Rational design of a conformation-switchable Ca2+- and Tb 3+-binding protein without the use of multiple coupled metal-binding sites

FEBS Journal

Volumn 275, Issue 20, 2008, Pages 5048-5061

  Li, Shunyi ^a,b   Yang, Wei ^c   Maniccia, Anna W ^a   Barrow Jr , Doyle ^a   Tjong, Harianto ^d   Zhou, Huan Xiang ^d   Yang, Jenny J ^a,e  

^a GEORGIA STATE UNIVERSITY   (United States)

^b HUBEI UNIVERSITY   (China)

^c CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^d Florida State University   (United States)

^e NONE   (United States)

Author keywords

Ca2+ binding; Conformational change; Protein design; Tb 3+ binding; Trigger

Indexed keywords

BINDING PROTEIN; CALCIUM BINDING PROTEIN; CALCIUM ION; TERBIUM;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; METAL BINDING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; STRUCTURE ANALYSIS;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, CD2; CALCIUM; CALCIUM-BINDING PROTEINS; HYDROGEN-ION CONCENTRATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN ENGINEERING; RATS; STATIC ELECTRICITY; TERBIUM;

RATTUS;

EID: 52449105981     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06638.x     Document Type: Article

References (54)

1. Ikura M Ames JB (2006) Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality. Proc Natl Acad Sci USA 103, 1159 1164.
2. Kretsinger RH (1976) Calcium-binding proteins. Annu Rev Biochem 45, 239 266.
3. Klee CB, Crouch TH Richman PG (1980) Calmodulin. Annu Rev Biochem 49, 489 515.
4. Meador WE, Means AR Quiocho FA (1993) Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures. Science 262, 1718 1721.
5. Chou JJ, Li S, Klee CB Bax A (2001) Solution structure of Ca(2+)-calmodulin reveals flexible hand-like properties of its domains. Nat Struct Biol 8, 990 997.
6. Frederick KK, Marlow MS, Valentine KG Wand AJ (2007) Conformational entropy in molecular recognition by proteins. Nature 448, 325 329.
7. Reid RE Hodges RS (1980) Co-operativity and calcium/magnesium binding to troponin C and muscle calcium binding to parvalbumin: an hypothesis. J Theor Biol 84, 401 444.
8. Falke JJ, Drake SK, Hazard AL Peersen OB (1994) Molecular tuning of ion binding to calcium signaling proteins. Q Rev Biophys 27, 219 290.
9. Linse S Forsen S (1995) Determinants that govern high-affinity calcium binding. Adv Second Messenger Phosphoprotein Res 30, 89 151.
10. Glusker JP (1991) Structural aspects of metal liganding to functional groups in proteins. Adv Protein Chem 42, 1 76.
11. Zhou Y, Yang W, Kirberger M, Lee HW, Ayalasomayajula G Yang JJ (2006) Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins. Proteins 65, 643 655.
12. Pidcock E Moore GR (2001) Structural characteristics of protein binding sites for calcium and lanthanide ions. J Biol Inorg Chem 6, 479 489.
13. Ababou A Desjarlais JR (2001) Solvation energetics and conformational change in EF-hand proteins. Protein Sci 10, 301 312.
14. Bunick CG, Nelson MR, Mangahas S, Hunter MJ, Sheehan JH, Mizoue LS, Bunick GJ Chazin WJ (2004) Designing sequence to control protein function in an EF-hand protein. J Am Chem Soc 126, 5990 5998.
15. Batey S, Randles LG, Steward A Clarke J (2005) Cooperative folding in a multi-domain protein. J Mol Biol 349, 1045 1059.
16. Yang JJ, Gawthrop A Ye Y (2003) Obtaining site-specific calcium-binding affinities of calmodulin. Protein Pept Lett 10, 331 345.
17. Ye Y, Lee HW, Yang W, Shealy S Yang JJ (2005) Probing site-specific calmodulin calcium and lanthanide affinity by grafting. J Am Chem Soc 127, 3743 3750.
18. Yang W, Lee HW, Hellinga H Yang JJ (2002) Structural analysis, identification, and design of calcium-binding sites in proteins. Proteins 47, 344 356.
19. Yang W, Jones LM, Isley L, Ye Y, Lee HW, Wilkins A, Liu ZR, Hellinga HW, Malchow R, Ghazi M et al. (2003) Rational design of a calcium-binding protein. J Am Chem Soc 125, 6165 6171.
20. Yang W, Wilkins AL, Ye Y, Liu ZR, Li SY, Urbauer JL, Hellinga HW, Kearney A, van der Merwe PA Yang JJ (2005) Design of a calcium-binding protein with desired structure in a cell adhesion molecule. J Am Chem Soc 127, 2085 2093.
21. 2+-binding protein. Biochemistry 44, 8267 8273.
22. Jones LM, Yang W, Maniccia AW, Harrison A, van der Merwe PA Yang JJ (2008) Rational design of a novel calcium-binding site adjacent to the ligand-binding site on CD2 increases its CD48 affinity. Protein Sci 17, 439 449.
23. Maniccia AW, Yang W, Li SY, Johnson JA Yang JJ (2006) Using protein design to dissect the effect of charged residues on metal binding and protein stability. Biochemistry 45, 5848 5856.
24. Driscoll PC, Cyster JG, Campbell ID Williams AF (1991) Structure of domain 1 of rat T lymphocyte CD2 antigen. Nature 353, 762 765.
