Asymmetry in the homodimeric ABC transporter MsbA recognized by a DARPin

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20395-20406

  Mittal, Anshumali ^a,c   Böhm, Simon ^b   Grütter, Markus G ^a   Bordignon, Enrica ^b   Seeger, Markus A ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c Life Science Zurich   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ANKYRIN; ATP BINDING; ATP HYDROLYSIS; BINDING EPITOPES; CONFORMATIONAL CHANGE; HOMODIMERS; IN-VITRO; LIPID A; MEMBRANE PROTEINS; NUCLEOTIDE-BINDING DOMAIN; ONE CHAIN; TRANSMEMBRANE DOMAIN;

ACTIVATION ANALYSIS; BIOLOGICAL MEMBRANES; CONFORMATIONS; ESCHERICHIA COLI; FACINGS; HYDROLYSIS; MAGNETIC RESONANCE; NUCLEOTIDES; PARAMAGNETISM; SUBSTRATES;

BINDING ENERGY;

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; BINDING PROTEIN; DESIGNED ANKYRIN REPEAT PROTEIN; EPITOPE; HOMODIMER; MEMBRANE PROTEIN; MSBA PROTEIN; NUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITOPE MAPPING; IN VITRO STUDY; MEMBRANE TRANSPORT; NONHUMAN; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; STOICHIOMETRY; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATE; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; LIPID A; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

ESCHERICHIA COLI; HARNESS;

EID: 84862012971     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.359794     Document Type: Article

References (51)

