The X-ray structure of NccX from Cupriavidus metallidurans 31A illustrates potential dangers of detergent solubilization when generating and interpreting crystal structures of membrane proteins

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31160-31172

  Ziani, Widade ^a   Maillard, Antoine P ^a   Petit Härtlein, Isabelle ^a   Garnier, Norbert ^b   Crouzy, Serge ^c   Girard, Eric ^a   Covès, Jacques ^a  

^a DIF   (France)

^b UNIVERSITÉ D'ORLÉANS   (France)

^c CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; DIMERIZATION; DIMERS; HYDROPHOBICITY; MOLECULAR DYNAMICS; PROTEINS; SOLUBILITY;

CUPRIAVIDUS METALLIDURANS; FULL-LENGTH PROTEINS; HYDROPHOBIC INTERACTIONS; MOLECULAR DYNAMICS SIMULATIONS; THREE-DIMENSIONAL STRUCTURE; TRANS-MEMBRANE PROTEINS; TRANSMEMBRANE HELICES; TRANSMEMBRANE SEGMENTS;

CRYSTAL STRUCTURE;

BACTERIAL PROTEIN; DETERGENT; MEMBRANE PROTEIN; NCCX PROTEIN; UNCLASSIFIED DRUG; METALLOPROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CUPRIAVIDUS; CUPRIAVIDUS METALLIDURANS; DIMERIZATION; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; SOLUBILIZATION; STRUCTURE ANALYSIS; X RAY ANALYSIS; AMINO ACID SEQUENCE; CHEMISTRY; CRYSTALLIZATION; GENE EXPRESSION REGULATION; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; CUPRIAVIDUS; DETERGENTS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; METALLOPROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 84909979346     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.586537     Document Type: Article

References (58)

