Nanobodies as probes for protein dynamics in vitro and in cells

Journal of Biological Chemistry

Volumn 291, Issue 8, 2016, Pages 3767-3775

  Dmitriev, Oleg Y ^a   Lutsenko, Svetlana ^b   Muyldermans, Serge ^c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CELLS; CYTOLOGY; DYNAMICS; MOLECULAR BIOLOGY; PROTEINS; STRUCTURAL DYNAMICS;

CELLULAR BEHAVIORS; CLINICAL RESEARCH; HIGH SOLUBILITY; MEMBRANE PROTEINS; PROTEIN DOMAINS; PROTEIN DYNAMICS; PROTEIN INTERACTION; RECEPTOR SIGNALING;

CELL SIGNALING;

ANTIBODY; INTRINSICALLY DISORDERED PROTEIN; MOLECULAR SCAFFOLD; NANOBODY; MEMBRANE PROTEIN; MOLECULAR PROBE;

ANTIBODY STRUCTURE; ANTIGEN BINDING; CELL FUNCTION; CELL LEVEL; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN DYNAMICS; PROTEIN INTERACTION; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; SOLUBILITY; ANIMAL; CHEMISTRY; METABOLISM; MOLECULAR PROBE; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; HUMANS; MEMBRANE PROTEINS; MOLECULAR PROBES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SINGLE-DOMAIN ANTIBODIES;

EID: 85016923945     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.679811     Document Type: Review

References (84)

