Fabs enable single particle cryoEM studies of small proteins

Structure

Volumn 20, Issue 4, 2012, Pages 582-592

  Wu, Shenping ^a   Avila Sakar, Agustin ^a   Kim, Jungmin ^b   Booth, David S ^a,b   Greenberg, Charles H ^a,b   Rossi, Andrea ^d   Liao, Maofu ^a   Li, Xueming ^a   Alian, Akram ^e   Griner, Sarah L ^a   Juge, Narinobu ^b   Yu, Yadong ^a   Mergel, Claudia M ^f   Chaparro Riggers, Javier ^d   Strop, Pavel ^d   Tampé, Robert ^f   Edwards, Robert H ^b,c   Stroud, Robert M ^a,c   Craik, Charles S ^b,c   Cheng, Yifan ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PFIZER INC   (United States)

^e TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^f GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; INTEGRASE; KEXIN; SUBTILISIN; VESICULAR GLUTAMATE TRANSPORTER 3;

ACCURACY; ANTIGEN BINDING; ARTICLE; COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT;

CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOGLOBULIN FAB FRAGMENTS; MODELS, MOLECULAR; MOLECULAR WEIGHT; PEPTIDE LIBRARY; PROPROTEIN CONVERTASES; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84859405812     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.02.017     Document Type: Article

References (64)

