Multiple conformations of full-length p53 detected with single-molecule fluorescence resonance energy transfer

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 49, 2009, Pages 20758-20763

  Huang, Fang ^a,e   Rajagopalan, Sridharan ^a   Settanni, Giovanni ^a   Marsh, Richard J ^b   Armoogum, Daven A ^b   Nicolaou, Nick ^b   Bain, Angus J ^b   Lerner, Eitan ^c   Haas, Elisha ^c   Ying, Liming ^d   Fersht, Alan R ^a  

^a MRC CENTRE FOR PROTEIN ENGINEERING   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c BAR ILAN UNIVERSITY   (Israel)

^d NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^e CHINA UNIVERSITY OF PETROLEUM   (China)

Author keywords

Domain domain interaction; FRET; Natively disordered; Quaternary structure; Time resolved

Indexed keywords

PROTEIN P53;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA BINDING; ELECTRON MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; PRIORITY JOURNAL; RADIATION SCATTERING;

AMINO ACIDS; ANIMALS; DIFFUSION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MICE; MODELS, MOLECULAR; MUTANT PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SCATTERING, SMALL ANGLE; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53; X-RAY DIFFRACTION;

MURINAE;

EID: 73949127938     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0909644106     Document Type: Article

References (48)

1. Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408:307-310.
2. Hainaut P, Wiman K (2005) 25 Years of p53 Research (Springer, New York).
3. Clore GM, et al. (1995) Refined solution structure of the oligomerization domain of the tumour suppressor p53. Nat Struct Biol 2:321-333.
4. Cho Y, Gorina S, Jeffrey PD, Pavletich NP(1994) Crystal structure of a p53 tumor suppressor-DNA complex: Understanding tumorigenic mutations. Science 265:346-355.
5. Dawson R, et al. (2003) The N-terminal domain of p53 is natively unfolded. J Mol Biol 332:1131-1141.
6. Müller-Tiemann BF, Halazonetis TD, Elting JJ (1998) Identification of an additional negative regulatory region for p53 sequence-specific DNA binding. Proc Natl Acad Sci USA 95:6079-6084.
7. Joerger AC, Hwee CA, Veprintsev DB, Blair CM, Fersht AR (2005) Structures of p53 cancer mutants and mechanism of rescue by second-site suppressor mutations. J Biol Chem 280:16030-16037.
8. Lee W,et al. (1994) Solution structure of the tetrameric minimum transforming domain of p53. Nat Struct Biol 1:877-890.
9. Tidow H, et al. (2007) Quaternary structures of tumor suppressor p53 and a specific p53-DNA complex. Proc Natl Acad Sci USA 104:12324-12329.
10. Wells M, et al. (2008) Structure of tumour suppressor p53 and its intrinsically disordered N-terminal transactivation domain. Proc Natl Acad Sci USA 105:5762-5767.
11. Okorokov AL, et al. (2006) The structure of p53 tumor suppressor protein reveals the basis for its functional plasticity. EMBO J 25:5191-5200.
12. Weiss S (2000) Measuring conformational dynamics of biomolecules by single molecule fluorescence spectroscopy. Nat Struct Biol 7:724-729.
13. Schuler B, EatonWA(2008) Protein folding studied by single-molecule FRET. Curr Opin Struc Biol 18:16-26.
14. Beechem JM, Haas E (1989) Simultaneous determination of intramolecular distance distributions and conformational dynamics by global analysis of energy transfer measurements. Biophys J 55:1225-1236.
15. Sherman E, Haran G (2006) Coil-globule transition in the denatured state of a small protein. Proc Natl Acad Sci USA 103:11539-11543.
16. Laurence TA, Kong X, Jäger M, Weiss S (2005) Probing structural heterogeneities and fluctuations of nucleic acids and denatured proteins. Proc Natl Acad Sci USA 102:17348-17353.
17. Mukhopadhyay S, Krishnan R, Lemke EA, Lindquist S, Deniz AA (2007) A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. Proc Natl Acad Sci USA 104:2649-2654.
18. Merchant KA, Best RB, Louis JM, Gopich IV, Eaton WA (2007) Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy any molecular simulations. Proc Natl Acad Sci USA 104:1528-1533.
19. Deniz AA, et al. (2000) Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc Natl Acad Sci USA 97:5179-5184.
20. Schuler B, Lipman EA, Eaton WA (2002) Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419:743-747.
21. Huang F, Sato S, Sharpe TD, Ying LM,Fersht AR(2007) Distinguishing between cooperative and unimodal downhill protein folding. Proc Natl Acad Sci USA 104:123-127.