1. 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
2. Broisat, A., Hernot, S., Toczek, J., De Vos, J., Riou, L. M., Martin, S., Ahmadi, M., Thielens, N, Wernery, U., Caveliers, V., Muyldermans, S., Lahoutte, T., Fagret, D., Ghezzi, C., and Devoogdt, N. (2012) Nanobodies targeting mouse/human VCAM1 for the nuclear imaging of atherosclerotic lesions. Circ. Res. 110, 927-937
3. Caussinus, E., Kanca, O., and Affolter, M. (2012) Fluorescent fusion protein knockout mediated by anti-GFP nanobody. Nat. Struct. Mol. Biol. 19, 117-121
4. Rothbauer, U., Zolghadr, K., Tillib, S., Nowak, D., Schermelleh, L., Gahl, A., Backmann, N, Conrath, K., Muyldermans, S., Cardoso, M. C., and Leonhardt, H. (2006) Targeting and tracing antigens in live cells with fluorescent nanobodies. Nat. Methods 3, 887-889
5. Pardon, E., Laeremans, T., Triest, S., Rasmussen, S. G., Wohlkönig, A., Ruf, A., Muyldermans, S., Hol, W. G., and Kobilka, B. K., and Steyaert, J. (2014) A general protocol for the generation of Nanobodies for structural biology. Nat Protoc. 9, 674-693
6. Stanfield, R. L., Dooley, H., Flajnik, M. F., and Wilson, I. A. (2004) Crystal structure of a shark single-domain antibody V region in complex with lysozyme. Science 305, 1770-1773
7. Zielonka, S., Empting, M., Grzeschik, J., Könning, D., Barelle, C. J., and Kolmar, H. (2015) Structural insights and biomedical potential of IgNAR scaffolds from sharks. MAbs 7, 15-25
8. H domains. J. Biol. Chem. 283, 3639-3654
9. Hs by a novel mutational approach. Protein Eng. Des. Sel. 19, 503-509
10. 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
11. + channel. Nature 423, 33-41
12. 2+-activated CT channel. Nature 516, 213-218
13. Banner, D. W., Gsell, B., Benz, J., Bertschinger, J., Burger, D., Brack, S., Cuppuleri, S., Debulpaep, M., Gast, A., Grabulovski, D., Hennig, M., Hilpert, H., Huber, W., Kuglstatter, A., Kusznir, E., Laeremans, T., Matile, H., Miscenic, C, Rufer, A. C, Schlatter, D., Steyaert, J., Stihle, M., Thoma, R., Weber, M., and Ruf, A. (2013) Mapping the conformational space accessible to BACE2 using surface mutants and cocrystals with Fab fragments, Fynomers and Xaperones. Acta Crystallogr. D Biol. Crystallogr. 69, 1124-1137
14. 2+ triggered S-layer assembly. Nature 487, 119-122
15. Ehrnstorfer, I. A., and Geertsma, E. R., Pardon, E., Steyaert, J., and Dutzler, R. (2014) Crystal structure of a SLC11 (NRAMP) transporter reveals the basis for transition-metal ion transport. Nat. Struct. Mol. Biol. 21, 990-996
16. Hassaine, G., Deluz, C, Grasso, L., Wyss, R., Tol, M. B., Hovius, R., Graff, A., Stahlberg, H., Tomizaki, T., Desmyter, A., Moreau, C, Li, X. D., Poitevin, F., Vogel, H., and Nury, H. (2014) X-ray structure of the mouse serotonin 5-HT3 receptor. Nature 512, 276-281
17. Korotkov, K. V., Pardon, E., Steyaert, J., and Hol, W. G. (2009) Crystal structure of the N-terminal domain of the secretin GspD from ETEC determined with the assistance of a nanobody. Structure 17, 255-265
18. Lam, A. Y., Pardon, E., Korotkov, K. V., and Hol, W. G., and Steyaert, J. (2009) Nanobody-aided structure determination of the EpsI:EpsJ pseudopilin heterodimer from Vibrio vulnificus. J. Struct. Biol. 166, 8-15
19. Park, Y. J., Pardon, E., Wu, M., Steyaert, J., and Hol, W. G. (2012) Crystal structure of a heterodimer of editosome interaction proteins in complex with two copies of a cross-reacting nanobody. Nucleic Acids Res. 40, 1828-1840
20. Pathare, G. R., Nagy, I., Śledz, P., Anderson, D. J., and Zhou, H. J., Pardon, E., Steyaert, J., Förster, F., Bracher, A., and Baumeister, W. (2014) Crystal structure of the proteasomal deubiquitylation module Rpn8-Rpn11. Proc. Natl. Acad. Sci. U.S.A. 111, 2984-2989
21. Schotte, L., Thys, B., Strauss, M., Filman, D. J., Rombaut, B., and Hogle, J. M. (2015) Characterization of poliovirus neutralization escape mutants of single-domain antibody fragments (VHHs). Antimicrob. Agents Chemother. 59, 4695-4706
22. Koromyslova, A. D., and Hansman, G. S. (2015) Nanobody binding to a conserved epitope promotes norovirus particle disassembly. J. Virol. 89, 2718-2730
23. Chaikuad, A., Keates, T., Vincke, C, Kaufholz, M., Zenn, M., Zimmermann, B., Gutiérrez, C, Zhang, R. G., Hatzos-Skintges, C, Joachimiak, A., Muyldermans, S., Herberg, F. W., Knapp, S., and Müller, S. (2014) Structure of cyclin G-associated kinase (GAK) trapped in different conformations using nanobodies. Biochem. J. 459, 59-69
