Single-molecule studies of the Im7 folding landscape

Journal of Molecular Biology

Volumn 398, Issue 1, 2010, Pages 132-145

  Pugh, Sara D ^a   Gell, Christopher ^a   Smith, D Alastair ^a   Radford, Sheena E ^a   Brockwell, David J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Fluorescence resonance energy transfer; Folding; Im7; Intermediate; Unfolded ensemble

Indexed keywords

CYSTEINE; IMMUNITY PROTEIN 7; PROTEIN; SODIUM SULFATE; UNCLASSIFIED DRUG; UREA;

ARTICLE; CONTROLLED STUDY; ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; NORMAL DISTRIBUTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY;

EID: 77950861847     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.02.048     Document Type: Article

References (61)

1. Bai Y., Sosnick T.R., Mayne L., Englander S.W. Protein folding intermediates: native-state hydrogen exchange. Science 1995, 269:192-197.
2. Chamberlain A.K., Handel T.M., Marqusee S. Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH. Nat. Struct. Biol. 1996, 3:782-787.
3. Chu R.A., Pei W.H., Takei J., Bai Y.W. Relationship between the native-state hydrogen exchange and folding pathways of a four-helix bundle protein. Biochemistry 2002, 41:7998-8003.
4. Cliff M.J., Higgins L.D., Sessions R.B., Waltho J.P., Clarke A.R. Beyond the EX1 limit: probing the structure of high-energy states in protein unfolding. J. Mol. Biol. 2004, 336:497-508.
5. Ferguson N., Capaldi A.P., James R., Kleanthous C., Radford S.E. Rapid folding with and without populated intermediates in the homologous four-helix proteins Im7 and Im9. J. Mol. Biol. 1999, 286:1597-1608.
6. Parker M.J., Marqusee S. A kinetic folding intermediate probed by native state hydrogen exchange. J. Mol. Biol. 2001, 305:593-602.
7. Tang Y., Grey M.J., McKnight J., Palmer A.G., Raleigh D.P. Multistate folding of the villin headpiece domain. J. Mol. Biol. 2006, 355:1066-1077.
8. Yan S., Kennedy S.D., Koide S. Thermodynamic and kinetic exploration of the energy landscape of Borrelia burgdorferi OspA by native-state hydrogen exchange. J. Mol. Biol. 2002, 323:363-375.
9. Brockwell D.J., Radford S.E. Intermediates: ubiquitous species on folding energy landscapes?. Curr. Opin. Struct. Biol. 2007, 17:30-37.
10. Friel C.T., Smith D.A., Vendruscolo M., Gsponer J., Radford S.E. The mechanism of folding of Im7 reveals competition between functional and kinetic evolutionary constraints. Nat. Struct. Mol. Biol. 2009, 16:318-324.
11. Religa T.L., Markson J.S., Mayor U., Freund S.M.V., Fersht A.R. Solution structure of a protein denatured state and folding intermediate. Nature 2005, 437:1053-1056.
12. Watters A.L., Deka P., Corrent C., Callender D., Varani G., Sosnick T., Baker D. The highly cooperative folding of small naturally occurring proteins is likely the result of natural selection. Cell 2007, 128:613-624.
13. Dennis C.A., Videler H., Pauptit R.A., Wallis R., James R., Moore G.R., Kleanthous C. A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochem. J. 1998, 333:183-191.
14. Gsponer J., Hopearuoho H., Whittaker S.B.M., Spence G.R., Moore G.R., Paci E., et al. Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7. Proc. Natl Acad. Sci. USA 2006, 103:99-104.
15. Capaldi A.P., Shastry M.C., Kleanthous C., Roder H., Radford S.E. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nat. Struct. Biol. 2001, 8:68-72.
16. Capaldi A.P., Kleanthous C., Radford S.E. Im7 folding mechanism: misfolding on a path to the native state. Nat. Struct. Biol. 2002, 9:209-216.
17. Friel C.T., Beddard G.S., Radford S.E. Switching two-state to three-state kinetics in the helical protein Im9 via the optimisation of stabilising non-native interactions by design. J. Mol. Biol. 2004, 342:261-273.
18. Gorski S.A., Le Duff C.S., Capaldi A.P., Kalverda A.P., Beddard G.S., Moore G.R., Radford S.E. Equilibrium hydrogen exchange reveals extensive hydrogen bonded secondary structure in the on-pathway intermediate of Im7. J. Mol. Biol. 2004, 337:183-193.
