Introduction of a disulfide bond leads to stabilization and crystallization of a ricin immunogen

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 4, 2011, Pages 1048-1060

  Compton, Jaimee R ^a   Legler, Patricia M ^a   Clingan, Benjamin V ^a   Olson, Mark A ^b   Millard, Charles B ^a  

^a WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

Aggregation; Crystal packing; Protein engineering; Subunit vaccine; Toxin; Unfolding

Indexed keywords

EPITOPE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; PLANT ANTIGEN; PLANT TOXIN; RICIN; RICIN TOXIN A 1-33 44-198; UNCLASSIFIED DRUG; VACCINE;

ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISULFIDE BOND; DRUG DESIGN; DRUG STRUCTURE; MELTING POINT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN VARIANT; RICINUS COMMUNIS; SIMULATION; SITE DIRECTED MUTAGENESIS; SOLUBILITY; STOICHIOMETRY;

ANIMALS; BLOTTING, WESTERN; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; EPITOPES; HUMANS; IMMUNOGLOBULIN G; MICE; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; RICIN; TRANSITION TEMPERATURE;

EID: 79952467216     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22933     Document Type: Article

References (58)

1. Dormitzer PR, Ulmer JB, Rappuoli R. Structure-based antigen design: a strategy for next generation vaccines. Trends Biotechnol 2008; 26: 659-667.
2. Serruto D, Rappuoli R. Post-genomic vaccine development. FEBS Lett 2006; 580: 2985-2992.
3. Rinaudo CD, Telford JL, Rappuoli R, Seib KL. Vaccinology in the genome era. J Clin Invest 2009; 119: 2515-2525.
4. Daugherty PS. Protein engineering with bacterial display. Curr Opin Struct Biol 2007; 17: 474-480.
5. Georgiou G, Stathopoulos C, Daugherty PS, Nayak AR, Iverson BL, Curtiss R, III. Display of heterologous proteins on the surface of microorganisms: from the screening of combinatorial libraries to live recombinant vaccines. Nat Biotechnol 1997; 15: 29-34.
6. Kumar S, Ochoa W, Singh P, Hsu C, Schneemann A, Manchester M, Olson M, Reddy V. Tomato bushy stunt virus (TBSV), a versatile platform for polyvalent display of antigenic epitopes and vaccine design. Virology 2009; 388: 185-190.
7. Millard CB, LeClaire RD. Ricin and related toxins. In: Romano JR, Salem H, editors. Chemical warfare agents: chemistry, pharmacology, toxicology and therapeutics. Boca Raton, FL: CRC Press; 2007. pp 466.
8. Schnell R, Borchmann P, Staak JO, Schindler J, Ghetie V, Vitetta ES, Engert A. Clinical evaluation of ricin A-chain immunotoxins in patients with Hodgkin's lymphoma. Ann Oncol 2003; 14: 729-736.
9. Vitetta ES, Smallshaw JE, Coleman E, Jafri H, Foster C, Munford R, Schindler J. A pilot clinical trial of a recombinant ricin vaccine in normal humans. Proc Natl Acad Sci USA 2006; 103: 2268-2273.
10. Kende M, Del Giudice G, Rivera N, Hewetson J. Enhancement of intranasal vaccination in mice with deglycosylated chain A ricin by LTR72, a novel mucosal adjuvant. Vaccine 2006; 24: 2213-2221.
11. Griffiths GD, Bailey SC, Hambrook JL, Keyte MP. Local and systemic responses against ricin toxin promoted by toxoid or peptide vaccines alone or in liposomal formulations. Vaccine 1998; 16: 530-535.
12. Olson MA, Carra JH, Roxas-Duncan V, Wannemacher RW, Smith LA, Millard CB. Finding a new vaccine in the ricin protein fold. Protein Eng Des Sel 2004; 17: 391-397.
13. Misna D, Monzingo AF, Katzin BJ, Ernst S, Robertus JD. Structure of recombinant ricin A chain at 2.3 A. Protein Sci 1993; 2: 429-435.
14. McHugh CA, Tammariello RF, Millard CB, Carra JH. Improved stability of a protein vaccine through elimination of a partially unfolded state. Protein Sci 2004; 13: 2736-2743.
