Dodecyl maltopyranoside enabled purification of active human GABA type a receptors for deep and direct proteomic sequencing

Molecular and Cellular Proteomics

Volumn 14, Issue 3, 2015, Pages 724-738

  Zhang, Xi ^a,b   Miller, Keith W ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CHOLESTEROL HYDROGEN SUCCINATE; MEMBRANE PROTEIN; PROTEINASE; CHOLESTEROL ESTER; CHOLESTERYL SUCCINATE; DODECYL MALTOPYRANOSIDE; MALTOSE;

ARTICLE; CELL GROWTH; CELL LYSATE; CONTROLLED STUDY; CRITICAL MICELLE CONCENTRATION; CRYSTALLIZATION; CRYSTALLOGRAPHY; CYTOLYSIS; DEGLYCOSYLATION; ELECTRON MICROSCOPY; EMBRYO; ENZYME ACTIVITY; FLOW RATE; GLYCOSYLATION; HEK293 CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIGAND BINDING; MASS SPECTROMETRY; MOLECULAR WEIGHT; PALMITOYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOMICS; SEQUENCE ANALYSIS; SOLUBILIZATION; STOICHIOMETRY; ULTRASOUND; AFFINITY CHROMATOGRAPHY; ANALOGS AND DERIVATIVES; BIOLOGICAL MODEL; CHEMISTRY; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; PROCEDURES;

CHOLESTEROL ESTERS; CHROMATOGRAPHY, AFFINITY; HEK293 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALTOSE; MODELS, BIOLOGICAL; PROTEOMICS; RECEPTORS, GABA-A; SEQUENCE ANALYSIS, PROTEIN;

EID: 84924289018     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.042556     Document Type: Article

References (70)

1. Pieper, U., Schlessinger, A., Kloppmann, E., Chang, G. A., Chou, J. J., Dumont, M. E., Fox, B. G., Fromme, P., Hendrickson, W. A., Malkowski, M. G., Rees, D. C., Stokes, D. L., Stowell, M. H., Wiener, M. C., Rost, B., Stroud, R. M., Stevens, R. C., and Sali, A. (2013) Coordinating the impact of structural genomics on the human alpha-helical transmembrane proteome. Nat. Struct. Mol. Biol. 20, 135-138
2. Olsen, R. W., and Sieghart, W. (2009) GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141-148
3. Forman, S. A., and Miller, K. W. (2012) Anesthetic sites and allosteric mechanisms of action on Cys-loop ligand-gated ion channels. Can. J. Anaesth. 58, 191-205
4. Baulac, S., Huberfeld, G., Gourfinkel-An, I., Mitropoulou, G., Beranger, A., Prud'homme, J. F., Baulac, M., Brice, A., Bruzzone, R., and LeGuern, E. (2001) First genetic evidence of GABA(A) receptor dysfunction in epilepsy: a mutation in the gamma2-subunit gene. Nat. Genet. 28, 46-48
5. Wallace, R. H., Marini, C., Petrou, S., Harkin, L. A., Bowser, D. N., Panchal, R. G., Williams, D. A., Sutherland, G. R., Mulley, J. C., Scheffer, I. E., and Berkovic, S. F. (2001) Mutant GABA(A) receptor gamma2-subunit in childhood absence epilepsy and febrile seizures. Nat. Genet. 28, 49-52
6. Macdonald, R. L., Gallagher, M. J., Feng, H. J., and Kang, J. (2004) GABA(A) receptor epilepsy mutations. Biochem. Pharmacol. 68, 1497-1506
7. Brooks-Kayal, A. R., Shumate, M. D., Jin, H., Rikhter, T. Y., and Coulter, D. A. (1998) Selective changes in single cell GABA(A) receptor subunit expression and function in temporal lobe epilepsy. Nat. Med. 4, 1166-1172
8. Marini, C., Harkin, L. A., Wallace, R. H., Mulley, J. C., Scheffer, I. E., and Berkovic, S. F. (2003) Childhood absence epilepsy and febrile seizures: a family with a GABA(A) receptor mutation. Brain 126, 230-240
9. Hernandez, C. C., Gurba, K. N., Hu, N., and Macdonald, R. L. (2011) The GABRA6 mutation, R46W, associated with childhood absence epilepsy, alters 6beta22 and 6beta2 GABA(A) receptor channel gating and expression. J. Physiol. 589, 5857-5878