25. Jones EY, Davis SJ, Williams AF, Harlos K Stuart DI (1992) Crystal structure at 2.8 Å resolution of a soluble form of the cell adhesion molecule CD2. Nature 360, 232 239.
26. Wagner G (1995) E-cadherin: a distant member of the immunoglobulin superfamily. Science 267, 342.
27. Yang JJ, Ye Y, Carroll A, Yang W Lee HW (2001) Structural biology of the cell adhesion protein CD2: alternatively folded states and structure-function relation. Curr Protein Pept Sci 2, 1 17.
28. Honig B Nicholls A (1995) Classical electrostatics in biology and chemistry. Science 268, 1144 1149.
29. Gilli R, Lafitte D, Lopez C, Kilhoffer M, Makarov A, Briand C Haiech J (1998) Thermodynamic analysis of calcium and magnesium binding to calmodulin. Biochemistry 37, 5450 5456.
30. Reddi AR Gibney BR (2007) Role of protons in the thermodynamic contribution of a Zn(II)-Cys4 site toward metalloprotein stability. Biochemistry 46, 3745 3758.
31. Griko YV Remeta DP (1999) Energetics of solvent and ligand-induced conformational changes in alpha-lactalbumin. Protein Sci 8, 554 561.
32. Protasevich I, Ranjbar B, Lobachov V, Makarov A, Gilli R, Briand C, Lafitte D Haiech J (1997) Conformation and thermal denaturation of apocalmodulin: role of electrostatic mutations. Biochemistry 36, 2017 2024.
33. Tsalkova TN Privalov PL (1985) Thermodynamic study of domain organization in troponin C and calmodulin. J Mol Biol 181, 533 544.
34. Schulman BA, Kim PS, Dobson CM Redfield C (1997) A residue-specific NMR view of the non-cooperative unfolding of a molten globule. Nat Struct Biol 4, 630 634.
35. 2+. Biochemistry 35, 5856 5869.
36. Smallridge RS, Whiteman P, Werner JM, Campbell ID, Handford PA Downing AK (2003) Solution structure and dynamics of a calcium binding epidermal growth factor-like domain pair from the neonatal region of human fibrillin-1. J Biol Chem 278, 12199 121206.
37. Gagne SM, Tsuda S, Spyracopoulos L, Kay LE Sykes BD (1998) Backbone and methyl dynamics of the regulatory domain of troponin C: anisotropic rotational diffusion and contribution of conformational entropy to calcium affinity. J Mol Biol 278, 667 686.
38. Strickler SS, Gribenko AV, Gribenko AV, Keiffer TR, Tomlinson J, Reihle T, Loladze VV Makhatadze GI (2006) Protein stability and surface electrostatics: a charged relationship. Biochemistry 45, 2761 2766.
39. Henzl MT, Agah S Larson JD (2003) Characterization of the metal ion-binding domains from rat alpha- and beta-parvalbumins. Biochemistry 42, 3594 3607.
40. Dong F Zhou HX (2002) Electrostatic contributions to T4 lysozyme stability: solvent-exposed charges versus semi-buried salt bridges. Biophys J 83, 1341 1347.
41. Prasad A Pedigo S (2005) Calcium-dependent stability studies of domains 1 and 2 of epithelial cadherin. Biochemistry 44, 13692 13701.
42. Chen HA, Pfuhl M, McAlister MS Driscoll PC (2000) Determination of pK(a) values of carboxyl groups in the N-terminal domain of rat CD2: anomalous pK(a) of a glutamate on the ligand-binding surface. Biochemistry 39, 6814 6824.
43. Jelesarov I Bosshard HR (1999) Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J Mol Recognit 12, 3 18.
44. 2+and phospholipids. Biochemistry 43, 11727 11739.
45. 15N NMR relaxation. Biochemistry 32, 9832 9844.
46. Hofer AM Brown EM (2003) Extracellular calcium sensing and signalling. Nat Rev Mol Cell Biol 4, 530 538.
47. Kemler R, Ozawa M Ringwald M (1989) Calcium-dependent cell adhesion molecules. Curr Opin Cell Biol 1, 892 897.
48. Mizoue LS Chazin WJ (2002) Engineering and design of ligand-induced conformational change in proteins. Curr Opin Struct Biol 12, 459 463.
49. Lu Y, Berry SM Pfister TD (2001) Engineering novel metalloproteins: design of metal-binding sites into native protein scaffolds. Chem Rev 101, 3047 3080.
50. Deng H, Chen G, Yang W Yang JJ (2006) Predicting calcium-binding sites in proteins - a graph theory and geometry approach. Proteins 64, 34 42.
51. Case DA, Darden TA, Cheatham TE III., Simmerling CL, Wang J, Duke RE, Luo R, Merz KM, Pearlman DA, Crowley M et al. (2006) AMBER 9. University of California, San Francisco, CA.
52. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A Simmerling C (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712 725.
53. Madura JD, Briggs JM, Wade R, Davis ME, Luty BA, Ilin A, Antosiewicz J, Gilson MK, Bagheri B, Scott LR et al. (1995) Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian Dynamics program. Comput Phys Commun 91, 57 95.
54. Dong F, Vijayakumar M Zhou HX (2003) Comparison of calculation and experiment implicates significant electrostatic contributions to the binding stability of barnase and barstar. Biophys J 85, 49 60.