1. Mergeay, M., Nies, D., Schlegel, H. G., Gerits, J., Charles, P., and Van Gijsegem, F. (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J. Bacteriol. 162, 328-334
2. Monchy, S., Benotmane, M. A., Janssen, P., Vallaeys, T., Taghavi, S., van der Lelie, D., and Mergeay, M. (2007) Plasmids pMOL28 and pMOL30 of Cupriavidus metallidurans are specialized in the maximal viable response to heavy metals. J. Bacteriol. 189, 7417-7425
3. von Rozycki, T., and Nies, D. H. (2009) Cupriavidus metallidurans evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek 96, 115-139
4. Janssen, P. J., Van Houdt, R., Moors, H., Monsieurs, P., Morin, N., Michaux, A., Benotmane, M. A., Leys, N., Vallaeys, T., Lapidus, A., Monchy, S., Médigue, C., Taghavi, S., McCorkle, S., Dunn, J., van der Lelie, D., and Mergeay, M. (2010) The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 5, e10433
5. Nies, D. H. (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27, 313-339
6. Grass, G., Grosse, C., and Nies, D. H. (2000) Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34. J. Bacteriol. 182, 1390-1398
7. Tibazarwa, C., Wuertz, S., Mergeay, M., Wyns, L., and van Der Lelie, D. (2000) Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J. Bacteriol. 182, 1399-1409
8. Grass, G., Fricke, B., and Nies, D. H. (2005) Control of expression of a periplasmic nickel efflux pump by periplasmic nickel concentrations. Biometals 18, 437-448
9. Pompidor, G., Maillard, A. P., Girard, E., Gambarelli, S., Kahn, R., and Covès, J. (2008) X-ray structure of the metal-sensor CnrX in both the apoand copper-bound forms. FEBS Lett. 582, 3954-3958
10. Trepreau, J., Girard, E., Maillard, A. P., de Rosny, E., Petit-Haertlein, I., Kahn, R., and Covès, J. (2011) Structural basis for metal sensing by CnrX. J. Mol. Biol. 408, 766-779
11. Trepreau, J., de Rosny, E., Duboc, C., Sarret, G., Petit-Hartlein, I., Maillard, A. P., Imberty, A., Proux, O., and Covès, J. (2011) Spectroscopic characterization of the metal-binding sites in the periplasmic metal-sensor domain of CnrX from Cupriavidus metallidurans CH34. Biochemistry 50, 9036-9045
12. Trepreau, J., Grosse, C., Mouesca, J.-M., Sarret, G., Girard, E., Petit-Haertlein, I., Kuennemann, S., Desbourdes, C., de Rosny, E., Maillard, A. P., Nies, D. H., and Covès, J. (2014) Metal sensing and signal transduction by CnrX from Cupriavidus metallidurans CH34: role of the only methionine assessed by a functional, spectroscopic, and theoretical study. Metallomics 6, 263-273
13. Maillard, A. P., Girard, E., Ziani, W., Petit-Härtlein, I., Kahn, R., and Covès, J. (2014) The crystal structure of the anti-σ factor CnrY in complex with the σ factor CnrH shows a new structural class of anti-σ factors targeting extracytoplasmic function σ factors. J. Mol. Biol. 426, 2313-2327
14. Russ, W. P., and Engelman, D. M. (1999) TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. U.S.A. 96, 863-868
15. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
16. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
17. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A 64, 112-122
18. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
19. Cowtan, K. (2010) Recent developments in classical density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 470-478
20. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025
21. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
22. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O. S., Vonrhein, C., and Womack, T. O. (2011) BUSTER, Version 2.11.15, Global Phasing Ltd., Cambridge, UK
23. Karplus, P. A., and Diederichs, K. (2012) Linking crystallographic model and data quality. Science 336, 1030-1033
24. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) Graphical tools for macromolecular crystallography in PHENIX. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
25. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38
26. Brooks, B. R., Brooks, C. L., 3rd, Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: the biomolecular simulation program. J. Comput. Chem. 30, 1545-1614
27. Neria, E., Fisher, S., and Karplus, M. (1996) Simulation of activation free energies in molecular systems. J. Chem. Phys. 105, 1902-1921
28. de Jong, D. H., Singh, G., Bennett, W. F., Arnarez, C., Wassenaar, T. A., Schäfer, L. V., Periole, X., Tieleman, D. P., and Marrink, S. J. (2013) Improved parameters for the MARTINI coarse-grained protein force field. J. Chem. Theory Comput. 9, 687-697
29. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701-1718
30. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
31. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P., and de Vries, A. H. (2007) The MARTINI force field: coarse-grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812-7824
32. Monticelli, L., Kandasamy, S. K., Periole, X., Larson, R. G., Tieleman, D. P., and Marrink, S. J. (2008) The MARTINI coarse-grained force field: extension to proteins. J. Chem. Theory Comput. 4, 819-834