1. Holland, I. B. (2011) ABC transporters, mechanisms and biology: an overview. Essays Biochem. 50, 1-17
2. Zhou, Z., White, K. A., Polissi, A., Georgopoulos, C., and Raetz, C. R. (1998) Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J. Biol. Chem. 273, 12466-12475 (Pubitemid 28240620)
3. Polissi, A., and Georgopoulos, C. (1996) Mutational analysis and properties of the msbA gene of Escherichia coli, coding for an essential ABC family transporter. Mol. Microbiol. 20, 1221-1233 (Pubitemid 26225430)
4. van Veen, H. W., Venema, K., Bolhuis, H., Oussenko, I., Kok, J., Poolman, B., Driessen, A. J., and Konings, W. N. (1996) Multidrug resistance mediated by a bacterial homolog of the human multidrug transporter MDR1. Proc. Natl. Acad. Sci. U.S.A. 93, 10668-10672 (Pubitemid 26333046)
5. Aller, S. G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P. M., Trinh, Y. T., Zhang, Q., Urbatsch, I. L., and Chang, G. (2009) Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722
6. Reuter, G., Janvilisri, T., Venter, H., Shahi, S., Balakrishnan, L., and van Veen, H. W. (2003) The ATP-binding cassette multidrug transporter LmrA and lipid transporter MsbA have overlapping substrate specificities. J. Biol. Chem. 278, 35193-35198 (Pubitemid 37102284)
7. Woebking, B., Reuter, G., Shilling, R. A., Velamakanni, S., Shahi, S., Venter, H., Balakrishnan, L., and van Veen, H. W. (2005) Drug-lipid A interactions on the Escherichia coli ABC transporter MsbA. J. Bacteriol. 187, 6363-6369 (Pubitemid 41318395)
8. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 (Pubitemid 44387602)
9. Ward, A., Reyes, C. L., Yu, J., Roth, C. B., and Chang, G. (2007) Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc. Natl. Acad. Sci. U.S.A. 104, 19005-19010
10. Zou, P., Bortolus, M., and McHaourab, H. S. (2009) Conformational cycle of the ABC transporter MsbA in liposomes: detailed analysis using double electron-electron resonance spectroscopy. J. Mol. Biol. 393, 586-597
11. Smriti, Zou, P., and McHaourab, H. S. (2009) Mapping daunorubicin-binding sites in the ATP-binding cassette transporter MsbA using site-specific quenching by spin labels. J. Biol. Chem. 284, 13904-13913
12. Borbat, P. P., Surendhran, K., Bortolus, M., Zou, P., Freed, J. H., and McHaourab, H. S. (2007) Conformational motion of the ABC transporter MsbA induced by ATP hydrolysis. PLoS Biol. 5, e271
13. Zou, P., and McHaourab, H. S. (2009) Alternating access of the putative substrate-binding chamber in the ABC transporter MsbA. J. Mol. Biol. 393, 574-585
14. Doshi, R., Woebking, B., and van Veen, H. W. (2010) Dissection of the conformational cycle of the multidrug/lipidA ABC exporter MsbA. Proteins 78, 2867-2872
15. Procko, E., O'Mara, M. L., Bennett, W. F., Tieleman, D. P., and Gaudet, R. (2009) The mechanism of ABC transporters: general lessons from structural and functional studies of an antigenic peptide transporter. FASEB J. 23, 1287-1302
16. Urbatsch, I. L., Sankaran, B., Weber, J., and Senior, A. E. (1995) P-glycoprotein is stably inhibited by vanadate-induced trapping of nucleotide at a single catalytic site. J. Biol. Chem. 270, 19383-19390
17. Orelle, C., Dalmas, O., Gros, P., Di Pietro, A., and Jault, J. M. (2003) The conserved glutamate residue adjacent to the Walker-B motif is the catalytic base for ATP hydrolysis in the ATP-binding cassette transporter BmrA. J. Biol. Chem. 278, 47002-47008 (Pubitemid 37452283)
18. Senior, A. E., al-Shawi, M. K., and Urbatsch, I. L. (1995) The catalytic cycle of P-glycoprotein. FEBS Lett. 377, 285-289 (Pubitemid 26025714)
19. Zaitseva, J., Oswald, C., Jumpertz, T., Jenewein, S., Wiedenmann, A., Holland, I. B., and Schmitt, L. (2006) A structural analysis of asymmetry required for catalytic activity of an ABC-ATPase domain dimer. EMBO J. 25, 3432-3443 (Pubitemid 44141799)
20. Dawson, R. J., and Locher, K. P. (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMP-PNP. FEBS Lett. 581, 935-938 (Pubitemid 46282725)
21. Aittoniemi, J., de Wet, H., Ashcroft, F. M., and Sansom, M. S. (2010) Asymmetric switching in a homodimeric ABC transporter: a stimulation study. PLoS Comput. Biol. 6, e1000762
22. Gyimesi, G., Ramachandran, S., Kota, P., Dokholyan, N. V., Sarkadi, B., and Hegedus, T. (2011) ATP hydrolysis at one of the two sites in ABC transporters initiates transport related conformational transitions. Biochim. Biophys. Acta 1808, 2954-2964
23. Binz, H. K., Amstutz, P., Kohl, A., Stumpp, M. T., Briand, C., Forrer, P., Grütter, M. G., and Plückthun, A. (2004) High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 22, 575-582 (Pubitemid 38590636)
24. Sennhauser, G., and Grütter, M. G. (2008) Chaperone-assisted crystallography with DARPins. Structure 16, 1443-1453
25. Sennhauser, G., Amstutz, P., Briand, C., Storchenegger, O., and Grütter, M. G. (2007) Drug export pathway of multidrug exporter AcrB revealed by DARPin inhibitors. Biol. 5, e7