10. Ding, L., Feng, H. J., Macdonald, R. L., Botzolakis, E. J., Hu, N., and Gallagher, M. J. (2010) GABA(A) receptor alpha1 subunit mutation A322D associated with autosomal dominant juvenile myoclonic epilepsy reduces the expression and alters the composition of wild type GABA(A) receptors. J. Biol. Chem. 285, 26390-26405
11. Jones-Davis, D. M., and Macdonald, R. L. (2003) GABA(A) receptor function and pharmacology in epilepsy and status epilepticus. Curr. Opin. Pharmacol. 3, 12-18
12. Gurba, K. N., Hernandez, C. C., Hu, N., and Macdonald, R. L. (2012) GABRB3 mutation, G32R, associated with childhood absence epilepsy alters alpha1beta3gamma2L gamma-aminobutyric acid type A (GABAA) receptor expression and channel gating. J. Biol. Chem. 287, 12083-12097
13. Hassaine, G., Deluz, C., Grasso, L., Wyss, R., Tol, M. B., Hovius, R., Graff, A., Stahlberg, H., Tomizaki, T., Desmyter, A., Moreau, C., Li, X. D., Poitevin, F., Vogel, H., and Nury, H. (2014) X-ray structure of the mouse serotonin 5-HT3 receptor. Nature 512, 276-281
14. Miller, P. S., and Aricescu, A. R. (2014) Crystal structure of a human GABAA receptor. Nature 512, 270-275
15. Luscher, B., Fuchs, T., and Kilpatrick, C. L. (2011) GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70, 385-409
16. Huttlin, E. L., Jedrychowski, M. P., Elias, J. E., Goswami, T., Rad, R., Beausoleil, S. A., Villen, J., Haas, W., Sowa, M. E., and Gygi, S. P. (2010) A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174-1189
17. Nobles, K. N., Xiao, K., Ahn, S., Shukla, A. K., Lam, C. M., Rajagopal, S., Strachan, R. T., Huang, T. Y., Bressler, E. A., Hara, M. R., Shenoy, S. K., Gygi, S. P., and Lefkowitz, R. J. (2011) Distinct phosphorylation sites on the beta(2)-adrenergic receptor establish a barcode that encodes differential functions of beta-arrestin. Sci. Signal. 4, ra51
18. Corringer, P. J., Poitevin, F., Prevost, M. S., Sauguet, L., Delarue, M., and Changeux, J. P. (2012) Structure and pharmacology of pentameric receptor channels: from bacteria to brain. Structure 20, 941-956
19. Bergmann, R., Kongsbak, K., Sorensen, P. L., Sander, T., and Balle, T. (2013) A unified model of the GABA(A) receptor comprising agonist and benzodiazepine binding sites. PLoS One 8, e52323
20. Baker, M. (2010) Making membrane proteins for structures: a trillion tiny tweaks. Nat. Methods 7, 429-434
21. Chen, E. I., Cociorva, D., Norris, J. L., and Yates, J. R., 3rd (2007) Optimization of mass spectrometry-compatible surfactants for shotgun proteomics. J. Proteome Res. 6, 2529-2538
22. Zhou, F., Lu, Y., Ficarro, S. B., Adelmant, G., Jiang, W., Luckey, C. J., and Marto, J. A. (2013) Genome-scale proteome quantification by DEEP SEQ mass spectrometry. Nat. Commun. 4, 2171
23. Yates, J. R., 3rd (2013) The revolution and evolution of shotgun proteomics for large-scale proteome analysis. J. Am. Chem. Soc. 135, 1629-1640
24. Wu, C. C., and Yates, J. R., 3rd (2003) The application of mass spectrometry to membrane proteomics. Nat. Biotechnol. 21, 262-267
25. Whitelegge, J. P. (2013) Integral membrane proteins and bilayer proteomics. Anal. Chem. 85, 2558-2568
26. Yip, G. M., Chen, Z. W., Edge, C. J., Smith, E. H., Dickinson, R., Hohenester, E., Townsend, R. R., Fuchs, K., Sieghart, W., Evers, A. S., and Franks, N. P. (2013) A propofol binding site on mammalian GABA receptors identified by photolabeling. Nat. Chem. Biol. 9, 715-720