33. Wassenaar, T. A., Pluhackova, K., Böckmann, R. A., Marrink, S. J., and Tieleman, D. P. (2014) Going backward: a flexible geometric approach to reverse transformation from coarse grained to atomistic models. J. Chem. Theory Comput. 10, 676-690
34. Wei, P., Liu, X., Hu, M.-H., Zuo, L.-M., Kai, M., Wang, R., and Luo, S.-Z. (2011) The dimerization interface of the glycoprotein Ibβ transmembrane domain corresponds to polar residues within a leucine zipper motif. Protein Sci. 20, 1814-1823
35. Sali, A., and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
36. Chothia, C., Levitt, M., and Richardson, D. (1981) Helix to helix packing in proteins. J. Mol. Biol. 145, 215-250
37. Ma, J., Yoshimura, M., Yamashita, E., Nakagawa, A., Ito, A., and Tsukihara, T. (2004) Structure of rat monoamine oxidase A and its specific recognitions for substrates and inhibitors. J. Mol. Biol. 338, 103-114
38. Son, S. Y., Ma, J., Kondou, Y., Yoshimura, M., Yamashita, E., and Tsukihara, T. (2008) Structure of human monoamine oxidase A at 2.2 A˚ resolution: the control of opening the entry for substrates/inhibitors. Proc. Natl. Acad. Sci. U.S.A. 105, 5739-5744
39. Rodrigues, M. L., Oliveira, T. F., Pereira, I. A., and Archer, M. (2006) X-ray structure of the membrane-bound cytochrome c quinol dehydrogenase NrfH reveals novel haem coordination. EMBO J. 25, 5951-5960
40. Monk, B. C., Tomasiak, T. M., Keniya, M. V., Huschmann, F. U., Tyndall, J. D., O'Connell, J. D., 3rd, Cannon, R. D., McDonald J. G., Rodriguez, A., Finer-Moore, J. S, and Stroud, R. M. (2014) Architecture of a single membrane spanning cytochrome P450 suggests constraints that orient the catalytic domain relative to a bilayer. Proc. Natl. Acad. Sci. U.S.A. 111, 3865-3870
41. Warschawski, D. E., Arnold, A. A., Beaugrand, M., Gravel, A., Chartrand, É., and Marcotte, I. (2011) Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim. Biophys. Acta 1808, 1957-1974
42. Tulumello, D. V., and Deber, C. M. (2012) Efficiency of detergents at maintaining membrane protein structures in their biologically relevant forms. Biochim. Biophys. Acta 1818, 1351-1358
43. Van Horn, W. D., Kim, H. J., Ellis, C. D., Hadziselimovic, A., Sulistijo, E. S., Karra, M. D., Tian, C., Sönnichsen, F. D., and Sanders, C. R. (2009) Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324, 1726-1729
44. Li, D., Lyons, J. A., Pye, V. E., Vogeley, L., Aragão, D., Kenyon, C. P., Shah, S. T., Doherty, C., Aherne, M., and Caffrey, M. (2013) Crystal structure of the integral membrane diacylglycerol kinase. Nature 497, 521-524
45. Berardi, M. J., Shih, W. M., Harrison, S. C., and Chou, J. J. (2011) Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 476, 109-113
46. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézéguet, V., Lauquin, G. J., and Brandolin, G. (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44
47. Zoonens, M., Comer, J., Masscheleyn, S., Pebay-Peyroula, E., Chipot, C., Miroux, B., and Dehez, F. (2013) Dangerous liaisons between detergents and membrane proteins. The case of mitochondrial uncoupling protein 2. J. Am. Chem. Soc. 135, 15174-15182
48. Zhou, H.-X., and Cross, T. A. (2013) Influences of membrane mimetic environments on membrane protein structures. Annu. Rev. Biophys. 42, 361-392
49. Lemmon, M. A., Flanagan, J. M., Treutlein, H. R., Zhang, J., and Engelman, D. M. (1992) Sequence specificity in the dimerization of transmembrane α-helices. Biochemistry 31, 12719-12725
50. Kleiger, G., Grothe, R., Mallick, P., and Eisenberg, D. (2002) GXXXG and AXXXA: common α-helical interaction motifs in proteins, particularly in extremophiles. Biochemistry 41, 5990-5997
51. Senes, A., Gerstein, M., and Engelman, D. M. (2000) Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with β-branched residues at neighboring positions. J. Mol. Biol. 296, 921-936
52. Senes, A., Engel, D. E., and DeGrado, W. F. (2004) Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479
53. Moore, D. T., Berger, B. W., and DeGrado, W. F. (2008) Protein-protein interactions in the membrane: sequence, structural, and biological motifs. Structure 16, 991-1001
54. Cymer, F., Veerappan, A., and Schneider, D. (2012) Transmembrane he-lix- helix interactions are modulated by the sequence context and by lipid bilayer properties. Biochim. Biophys. Acta 1818, 963-973
55. Melnyk, R. A., Kim, S., Curran, A. R., Engelman, D. M., Bowie, J. U., and Deber, C. M. (2004) The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication. J. Biol. Chem. 279, 16591-16597
56. Psachoulia, E., Marshall, D. P., and Sansom, M. S. (2010) Molecular dynamics simulations of the dimerization of transmembrane α-helices. Acc. Chem. Res. 43, 388-396
57. Aci-Sèche, S., Sawma, P., Hubert, P., Sturgis, J. N., Bagnard, D., Jacob, L., Genest, M., and Garnier, N. (2014) Transmembrane recognition of the semaphorin co-receptors neuropilin 1 and plexin A1: coarse-grained simulations. PLoS One 9, e97779
58. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612