24. Dreier, B., and Plückthun, A. (2012) Rapid selection of high-affinity binders using ribosome display. Methods Mol. Biol. 805, 261-286
25. Skrlec, K., Strukelj, B., and Berlec, A. (2015) Non-immunoglobulin scaffolds: a focus on their targets. Trends Biotechnol. 33, 408-418
26. Plückthun, A. (2015) Designed ankyrin repeat proteins (DARPins): binding proteins for research, diagnostics, and therapy. Annu. Rev. Pharmacol. Toxicol. 55, 489-511
27. Koide, S., Koide, A., and Lipovsek, D. (2012) Target-binding proteins based on the 10th human fibronectin type III domain (10Fn3). Methods Enzymol. 503, 135-156
28. Löfblom, J., Feldwisch, J., Tolmachev, V., Carlsson, J., Ståhl, S., and Frejd, F. Y. (2010) Affibody molecules: engineered proteins for therapeutic, diagnostic and biotechnological applications. FEBS Lett. 584, 2670-2680
29. Gebauer, M., and Skerra, A. (2012) Anticalins small engineered binding proteins based on thelipocalin scaffold. Methods Enzymol. 503, 157-188
30. Gilbreth, R. N, and Koide, S. (2012) Structural insights for engineering binding proteins based on non-antibody scaffolds. Curr. Opin. Struct. Biol. 22, 413-420
31. Sennhauser, G., and Grütter, M. G. (2008) Chaperone-assisted crystallography with DARPins. Structure 16, 1443-1453
32. Du, D., Wang, Z., James, N. R., and Voss, J. E., Klimont, E., Ohene-Agyei, T., Venter, H, Chiu, W., and Luisi, B. F. (2014) Structure of the AcrAB-TolC multidrug efflux pump. Nature 509, 512-515
33. Eicher, T., and Cha, H. J., Seeger, M. A., Brandstätter, L., El-Delik, J., Bohnert, J. A., Kern, W. V, Verrey, F., Grütter, M. G., Diederichs, K., and Pos, K. M. (2012) 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. 109, 5687-5692
34. Eicher, T., and Seeger, M. A., Anselmi, C, Zhou, W., Brandstätter, L., Verrey, F., Diederichs, K., Faraldo-Gómez, J. D., and Pos, K. M. (2014) Coupling of remote alternating-access transport mechanisms for protons and substrates in the multidrug efflux pump AcrB. Elife 3, e03145
35. +-coupled, substrate-bound MATE multidrug transporter. Proc. Natl. Acad. Sci. U.S.A. 110, 2099-2104
36. Stockbridge, R. B., Kolmakova-Partensky, L., Shane, T., Koide, A., Koide, S., Miller, C, and Newstead, S. (2015) Crystal structures of a double-barrelled fluoride ion channel. Nature 525, 548-551
37. H antibody fragment in complex with lysozyme. Nat. Struct. Biol. 3, 803-811
38. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: aprogram for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55, 29-32
39. DeLano, W. L. (2014) The PyMOL Molecular Graphics System, Version 1.7.4, Schrödinger, LLC, New York
40. De Genst, E., Silence, K., Decanniere, K., Conrath, K., Loris, R., Kinne, J., Muyldermans, S., and Wyns, L. (2006) Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. Proc. Natl. Acad. Sci. U.S.A. 103, 4586-4591
41. HH and specific mechanisms enlarge the antigen-binding repertoire. EMBO J. 19, 921-930
42. Schmitz, K. R., Bagchi, A., Roovers, R. C., van Bergen en Henegouwen, P. M., and Ferguson, K. M. (2013) Structural evaluation of EGFR inhibition mechanisms for nanobodies/VHH domains. Structure 21, 1214-1224
43. Stijlemans, B., Conrath, K., Cortez-Retamozo, V., Van Xong, H., Wyns, L., Senter, P., Revets, H., De Baetselier, P., Muyldermans, S., and Magez, S. (2004) Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies: African trypanosomes as paradigm. J. Biol. Chem. 279, 1256-1261
44. Kirchhofer, A., Helma, J., Schmidthals, K., Frauer, C., Cui, S., Karcher, A., Pellis, M., Muyldermans, S., Casas-Delucchi, C. S., Cardoso, M. C., Leonhardt, H., Hopfner, K. P., and Rothbauer, U. (2010) Modulation of protein properties in living cells using nanobodies. Nat. Struct. Mol. Biol. 17, 133-138
45. Rudolph, M. J., and Vance, D. J., Cheung, J., Franklin, M. C., Burshteyn, F., and Cassidy, M. S., Gary, E. N., Herrera, C., Shoemaker, C. B., and Mantis, N. J. (2014) Crystal structures of ricin toxin's enzymatic subunit (RTA) in complex with neutralizing and non-neutralizing single-chain antibodies. J. Mol. Biol. 426, 3057-3068