27. Kang, S. U., Heo, S., and Lubec, G. (2011) Mass spectrometric analysis of GABAA receptor subtypes and phosphorylations from mouse hippocampus. Proteomics 11, 2171-2181
28. Chen, Z. W., Fuchs, K., Sieghart, W., Townsend, R. R., and Evers, A. S. (2012) Deep amino acid sequencing of native brain GABAA receptors using high-resolution mass spectrometry. Mol. Cell. Proteomics 11, M111 011445
29. Kang, S. U., Fuchs, K., Sieghart, W., Pollak, A., Csaszar, E., and Lubec, G. (2009) Gel-based mass spectrometric analysis of a strongly hydrophobic GABAA-receptor subunit containing four transmembrane domains. Nat. Protoc. 4, 1093-1102
30. Kang, S. U., Fuchs, K., Sieghart, W., and Lubec, G. (2008) Gel-based mass spectrometric analysis of recombinant GABA(A) receptor subunits representing strongly hydrophobic transmembrane proteins. J. Proteome Res. 7, 3498-3506
31. Manza, L. L., Stamer, S. L., Ham, A. J., Codreanu, S. G., and Liebler, D. C. (2005) Sample preparation and digestion for proteomic analyses using spin filters. Proteomics 5, 1742-1745
32. Wisniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362
33. Wisniewski, J. R., and Mann, M. (2012) Consecutive proteolytic digestion in an enzyme reactor increases depth of proteomic and phosphoproteomic analysis. Anal. Chem. 84, 2631-2637
34. Nagaraj, N., Lu, A., Mann, M., and Wisniewski, J. R. (2008) Detergent-based but gel-free method allows identification of several hundred membrane proteins in single LC-MS runs. J. Proteome Res. 7, 5028-5032
35. Newby, Z. E., O'Connell, J. D., 3rd, Gruswitz, F., Hays, F. A., Harries, W. E., Harwood, I. M., Ho, J. D., Lee, J. K., Savage, D. F., Miercke, L. J., and Stroud, R. M. (2009) A general protocol for the crystallization of membrane proteins for X-ray structural investigation. Nat. Protoc. 4, 619-637
36. Drew, D., Newstead, S., Sonoda, Y., Kim, H., von Heijne, G., and Iwata, S. (2008) GFP-based optimization scheme for the overexpression and purification of eukaryotic membrane proteins in Saccharomyces cerevisiae. Nat. Protoc. 3, 784-798
37. Garavito, R. M., and Ferguson-Miller, S. (2001) Detergents as tools in membrane biochemistry. J. Biol. Chem. 276, 32403-32406
38. Rosevear, P., VanAken, T., Baxter, J., and Ferguson-Miller, S. (1980) Alkyl glycoside detergents: a simpler synthesis and their effects on kinetic and physical properties of cytochrome c oxidase. Biochemistry 19, 4108-4115
39. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258-1265
40. Hilf, R. J., and Dutzler, R. (2008) X-ray structure of a prokaryotic pentameric ligand-gated ion channel. Nature 452, 375-379
41. Hibbs, R. E., and Gouaux, E. (2011) Principles of activation and permeation in an anion-selective Cys-loop receptor. Nature 474, 54-60
42. Liu, W., Chun, E., Thompson, A. A., Chubukov, P., Xu, F., Katritch, V., Han, G. W., Roth, C. B., Heitman, L. H., AP, I. J., Cherezov, V., and Stevens, R. C. (2012) Structural basis for allosteric regulation of GPCRs by sodium ions. Science 337, 232-236
43. Brohawn, S. G., del Marmol, J., and MacKinnon, R. (2012) Crystal structure of the human K2P TRAAK, a lipid-and mechano-sensitive K+ ion channel. Science 335, 436-441