15. Olson MA, Yeh IC, Lee MS. Coarse-grained lattice model simulations of sequence-structure fitness of a ribosome-inactivating protein. Biopolymers 2008; 89: 153-159.
16. Flory PJ. Theory of elastic mechanisms of fibrous proteins. J Am Chem Soc 1956; 78: 5222-5235.
17. Matsumura M, Becktel WJ, Levitt M, Matthews BW. Stabilization of phage T4 lysozyme by engineered disulfide bonds. Proc Natl Acad Sci USA 1989; 86: 6562-6566.
18. Pace CN, Grimsley GR, Thomson JA, Barnett BJ. Conformational stability and activity of ribonuclease T1 with zero, one, and two intact disulfide bonds. J Biol Chem 1988; 263: 11820-11825.
19. Doig AJ, Williams DH. Is the hydrophobic effect stabilizing or destabilizing in proteins? The contribution of disulphide bonds to protein stability. J Mol Biol 1991; 217: 389-398.
20. Wetzel R. Harnessing disulfide bonds using protein engineering. Trends Biochem Sci 1987; 12: 478-482.
21. Betz SF. Disulfide bonds and the stability of globular proteins. Protein Sci 1993; 2: 1551-1558.
22. Siadat OR, Lougarre A, Lamouroux L, Ladurantie C, Fournier D. The effect of engineered disulfide bonds on the stability of Drosophila melanogaster acetylcholinesterase. BMC Biochem 2006; 7: 12.
23. Clarke J, Fersht AR. Engineered disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation. Biochemistry 1993; 32: 4322-4329.
24. Feig M, Karanicolas J, Brooks CL, III. MMTSB Tool Set: enhanced sampling and multiscale modeling methods for applications in structural biology. J Mol Graph Model 2004; 22: 377-395.
25. Yeh IC, Lee MS, Olson MA. Calculation of protein heat capacity from replica-exchange molecular dynamics simulations with different implicit solvent models. J Phys Chem B 2008; 112: 15064-15073.
26. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959; 82: 70-77.
27. Lemley PV, Amanatides P, Wright DC. Identification and characterization of a monoclonal antibody that neutralizes ricin toxicity in vitro and in vivo. Hybridoma 1994; 13: 417-421.
28. Mantis NJ, McGuinness CR, Sonuyi O, Edwards G, Farrant SA. Immunoglobulin A antibodies against ricin A and B subunits protect epithelial cells from ricin intoxication. Infect Immun 2006; 74: 3455-3462.
29. Neal LM, O'Hara J, Brey RN, III, Mantis NJ. A monoclonal immunoglobulin G antibody directed against an immunodominant linear epitope on the ricin A chain confers systemic and mucosal immunity to ricin. Infect Immun 2010; 78: 552-561.
30. Castelletti D, Fracasso G, Righetti S, Tridente G, Schnell R, Engert A, Colombatti M. A dominant linear B-cell epitope of ricin A-chain is the target of a neutralizing antibody response in Hodgkin's lymphoma patients treated with an anti-CD25 immunotoxin. Clin Exp Immunol 2004; 136: 365-372.
31. Navaza J. Implementation of molecular replacement in AMoRe. Acta Crystallogr D Biol Crystallogr 2001; 57: 1367-1372.
32. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994; 50: 760-763.
33. Voss NR, Gerstein M, Steitz TA, Moore PB. The geometry of the ribosomal polypeptide exit tunnel. J Mol Biol 2006; 360: 893-906.
34. Schmidt B, Hogg PJ. Search for allosteric disulfide bonds in NMR structures. BMC Struct Biol 2007; 7: 49.
35. Hazes B, Dijkstra BW. Model building of disulfide bonds in proteins with known three-dimensional structure. Protein Eng 1988; 2: 119-125.
36. Dombkowski AA. Disulfide by Design: a computational method for the rational design of disulfide bonds in proteins. Bioinformatics 2003; 19: 1852-1853.
37. Wetzel R, Perry LJ, Baase WA, Becktel WJ. Disulfide bonds and thermal stability in T4 lysozyme. Proc Natl Acad Sci USA 1988; 85: 401-405.
