Outward-facing conformers of LacY stabilized by nanobodies

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 52, 2014, Pages 18548-18553

  Smirnova, Irina ^a   Kasho, Vladimir ^a   Jiang, Xiaoxu ^a   Pardon, Els ^b,c   Steyaert, Jan ^b,c   Kaback, H Ronald ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Fluorescence; Major facilitator superfamily; Membrane transport proteins

Indexed keywords

EPITOPE; LACTOSE PERMEASE; NANOBODY; PROTEOLIPOSOME; SUGAR; COTRANSPORTER; ESCHERICHIA COLI PROTEIN; GLUCOSE TRANSPORTER; LACTOSE; LACY PROTEIN, E COLI; MULTIPROTEIN COMPLEX; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; COMPLEMENTARITY DETERMINING REGION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME CONFORMATION; ENZYME STABILITY; ESCHERICHIA COLI; FLOW KINETICS; FLUOROMETRY; MEMBRANE VESICLE; MICELLE; NONHUMAN; PRIORITY JOURNAL; SPHEROPLAST; ACTIVE TRANSPORT; CHEMISTRY; CYTOPLASM; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN STABILITY;

CAMELIDAE; ESCHERICHIA COLI;

BIOLOGICAL TRANSPORT, ACTIVE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LACTOSE; MONOSACCHARIDE TRANSPORT PROTEINS; MULTIPROTEIN COMPLEXES; MUTATION; PERIPLASM; PROTEIN BINDING; PROTEIN STABILITY; SYMPORTERS;

EID: 84924299914     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422265112     Document Type: Article

References (41)