22. Andrecka J, et al. (2008) Single-molecule tracking of mRNA exiting from RNA polymerase II. Proc Natl Acad Sci USA 105:135-140.
23. Henzler-Wildman KA, et al. (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450:838-844.
24. Sharma S, et al. (2008) Monitoring protein conformation along the pathway of chaperonin-assisted folding. Cell 133:142-153.
25. Diez M, et al. (2004) Proton-powered subunit rotation in single membrane-bound F 0F1-ATP synthase. Nat Struct Mol Biol 11:135-141.
26. Mori T, Vale RD, Tomishige M (2007) How kinesin waits between steps. Nature 450:750-754.
27. Majumdar DS, et al. (2007) Single-molecule FRET reveals sugar-induced conformational dynamics in LacY. Proc Natl Acad Sci USA 104:12640-12645.
28. Kapanidis AN, et al. (2004) Fluorescence-aided molecule sorting: Analysis of structure and interactions by alternating-laser excitation of single molecules. Proc Natl Acad Sci USA 101:8936-8941.
29. Haas E (2005) The study of protein folding and dynamics by determination of intramolecular distance distributions and their fluctuations using ensemble and single-molecule FRET measurements. ChemPhysChem 6:858-870.
30. Joerger AC, Allen MD, Fersht AR (2004) Crystal structure of a superstable mutant of human p53 core domain: Insights into the mechanism of rescuing oncogenic mutations. J Biol Chem 279:1291-1296.
31. Huang F, Settanni G, Fersht AR (2008) Fluorescence resonance energy transfer analysis of the folding pathway of Engrailed homeodomain. Protein Eng Des Sel 21:131-146.
32. Haran G, Haas E, Szpikowska BK, Mas MT (1992) Domain motions in phosphoglycerate kinase: Determination of interdomain distance distributions by site-specific labeling and time-resolved fluorescence energy transfer. Proc Natl Acad Sci USA 89:11764-11768.
33. Kussie PH, et al. (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 274:948-953.
34. Best RB, et al. (2007) Effect of flexibility and cis residues in single-molecule FRET studies of polyproline. Proc Natl Acad Sci USA 104:18964-18969.
35. Doose S, Neuweiler H, Barsch H, Sauer M (2007) Probing polyproline structure and dynamics by photoinduced electron transfer provides evidence for deviations from a regular polyproline type II helix. Proc Natl Acad Sci USA 104:17400-17405.
36. Huang F, Nau WM (2003) A conformational flexibility scale for amino acids in peptides. Angew Chem Int Ed 42:2269-2272.
37. Zagrovic B, et al. (2005) Unusual compactness of a polyproline type II structure. Proc Natl Acad Sci USA 102:11698-11703.
38. Möglich A, Joder K, Kiefhaber T (2006) End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation. Proc Natl Acad Sci USA 103:12394-12399.
39. Haas E, Katchalski-Katzir E, Steinberg IZ (1978) Brownian motion of the ends of oligopeptide chains in solution as estimated by energy transfer between the chain ends. Biopolymers 17:11-31.
40. Navon A, Ittah V, Landsman P, Scheraga HA, Haas E (2001) Distributions of intramolecular distances in the reduced and denatured states of bovine pancreatic ribonuclease A. Folding initiation structures in the C-terminal portions of the reduced protein. Biochemistry 40:105-118.
41. Huang F, Hudgins RR, Nau WM (2004) Primary and secondary structure dependence of peptide flexibility assessed by fluorescence-based measurement of end-to-end collision rates. J Am Chem Soc 126:16665-16675.
42. Sakamoto H, Lewis MS, Kodama H, Appella E, Sakaguchi K (1994) Specific sequences from the carboxyl terminus of human p53 gene product form anti-parallel tetramers in solution. Proc Natl Acad Sci USA 91:8974-8978.
43. Adams SR, et al. (2002) New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: Synthesis and biological applications. J Am Chem Soc 124:6063-6076.
44. Hillger F, et al. (2008) Probing protein-chaperone interactions with single-molecule fluorescence spectroscopy. Angew Chem Int Ed 47:6184-6188.
45. Rajagopalan S, Andreeva A, Teufel DP, Freund SM, Fersht AR (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.
46. Veprintsev DB, et al. (2006) Core domain interactions in full-length p53 in solution. Proc Natl Acad Sci USA 103:2115-2119.
47. Yu GW, et al. (2006) The central region ofHDM2provides a second binding site for p53. Proc Natl Acad Sci USA 103:1227-1232.
48. Nikolova PV, Henckel J, Lane DP, Fersht AR (1998) Semirational design of active tumor suppressor p53 DNA binding domain with enhanced stability. Proc Natl Acad Sci USA 95:14675-14680.