38. Wells JA, Powers DB. In vivo formation and stability of engineered disulfide bonds in subtilisin. J Biol Chem 1986; 261: 6564-6570.
39. Heinz DW, Matthews BW. Rapid crystallization of T4 lysozyme by intermolecular disulfide cross-linking. Protein Eng 1994; 7: 301-307.
40. Castelletti D, Colombatti M. Peptide analogues of a T-cell epitope of ricin toxin A-chain prevent agonist-mediated human T-cell response. Int Immunol 2005; 17: 365-372.
41. Matsumura M, Matthews BW. Stabilization of functional proteins by introduction of multiple disulfide bonds. Methods Enzymol 1991; 202: 336-356.
42. Chrunyk BA, Evans J, Lillquist J, Young P, Wetzel R. Inclusion body formation and protein stability in sequence variants of interleukin-1 beta. J Biol Chem 1993; 268: 18053-18061.
43. Eijsink VG, Bjork A, Gaseidnes S, Sirevag R, Synstad B, van den Burg B, Vriend G. Rational engineering of enzyme stability. J Biotechnol 2004; 113: 105-120.
44. Martensson LG, Karlsson M, Carlsson U. Dramatic stabilization of the native state of human carbonic anhydrase II by an engineered disulfide bond. Biochemistry 2002; 41: 15867-15875.
45. Ko JH, Jang WH, Kim EK, Lee HB, Park KD, Chung JH, Yoo OJ. Enhancement of thermostability and catalytic efficiency of AprP, an alkaline protease from Pseudomonas sp., by the introduction of a disulfide bond. Biochem Biophys Res Commun 1996; 221: 631-635.
46. Hagihara Y, Mine S, Uegaki K. Stabilization of an immunoglobulin fold domain by an engineered disulfide bond at the buried hydrophobic region. J Biol Chem 2007; 282: 36489-36495.
47. Reading NS, Aust SD. Engineering a disulfide bond in recombinant manganese peroxidase results in increased thermostability. Biotechnol Prog 2000; 16: 326-333.
48. Chen L, Yu C, Zhou X, Zhang Y. Rational introduction of disulfide bond to enhance optimal temperature of Lipomyces starkeyi alpha-dextranase expressed in Pichia pastoris. J Microbiol Biotechnol 2009; 19: 1506-1513.
49. Wakarchuk WW, Sung WL, Campbell RL, Cunningham A, Watson DC, Yaguchi M. Thermostabilization of the Bacillus circulans xylanase by the introduction of disulfide bonds. Protein Eng 1994; 7: 1379-1386.
50. Thornton JM. Disulphide bridges in globular proteins. J Mol Biol 1981; 151: 261-287.
51. Mitchinson C, Wells JA. Protein engineering of disulfide bonds in subtilisin BPN'. Biochemistry 1989; 28: 4807-4815.
52. Schellman JA. The stability of hydrogen-bonded peptide structures in aqueous solution. C R Trav Lab Carlsberg Chim 1955; 29: 230-259.
53. Katz BA, Kossiakoff A. The crystallographically determined structures of atypical strained disulfides engineered into subtilisin. J Biol Chem 1986; 261: 15480-15485.
54. Hinck AP, Truckses DM, Markley JL. Engineered disulfide bonds in staphylococcal nuclease: effects on the stability and conformation of the folded protein. Biochemistry 1996; 35: 10328-10338.
55. van den Burg B, Eijsink VG. Selection of mutations for increased protein stability. Curr Opin Biotechnol 2002; 13: 333-337.
56. Argent RH, Parrott AM, Day PJ, Roberts LM, Stockley PG, Lord JM, Radford SE. Ribosome-mediated folding of partially unfolded ricin A-chain. J Biol Chem 2000; 275: 9263-9269.
57. Argent RH, Roberts LM, Wales R, Robertus JD, Lord JM. Introduction of a disulfide bond into ricin A chain decreases the cytotoxicity of the ricin holotoxin. J Biol Chem 1994; 269: 26705-26710.
58. Arreguin-Espinosa R, Fenton B, Vazquez-Contreras E, Arreguin B, Garcia-Hernandez E. PFA, a novel mollusk agglutinin, is structurally related to the ribosome-inactivating protein superfamily. Arch Biochem Biophys 2001; 394: 151-155.