Rational modification of protein stability by targeting surface sites leads to complicated results

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

Volumn 110, Issue 28, 2013, Pages 11337-11342

  Xiao, Shifeng ^a   Patsalo, Vadim ^a,b   Shan, Bing ^a   Bi, Yuan ^a   Green, David F ^a,b   Raleigh, Daniel P ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b Stony Brook University   (United States)

Author keywords

Atomistic simulations; Nuclear magnetic resonance; pH dependent stability; Protein biophysics; Protein pKa measurements

Indexed keywords

LYSINE; MUTANT PROTEIN; SOLVENT; VILLIN;

ARTICLE; CHEMICAL MODIFICATION; CRYSTAL STRUCTURE; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PKA; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN UNFOLDING; STATIC ELECTRICITY; SURFACE CHARGE; THERMODYNAMICS;

ATOMISTIC SIMULATIONS; NUCLEAR MAGNETIC RESONANCE; PH-DEPENDENT STABILITY; PROTEIN BIOPHYSICS; PROTEIN PKA MEASUREMENTS;

AMINO ACID SEQUENCE; BINDING SITES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEINS; SOLUBILITY; STATIC ELECTRICITY;

EID: 84879898263     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222245110     Document Type: Article

References (48)

1. Makhatadze GI, Loladze VV, Ermolenko DN, Chen X, Thomas ST (2003) Contribution of surface salt bridges to protein stability: Guidelines for protein engineering. J Mol Biol 327(5):1135-1148. (Pubitemid 36363718)
2. Bashford D, Karplus M (1990) pKa' s of ionizable groups in proteins: Atomic detail from a continuum electrostatic model. Biochemistry 29(44):10219-10225. (Pubitemid 20384527)
3. Strickler SS, et al. (2006) Protein stability and surface electrostatics: A charged relationship. Biochemistry 45(9):2761-2766. (Pubitemid 43334524)
4. Loladze VV, Ibarra-Molero B, Sanchez-Ruiz JM, Makhatadze GI (1999) Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry 38(50):16419-16423.
5. Spector S, et al. (2000) Rational modification of protein stability by the mutation of charged surface residues. Biochemistry 39(5):872-879. (Pubitemid 30075313)
6. Hendsch ZS, Tidor B (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis. Protein Sci 3(2):211-226. (Pubitemid 24086354)
7. Honig B, Nicholls A (1995) Classical electrostatics in biology and chemistry. Science 268(5214):1144-1149.
8. Duan Y, Kollman PA (1998) Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science 282(5389):740-744. (Pubitemid 28489385)
9. Kubelka J, Chiu TK, Davies DR, Eaton WA, Hofrichter J (2006) Sub-microsecond protein folding. J Mol Biol 359(3):546-553. (Pubitemid 43767258)
10. Kubelka J, Eaton WA, Hofrichter J (2003) Experimental tests of villin subdomain folding simulations. J Mol Biol 329(4):625-630. (Pubitemid 36629358)
11. Brewer SH, et al. (2005) Effect of modulating unfolded state structure on the folding kinetics of the villin headpiece subdomain. Proc Natl Acad Sci USA 102(46):16662-16667. (Pubitemid 41688833)
12. Ensign DL, Kasson PM, Pande VS (2007) Heterogeneity even at the speed limit of folding: Large-scale molecular dynamics study of a fast-folding variant of the villin headpiece. J Mol Biol 374(3):806-816. (Pubitemid 350019606)
13. Zagrovic B, Snow CD, Shirts MR, Pande VS (2002) Simulation of folding of a small alpha-helical protein in atomistic detail using worldwide-distributed computing. J Mol Biol 323(5):927-937. (Pubitemid 35341065)
14. Wang MH, et al. (2003) Dynamic NMR line-shape analysis demonstrates that the villin headpiece subdomain folds on the microsecond time scale. J Am Chem Soc 125(20):6032-6033.
15. Shaw DE, et al. (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330(6002):341-346.
16. Lindorff-Larsen K, Piana S, Dror RO, Shaw DE (2011) How fast-folding proteins fold. Science 334(6055):517-520.
17. Piana S, Lindorff-Larsen K, Shaw DE (2012) Protein folding kinetics and thermodynamics from atomistic simulation. Proc Natl Acad Sci USA 109(44):17845-17850.
18. Xiao S, Raleigh DP (2010) A critical assessment of putative gatekeeper interactions in the villin headpiece helical subdomain. J Mol Biol 401(2):274-285.
19. Bi Y, et al. (2007) Rational design, structural and thermodynamic characterization of a hyperstable variant of the villin headpiece helical subdomain. Biochemistry 46(25):7497-7505. (Pubitemid 46986376)
20. Chiu TK, et al. (2005) High-resolution x-ray crystal structures of the villin headpiece subdomain, an ultrafast folding protein. Proc Natl Acad Sci USA 102(21):7517-7522. (Pubitemid 40741003)
21. Pace CN, Grimsley GR, Scholtz JM (2009) Protein ionizable groups: pK values and their contribution to protein stability and solubility. J Biol Chem 284(20):13285-13289.
