New concepts and aids to facilitate crystallization

Current Opinion in Structural Biology

Volumn 23, Issue 3, 2013, Pages 409-416

  Bukowska, Magdalena A ^a   Grütter, Markus G ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; CHAPERONE; FIBRONECTIN; G PROTEIN COUPLED RECEPTOR; HYBRID PROTEIN; IMMUNOGLOBULIN F(AB) FRAGMENT; LIPOCALIN; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; NANOBODY;

BINDING SITE; COMPLEMENTARITY DETERMINING REGION; COMPLEX FORMATION; CRYSTALLIZATION; CRYSTALLOGRAPHY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN ENGINEERING; REVIEW; STRUCTURE ANALYSIS;

ANTIBODIES; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HUMANS; MOLECULAR CHAPERONES; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEINS;

EID: 84879177985     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.03.003     Document Type: Review

References (70)

1. Koide S. Engineering of recombinant crystallization chaperones. Curr Opin Struct Biol 2009, 19:49-457.
2. Sennhauser G., Grutter M.G. Chaperone-assisted crystallography with DARPins. Structure 2008, 16:1443-1453.
3. Steyaert J., Kobilka B.K. Nanobody stabilization of G protein-coupled receptor conformational states. Curr Opin Struct Biol 2011, 21:567-572.
4. Zou Y., Weis W.I., Kobilka B.K. N-terminal T4 lysozyme fusion facilitates crystallization of a G protein coupled receptor. PLoS ONE 2012, 7:e46039.
5. Krishnamurthy H., Gouaux E. X-ray structures of LeuT in substrate-free outward-open and Apo inward-open states. Nature 2012, 481:469-474.
6. + channel. Proc Natl Acad Sci U S A 2013, 110:2129-2134.
7. + ion channel. Science 2012, 335:436-441.
8. Tsukazaki T., Mori H., Fukai S., Ishitani R., Mori T., Dohmae N., Perederina A., Sugita Y., Vassylyev D.G., Ito K., Nureki O. Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 2008, 455:988-991.
9. Inaba K., Murakami S., Nakagawa A., Iida H., Kinjo M., Ito K., Suzuki M. Dynamic nature of disulphide bond formation catalysts revealed by crystal structures of DsbB. EMBO J 2009, 28:779-791.
10. +-independent amino acid transporter. Science 2009, 325:1010-1014.
11. Fang Y., Jayaram H., Shane T., Kolmakova-Partensky L., Wu F., Williams C., Xiong Y., Miller C. Structure of a prokaryotic virtual proton pump at 3.2Å resolution. Nature 2009, 460:1040-1043.
12. Hibbs R.E., Gouaux E. Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 2011, 474:54-60.
13. 2O generation by bacterial nitric oxide reductase. Science 2010, 330:1666-1670.
14. Rasmussen S.G., Choi H.J., Rosenbaum D.M., Kobilka T.S., Thian F.S., Edwards P.C., Burghammer M., Ratnala V.R., Sanishvili R., Fischetti R.F., Schertler G.F., et al. Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 2007, 450:383-387.
15. Hino T., Arakawa T., Iwanari H., Yurugi-Kobayashi T., Ikeda-Suno C., Nakada-Nakura Y., Kusano-Arai O., Weyand S., Shimamura T., Nomura N., Cameron A.D., et al. G-protein-coupled receptor inactivation by an allosteric inverse-agonist antibody. Nature 2012, 482:237-240.
16. Serriere J., Dugua J.M., Bossus M., Verrier B., Haser R., Gouet P., Guillon C. Fab'-induced folding of antigenic N-terminal peptides from intrinsically disordered HIV-1 TAT revealed by X-ray crystallography. J Mol Biol 2011, 405:33-42.
17. Skrabana R., Dvorsky R., Sevcik J., Novak M. Monoclonal antibody MN423 as a stable mold facilitates structure determination of disordered tau protein. J Struct Biol 2010, 171:74-81.
18. Wu M., Park Y.J., Pardon E., Turley S., Hayhurst A., Deng J., Steyaert J., Hol W.G. Structures of a key interaction protein from the Trypanosoma brucei editosome in complex with single domain antibodies. J Struct Biol 2011, 174:124-136.
