Stress sensor triggers conformational response of the integral membrane protein microsomal glutathione transferase 1

Biochemistry

Volumn 43, Issue 35, 2004, Pages 11145-11152

  Busenlehner, Laura S ^a   Codreanu, Simona G ^a   Holm, Peter J ^b   Bhakat, Priyaranjan ^b   Hebert, Hans ^b   Morgenstern, Ralf ^b   Armstrong, Richard N ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC ACTIVATION; OXIDATIVE STRESS;

ACTIVATION ENERGY; CATALYSIS; OXIDATION;

PROTEINS;

CYSTEINE; GLUTATHIONE TRANSFERASE; INTEGRAL MEMBRANE PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ALKYLATION; ANIMAL CELL; ARTICLE; BINDING SITE; CATALYSIS; CHEMICAL MODIFICATION; CHEMICAL REACTION KINETICS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ANALYSIS; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; RAT; SENSOR;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DEUTERIUM EXCHANGE MEASUREMENT; ETHYLMALEIMIDE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; KINETICS; MALE; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICROSOMES, LIVER; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEOLIPIDS; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA;

EID: 4444316044     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048716k     Document Type: Article

References (33)

1. Jakobsson, P.-J., Morgenstern, R., Mancini, J., Ford-Hutchinson, A., and Persson, B. (1999) Common structural features of MAPEG-A widespread superfamily of membrane associated proteins in eicosanoid and glutathione metabolism, Protein Sci. 8, 689-692.
2. Mosialou, E., Piemonte, F., Andersson, C., Vos, R. M. E., van Bladeren, P. J., and Morgenstern, R. (1995) Microsomal glutathione transferase: Lipid-Derived Substrates and Lipid Dependence, Arch. Biochem. Biophys. 320, 210-216.
3. Kelner, M. J., Bagnell, R. D., Montoya, M. A., Estes, L. A., Forsberg, L., and Morgenstern, R. (2000) Structural organization of the microsomal glutathione S-transferase gene (MGST1) on chromosome 12p13.1-13.2. Identification of the correct promoter region and demonstration of transcriptional regulation in response to oxidative stress, J. Biol. Chem. 275 13000-13006.
4. Svensson, R., Rinaldi, R., Swedmark, S., and Morgenstern, R. (2000) Reactivity of cysteine-49 and its influence on the activation of microsomal glutathione transferase 1: Evidence for subunit interaction, Biochemistry 39, 15144-15149.
5. Sun, T.-H., and Morgenstern, R. (1997) Binding of glutathione and ah an inhibitor to microsomal glutathione transferase, Biochem. J. 326, 193-196.
6. Morgenstern, R., Svensson, R. Bernat, B. A., and Armstrong, R. N. (2001) Kinetic analysis of the slow ionization of glutathione by microsomal glutathione transferase MGST1, Biochemistry 40, 3378-3384.
7. Lengqvist, J., Svensson, R., Evergren, E., Morgenstern, R., and Griffiths, W. J. (2004) Observation of an Intact Noncovalent Homotrimer of Detergent-solubilized Rat Microsomal Glutathione Transferase-1 by Electrospray Mass Spectrometry, J. Biol. Chem. 279, 13311-13316.
8. Svensson, R., Ålander, J., Armstrong, R. N., and Morgenstern, R. (2004) Kinetic characterization of thiolate anion formation and chemical catalysis of activated microsomal glutathione transferase 1, Biochemistry 43, 8869-8877.
9. Schmidt-Krey, I., Mitsuoka, K., Hirai, T., Murata, K., Cheng, Y., Fujiyoshi, Y., Morgenstern, R., and Hebert, H. (2000) The three-dimensional map of microsomal glutathione transferase 1 at 6 Å resolution, EMBO J. 19, 6311-6316.
10. Holm, P. J., Morgenstern, R., and Hebert, H. (2002) The 3-D structure of microsomal glutathione transferase 1 at 6 Å resolution as determined by electron crystallography of p22121 crystals, Biochim. Biophys. Acta 1594, 276-285.
11. Englander, J. J., Rogero, J. R., and Englander, S. W. (1985) Protein hydrogen exchange studied by the fragment separation method, Anal. Biochem. 147, 234-244.
12. Zhang, Z., and Smith, D. L. (1993) Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation, Protein Sci. 2, 522-531.