26. Monroe, N., Sennhauser, G., Seeger, M. A., Briand, C., and Grütter, M. G. (2011) Designed ankyrin repeat protein binders for the crystallization of AcrB: plasticity of the dominant interface. J. Struct. Biol. 174, 269-281
27. Murakami, S., Nakashima, R., Yamashita, E., Matsumoto, T., and Yamaguchi, A. (2006) Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443, 173-179 (Pubitemid 44387601)
28. Seeger, M. A., Schiefner, A., Eicher, T., Verrey, F., Diederichs, K., and Pos, K. M. (2006) Structural asymmetry of AcrB trimer suggests a peristaltic pump mechanism. Science 313, 1295-1298 (Pubitemid 44330954)
29. Huber, T., Steiner, D., Röthlisberger, D., and Plückthun, A. (2007) In vitro selection and characterization of DARPins and Fab fragments for the cocrystallization of membrane proteins: The Na(+)-citrate symporter CitS as an example. J. Struct. Biol. 159, 206-221 (Pubitemid 47095399)
30. Zahnd, C., Amstutz, P., and Plückthun, A. (2007) Ribosome display: selecting and evolving proteins in vitro that specifically bind to a target. Nat. Methods 4, 269-279 (Pubitemid 46358879)
31. Deleted in proof
32. Loo, T. W. (2001) Determining the dimensions of the drug-binding domain of human P-glycoprotein using thiol cross-linking compounds as molecular rulers. J. Biol. Chem. 276, 36877-36880
33. Venter, H., Velamakanni, S., Balakrishnan, L., and van Veen, H. W. (2008) On the energy-dependence of Hoechst 33342 transport by the ABC transporter LmrA. Biochem. Pharmacol. 75, 866-874 (Pubitemid 351174118)
34. Geertsma, E. R., Nik Mahmood, N. A., Schuurman-Wolters, G. K., and Poolman, B. (2008) Membrane reconstitution of ABC transporters and assays of translocator function. Nat. Protoc. 3, 256-266 (Pubitemid 351266510)
35. Pannier, M., Veit, S., Godt, A., Jeschke, G., and Spiess, H. W. (2000) Dead-time free measurement of dipole-dipole interactions between electron spins. J. Magn Reson 142, 331-340
36. Forrer, J., García-Rubio, I., Schuhmam, R., Tschaggelar, R., and Harmer, J. (2008) Cryogenic Q-band (35GHz) probehead featuring large excitation microwave fields for pulse and continuous wave electron paramagnetic resonance spectroscopy: performance and applications. J. Magn Reson 190, 280-291
37. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J., Timmel, C. R., Hilger, D., and Jung, H. (2006) DeerAnalysis2006 - a comprehensive software package for analyzing pulsed ELDOR data. Appl. Magn. Res. 30, 473-498
38. Polyhach, Y., Bordignon, E., and Jeschke, G. (2011) Rotamer libraries of spin labelled cysteines for protein studies. Phys. Chem. Chem. Phys. 13, 2356-2366
39. Binz, H. K., Stumpp, M. T., Forrer, P., Amstutz, P., and Plückthun, A. (2003) Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J. Mol. Biol. 332, 489-503 (Pubitemid 37020959)
40. Kohl, A., Binz, H. K., Forrer, P., Stumpp, M. T., Plückthun, A., and Grütter, M. G. (2003) Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc. Natl. Acad. Sci. U.S.A. 100, 1700-1705 (Pubitemid 36254511)
41. Eckford, P. D., and Sharom, F. J. (2008) Functional characterization of Escherichia coli MsbA: interaction with nucleotides and substrates. J. Biol. Chem. 283, 12840-12850
42. Schultz, K. M., Merten, J. A., and Klug, C. S. (2011) Characterization of the E506Q and H537A dysfunctional mutants in the E. coli ABC transporter MsbA. Biochemistry 50, 3599-3608
43. Deleted in proof
44. Jeschke, G., Sajid, M., Schulte, M., and Godt, A. (2009) Three-spin correlations in double electron-electron resonance. Phys. Chem. Chem. Phys. 11, 6580-6591
45. Alvarado, D., Klein, D. E., and Lemmon, M. A. (2010) Structural basis for negative cooperativity in growth factor binding to an EGF receptor. Cell 142, 568-579
46. Renatus, M., Stennicke, H. R., Scott, F. L., Liddington, R. C., and Salvesen, G. S. (2001) Dimer formation drives the activation of the cell death protease caspase 9. Proc. Natl. Acad. Sci. U.S.A. 98, 14250-14255 (Pubitemid 33121378)
47. Wiener, M. C. (2004) A pedestrian guide to membrane protein crystallization. Methods 34, 364-372
48. Booth, P. J. (2005) Sane in the membrane: designing systems to modulate membrane proteins. Curr. Opin. Struct. Biol. 15, 435-440
49. Ritchie, T. K., Kwon, H., and Atkins, W. M. (2011) Conformational analysis of human ATP-binding cassette transporter ABCB1 in lipid nanodiscs and inhibition by the antibodies MRK16 and UIC2. J. Biol. Chem. 286, 39489-39496
50. Koide, S. (2009) Engineering of recombinant crystallization chaperones. Curr. Opin. Struct. Biol. 19, 449-457
51. Lee, S. Y., Lee, A., Chen, J., and MacKinnon, R. (2005) Structure of the KvAP voltage-dependent K+ channel and its dependence on the lipid membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 15441-15446 (Pubitemid 41528076)