19. Park Y.J., Pardon E., Wu M., Steyaert J., Hol W.G. Crystal structure of a heterodimer of editosome interaction proteins in complex with two copies of a cross-reacting nanobody. Nucleic Acids Res 2012, 40:1828-1840.
20. Park Y.J., Budiarto T., Wu M., Pardon E., Steyaert J., Hol W.G. The structure of the c-terminal domain of the largest editosome interaction protein and its role in promoting RNA binding by RNA-editing ligase L2. Nucleic Acids Res 2012, 40:6966-6977.
21. Domanska K., Vanderhaegen S., Srinivasan V., Pardon E., Dupeux F., Marquez J.A., Giorgetti S., Stoppini M., Wyns L., Bellotti V., Steyaert J. Atomic structure of a nanobody-trapped domain-swapped dimer of an amyloidogenic beta2-microglobulin variant. Proc Natl Acad Sci U S A 2011, 108:1314-1319.
22. 2+ triggered S-layer assembly. Nature 2012, 487:119-122.
23. Rasmussen S.G., Choi H.J., Fung J.J., Pardon E., Casarosa P., Chae P.S., Devree B.T., Rosenbaum D.M., Thian F.S., Kobilka T.S., Schnapp A., et al. Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 2011, 469:175-180.
24. Rasmussen S.G., DeVree B.T., Zou Y., Kruse A.C., Chung K.Y., Kobilka T.S., Thian F.S., Chae P.S., Pardon E., Calinski D., Mathiesen J.M., et al. Crystal structure of the beta2 adrenergic receptor-GS protein complex. Nature 2011, 477:549-555.
25. Fellouse F.A., Wiesmann C., Sidhu S.S. Synthetic antibodies from a four-amino-acid code: a dominant role for tyrosine in antigen recognition. Proc Natl Acad Sci U S A 2004, 101:12467-12472.
26. Fisher R.D., Ultsch M., Lingel A., Schaefer G., Shao L., Birtalan S., Sidhu S.S., Eigenbrot C. Structure of the complex between HER2 and an antibody paratope formed by side chains from tryptophan and serine. J Mol Biol 2010, 402:217-229.
27. Persson H., Ye W., Wernimont A., Adams J.J., Koide A., Koide S., Lam R., Sidhu S.S. CDR-H3 diversity is not required for antigen recognition by synthetic antibodies. J Mol Biol 2013, 425:803-811.
28. Koldobskaya Y., Duguid E.M., Shechner D.M., Suslov N.B., Ye J., Sidhu S.S., Bartel D.P., Koide S., Kossiakoff A.A., Piccirilli J.A. A portable RNA sequence whose recognition by a synthetic antibody facilitates structural determination. Nat Struct Mol Biol 2011, 18:100-106.
29. Ye J.D., Tereshko V., Frederiksen J.K., Koide A., Fellouse F.A., Sidhu S.S., Koide S., Kossiakoff A.A., Piccirilli J.A. Synthetic antibodies for specific recognition and crystallization of structured RNA. Proc Natl Acad Sci U S A 2008, 105:82-87.
30. Ravindran P.P., Heroux A., Ye J.D. Improvement of the crystallizability and expression of an RNA crystallization chaperone. J Biochem 2011, 150:535-543.
31. Schiefner A., Chatwell L., Korner J., Neumaier I., Colby D.W., Volkmer R., Wittrup K.D., Skerra A. A disulfide-free single-domain V(L) intrabody with blocking activity towards huntingtin reveals a novel mode of epitope recognition. J Mol Biol 2011, 414:337-355.
32. Gilbreth R.N., Koide S. Structural insights for engineering binding proteins based on non-antibody scaffolds. Curr Opin Struct Biol 2012, 22:413-420.
33. Binz H.K., Amstutz P., Kohl A., Stumpp M.T., Briand C., Forrer P., Grutter M.G., Pluckthun A. High-affinity binders selected from designed ankyrin repeat protein libraries. Nat Biotechnol 2004, 22:575-582.
34. Kummer L., Parizek P., Rube P., Millgramm B., Prinz A., Mittl P.R., Kaufholz M., Zimmermann B., Herberg F.W., Pluckthun A. Structural and functional analysis of phosphorylation-specific binders of the kinase ERK from designed ankyrin repeat protein libraries. Proc Natl Acad Sci U S A 2012, 109:E2248-E2257.
35. Grubisha O., Kaminska M., Duquerroy S., Fontan E., Cordier F., Haouz A., Raynal B., Chiaravalli J., Delepierre M., Israel A., Veron M., et al. DARPin-assisted crystallography of the CC2-LZ domain of NEMO reveals a coupling between dimerization and ubiquitin binding. J Mol Biol 2010, 395:89-104.