44. Chae, P. S., Rasmussen, S. G., Rana, R. R., Gotfryd, K., Chandra, R., Goren, M. A., Kruse, A. C., Nurva, S., Loland, C. J., Pierre, Y., Drew, D., Popot, J. L., Picot, D., Fox, B. G., Guan, L., Gether, U., Byrne, B., Kobilka, B., and Gellman, S. H. (2010) Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization, and crystallization of mem-brane proteins. Nat. Methods 7, 1003-1008
45. Rasmussen, S. G., DeVree, B. T., Zou, Y., Kruse, A. C., Chung, K. Y., Kobilka, T. S., Thian, F. S., Chae, P. S., Pardon, E., Calinski, D., Mathiesen, J. M., Shah, S. T., Lyons, J. A., Caffrey, M., Gellman, S. H., Steyaert, J., Skiniotis, G., Weis, W. I., Sunahara, R. K., and Kobilka, B. K. (2011) Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477, 549-555
46. Chung, K. Y., Kim, T. H., Manglik, A., Alvares, R., Kobilka, B. K., and Prosser, R. S. (2012) Role of detergents in conformational exchange of a G protein-coupled receptor. J. Biol. Chem. 287, 36305-36311
47. Tao, H., Fu, Y., Thompson, A., Lee, S. C., Mahoney, N., Stevens, R. C., and Zhang, Q. (2012) Synthesis and properties of dodecyl trehaloside detergents for membrane protein studies. Langmuir 28, 11173-11181
48. Lee, S. C., Bennett, B. C., Hong, W. X., Fu, Y., Baker, K. A., Marcoux, J., Robinson, C. V., Ward, A. B., Halpert, J. R., Stevens, R. C., Stout, C. D., Yeager, M. J., and Zhang, Q. (2013) Steroid-based facial amphiphiles for stabilization and crystallization of membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 110, E1203-1211
49. Thompson, D. A., Suarez-Villafane, M., and Ferguson-Miller, S. (1982) The active form of cytochrome c oxidase: effects of detergent, the intact membrane, and radiation inactivation. Biophys. J. 37, 285-293
50. Cristoni, S., and Bernardi, L. R. (2003) Development of new methodologies for the mass spectrometry study of bioorganic macromolecules. Mass Spectrom. Rev. 22, 369-406
51. Laganowsky, A., Reading, E., Hopper, J. T., and Robinson, C. V. (2013) Mass spectrometry of intact membrane protein complexes. Nat. Protoc. 8, 639-651
52. Zhang, X., Chien, E. Y., Chalmers, M. J., Pascal, B. D., Gatchalian, J., Stevens, R. C., and Griffin, P. R. (2010) Dynamics of the beta2-adrenergic G-protein coupled receptor revealed by hydrogen-deuterium exchange. Anal. Chem. 82, 1100-1108
53. Tao, H., Lee, S. C., Moeller, A., Roy, R. S., Siu, F. Y., Zimmermann, J., Stevens, R. C., Potter, C. S., Carragher, B., and Zhang, Q. (2013) Engineered nanostructured beta-sheet peptides protect membrane proteins. Nat. Methods 10, 759-761
54. McGregor, C. L., Chen, L., Pomroy, N. C., Hwang, P., Go, S., Chakrabartty, A., and Prive, G. G. (2003) Lipopeptide detergents designed for the structural study of membrane proteins. Nat. Biotechnol. 21, 171-176
55. Zhang, X., Tamot, B., Hiser, C., Reid, G. E., Benning, C., and Ferguson-Miller, S. (2011) Cardiolipin deficiency in Rhodobacter sphaeroides alters the lipid profile of membranes and of crystallized cytochrome oxidase, but structure and function are maintained. Biochemistry 50, 3879-3890
56. Dostalova, Z., Zhou, X., Liu, A., Zhang, X., Zhang, Y., Desai, R., Forman, S. A., and Miller, K. W. (2014) Human alpha1beta3gamma2L gammaaminobutyric acid type A receptors: High-level production and purification in a functional state. Protein Sci. 23, 157-166
