Time-resolved fourier transform infrared spectroscopy of the nucleotide-binding domain from the ATP-binding cassette transporter MsbA: ATP hydrolysis is the rate-limiting step in the catalytic cycle

Journal of Biological Chemistry

Volumn 287, Issue 28, 2012, Pages 23923-23931

  Syberg, Falk ^a   Suveyzdis, Yan ^a   Kötting, Carsten ^a   Gerwert, Klaus ^a   Hofmann, Eckhard ^a,b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b LS Biophysik   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APPARENT RATE CONSTANT; ATOMIC LEVELS; ATP HYDROLYSIS; ATP-BINDING CASSETTE TRANSPORTERS; CATALYTIC CYCLES; CATALYTIC SITES; CONFORMATIONAL CHANGE; COOPERATIVITY; CYTOPLASMIC MEMBRANE; GLOBAL FIT ANALYSIS; HILL COEFFICIENT; HYDROLYSIS REACTION; ISOTOPICALLY LABELED; LIPID A; MEMBRANE PROTEINS; MOLECULAR REACTIONS; MULTIDRUG RESISTANCE; NUCLEOTIDE-BINDING DOMAIN; P-GLYCOPROTEIN; RATE-LIMITING STEPS; SPATIO-TEMPORAL RESOLUTION; TIME-RESOLVED FOURIER TRANSFORM INFRARED SPECTROSCOPIES; TIME-RESOLVED FT-IR; TRANSPORT CYCLE; TRANSPORT SUBSTRATES; X-RAY STRUCTURE;

BIOCHEMISTRY; CELL MEMBRANES; ESCHERICHIA COLI; FOURIER TRANSFORM INFRARED SPECTROSCOPY; NUCLEOTIDES; RATE CONSTANTS;

HYDROLYSIS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MEMBRANE PROTEIN; MSBA PROTEIN; PHOSPHATE;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ESCHERICHIA COLI; HILL COEFFICIENT; HYDROLYSIS; INFRARED SPECTROSCOPY; ISOTOPE LABELING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE BINDING DOMAIN; NUCLEOTIDE SEQUENCE; PHYSICAL PARAMETERS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION;

ADENOSINE TRIPHOSPHATE; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; CATALYSIS; ESCHERICHIA COLI; HUMANS; HYDROLYSIS; KINETICS; OXYGEN ISOTOPES; P-GLYCOPROTEINS; PHOSPHATES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TIME FACTORS;

ESCHERICHIA COLI;

EID: 84863614150     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.359208     Document Type: Article

References (61)