36. Lo Y.C., Lin S.C., Rospigliosi C.C., Conze D.B., Wu C.J., Ashwell J.D., Eliezer D., Wu H. Structural basis for recognition of diubiquitins by NEMO. Mol Cell 2009, 33:602-615.
37. Rahighi S., Ikeda F., Kawasaki M., Akutsu M., Suzuki N., Kato R., Kensche T., Uejima T., Bloor S., Komander D., Randow F., et al. Specific recognition of linear ubiquitin chains by NEMO is important for nf-kappab activation. Cell 2009, 136:1098-1109.
38. Veesler D., Dreier B., Blangy S., Lichiere J., Tremblay D., Moineau S., Spinelli S., Tegoni M., Pluckthun A., Campanacci V., Cambillau C. Crystal structure and function of a DARPin neutralizing inhibitor of lactococcal phage TP901-1: comparison of DARPin and camelid vhh binding mode. J Biol Chem 2009, 284:30718-30726.
39. Spinelli S., Desmyter A., Verrips C.T., de Haard H.J., Moineau S., Cambillau C. Lactococcal bacteriophage P2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses. Nat Struct Mol Biol 2006, 13:85-89.
40. Sennhauser G., Amstutz P., Briand C., Storchenegger O., Grutter M.G. Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. PLoS Biol 2007, 5:e7.
41. Monroe N., Sennhauser G., Seeger M.A., Briand C., Grutter M.G. Designed ankyrin repeat protein binders for the crystallization of AcrB: plasticity of the dominant interface. J Struct Biol 2011, 174:269-281.
42. Eicher T., Cha H.J., Seeger M.A., Brandstatter L., El-Delik J., Bohnert J.A., Kern W.V., Verrey F., Grutter M.G., Diederichs K., Pos K.M. Transport of drugs by the multidrug transporter AcrB involves an access and a deep binding pocket that are separated by a switch-loop. Proc Natl Acad Sci U S A 2012, 109:5687-5692.
43. Schroeder T., Barandun J., Flutsch A., Briand C., Mittl P.R., Grutter M.G. Specific inhibition of caspase-3 by a competitive DARPin: molecular mimicry between native and designed inhibitors. Structure 2013, 21:277-289.
44. Pecqueur L., Duellberg C., Dreier B., Jiang Q., Wang C., Pluckthun A., Surrey T., Gigant B., Knossow M. A designed ankyrin repeat protein selected to bind to tubulin caps the microtubule plus end. Proc Natl Acad Sci U S A 2012, 109:12011-12016.
45. Dreier B., Honegger A., Hess C., Nagy-Davidescu G., Mittl P.R., Grutter M.G., Belousova N., Mikheeva G., Krasnykh V., Pluckthun A. Development of a generic adenovirus delivery system based on structure-guided design of bispecific trimeric DARPin adapters. Proc Natl Acad Sci U S A 2013, 110:E869-E877.
46. Kim B., Eggel A., Tarchevskaya S.S., Vogel M., Prinz H., Jardetzky T.S. Accelerated disassembly of IgE-receptor complexes by a disruptive macromolecular inhibitor. Nature 2012, 491:613-617.
47. Gilbreth R.N., Truong K., Madu I., Koide A., Wojcik J.B., Li N.S., Piccirilli J.A., Chen Y., Koide S. Isoform-specific monobody inhibitors of small ubiquitin-related modifiers engineered using structure-guided library design. Proc Natl Acad Sci U S A 2011, 108:7751-7756.
48. Koide A., Wojcik J., Gilbreth R.N., Hoey R.J., Koide S. Teaching an old scaffold new tricks: monobodies constructed using alternative surfaces of the FN3 scaffold. J Mol Biol 2012, 415:393-405.
49. Wojcik J., Hantschel O., Grebien F., Kaupe I., Bennett K.L., Barkinge J., Jones R.B., Koide A., Superti-Furga G., Koide S. A potent and highly specific FN3 monobody inhibitor of the ABL SH2 domain. Nat Struct Mol Biol 2010, 17:519-527.
50. Ramamurthy V., Krystek S.R., Bush A., Wei A., Emanuel S.L., Das Gupta R., Janjua A., Cheng L., Murdock M., Abramczyk B., Cohen D., et al. Structures of adnectin/protein complexes reveal an expanded binding footprint. Structure 2012, 20:259-269.