1. U. Aebi, B. ten Heggeler, L. Onorato, J. Kistler, and M.K. Showe New method for localizing proteins in periodic structures: Fab fragment labeling combined with image processing of electron micrographs Proc. Natl. Acad. Sci. USA 74 1977 5514 5518
2. A. Alian, S.L. Griner, V. Chiang, M. Tsiang, G. Jones, G. Birkus, R. Geleziunas, A.D. Leavitt, and R.M. Stroud Catalytically-active complex of HIV-1 integrase with a viral DNA substrate binds anti-integrase drugs Proc. Natl. Acad. Sci. USA 106 2009 8192 8197
3. J.P. Armache, A. Jarasch, A.M. Anger, E. Villa, T. Becker, S. Bhushan, F. Jossinet, M. Habeck, G. Dindar, and S. Franckenberg Localization of eukaryote-specific ribosomal proteins in a 5.5- cryo-EM map of the 80S eukaryotic ribosome Proc. Natl. Acad. Sci. USA 107 2010 19754 19759
4. J.C. Chan, D.E. Piper, Q. Cao, D. Liu, C. King, W. Wang, J. Tang, Q. Liu, J. Higbee, and Z. Xia A proprotein convertase subtilisin/kexin type 9 neutralizing antibody reduces serum cholesterol in mice and nonhuman primates Proc. Natl. Acad. Sci. USA 106 2009 9820 9825
5. J.C. Chen, J. Krucinski, L.J. Miercke, J.S. Finer-Moore, A.H. Tang, A.D. Leavitt, and R.M. Stroud Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding Proc. Natl. Acad. Sci. USA 97 2000 8233 8238
6. J.Z. Chen, E.C. Settembre, S.T. Aoki, X. Zhang, A.R. Bellamy, P.R. Dormitzer, S.C. Harrison, and N. Grigorieff Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM Proc. Natl. Acad. Sci. USA 106 2009 10644 10648
7. Y. Cheng, O. Zak, P. Aisen, S.C. Harrison, and T. Walz Structure of the human transferrin receptor-transferrin complex Cell 116 2004 565 576
8. Y. Cheng, E. Wolf, M. Larvie, O. Zak, P. Aisen, N. Grigorieff, S.C. Harrison, and T. Walz Single particle reconstructions of the transferrin-transferrin receptor complex obtained with different specimen preparation techniques J. Mol. Biol. 355 2006 1048 1065
9. Y. Cong, M.L. Baker, J. Jakana, D. Woolford, E.J. Miller, S. Reissmann, R.N. Kumar, A.M. Redding-Johanson, T.S. Batth, and A. Mukhopadhyay 4.0-A resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement Proc. Natl. Acad. Sci. USA 107 2010 4967 4972
10. J.F. Conway, N. Cheng, A. Zlotnick, S.J. Stahl, P.T. Wingfield, D.M. Belnap, U. Kanngiesser, M. Noah, and A.C. Steven Hepatitis B virus capsid: localization of the putative immunodominant loop (residues 78 to 83) on the capsid surface, and implications for the distinction between c and e-antigens J. Mol. Biol. 279 1998 1111 1121
11. J.F. Conway, N.R. Watts, D.M. Belnap, N. Cheng, S.J. Stahl, P.T. Wingfield, and A.C. Steven Characterization of a conformational epitope on hepatitis B virus core antigen and quasiequivalent variations in antibody binding J. Virol. 77 2003 6466 6473
12. P. Costet, M. Krempf, and B. Cariou PCSK9 and LDL cholesterol: unravelling the target to design the bullet Trends Biochem. Sci. 33 2008 426 434
13. D. Cunningham, D.E. Danley, K.F. Geoghegan, M.C. Griffor, J.L. Hawkins, T.A. Subashi, A.H. Varghese, M.J. Ammirati, J.S. Culp, and L.R. Hoth Structural and biophysical studies of PCSK9 and its mutants linked to familial hypercholesterolemia Nat. Struct. Mol. Biol. 14 2007 413 419
14. S. Duriseti, D.H. Goetz, D.R. Hostetter, A.M. LeBeau, Y. Wei, and C.S. Craik Antagonistic anti-urokinase plasminogen activator receptor (uPAR) antibodies significantly inhibit uPAR-mediated cellular signaling and migration J. Biol. Chem. 285 2010 26878 26888
15. F.A. Fellouse, K. Esaki, S. Birtalan, D. Raptis, V.J. Cancasci, A. Koide, P. Jhurani, M. Vasser, C. Wiesmann, and A.A. Kossiakoff High-throughput generation of synthetic antibodies from highly functional minimalist phage-displayed libraries J. Mol. Biol. 373 2007 924 940
16. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
17. R.M. Glaeser, D. Typke, P.C. Tiemeijer, J. Pulokas, and A. Cheng Precise beam-tilt alignment and collimation are required to minimize the phase error associated with coma in high-resolution cryo-EM J. Struct. Biol. 174 2011 1 10
18. N. Grigorieff FREALIGN: high-resolution refinement of single particle structures J. Struct. Biol. 157 2007 117 125