1. Higgins, C. F. (1995) The ABC of channel regulation. Cell 82, 693-6962.
2. Schmitt, L., and Tampé, R. (2002) Structure and mechanism ofABC transporters. Curr. Opin. Struct. Biol. 12, 754-760
3. Davidson, A. L., Dassa, E., Orelle, C., and Chen, J. (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317-364 (Pubitemid 351822295)
4. Jones, P. M., O'Mara, M. L., and George, A. M. (2009) ABC transporters: a riddle wrapped in a mystery inside an enigma. Trends Biochem. Sci. 34, 520-531
5. Licht, A., and Schneider, E. (2011) ATP-binding cassette systems: structures, mechanisms, and functions. Cent. Eur. J. Biol. 6, 785-801
6. Kerr, I. D., Jones, P. M., and George, A. M. (2010) Multidrug efflux pumps: the structures of prokaryotic ATP-binding cassette transporter efflux pumps and implications for our understanding of eukaryotic P-glycoproteins and homologues. FEBS J. 277, 550-563
7. Sharom, F. J. (2011) The P-glycoprotein multidrug transporter. Essays Biochem. 50, 161-178
8. 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
9. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature 443, 180-185 (Pubitemid 44387602)
10. Dawson, R. J., and Locher, K. P. (2007) Structure of the multidrug ABC transporter Sav1866 from Staphylococcus aureus in complex with AMPPNP. FEBS Lett. 581, 935-938 (Pubitemid 46282725)
11. 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
12. Doerrler, W. T., Reedy, M. C., and Raetz, C. R. (2001) An Escherichia coli mutant defective in lipid export. J. Biol. Chem. 276, 11461-11464
13. Eckford, P. D., and Sharom, F. J. (2010) The reconstituted Escherichia coli MsbA protein displays lipid flippase activity. Biochem. J. 429, 195-203
14. 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)
15. Karow, M., and Georgopoulos, C. (1993) The essential Escherichia coli msbA gene, a multicopy suppressor of null mutations in the htrB gene, is related to the universally conserved family of ATP-dependent translocators. Mol. Microbiol. 7, 69-79 (Pubitemid 23011097)
16. 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
17. 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
18. Schultz, K. M., Merten, J. A., and Klug, C. S. (2011) Effects of the L511P and D512G mutations on the Escherichia coli ABC transporter MsbA. Biochemistry 50, 2594-2602
19. Westfahl, K. M., Merten, J. A., Buchaklian, A. H., and Klug, C. S. (2008) Functionally important ATP binding and hydrolysis sites in Escherichia coli MsbA. Biochemistry 47, 13878-13886
20. 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
21. Doshi, R., Woebking, B., and van Veen, H. W. (2010) Dissection of the conformational cycle of the multidrug/lipid A ABC exporter MsbA. Proteins 78, 2867-2872
22. Siarheyeva, A., and Sharom, F. J. (2009) The ABC transporter MsbA interacts with lipid A and amphipathic drugs at different sites. Biochem. J. 419, 317-328
23. Smriti, Zou, P., and Mchaourab, H. S. (2009) Mapping daunorubicin-binding sites in the ATP-binding cassette transporter MsbA using sitespecific quenching by spin labels. J. Biol. Chem. 284, 13904-13913
24. Grimard, V., Vigano, C., Margolles, A., Wattiez, R., van Veen, H. W., Konings, W. N., Ruysschaert, J. M., and Goormaghtigh, E. (2001) Structure and dynamics of the membrane-embedded domain of LmrA investigated by coupling polarized ATR-FTIR spectroscopy and 1H/2H exchange. Biochemistry 40, 11876-11886 (Pubitemid 32906049)
25. Gustot, A., Smriti, Ruysschaert, J. M., Mchaourab, H., and Govaerts, C. (2010) Lipid composition regulates the orientation of transmembrane helices in HorA, an ABC multidrug transporter. J. Biol. Chem. 285, 14144-14151
26. Gerwert, K. (1999) Molecular reaction mechanisms of proteins monitored by time-resolved FTIR spectroscopy. Biol. Chem. 380, 931-935
27. Cepus, V., Ulbrich, C., Allin, C., Troullier, A., and Gerwert, K. (1998) Fourier transform infrared photolysis studies of caged compounds. Methods Enzymol. 291, 223-245 (Pubitemid 28304424)
28. Kötting, C., Kallenbach, A., Suveyzdis, Y., Wittinghofer, A., and Gerwert, K. (2008) The GAP arginine finger movement into the catalytic site of Ras increases the activation entropy. Proc. Natl. Acad. Sci. U.S.A. 105, 6260-6265 (Pubitemid 351758334)
29. Chakrabarti, P. P., Daumke, O., Suveyzdis, Y., Kötting, C., Gerwert, K., and Wittinghofer, A. (2007) Insight into catalysis of a unique GTPase reaction by a combined biochemical and FTIR approach. J. Mol. Biol. 367, 983-995 (Pubitemid 46389620)
30. Brucker, S., Gerwert, K., and Kötting, C. (2010) Tyr-39 of Ran preserves the Ran·GTP gradient by inhibiting GTP hydrolysis. J. Mol. Biol. 401, 1-6
31. Völlmecke, C., Kötting, C., Gerwert, K., and Lübben, M. (2009) Spectroscopic investigation of the reaction mechanism of CopB-B, the catalytic fragment from an archaeal thermophilic ATP-driven heavy metal transporter. FEBS J. 276, 6172-6186
32. +-ATPase studied by infrared spectroscopy. Biophys. J. 96, 3433-3442
33. 2+-ATPase: kinetics of the high affinity calcium binding at low temperature. Biophys. J. 71, 2970-2983
34. 2+-ATPase studied by time-resolved infrared spectroscopy. Spectroscopy 22, 63-82
