva,E., Bochkarev,A. and Arrowsmith,C.H. (2006) p53 transcriptional activation domain: a molecular chameleon? Cell Cycle, 5, 489-494.
27. Sirbu,B.M., Lachmayer,S.J., Wulfing,V., Marten,L.M., Clarkson,K.E., Lee,L.W., Gheorghiu,L., Zou,L., Powell,S.N., Dahm-Daphi,J. et al. (2011) ATR-p53 restricts homologous recombination in response to replicative stress but does not limit DNA interstrand crosslink repair in lung cancer cells. PLoS One, 6, e23053.
28. Pretto,D.I., Tsutakawa,S., Brosey,C.A., Castillo,A., Chagot,M.E., Smith,J.A., Tainer,J.A. and Chazin,W.J. (2010) Structural dynamics and single-stranded DNA binding activity of the three N-terminal domains of the large subunit of replication protein A from small angle X-ray scattering. Biochemistry, 49, 2880-2889.
29. Henricksen,L.A., Umbricht,C.B. and Wold,M.S. (1994) Recombinant replication protein A: expression, complex formation, and functional characterization J. Biol. Chem., 269, 11121-11132.
30. Sheffield,P., Garrard,S. and Derewenda,Z. (1999) Overcoming expression and purification problems of RhoGDI using a family of ''parallel'' expression vectors. Protein Expr. Purif., 15, 34-39.
31. Huibregtse,J.M., Scheffner,M. and Howley,P.M. (1991) A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J., 10, 4129-4135.
32. Press,W.H., Teukolsky,S.A., Vetterling,W.T. and Flannery,B.P. (2007) Numerical Recipes: The Art of Scientific Computing, 3rd edn. Cambridge University Press, Cambridge England.
33. Draper,N.R. and Smith,H. (1981) Applied Regression Analysis, 2nd edn. John Wiley and Sons.
34. Van Der Spoel,D., Lindahl,E., Hess,B., Groenhof,G., Mark,A.E. and Berendsen,H.J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem., 26, 1701-1718.
35. Lee,M.R., Duan,Y. and Kollman,P.A. (2001) State of the art in studying protein folding and protein structure prediction using molecular dynamics methods. J. Mol. Graph. Model., 19, 146-149.
36. Jorgensen,W.L., Chandrasekhar,J., Buckner,J.K. and Madura,J.D. (1986) Computer simulations of organic reactions in solution. Ann. N. Y. Acad. Sci., 482, 198-209.
37. Villa,A., Mark,A.E., Saracino,G.A., Cosentino,D.P., Moro,G. and Salmona,M. (2006) Conformational polymorphism of the PrP106-126 peptide in different environments: a molecular dynamics study. J. Phys. Chem. B, 110, 1423-1428.
38. Bussi,G., Donadio,D. and Parrinello,M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys., 126, 014101.
39. Hess,B., Bekker,H., Berendsen,H.J.C. and Fraaije,J.G.E.M. (1997) LINCS: a linear constraint solver for molecular simulations. J Comput. Chem., 18, 1463-1472.
40. Miyamoto,S. and Kollman,P.A. (1992) Settle-an analytical version of the shake and rattle algorithm for rigid water models. J. Comput. Chem., 13, 952-962.
41. Tironi,I., Sperb,R., Smith,P. and van Gunsteren,W. (1995) A generalized reaction field method for molecular-dynamics simulations. J. Phys. Chem., 102, 5451-5459.
42. van der Spoel,D., Lindahl,E., Hess,B., van Buuren,A.R., Apol,E., Meulenhoff,P.J., Tieleman,D.P., Sijbers,A.L., Teemu,M. and Feenstra,K.A. (2010), Gromacs user manual version 4.5.4.
43. Atilgan,A.R., Durell,S.R., Jernigan,R.L., Demirel,M.C., Keskin,O. and Bahar,I. (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys. J., 80, 505-515.
44. Bakan,A., Meireles,L.M. and Bahar,I. (2011) ProDy: protein dynamics inferred from theory and experiments. Bioinformatics, 27, 1575-1577.
