Toward chaperone-assisted crystallography: Protein engineering enhancement of crystal packing and X-ray phasing capabilities of a camelid single-domain antibody (VHH) scaffold

Protein Science

Volumn 17, Issue 7, 2008, Pages 1175-1187

  Tereshko, Valentina ^a   Uysal, Serdar ^a   Koide, Akiko ^a   Margalef, Katrina ^a   Koide, Shohei ^a   Kossiakoff, Anthony A ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Camelid single domain antibody; Crystallization; SeMet phasing; VHH; X ray diffraction; Yeast surface display

Indexed keywords

ANTIBODY; CHAPERONE; METHIONINE; RIBONUCLEASE A;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIFFRACTION; HIGH THROUGHPUT SCREENING; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANTIBODIES; CRYSTALLOGRAPHY, X-RAY; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN ENGINEERING;

CAMELIDAE;

EID: 46449122768     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.034892.108     Document Type: Article

References (48)

1. Adams, P.D., Pannu, N.S., Read, R.J., and Brunger, A.T. 1997. Cross-validated maximum likelihood enhances crystallographic simulated annealing refinement. Proc. Natl. Acad. Sci. 94: 5018-5023.
2. Barthelemy, P.A., Raab, H., Appleton, B.A., Bond, C.J., Wu, P., Wiesmann, C., and Sidhu, S.S. 2008. Comprehensive analysis of the factors contributing to the stability and solubility of autonomous human VH domains. J. Biol. Chem. 283: 3639-3654.
3. Boder, E.T. and Wittrup, K.D. 2000. Yeast surface display for directed evolution of protein expression, affinity, and stability. Methods Enzymol. 328: 430-444.
4. Bradbury, A.R.M. and Marks, J.D. 2004. Antibodies from phage antibody libraries. J. Immunol. Methods 290: 29-49.
5. Brekke, O.H. and Loset, G.A. 2003. New technologies in therapeutic antibody development. Curr. Opin. Pharmacol. 3: 544-550.
6. Cambillau, C. and Roussel, A. 1997. Turbo Frodo, version OpenGL.1. University Aix-Marseille II, Marseille, France.
7. Carson, M. 1996. Ribbons. Methods Enzymol. 277: 493-505.
8. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. D50: 760-763.
9. Dauter, Z. 2006. Current state and prospects of macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. D62: 1-11.
10. Decanniere, K., Desmyter, A., Lauwereys, M., Ghahroudi, M.A., Muyldermans, S., and Wyns, L. 1999. A single-domain antibody fragment in complex with RNaseA: Non-canonical loop structures and nanomolar affinity using two CDR loops. Struct. Fold. Des. 7: 361-370.
11. Decanniere, K., Muyldermans, S., and Wyns, L. 2000. Canonical antigen-binding loop structures in immunoglobulins: More structures, more canonical cases? J. Mol. Biol. 300: 83-91.
12. Derewenda, Z.S. 2004. Rational protein crystallization by mutational surface engineering. Structure 12: 529-535.
13. Derewenda, Z.S. and Vekilov, P.G. 2006. Entropy and surface engineering in protein crystallization. Acta Crystallogr. D Biol. Crystallogr. D62: 116-124.
14. Ding, J., Das, K., Hsiou, Y., Sarafianos, S.G., Clark Jr., A.D., Jacobo-Molina, A., Tantillo, C., Hughes, S.H., and Arnold, E. 1998. Structure and functional implications of the polymerase active site region in a complex of HIV-1 RT with a double-stranded DNA template-primer and an antibody Fab fragment at 2.8 Å resolution. J. Mol. Biol. 284: 1095-1111.
15. Fellouse, F.A., Esaki, K., Birtalan, S., Raptis, D., Cancasci, V.J., Koide, A., Jhurani, P., Vasser, M., Wiesmann, C., Kossiakoff, A.A., et al. 2007. High-throughput generation of synthetic antibodies from highly functional minimalist phage-displayed libraries. J. Mol. Biol. 373: 924-940.
16. Gassner, N.C., Baase, W.A., and Matthews, B.W. 1996. A test of the "jigsaw puzzle" model for protein folding by multiple methionine substitutions within the core of T4 lysozyme. Proc. Natl. Acad. Sci. 93: 12155-12158.
17. Gietz, R.D. and Woods, R.A. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350: 87-96.
18. Hamers-Casterman, C., Atarhouch, T., Muyldermans, S., Robinson, G., Hamers, C., Songa, E.B., Bendahman, N., and Hamers, R. 1993. Naturally occurring antibodies devoid of light chains. Nature 363: 446-448.
19. Hendrickson, W.A. 1991. Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254: 51-58.
20. Hendrickson, W.A. 1999. Maturation of MAD phasing for the determination of macromolecular structures. J. Synchrotron Radiat. 6: 845-851.