19. Spence G.R., Capaldi A.P., Radford S.E. Trapping the on-pathway folding intermediate of Im7 at equilibrium. J. Mol. Biol. 2004, 341:215-226.
20. Whittaker S.B., Spence G.R., Gunter Grossmann J., Radford S.E., Moore G.R. NMR analysis of the conformational properties of the trapped on-pathway folding intermediate of the bacterial immunity protein Im7. J. Mol. Biol. 2007, 366:1001-1015.
21. Gell C., Brockwell D., Smith A. Handbook of Single Molecule Fluorescence Spectroscopy 2006, Oxford University Press, New York, NY.
22. Deniz A.A., Dahan M., Grunwell J.R., Ha T., Faulhaber A.E., Chemla D.S., et al. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: observation of Forster distance dependence and subpopulations. Proc. Natl Acad. Sci. USA 1999, 96:3670-3675.
23. Deniz A.A., Laurence T.A., Beligere G.S., Dahan M., Martin A.B., Chemla D.S., et al. Single-molecule protein folding: diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc. Natl Acad. Sci. USA 2000, 97:5179-5184.
24. Ha T., Ting A.Y., Liang J., Caldwell W.B., Deniz A.A., Chemla D.S., et al. Single-molecule fluorescence spectroscopy of enzyme conformational dynamics and cleavage mechanism. Proc. Natl Acad. Sci. USA 1999, 96:893-898.
25. Kuzmenkina E.V., Heyes C.D., Nienhaus G.U. Single-molecule FRET study of denaturant induced unfolding of RNase H. J. Mol. Biol. 2006, 357:313-324.
26. Rhoades E., Gussakovsky E., Haran G. Watching proteins fold one molecule at a time. Proc. Natl Acad. Sci. USA 2003, 100:3197-3202.
27. Schuler B., Lipman E.A., Eaton W.A. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 2002, 419:743-747.
28. Zhuang X., Bartley L.E., Babcock H.P., Russell R., Ha T., Herschlag D., Chu S. A single-molecule study of RNA catalysis and folding. Science 2000, 288:2048-2051.
29. Chung H.S., Louis J.M., Eaton W.A. Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories. Proc. Natl Acad. Sci. USA 2009, 106:11837-11844.
30. Tezuka-Kawakami T., Gell C., Brockwell D.J., Radford S.E., Smith D.A. Urea-induced unfolding of the immunity protein Im9 monitored by spFRET. Biophys. J. 2006, 91:L42-L44.
31. Rothwell P.J., Berger S., Kensch O., Felekyan S., Antonik M., Wohrl B.M., et al. Multiparameter single-molecule fluorescence spectroscopy reveals heterogeneity of HIV-1 reverse transcriptase:primer/template complexes. Proc. Natl Acad. Sci. USA 2003, 100:1655-1660.
32. Dahan M., Deniz A.A., Ha T.J., Chemla D.S., Schultz P.G., Weiss S. Ratiometric measurement and identification of single diffusing molecules. Chem. Phys. 1999, 247:85-106.
33. Nir E., Michalet X., Hamadani K.M., Laurence T.A., Neuhauser D., Kovchegov Y., Weiss S. Shot-noise limited single-molecule FRET histograms: comparison between theory and experiments. J. Phys. Chem. B 2006, 110:22103-22124.
34. Merchant K.A., Best R.B., Louis J.M., Gopich I.V., Eaton W.A. Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations. Proc. Natl Acad. Sci. USA 2007, 104:1528-1533.
35. Cobos E.S., Radford S.E. Sulfate-induced effects in the on-pathway intermediate of the bacterial immunity protein Im7. Biochemistry 2006, 45:2274-2282.
36. Gorski S.A., Capaldi A.P., Kleanthous C., Radford S.E. Acidic conditions stabilise intermediates populated during the folding of Im7 and Im9. J. Mol. Biol. 2001, 312:849-863.
37. Haugland R.P. The Handbook: A Guide to Fluorescent Probes and Labeling Technologies 2005, Invitrogen Corp., Carlsbad, CA. 10th edit.
38. Panchuk-Voloshina N., Haugland R.P., Bishop-Stewart J., Bhalgat M.K., Millard P.J., Mao F., et al. Alexa dyes, a series of new fluorescent dyes that yield exceptionally bright, photostable conjugates. J. Histochem. Cytochem. 1999, 47:1179-1188.
39. Huang F., Sato S., Sharpe T.D., Ying L.M., Fersht A.R. Distinguishing between cooperative and unimodal downhill protein folding. Proc. Natl Acad. Sci. USA 2007, 104:123-127.