19. R. Henderson The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules Q. Rev. Biophys. 28 1995 171 193
20. J.D. Horton, J.C. Cohen, and H.H. Hobbs Molecular biology of PCSK9: its role in LDL metabolism Trends Biochem. Sci. 32 2007 71 77
21. J.D. Horton, J.C. Cohen, and H.H. Hobbs PCSK9: a convertase that coordinates LDL catabolism J. Lipid Res. 50 Suppl 2009 S172 S177
22. G.J. Jensen, and R.D. Kornberg Single-particle selection and alignment with heavy atom cluster-antibody conjugates Proc. Natl. Acad. Sci. USA 95 1998 9262 9267
23. Q.X. Jiang, D.N. Wang, and R. MacKinnon Electron microscopic analysis of KvAP voltage-dependent K+ channels in an open conformation Nature 430 2004 806 810
24. E. Kandiah, N.R. Watts, N. Cheng, G. Cardone, S.J. Stahl, T. Heller, T.J. Liang, P.T. Wingfield, and A.C. Steven Cryo-EM study of Hepatitis B virus core antigen capsids decorated with antibodies from a human patient J. Struct. Biol. 177 2012 145 151
25. J. Kim, R.M. Stroud, and C.S. Craik Rapid identification of recombinant Fabs that bind to membrane proteins Methods 55 2011 303 309
26. P.A. Kratz, B. Böttcher, and M. Nassal Native display of complete foreign protein domains on the surface of hepatitis B virus capsids Proc. Natl. Acad. Sci. USA 96 1999 1915 1920
27. L. Krishnan, X. Li, H.L. Naraharisetty, S. Hare, P. Cherepanov, and A. Engelman Structure-based modeling of the functional HIV-1 intasome and its inhibition Proc. Natl. Acad. Sci. USA 107 2010 15910 15915
28. G. Kukolj, and A.M. Skalka Enhanced and coordinated processing of synapsed viral DNA ends by retroviral integrases in vitro Genes Dev. 9 1995 2556 2567
29. H.J. Kwon, T.A. Lagace, M.C. McNutt, J.D. Horton, and J. Deisenhofer Molecular basis for LDL receptor recognition by PCSK9 Proc. Natl. Acad. Sci. USA 105 2008 1820 1825
30. G.Z. Lederkremer, Y. Cheng, B.M. Petre, E. Vogan, S. Springer, R. Schekman, T. Walz, and T. Kirchhausen Structure of the Sec23p/24p and Sec13p/31p complexes of COPII Proc. Natl. Acad. Sci. USA 98 2001 10704 10709
31. X. Li, N. Grigorieff, and Y. Cheng GPU-enabled FREALIGN: accelerating single particle 3D reconstruction and refinement in Fourier space on graphics processors J. Struct. Biol. 172 2010 407 412
32. H. Liang, J. Chaparro-Riggers, P. Strop, T. Geng, J.E. Sutton, D. Tsai, L. Bai, Y. Abdiche, J. Dilley, and J. Yu Proprotein convertase substilisin/kexin type 9 antagonism reduces low-density lipoprotein cholesterol in statin-treated hypercholesterolemic nonhuman primates J. Pharmacol. Exp. Ther. 340 2012 228 236
33. S. Maignan, J.P. Guilloteau, Q. Zhou-Liu, C. Clément-Mella, and V. Mikol Crystal structures of the catalytic domain of HIV-1 integrase free and complexed with its metal cofactor: high level of similarity of the active site with other viral integrases J. Mol. Biol. 282 1998 359 368
34. W.A. Marasco, and J. Sui The growth and potential of human antiviral monoclonal antibody therapeutics Nat. Biotechnol. 25 2007 1421 1434
35. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Struct. Biol. 142 2003 334 347
36. K. Murata, X. Liu, R. Danev, J. Jakana, M.F. Schmid, J. King, K. Nagayama, and W. Chiu Zernike phase contrast cryo-electron microscopy and tomography for structure determination at nanometer and subnanometer resolutions Structure 18 2010 903 912
37. T. Nakagawa, Y. Cheng, E. Ramm, M. Sheng, and T. Walz Structure and different conformational states of native AMPA receptor complexes Nature 433 2005 545 549
38. K. Newton, M.L. Matsumoto, I.E. Wertz, D.S. Kirkpatrick, J.R. Lill, J. Tan, D. Dugger, N. Gordon, S.S. Sidhu, and F.A. Fellouse Ubiquitin chain editing revealed by polyubiquitin linkage-specific antibodies Cell 134 2008 668 678
39. M. Ohi, Y. Li, Y. Cheng, and T. Walz Negative Staining and Image Classification - Powerful Tools in Modern Electron Microscopy Biol. Proced. Online 6 2004 23 34
40. P. Osenkowski, H. Li, W. Ye, D. Li, L. Aeschbach, P.C. Fraering, M.S. Wolfe, D.J. Selkoe, and H. Li Cryoelectron microscopy structure of purified gamma-secretase at 12 A resolution J. Mol. Biol. 385 2009 642 652