13. Johnson, R. S., and Walsh, K. A. (1994) Mass spectrometric measurement of protein amide hydrogen exchange rates of apo- and holo-myoglobin, Protein Sci. 3, 2411-2418.
14. Hoofnagle, A. N., Resing, K. A., and Ahn, N. G. (2003) Protein analysis by hydrogen exchange mass spectrometry, Annu. Rev. Biophys. Biomol. Struct. 32, 1-25.
15. Demmers, J. A. A., van Duijn, E., Haverkamp, J., Greathouse, D. V., Koeppe, R. E., 2nd, Heck, A. J., and Killian, J. A. (2001) Interfacial positioning and stability of transmembrane peptides in lipid bilayers studied by combining hydrogen/deuterium exchange and mass spectrometry, J. Biol. Chem. 276, 34501-34508.
16. Morgenstern, R., Guthenberg, C., and Depierre, J. W. (1982) Microsomal glutathione S-transferase. Purification, initial characterization and demonstration that it is not identical to the cytosolic glutathione S-transferases A, B and C, Eur. J. Biochem. 128, 243-248.
17. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman's reagent, Methods Enzymol. 91, 49-60.
18. Schmidt-Krey, I., Lundqvist, G., Morgenstern, R., and Hebert, H. (1998) Parameters for the Two-Dimensional Crystallization of the Membrane Protein Microsomal Glutathione Transferase, J. Struct. Biol. 123, 87-96.
19. Hebert. H., Schmidt-Krey, I., and Morgenstern, R. (1995) The projection structure of microsomal glutathione transferase, EMBO J. 14, 3864-3869.
20. Schmidt-Krey, I., Murata, K., Hirai, T., Mitsuoka, K., Cheng, Y., Morgenstern, R., Fujiyoshi, Y., and Hebert, H. (1999) The projection structure of the membrane protein microsomal glutathione transferase at 3 Å resolution as determined from two-dimensional hexagonal crystals, J. Mol. Biol. 288, 243-253.
21. Henderson, R., Baldwin, J. M., Downing, K. H., Lepault, J., and Zemlin, F. (1986) Structure of purple membrane from halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution, Ultramicroscopy 19, 147-178.
22. Fujiyoshi, Y., Mizusaki, T., Morikawa, K., Yamagishi, H., Aoki, Y., Kihara, H., and Harada, Y. (1991) Development of a superfluid helium stage for high-resolution electron microscopy, Ultramicroscopy 38, 241-251.
23. Wilkins, M. R., Lindskog, I., Gasteiger, E., Bairoch, A., Sanchez, J. C., Hochstrasser, D. F., and Appel, R. D. (1997) Detailed peptide characterization using PEPTIDEMASS - a World-Wide-Web-accessible tool, Electrophoresis 18, 403-408.
24. Clauser K. R., Baker, P. R., and Burlingame, A. L. (1999) Role of accurate mass measurement (±10 ppm) in protein identification strategies employing MS or MS/MS and database searching, Anal. Chem. 71, 2871-2882.
25. Morgenstern, R., and DePierre, J. W. (1983) Microsomal glutathione transferase. Purification in unactivated form and further characterization of the activation process, substrate specificity and amino acid composition, Eur. J. Biochem. 134, 591-597.
26. Codreanu, S. G., Ladner, J. E., Xiao, G., Stourman, N. V., Hachey, D. L., Gilliland, G. L., and Armstrong, R. N. (2002) Local protein dynamics and catalysis: detection of segmental motion associated with rate-limiting product release by a glutathione transferase, Biochemistry 41, 15161-15172.
27. Zhang, Z., and Marshall, A. G. (1998) A universal algorithm for fast and automated charge state deconvolution of electrospray mass-to-charge ratio spectra, J. Am. Soc. Mass. Spectrom. 9, 225-233.
28. Henderson, R., Baldwin, J. M., Downing, K. H., Lepault, J., and Zemlin, F. (1986) Structure of purple membrane from halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution, Ultramicroscopy 19, 147-178.
29. Collaborative Computational Project, Number 4 (1994) The CCP4 Suite: Programs for Protein Crystallography, Acta Crystallogr. D50, 760-763.
30. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
31. Harris, M., and Jones, T. A. (2001) Molray - A web interface between O and the POV-Ray ray tracer, Acta Crystallogr. D57, 1201-1203.
32. Persistence of Vision Raytracer, http://www.povray.org.
33. Liu, W., Eilers, M., Patel, A. B., and Smith, S. O. (2004) Helix packing moments reveal diversity and conservation in membrane protein structure, J. Mol. Biol. 337, 713-729.