40. Huang F., Ying L.M., Fersht A.R. Direct observation of barrier-limited folding of BBL by single-molecule fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA 2009, 106:16239-16244.
41. Bartlett A.I., Radford S.E. Desolvation and development of specific hydrophobic core packing during Im7 folding. J. Mol. Biol. 2010, 396:1329-1345.
42. Laurence T.A., Kong X., Jager M., Weiss S. Probing structural heterogeneities and fluctuations of nucleic acids and denatured proteins. Proc. Natl Acad. Sci. USA 2005, 102:17348-17353.
43. Magg C., Schmid F.X. Rapid collapse precedes the fast two-state folding of the cold shock protein. J. Mol. Biol. 2004, 335:1309-1323.
44. Magg C., Kubelka J., Holtermann G., Haas E., Schmid F.X. Specificity of the initial collapse in the folding of the cold shock protein. J. Mol. Biol. 2006, 360:1067-1080.
45. Hoffmann A., Kane A., Nettels D., Hertzog D.E., Baumgartel P., Lengefeld J., et al. Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy. Proc. Natl Acad. Sci. USA 2007, 104:105-110.
46. Huang F., Lerner E., Sato S., Amir D., Haas E., Fersht A.R. Time-resolved fluorescence resonance energy transfer study shows a compact denatured state of the B domain of protein A. Biochemistry 2009, 48:3468-3476.
47. Liu P.C., Meng X.L., Qu P., Zhao X.S., Wang C.C. Subdomain-specific collapse of denatured staphylococcal nuclease revealed by single molecule fluorescence resonance energy transfer measurements. J. Phys. Chem. B 2009, 113:12030-12036.
48. Mukhopadhyay S., Krishnan R., Lemke E.A., Lindquist S., Deniz A.A. A natively unfolded yeast prion monomer adopts an ensemble of collapsed and rapidly fluctuating structures. Proc. Natl Acad. Sci. USA 2007, 104:2649-2654.
49. Sherman E., Haran G. Coil-globule transition in the denatured state of a small protein. Proc. Natl Acad. Sci. USA 2006, 103:11539-11543.
50. Alonso D.O.V., Dill K.A. Solvent denaturation and stabilisation of globular proteins. Biochemistry 1991, 30:5974-5985.
51. Ziv G., Thirumalai D., Haran G. Collapse transition in proteins. Phys. Chem. Chem. Phys. 2009, 11:83-93.
52. Arai M., Kondrashkina E., Kayatekin C., Matthews C.R., Iwakura M., Bilsel O. Microsecond hydrophobic collapse in the folding of Escherichia coli dihydrofolate reductase, an alpha/beta-type protein. J. Mol. Biol. 2007, 368:219-229.
53. Kohn J.E., Gillespie B., Plaxco K.W. Non-sequence-specific interactions can account for the compaction of proteins unfolded under "native" conditions. J. Mol. Biol. 2009, 394:343-350.
54. Sinha K.K., Udgaonkar J.B. Dissecting the non-specific and specific components of the initial folding reaction of barstar by multi-site FRET measurements. J. Mol. Biol. 2007, 370:385-405.
55. Ziv G., Haran G. Protein folding, protein collapse, and tanford's transfer model: lessons from single-molecule FRET. J. Am. Chem. Soc. 2009, 131:2942-2947.
56. Choy W.Y., Forman-Kay J.D. Calculation of ensembles of structures representing the unfolded state of an SH3 domain. J. Mol. Biol. 2001, 308:1011-1032.
57. Vendruscolo M. Determination of conformationally heterogeneous states of proteins. Curr. Opin. Struct. Biol. 2007, 17:15-20.
58. Lindorff-Larsen K., Kristjansdottir S., Teilum K., Fieber W., Dobson C.M., Poulsen F.M., Vendruscolo M. Determination of an ensemble of structures representing the denatured state of the bovine acyl-coenzyme A binding protein. J. Am. Chem. Soc. 2004, 126:3291-3299.
59. Jensen M.R., Markwick P.R.L., Meier S., Griesinger C., Zweckstetter M., Grzesiek S., et al. Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings. Structure 2009, 17:1169-1185.
60. Santoro M., Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 1988, 27:8063-8068.
61. Gell C., Sabir T., Westwood J., Rashid A., Smith D.A.M., Harris S.A., Stockley P.G. Single-molecule fluorescence resonance energy transfer assays reveal heterogeneous folding ensembles in a simple RNA stem-loop. J. Mol. Biol. 2008, 384:264-278.