57. Zhang, X., and Miller, K. W. (2014) Novel integrated ultra-deep quantitativestructural membrane proteomics discovered PTM signatures for human Cys-loop receptor subunit bias. Submitted. (under review at MCP)
58. Pascal, B. D., Willis, S., Lauer, J. L., Landgraf, R. R., West, G. M., Marciano, D., Novick, S., Goswami, D., Chalmers, M. J., and Griffin, P. R. (2012) HDX workbench: software for the analysis of H/D exchange MS data. J. Am. Soc. Mass Spectrom. 23, 1512-1521
59. Mellacheruvu, D., Wright, Z., Couzens, A. L., Lambert, J. P., St-Denis, N. A., Li, T., Miteva, Y. V., Hauri, S., Sardiu, M. E., Low, T. Y., Halim, V. A., Bagshaw, R. D., Hubner, N. C., Al-Hakim, A., Bouchard, A., Faubert, D., Fermin, D., Dunham, W. H., Goudreault, M., Lin, Z. Y., Badillo, B. G., Pawson, T., Durocher, D., Coulombe, B., Aebersold, R., Superti-Furga, G., Colinge, J., Heck, A. J., Choi, H., Gstaiger, M., Mohammed, S., Cristea, I. M., Bennett, K. L., Washburn, M. P., Raught, B., Ewing, R. M., Gingras, A. C., and Nesvizhskii, A. I. (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat. Methods 10, 730-736
60. Norton, W. T., Abe, T., Poduslo, S. E., and DeVries, G. H. (1975) The lipid composition of isolated brain cells and axons. J. Neurosci. Res. 1, 57-75
61. Zhang, X., Hiser, C., Tamot, B., Benning, C., Reid, G. E., and Ferguson-Miller, S. M. (2011) Combined genetic and metabolic manipulation of lipids in Rhodobacter sphaeroides reveals non-phospholipid substitutions in fully active cytochrome c oxidase. Biochemistry 50, 3891-3902
62. Savechenkov, P. Y., Zhang, X., Chiara, D. C., Stewart, D. S., Ge, R., Zhou, X., Raines, D. E., Cohen, J. B., Forman, S. A., Miller, K. W., and Bruzik, K. S. (2012) Allyl m-trifluoromethyldiazirine mephobarbital: an unusually potent enantioselective and photoreactive barbiturate general anesthetic. J. Med. Chem. 55, 6554-6565
63. Hansen, S. B., Talley, T. T., Radic, Z., and Taylor, P. (2004) Structural and ligand recognition characteristics of an acetylcholine-binding protein from Aplysia californica. J. Biol. Chem. 279, 24197-24202
64. Dephoure, N., Gould, K. L., Gygi, S. P., and Kellogg, D. R. (2013) Mapping and analysis of phosphorylation sites: a quick guide for cell biologists. Mol. Biol. Cell 24, 535-542
65. Zielinska, D. F., Gnad, F., Wisniewski, J. R., and Mann, M. (2010) Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907
66. Zielinska, D. F., Gnad, F., Schropp, K., Wisniewski, J. R., and Mann, M. (2012) Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery. Mol. Cell 46, 542-548
67. Chang, W., Gelman, M. S., and Prives, J. M. (1997) Calnexin-dependent enhancement of nicotinic acetylcholine receptor assembly and surface expression. J. Biol. Chem. 272, 28925-28932
68. Keller, S. H., Lindstrom, J., and Taylor, P. (1996) Involvement of the chaperone protein calnexin and the acetylcholine receptor beta-subunit in the assembly and cell surface expression of the receptor. J. Biol. Chem. 271, 22871-22877
69. Keller, S. H., Lindstrom, J., and Taylor, P. (1998) Inhibition of glucose trimming with castanospermine reduces calnexin association and promotes proteasome degradation of the alpha-subunit of the nicotinic acetylcholine receptor. J. Biol. Chem. 273, 17064-17072
70. Itakura, M., Tsujimura, J., Yamamori, S., Ohkido, T., and Takahashi, M. (2013) NMDA receptor-dependent recruitment of calnexin to the neuronal plasma membrane. Neurosci. Lett. 550, 173-178