1. Saier MH, Jr (2000) Families of transmembrane sugar transport proteins. Mol Microbiol 35(4):699-710.
2. Guan L, Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35:67-91.
3. Madej MG, Kaback HR (2014) The life and times of Lac permease: Crystals ain't enough, but they certainly do help. Membrane Transporter Function: To Structure and Beyond, eds Ziegler C, Kraemer R, Springer Series in Biophysics: Transporters (Springer Heidelberg, Germany) Vol 17, pp 121-158.
4. Smirnova I, Kasho V, Kaback HR (2011) Lactose permease and the alternating access mechanism. Biochemistry 50(45):9684-9693.
5. Kaback HR, Smirnova I, Kasho V, Nie Y, Zhou Y (2011) The alternating access transport mechanism in LacY. J Membr Biol 239(1-2):85-93.
6. Smirnova I, et al. (2007) Sugar binding induces an outward facing conformation of LacY. Proc Natl Acad Sci USA 104(42):16504-16509.
7. Madej MG, Soro SN, Kaback HR (2012) Apo-intermediate in the transport cycle of lactose permease (LacY). Proc Natl Acad Sci USA 109(44):E2970-E2978.
8. Abramson J, et al. (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301(5633):610-615.
9. Mirza O, Guan L, Verner G, Iwata S, Kaback HR (2006) Structural evidence for induced fit and a mechanism for sugar/H+ symport in LacY. EMBO J 25(6):1177-1183.
10. Guan L, Mirza O, Verner G, Iwata S, Kaback HR (2007) Structural determination of wild-type lactose permease. Proc Natl Acad Sci USA 104(39):15294-15298.
11. Chaptal V, et al. (2011) Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition. Proc Natl Acad Sci USA 108(23):9361-9366.
12. Majumdar DS, et al. (2007) Single-molecule FRET reveals sugar-induced conformational dynamics in LacY. Proc Natl Acad Sci USA 104(31):12640-12645.
13. Kaback HR, et al. (2007) Site-directed alkylation and the alternating access model for LacY. Proc Natl Acad Sci USA 104(2):491-494.
14. Zhou Y, Guan L, Freites JA, Kaback HR (2008) Opening and closing of the periplasmic gate in lactose permease. Proc Natl Acad Sci USA 105(10):3774-3778.
15. Smirnova I, Kasho V, Sugihara J, Kaback HR (2009) Probing of the rates of alternating access in LacY with Trp fluorescence. Proc Natl Acad Sci USA 106(51):21561-21566.
16. Nie Y, Kaback HR (2010) Sugar binding induces the same global conformational change in purified LacY as in the native bacterial membrane. Proc Natl Acad Sci USA 107(21):9903-9908.
17. Kumar H, et al. (2014) Structure of sugar-bound LacY. Proc Natl Acad Sci USA 111(5):1784-1788.
18. Smirnova I, Kasho V, Sugihara J, Kaback HR (2011) Opening the periplasmic cavity in lactose permease is the limiting step for sugar binding. Proc Natl Acad Sci USA 108(37):15147-15151.
19. Smirnova I, Kasho V, Kaback HR (2014) Real-time conformational changes in LacY. Proc Natl Acad Sci USA 111(23):8440-8445.
20. Smirnova I, Kasho V, Sugihara J, Kaback HR (2013) Trp replacements for tightly interacting Gly-Gly pairs in LacY stabilize an outward-facing conformation. Proc Natl Acad Sci USA 110(22):8876-8881.
21. Fersht A (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (W. H. Freeman, New York), pp xxi, 631 pp.
22. Viitanen P, Garcia ML, Kaback HR (1984) Purified reconstituted lac carrier protein from Escherichia coli is fully functional. Proc Natl Acad Sci USA 81(6):1629-1633.
23. Rasmussen SG, et al. (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 477(7366):549-555.
24. Steyaert J, Kobilka BK (2011) Nanobody stabilization of G protein-coupled receptor conformational states. Curr Opin Struct Biol 21(4):567-572.
25. Muyldermans S (2013) Nanobodies: Natural single-domain antibodies. Annu Rev Biochem 82:775-797.
26. Ring AM, et al. (2013) Adrenaline-activated structure of β2-adrenoceptor stabilized by an engineered nanobody. Nature 502(7472):575-579.
27. Staus DP, et al. (2014) Regulation of β2-adrenergic receptor function by conformationally selective single-domain intrabodies. Mol Pharmacol 85(3):472-481.
28. Pardon E, et al. (2014) A general protocol for the generation of nanobodies for structural biology. Nat Protoc 9(3):674-693.
29. Herzlinger D, Viitanen P, Carrasco N, Kaback HR (1984) Monoclonal antibodies against the lac carrier protein from Escherichia coli. 2. Binding studies with membrane vesicles and proteoliposomes reconstituted with purified lac carrier protein. Biochemistry 23(16):3688-3693.
30. Kaback HR (1971) Bacterial membranes. Methods in Enzymology, eds Kaplan NP, Jakoby WB, Colowick NP (Elsevier, New York), Vol XXII, pp 99-120.
31. Short SA, et al. (1974) Determination of the absolute number of Escherichia coli membrane vesicles that catalyze active transport. Proc Natl Acad Sci USA 71(12):5032-5036.
32. Owen P, Kaback HR (1978) Molecular structure of membrane vesicles from Escherichia coli. Proc Natl Acad Sci USA 75(7):3148-3152.
33. Owen P, Kaback HR (1979) Antigenic architecture of membrane vesicles from Escherichia coli. Biochemistry 18(8):1422-1426.
34. Owen P, Kaback HR (1979) Immunochemical analysis of membrane vesicles from Escherichia coli. Biochemistry 18(8):1413-1422.
35. Wu J, Kaback HR (1994) Cysteine 148 in the lactose permease of Escherichia coli is a component of a substrate binding site. 2. Site-directed fluorescence studies. Biochemistry 33(40):12166-12171.
36. He MM, Kaback HR (1997) Interaction between residues Glu269 (helix VIII) and His322 (helix X) of the lactose permease of Escherichia coli is essential for substrate binding. Biochemistry 36(44):13688-13692.
37. Mansoor SE, Farrens DL (2004) High-throughput protein structural analysis using site-directed fluorescence labeling and the bimane derivative (2-pyridyl)dithiobimane. Biochemistry 43(29):9426-9438.
38. Mansoor SE, Dewitt MA, Farrens DL (2010) Distance mapping in proteins using fluorescence spectroscopy: The tryptophan-induced quenching (TrIQ) method. Biochemistry 49(45):9722-9731.
39. Smirnova IN, Kasho V, Kaback HR (2008) Protonation and sugar binding to LacY. Proc Natl Acad Sci USA 105(26):8896-8901.
40. BiasiniM, et al. (2014) SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42(Web Server issue):W252-W258.
41. Guex N, Peitsch MC, Schwede T (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective. Electrophoresis 30(Suppl 1):S162-S173.