21. Hoogenboom, H.R. 2005. Selecting and screening recombinant antibody libraries. Nat. Biotechnol. 23: 1105-1116.
22. Hunte, C. and Michel, H. 2002. Crystallisation of membrane proteins mediated by antibody fragments. Curr. Opin. Struct. Biol. 12: 503-508.
23. 1-complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure 8: 669-684.
24. Huang, J., Koide, A., Nettle, K.W., Greene, G.L., and Koide, S. 2006. Conformation-specific affinity purification of proteins using engineered binding proteins: Application to the estrogen receptor. Protein Expr. Purif. 47: 348-354.
25. Iwata, S., Ostermeier, C., Ludwig, B., and Michel, H. 1995. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376: 660-669.
26. Koide, A., Tereshko, V., Uysal, S., Margalef, K., Kossiakoff, A.A., and Koide, S. 2007a. Exploring the capacity of minimalist protein interfaces: Interface energetics and affinity maturation to picomolar KD of a single-domain antibody with a flat paratope. J. Mol. Biol. 373: 941-953.
27. Koide, A., Gilbreth, R.N., Esaki, K., Tereshko, V., and Koide, S. 2007b. High-affinity single-domain binding proteins with a binary-code interface. Proc. Natl. Acad. Sci. 104: 6632-6637.
28. Koradi, R., Billeter, M., and Wuthrich, K. 1996. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14: 51-55.
29. Kovari, L.C., Momany, C., and Rossmann, M.G. 1995. The use of antibody fragments for crystallization and structure determinations. Structure 3: 1291-1293.
30. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J., and Hendrickson, W.A. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
31. Lamzin, V.S., Perrakis, A., and Wilson, K.S. 2001. The ARP/WARP suite for automated construction and refinement of protein models. In International tables for crystallography: Crystallography of biological macromolecules, Vol. F (eds. M.G. Rossmann and E. Arnold), pp. 720-722. Kluwer Academic, Dordrecht, The Netherlands.
32. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
33. Li, H., Dunn, J.J., Luft, B.J., and Lawson, C.L. 1997. Crystal structure of Lyme disease antigen outer surface protein A complexed with an Fab. Proc. Natl. Acad. Sci. 94: 3584-3589.
34. McCafferty, M.C. 1990. Immunity to Chlamydia psittaci with particular reference to sheep. Vet. Microbiol. 25: 87-99.
35. McPherson, A. 2004. Protein crystallization in the structural genomics era. J. Struct. Funct. Genomics 5: 3-12.
36. Murshudov, G.N., Vagin, A.A., and Dodson, E. 1997. Refinement of macromolecular structures by maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. D53: 240-255.
37. Muyldermans, S. 2001. Single domain camel antibodies: Current status. J. Biotechnol. 74: 277-302.
38. Ostermeier, C., Iwata, S., Ludwig, B., and Michel, H. 1995. Fv fragment-mediated crystallization of the membrane protein bacterial cytochrome c oxidase. Nat. Struct. Biol. 2: 842-846.
39. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
40. Schneider, T.R. and Sheldrick, G.M. 2002. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. D58: 1772-1779.
41. Schweizer, A., Roschitzki-Voser, H., Amstutz, P., Briand, C., Gulotti-Georgieva, M., Prenosil, E., Binz, H.K., Capitani, G., Baici, A., Plückthun, A., et al. 2007. Inhibition of caspase-2 by a designed ankyrin repeat protein: Specificity, structure, and inhibition mechanism. Structure 15: 625-636.
42. Terwilliger, T.C. 2000. Maximum likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. D56: 965-972.
43. Terwilliger, T.C. 2002. Automated main-chain model-building by template-matching and iterative fragment extension. Acta Crystallogr. D Biol. Crystallogr. D59: 34-44.
44. Terwilliger, T.C. and Berendzen, J. 1999. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. D55: 849-861.
45. Vagin, A.A. and Teplyakov, A. 1997. MOLREP: An automated program for molecular replacement. J. Appl. Crystallogr. 30: 1022-1025.
46. Venturi, M. and Hunte, C. 2003. Monoclonal antibodies for the structural analysis of the Na+/H+ antiporter NhaA from Escherichia coli. Biochim. Biophys. Acta 1610: 46-50.
47. Weiss, D.J., Watanabe, C.K., Zhong, A., Goddard, A., and Sidhu, S.S. 2000. Rapid mapping of protein functional epitopes by combinatorial alanine scanning. Proc. Natl. Acad. Sci. 97: 8950-8954.
48. Weselak, M., Patch, M.G., Selby, T.L., Knebel, G., and Stevens, R.C. 2003. Robotics for automated crystal formation and analysis. Methods Enzymol. 368: 45-76.