45. Trott,O. and Olson,A.J. (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem., 31, 455-461.
46. Wolf,L.K. (2009) Digital Briefs. Chemical & Engineering News, 87, 31.
47. Seeliger,D. and de Groot,B.L. (2010) Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J. Comput. Aided Mol. Des., 24, 417-422.
48. Wiyono,B., Tachibana,S. and Tinambunan,D. (2007) Reaction of abietic acid with maleic anhydride and fumaric acid and attempts to find the fundamental component of fortified rosin. Pak. J. Biol. Sci., 10, 1588-1595.
49. Umezu,K., Sugawara,N., Chen,C., Haber,J.E. and Kolodner,R.D. (1998) Genetic analysis of yeast RPA1 reveals its multiple functions in DNA metabolism. Genetics, 148, 989-1005.
50. Zou,L. and Elledge,S.J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548.
51. Jacobs,D.M., Lipton,A.S., Isern,N.G., Daughdrill,G.W., Lowry,D.F., Gomes,X. and Wold,M.S. (1999) Human replication protein A: global fold of the N-terminal RPA-70 domain reveals a basic cleft and flexible C-terminal linker. J. Biomol. NMR, 14, 321-331.
52. Nussinov,R. and Ma,B. (2012) Protein dynamics and conformational selection in bidirectional signal transduction. BMC Biol., 10, 2.
53. Boehr,D.D. (2012) Promiscuity in protein-RNA interactions: conformational ensembles facilitate molecular recognition in the spliceosome: conformational diversity in U2AF(6)(5) facilitates binding to diverse RNA sequences. Bioessays, 34, 174-180.
54. Fanning,E., Klimovich,V. and Nager,A.R. (2006) A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res., 34, 4126-4137.
55. Romanova,L.Y., Willers,H., Blagosklonny,M.V. and Powell,S.N. (2004) The interaction of p53 with replication protein A mediates suppression of homologous recombination. Oncogene, 23, 9025-9033.
56. Shammas,M.A., Shmookler Reis,R.J., Koley,H., Batchu,R.B., Li,C. and Munshi,N.C. (2009) Dysfunctional homologous recombination mediates genomic instability and progression in myeloma. Blood, 113, 2290-2297.
57. Plo,I., Nakatake,M., Malivert,L., de Villartay,J.P., Giraudier,S., Villeval,J.L., Wiesmuller,L. and Vainchenker,W. (2008) JAK2 stimulates homologous recombination and genetic instability: potential implication in the heterogeneity of myeloproliferative disorders. Blood, 112, 1402-1412.
58. Liu,Y., Kvaratskhelia,M., Hess,S., Qu,Y. and Zou,Y. (2005) Modulation of replication protein A function by its hyperphosphorylation-induced conformational change involving DNA binding domain B. J. Biol. Chem., 280, 32775-32783.
59. Patrick,S.M. and Turchi,J.J. (2001) Stopped-flow kinetic analysis of replication protein A-binding DNA: damage recognition and affinity for single-stranded DNA reveal differential contributions of k(on) and k(off) rate constants. J. Biol. Chem., 276, 22630-22637.
60. Roy,R., Kozlov,A.G., Lohman,T.M. and Ha,T. (2009) SSB protein diffusion on single-stranded DNA stimulates RecA filament formation. Nature, 461, 1092-1097.
61. Kim,C., Paulus,B.F. and Wold,M.S. (1994) Interactions of human replication protein A with oligonucleotides. Biochemistry, 33, 14197-14206.
62. Miller,S.D., Moses,K., Jayaraman,L. and Prives,C. (1997) Complex formation between p53 and replication protein A inhibits the sequence-specific DNA binding of p53 and is regulated by singlestranded DNA. Mol.Cell. Biol., 17, 2194-2201.
63. Souza-Fagundes,E.M., Frank,A.O., Feldkamp,M.D., Dorset,D.C., Chazin,W.J., Rossanese,O.W., Olejniczak,E.T. and Fesik,S.W. (2012) A high-throughput fluorescence polarization anisotropy assay for the 70N domain of replication protein A. Anal. Biochem., 421, 742-749.