22. Isom DG, Castañeda CA, Cannon BR, García-Moreno B (2011) Large shifts in pKa values of lysine residues buried inside a protein. Proc Natl Acad Sci USA 108(13):5260-5265.
23. Tollinger M, Crowhurst KA, Kay LE, Forman-Kay JD (2003) Site-specific contributions to the pH dependence of protein stability. Proc Natl Acad Sci USA 100(8):4545-4550. (Pubitemid 36457767)
24. Wallace JA, Shen JK (2009) Predicting pKa values with continuous constant pH molecular dynamics. Methods Enzymol 466:455-475.
25. Arthur EJ, Yesselman JD, Brooks CL, 3rd (2011) Predicting extreme pKa shifts in staphylococcal nuclease mutants with constant pH molecular dynamics. Proteins 79(12):3276-3286.
26. Pey AL, Rodriguez-Larrea D, Gavira JA, Garcia-Moreno B, Sanchez-Ruiz JM (2010) Modulation of buried ionizable groups in proteins with engineered surface charge. J Am Chem Soc 132(4):1218-1219.
27. Yang AS, Honig B (1993) On the pH dependence of protein stability. J Mol Biol 231(2):459-474.
28. Tanford C (1970) Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv Protein Chem 24:1-95.
29. Kuhlman B, Luisi DL, Young P, Raleigh DP (1999) pKa values and the pH dependent stability of the N-terminal domain of L9 as probes of electrostatic interactions in the denatured state. Differentiation between local and nonlocal interactions. Biochemistry 38(15):4896-4903.
30. Swint-Kruse L, Robertson AD (1995) Hydrogen bonds and the pH dependence of ovomucoid third domain stability. Biochemistry 34(14):4724-4732.
31. Tan YJ, Oliveberg M, Davis B, Fersht AR (1995) Perturbed pKA-values in the denatured states of proteins. J Mol Biol 254(5):980-992.
32. Oliveberg M, Arcus VL, Fersht AR (1995) pKA values of carboxyl groups in the native and denatured states of barnase: The pKA values of the denatured state are on average 0.4 units lower than those of model compounds. Biochemistry 34(29):9424-9433.
33. Meng W, Shan B, Tang Y, Raleigh DP (2009) Native like structure in the unfolded state of the villin headpiece helical subdomain, an ultrafast folding protein. Protein Sci 18(8):1692-1701.
34. Tang YF, Goger MJ, Raleigh DP (2006) NMR characterization of a peptide model provides evidence for significant structure in the unfolded state of the villin headpiece helical subdomain. Biochemistry 45(22):6940-6946. (Pubitemid 43856678)
35. Tang YF, Rigotti DJ, Fairman R, Raleigh DP (2004) Peptide models provide evidence for significant structure in the denatured state of a rapidly folding protein: The villin headpiece subdomain. Biochemistry 43(11):3264-3272. (Pubitemid 38352276)
36. Trefethen JM, Pace CN, Scholtz JM, Brems DN (2005) Charge-charge interactions in the denatured state influence the folding kinetics of ribonuclease Sa. Protein Sci 14(7):1934-1938. (Pubitemid 40994166)
37. Cho J-H, Sato S, Horng JC, Anil B, Raleigh DP (2008) Electrostatic interactions in the denatured state ensemble: Their effect upon protein folding and protein stability. Arch Biochem Biophys 469(1):20-28. (Pubitemid 350212848)
38. Pace CN, Alston RW, Shaw KL (2000) Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci 9(7):1395-1398. (Pubitemid 30602294)
39. Zhou H-X (2002) A Gaussian-chain model for treating residual charge-charge interactions in the unfolded state of proteins. Proc Natl Acad Sci USA 99(6):3569-3574.
40. Kundrotas PJ, Karshikoff A (2002) Modeling of denatured state for calculation of the electrostatic contribution to protein stability. Protein Sci 11(7):1681-1686. (Pubitemid 34663547)
41. Guzman-Casado M, Parody-Morreale A, Robic S, Marqusee S, Sanchez-Ruiz JM (2003) Energetic evidence for formation of a pH-dependent hydrophobic cluster in the denatured state of Thermus thermophilus ribonuclease H. J Mol Biol 329(4):731-743. (Pubitemid 36629367)
42. Whitten ST, García-Moreno E B (2000) pH dependence of stability of staphylococcal nuclease: Evidence of substantial electrostatic interactions in the denatured state. Biochemistry 39(46):14292-14304.
43. Cho JH, Raleigh DP (2005) Mutational analysis demonstrates that specific electrostatic interactions can play a key role in the denatured state ensemble of proteins. J Mol Biol 353(1):174-185.
44. Brooks BR, et al. (2009) CHARMM: The biomolecular simulation program. J Comput Chem 30(10):1545-1614.
45. MacKerell A, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102(18):3586-3616.
46. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26(16):1781-1802. (Pubitemid 43078511)
47. Nina M, Beglov D, Roux B (1997) Atomic radii for continuum electrostatics calculations based on molecular dynamics free energy simulations. J Phys Chem B 101(26):5239-5248. (Pubitemid 127609289)
48. Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14(1):27-28, 33-38.