51. Salier J.P., Akerstrom B., Borregaard N., Flower D.R. Lipocalins in bioscience: the first family gathering. Bioessays 2004, 26:456-458.
52. Schonfeld D., Matschiner G., Chatwell L., Trentmann S., Gille H., Hulsmeyer M., Brown N., Kaye P.M., Schlehuber S., Hohlbaum A.M., Skerra A. An engineered lipocalin specific for CTLA-4 reveals a combining site with structural and conformational features similar to antibodies. Proc Natl Acad Sci U S A 2009, 106:8198-8203.
53. Gebauer M., Schiefner A., Matschiner G., Skerra A. Combinatorial design of an anticalin directed against the extra-domain B for the specific targeting of oncofetal fibronectin. J Mol Biol 2013, 425:780-802.
54. Nygren P.A. Alternative binding proteins: affibody binding proteins developed from a small three-helix bundle scaffold. FEBS J 2008, 275:2668-2676.
55. Cyranka-Czaja A., Otlewski J. A novel, stable, helical scaffold as an alternative binder-construction of phage display libraries. Acta Biochim Pol 2012, 59:383-390.
56. Eigenbrot C., Ultsch M., Dubnovitsky A., Abrahmsen L., Hard T. Structural basis for high-affinity HER2 receptor binding by an engineered protein. Proc Natl Acad Sci U S A 2010, 107:15039-15044.
57. Hoyer W., Gronwall C., Jonsson A., Stahl S., Hard T. Stabilization of a beta-hairpin in monomeric Alzheimer's amyloid-beta peptide inhibits amyloid formation. Proc Natl Acad Sci U S A 2008, 105:5099-5104.
58. Hogbom M., Eklund M., Nygren P.A., Nordlund P. Structural basis for recognition by an in vitro evolved affibody. Proc Natl Acad Sci U S A 2003, 100:3191-3196.
59. Lendel C., Dogan J., Hard T. Structural basis for molecular recognition in an affibody: affibody complex. J Mol Biol 2006, 359:1293-1304.
60. Bertschinger J., Grabulovski D., Neri D. Selection of single domain binding proteins by covalent DNA display. Protein Eng Des Sel 2007, 20:57-68.
61. Grabulovski D., Kaspar M., Neri D. A novel, non-immunogenic FYN SH3-derived binding protein with tumor vascular targeting properties. J Biol Chem 2007, 282:3196-3204.
62. Schlatter D., Brack S., Banner D.W., Batey S., Benz J., Bertschinger J., Huber W., Joseph C., Rufer A., van der Klooster A., Weber M., et al. Generation, characterization and structural data of chymase binding proteins based on the human FYN kinase SH3 domain. MAbs 2012, 4:497-508.
63. Warne T., Serrano-Vega M.J., Baker J.G., Moukhametzianov R., Edwards P.C., Henderson R., Leslie A.G., Tate C.G., Schertler G.F. Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 2008, 454:486-491.
64. Tate C.G., Schertler G.F. Engineering G protein-coupled receptors to facilitate their structure determination. Curr Opin Struct Biol 2009, 19:386-395.
65. White J.F., Noinaj N., Shibata Y., Love J., Kloss B., Xu F., Gvozdenovic-Jeremic J., Shah P., Shiloach J., Tate C.G., Grisshammer R. Structure of the agonist-bound neurotensin receptor. Nature 2012, 490:508-513.
66. Cherezov V. Lipidic cubic phase technologies for membrane protein structural studies. Curr Opin Struct Biol 2011, 21:559-566.
67. Zocher M., Fung J.J., Kobilka B.K., Muller D.J. Ligand-specific interactions modulate kinetic, energetic, and mechanical properties of the human beta2 adrenergic receptor. Structure 2012, 20:1391-1402.
68. Chun E., Thompson A.A., Liu W., Roth C.B., Griffith M.T., Katritch V., Kunken J., Xu F., Cherezov V., Hanson M.A., Stevens R.C. Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure 2012, 20:967-976.
69. Kim J., Stroud R.M., Craik C.S. Rapid identification of recombinant Fabs that bind to membrane proteins. Methods 2011, 55:303-309.
70. Paduch M., Koide A., Uysal S., Rizk S.S., Koide S., Kossiakoff A.A. Generating conformation-specific synthetic antibodies to TRAP proteins in selected functional states. Methods 2013, 10.1016/j.ymeth.2012.12.010.