46. Even-Desrumeaux, K., Nevoltris, D., and Lavaut, M. N., Alim, K., Borg, J. P., Audebert, S., Kerfelec, B., Baty, D., and Chames, P. (2014) Masked selection: a straightforward and flexible approach for the selection of binders against specific epitopes and differentially expressed proteins by phage display. Mol. Cell. Proteomics 13, 653-665
47. van der Linden, R. H., Frenken, L. G., de Geus, B., Harmsen, M. M., Ruuls, R. C., Stok, W., de Ron, L., Wilson, S., Davis, P., and Verrips, C. T. (1999) Comparison of physical chemical properties of llama VHH antibody fragments and mouse monoclonal antibodies. Biochim. Biophys. Acta 1431, 37-46
48. Ashour, J., and Schmidt, F. I., Hanke, L., Cragnolini, J., Cavallari, M., Altenburg, A., Brewer, R., Ingram, J., Shoemaker, C., and Ploegh, H. L. (2015) Intracellular expression of camelid single-domain antibodies specific for influenza virus nucleoprotein uncovers distinct features of its nuclear localization. J. Virol. 89, 2792-2800
49. Bleck, M., and Itano, M. S., Johnson, D. S., Thomas, V.K., North, A. J., and Bieniasz, P. D., and Simon, S. M. (2014) Temporal and spatial organization of ESCRT protein recruitment during HIV-1 budding. Proc. Natl. Acad. Sci. U.S.A. 111, 12211-12216
50. Li, Z., and Theile, C. S., Chen, G. Y., Bilate, A. M., and Duarte, J. N., Avalos, A. M., Fang, T., Barberena, R., Sato, S., and Ploegh, H. L. (2015) Fluorophore-conjugated Holliday junctions for generating super-bright antibodies and antibody fragments. Angew. Chem. Int. Ed Engl. 54, 11706-11710
51. Platonova, E., and Winterflood, C. M., Junemann, A., Albrecht, D., Faix, J., and Ewers, H. (2015) Single-molecule microscopy of molecules tagged with GFP or RFP derivatives in mammalian cells using nanobody binders. Methods 88, 89-97
52. Ries, J., Kaplan, C., Platonova, E., Eghlidi, H., and Ewers, H. (2012) A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat. Methods 9, 582-584
53. Gadella, T. W., Jr., and Jovin, T. M. (1995) Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy: a stereochemical model for tyrosine kinase receptor activation. J. Cell Biol. 129, 1543-1558
54. Moriki, T., Maruyama, H., and Maruyama, I. N. (2001) Activation of preformed EGF receptor dimers by ligand-induced rotation of the transmembrane domain. J. Mol. Biol. 311, 1011-1026
55. Nevoltris, D., Lombard, B., Dupuis, E., Mathis, G., Chames, P., and Baty, D. (2015) Conformational nanobodies reveal tethered epidermal growth factor receptor involved in EGFR/ErbB2 predimers. ACS Nano. 9, 1388-1399
56. De Clercq, S., Zwaenepoel, O., Martens, E., Vandekerckhove, J., Guillabert, A., and Gettemans, J. (2013) Nanobody-induced perturbation of LFA-1/L-plastin phosphorylation impairs MTOC docking, immune synapse formation and T cell activation. Cell. Mol. Life Sci. 70, 909-922
57. Ward, A. B., Szewczyk, P., Grimard, V., Lee, C. W., Martinez, L., Doshi, R., Caya, A., Villaluz, M., Pardon, E., Cregger, C., Swartz, D. J., and Falson, P. G., Urbatsch, I. L., Govaerts, C., Steyaert, J., and Chang, G. (2013) Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain. Proc. Natl. Acad. Sci. U.S.A. 110, 13386-13391
58. 2-adrenergic G protein-coupled receptor. Science 318, 1258-1265
59. 2-adrenergic receptor function. Science 318, 1266-1273
60. Weis, W. I., and Kobilka, B. K. (2008) Structural insights into G-proteincoupled receptor activation. Curr. Opin. Struct. Biol. 18, 734-740
61. 2 adrenoceptor. Nature 469, 175-180
62. 2-adrenoceptor stabilized by an engineered nanobody. Nature 502, 575-579
63. Kruse, A. C, Ring, A. M., Manglik, A., Hu, J., Hu, K., Eitel, K., Hübner, H., Pardon, E., Valant, C, and Sexton, P. M., Christopoulos, A., Felder, C. C, Gmeiner, P., Steyaert, J., Weis, W. I., Garcia, K. C, Wess, J., and Kobilka, B. K. (2013) Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 504, 101-106
64. s protein complex. Nature 477, 549-555
65. 2-adrenergic receptor function by conformationally selective single-domain intrabodies. Mol. Pharmacol. 85, 472-481
66. Irannejad, R., Tomshine, J. C, Tomshine, J. R., Chevalier, M., and Mahoney, J. P., Steyaert, J., Rasmussen, S. G., and Sunahara, R. K., El-Samad, H., Huang, B., and von Zastrow, M. (2013) Conformational biosensors reveal GPCR signalling from endosomes. Nature 495, 534-538
67. Loris, R., Marianovsky, I., Lah, J., Laeremans, T., Engelberg-Kulka, H, Glaser, G., Muyldermans, S., and Wyns, L. (2003) Crystal structure of the intrinsically flexible addiction antidote MazE. J. Biol. Chem. 278, 28252-28257