35. Jun, B., and Kim, S. (2010) Real-time structural transitions are coupled to chemical steps in ATP hydrolysis by Eg5 kinesin. J. Biol. Chem. 285, 11073-11077
36. Park, C. H., and Givens, R. S. (1997) New photoactivated protecting groups. 6. p-Hydroxyphenacyl: a phototrigger for chemical and biochemical probes. J. Am. Chem. Soc. 119, 2453-2463
37. Walker, J. W., Reid, G. P., McCray, J. A., and Trentham, D. R. (1988) Photolabile 1-(2-nitrophenyl)ethyl phosphate esters of adenine nucleotide analogues. Synthesis and mechanism of photolysis. J. Am. Chem. Soc. 110, 7170-7177
38. Du, X., Frei, H., and Kim, S. H. (2000) The mechanism of GTP hydrolysis by Ras probed by Fourier transform infrared spectroscopy. J. Biol. Chem. 275, 8492-8500 (Pubitemid 30180196)
39. 18O on the phosphate group. Anal. Biochem. 119, 322-324
40. Hoard, D. E., and Ott, D. G. (1965) Conversion of mono- and oligodeoxy-ribonucleotides to 5′-triphosphates. J. Am. Chem. Soc. 87, 1785-1788
41. +-ATPase from plasma membranes of Saccharomyces cerevisiae and Avena sativa roots: purification and reconstitution. Methods Enzymol. 157, 533-544
42. Hessling, B., Souvignier, G., and Gerwert, K. (1993) A model-independent approach to assigning bacteriorhodopsin's intramolecular reactions to photocycle intermediates. Biophys. J. 65, 1929-1941 (Pubitemid 23334860)
43. Benabdelhak, H., Schmitt, L., Horn, C., Jumel, K., Blight, M. A., and Holland, I. B. (2005) Positive cooperative activity and dimerization of the isolated ABC ATPase domain of HlyB from Escherichia coli. Biochem. J. 386, 489-495 (Pubitemid 40445873)
44. Janas, E. (2003) The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p. J. Biol. Chem. 278, 26862-26869
45. Nikaido, K., Liu, P. Q., and Ames, G. F. (1997) Purification and characterization of HisP, the ATP-binding subunit of a traffic ATPase (ABC transporter), the histidine permease of Salmonella typhimurium. Solubility, dimerization, and ATPase activity. J. Biol. Chem. 272, 27745-27752 (Pubitemid 27473572)
46. Gerwert, K., Souvignier, G., and Hess, B. (1990) Simultaneous monitoring of light-induced changes in protein side group protonation, chromophore isomerization, and backbone motion of bacteriorhodopsin by time-resolved Fourier transform infrared spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 87, 9774-9778 (Pubitemid 120016526)
47. Allin, C., and Gerwert, K. (2001) Ras catalyzes GTP hydrolysis by shifting negative charges from γ- to β-phosphate as revealed by time-resolved FTIR difference spectroscopy. Biochemistry 40, 3037-3046 (Pubitemid 32205346)
48. Klähn, M., Mathias, G., Kötting, C., Nonella, M., Schlitter, J., Gerwert, K., and Tavan, P. (2004) IR spectra of phosphate ions in aqueous solution: predictions of a DFT/MM approach compared with observations. J. Phys. Chem. A 108, 6186-6194
49. Rammelsberg, R., Boulas, S., Chorongiewski, H., and Gerwert, K. (1999) Set-up for time-resolved step scan FTIR spectroscopy of noncyclic reactions. Vibrational Spectroscopy 19, 143-149 (Pubitemid 129590813)
50. Kerr, I. D., Berridge, G., Linton, K. J., Higgins, C. F., and Callaghan, R. (2003) Definition of the domain boundaries is critical to the expression of the nucleotide-binding domains of P-glycoprotein. Eur. Biophys. J. 32, 644-654 (Pubitemid 37413249)
51. Doerrler, W. T., and Raetz, C. R. (2002) ATPase activity of the MsbA lipid flippase of Escherichia coli. J. Biol. Chem. 277, 36697-36705
52. Kawai, T., Caaveiro, J. M., Abe, R., Katagiri, T., and Tsumoto, K. (2011) Catalytic activity of MsbA reconstituted in nanodisc particles is modulated by remote interactions with the bilayer. FEBS Lett. 585, 3533-3537
53. 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
54. 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
55. Sauna, Z. E., Kim, I. W., Nandigama, K., Kopp, S., Chiba, P., and Ambudkar, S. V. (2007) Catalytic cycle of ATP hydrolysis by P-glycoprotein: evidence for formation of the E·S reaction intermediate with ATPγS, a non-hydrolyzable analogue of ATP. Biochemistry 46, 13787-13799 (Pubitemid 350223906)
56. 2+: vibrational study of coordination sites by use of 18O-labeled triphosphates. J. Am. Chem. Soc. 110, 392-397
57. Karpowich, N., Martsinkevich, O., Millen, L., Yuan, Y. R., Dai, P. L., MacVey, K., Thomas, P. J., and Hunt, J. F. (2001) Crystal structures of the MJ1267 ATP-binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure 9, 571-586 (Pubitemid 32695582)
58. Oswald, C., Holland, I. B., and Schmitt, L. (2006) The motor domains of ABC-transporters. What can structures tell us? Naunyn-Schmiedeberg's Arch. Pharmacol. 372, 385-399
59. 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)
60. Zaitseva, J., Jenewein, S., Wiedenmann, A., Benabdelhak, H., Holland, I. B., and Schmitt, L. (2005) Functional characterization and ATP-induced dimerization of the isolated ABC domain of the hemolysin B transporter. Biochemistry 44, 9680-9690 (Pubitemid 40994362)
61. van der Does, C., Presenti, C., Schulze, K., Dinkelaker, S., and Tampé, R. (2006) Kinetics of the ATP hydrolysis cycle of the nucleotide-binding domain of Mdl1 studied by a novel site-specific labeling technique. J. Biol. Chem. 281, 5694-5701 (Pubitemid 43847667)