41. P. Penczek, N. Ban, R.A. Grassucci, R.K. Agrawal, and J. Frank Haloarcula marismortui 50S subunit-complementarity of electron microscopy and X-Ray crystallographic information J. Struct. Biol. 128 1999 44 50
42. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
43. M. Radermacher, T. Wagenknecht, A. Verschoor, and J. Frank Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli J. Microsc. 146 1987 113 136
44. S.G. Rasmussen, H.J. Choi, J.J. Fung, E. Pardon, P. Casarosa, P.S. Chae, B.T. Devree, D.M. Rosenbaum, F.S. Thian, and T.S. Kobilka Structure of a nanobody-stabilized active state of the β(2) adrenoceptor Nature 469 2011 175 180
45. G. Ren, K. Gao, F.D. Bushman, and M. Yeager Single-particle image reconstruction of a tetramer of HIV integrase bound to DNA J. Mol. Biol. 366 2007 286 294
46. P.B. Rosenthal, and R. Henderson Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy J. Mol. Biol. 333 2003 721 745
47. J. Roth The silver anniversary of gold: 25 years of the colloidal gold marker system for immunocytochemistry and histochemistry Histochem. Cell Biol. 106 1996 1 8
48. A. Saad, S.J. Ludtke, J. Jakana, F.J. Rixon, H. Tsuruta, and W. Chiu Fourier amplitude decay of electron cryomicroscopic images of single particles and effects on structure determination J. Struct. Biol. 133 2001 32 42
49. A. Savarino A historical sketch of the discovery and development of HIV-1 integrase inhibitors Expert Opin. Investig. Drugs 15 2006 1507 1522
50. T.R. Shaikh, H. Gao, W.T. Baxter, F.J. Asturias, N. Boisset, A. Leith, and J. Frank SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs Nat. Protoc. 3 2008 1941 1974
51. C.A. Sotriffer, B.M. Rode, J.M. Varga, and K.R. Liedl Elbow flexibility and ligand-induced domain rearrangements in antibody Fab NC6.8: large effects of a small hapten Biophys. J. 79 2000 614 628
52. R.L. Stanfield, A. Zemla, I.A. Wilson, and B. Rupp Antibody elbow angles are influenced by their light chain class J. Mol. Biol. 357 2006 1566 1574
53. D. Steinberg, and J.L. Witztum Inhibition of PCSK9: a powerful weapon for achieving ideal LDL cholesterol levels Proc. Natl. Acad. Sci. USA 106 2009 9546 9547
54. P.L. Stewart, C.Y. Chiu, S. Huang, T. Muir, Y. Zhao, B. Chait, P. Mathias, and G.R. Nemerow Cryo-EM visualization of an exposed RGD epitope on adenovirus that escapes antibody neutralization EMBO J. 16 1997 1189 1198
55. M.H.V. Van Regenmortel Molecular dissection of protein antigens Volume 1 1992 CRC Press Boca Raton
56. J.Y. Wang, H. Ling, W. Yang, and R. Craigie Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein EMBO J. 20 2001 7333 7343
57. M. Wolf, R.L. Garcea, N. Grigorieff, and S.C. Harrison Subunit interactions in bovine papillomavirus Proc. Natl. Acad. Sci. USA 107 2010 6298 6303
58. J.D. Ye, V. Tereshko, J.K. Frederiksen, A. Koide, F.A. Fellouse, S.S. Sidhu, S. Koide, A.A. Kossiakoff, and J.A. Piccirilli Synthetic antibodies for specific recognition and crystallization of structured RNA Proc. Natl. Acad. Sci. USA 105 2008 82 87
59. X. Yu, L. Jin, and Z.H. Zhou 3.88 A structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy Nature 453 2008 415 419
60. D.W. Zhang, T.A. Lagace, R. Garuti, Z. Zhao, M. McDonald, J.D. Horton, J.C. Cohen, and H.H. Hobbs Binding of proprotein convertase subtilisin/kexin type 9 to epidermal growth factor-like repeat A of low density lipoprotein receptor decreases receptor recycling and increases degradation J. Biol. Chem. 282 2007 18602 18612
61. X. Zhang, E. Settembre, C. Xu, P.R. Dormitzer, R. Bellamy, S.C. Harrison, and N. Grigorieff Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction Proc. Natl. Acad. Sci. USA 105 2008 1867 1872
62. X. Zhang, L. Jin, Q. Fang, W.H. Hui, and Z.H. Zhou 3.3 A cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry Cell 141 2010 472 482
63. S.Q. Zheng, J.M. Kollman, M.B. Braunfeld, J.W. Sedat, and D.A. Agard Automated acquisition of electron microscopic random conical tilt sets J. Struct. Biol. 157 2007 148 155
64. A. Zutz, J. Hoffmann, U.A. Hellmich, C. Glaubitz, B. Ludwig, B. Brutschy, and R. Tampé Asymmetric ATP hydrolysis cycle of the heterodimeric multidrug ABC transport complex TmrAB from Thermus thermophilus J. Biol. Chem. 286 2011 7104 7115