68. Abskharon, R. N., Giachin, G., Wohlkonig, A., Soror, S. H, Pardon, E., Legname, G., and Steyaert, J. (2014) Probing the N-terminal /3-sheet conversion in the crystal structure of the human prion protein bound to a nanobody. J. Am. Chem. Soc. 136, 937-944
69. Marley, J., Lu, M., and Bracken, C. (2001) A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20, 71-75
70. De Genst E., Chan, P. H, Pardon, E., and Hsu, S. T., Kumita, J. R., Christodoulou, J., Menzer, L., and Chirgadze, D. Y., Robinson, C. V., Muyldermans, S., Matagne, A., Wyns, L., Dobson, C. M., and Dumoulin, M. (2013) A nanobody binding to non-amyloidogenic regions of the protein human lysozyme enhances partial unfolding but inhibits amyloid fibril formation. J. Phys. Chem. B 117, 13245-13258
71. De Genst, E. J., Guilliams, T., Wellens, J., and O'Day, E. M., Waudby, C. A., Meehan, S., Dumoulin, M., and Hsu, S. T., Cremades, N., Verschueren, K. H., Pardon, E., Wyns, L., Steyaert, J., Christodoulou, J., and Dobson, C. M. (2010) Structure and properties of a complex of α-synuclein and a single-domain camelid antibody. J. Mol. Biol. 402, 326-343
72. Guilliams, T., El-Turk, F., Buell, A. K., and O'Day, E. M., Aprile, F. A., Esbjörner, E. K., Vendruscolo, M., Cremades, N., Pardon, E., Wyns, L., and Welland, M. E., Steyaert, J., Christodoulou, J., Dobson, C. M., and De Genst, E. (2013) Nanobodies raised against monomeric α-synuclein distinguish between fibrils at different maturation stages. J. Mol. Biol. 425, 2397-2411
73. Oyen, D., Wechselberger, R., Srinivasan, V., Steyaert, J., and Barlow, J. N. (2013) Mechanistic analysis of allosteric and non-allosteric effects arising from nanobody binding to two epitopes of the dihydrofolate reductase of Escherichia coli. Biochim. Biophys. Acta 1834, 2147-2157
74. Lutsenko, S., and Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007) Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046
75. Hasan, N. M., and Lutsenko, S. (2012) Regulation of copper transporters in human cells. Curr. Top. Membr. 69, 137-161
76. Banci, L., Bertini, I., Cantini, F., Massagni, C, Migliardi, M., and Rosato, A. (2009) An NMR study of the interaction of the N-terminal cytoplasmic tail of the Wilson disease protein with copper(I)-HAH1. J. Biol. Chem. 284, 9354-9360
77. Huang, Y., Nokhrin, S., Hassanzadeh-Ghassabeh, G., Yu, C. H., Yang, H, Barry, A. N, Tonelli, M., and Markley, J. L., Muyldermans, S., Dmitriev, O. Y., and Lutsenko, S. (2014) Interactions between metal-binding domains modulate intracellular targeting of Cu(I)-ATPase ATP7B, as revealed by nanobody binding. J. Biol. Chem. 289, 32682-32693
78. Pufahl, R. A., and Singer, C. P., Peariso, K. L., Lin, S. J., and Schmidt, P. J., Fahrni, C. J., Culotta, V. C, Penner-Hahn, J. E., and O'Halloran, T. V. (1997) Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278, 853-856
79. Walker, J. M., Huster, D., Ralle, M., Morgan, C. T., and Blackburn, N. J., and Lutsenko, S. (2004) The N-terminal metal-binding site 2 of the Wilson's Disease Protein plays a key role in the transfer of copper from Atox1. J. Biol. Chem. 279, 15376-15384
80. Schushan, M., Bhattacharjee, A., Ben-Tal, N, and Lutsenko, S. (2012) A structural model of the copper ATPase ATP7B to facilitate analysis of Wilson disease-causing mutations and studies of the transport mechanism. Metallomics. 4, 669-678
81. Gourdon, P., and Liu, X. Y., Skjørringe, T., Morth, J. P., Møller, L. B., Pedersen, B. P., and Nissen, P. (2011) Crystal structure of a copper-transporting PIB-type ATPase. Nature 475, 59-64
82. Achila, D., Banci, L., Bertini, I., Bunce, J., Ciofi-Baffoni, S., and Huffman, D. L. (2006) Structure of human Wilson protein domains 5 and 6 and their interplay with domain 4 and the copper chaperone HAH1 in copper uptake. Proc. Natl. Acad. Sci. U.S.A. 103, 5729-5734
83. Banci, L., Bertini, I., Cantini, F., Rosenzweig, A. C, and Yatsunyk, L. A. (2008) Metal binding domains 3 and 4 of the Wilson disease protein: solution structure and interaction with the copper(I) chaperone HAH1. Biochemistry 47, 7423-7429
84. Dolgova, N. V., Nokhrin, S., Yu, C. H, George, G. N., and Dmitriev, O. Y. (2013) Copper chaperone Atox1 interacts with the metal-binding domain of Wilson's disease protein in cisplatin detoxification. Biochem. J. 454, 147-156