Synthesis, purification, and characterization of single helix membrane peptides and proteins for nmr spectroscopy

Methods in Molecular Biology

Volumn 831, Issue , 2012, Pages 333-357

  Itaya, Miki ^a   Brett, Ian C ^a   Smith, Steven O ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Epo receptor; Gp55 P; Membrane protein; NMR spectroscopy; Transmembrane

Indexed keywords

MALTOSE BINDING PROTEIN; MEMBRANE PROTEIN; PEPTIDE;

ARTICLE; BIOSYNTHESIS; CHEMICAL PHENOMENA; CHEMISTRY; CIRCULAR DICHROISM; GEL CHROMATOGRAPHY; INFRARED SPECTROSCOPY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE; PEPTIDE SYNTHESIS; PROTEIN CONFORMATION;

CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MALTOSE-BINDING PROTEINS; MASS SPECTROMETRY; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE BIOSYNTHESIS; PEPTIDES; PROTEIN CONFORMATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84862917921     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-61779-480-3_18     Document Type: Article

References (72)

1. Opella, S. J., and Marassi, F. M. (2004) Structure determination of membrane proteins by NMR spectroscopy. Chem. Rev. 104, 3587-3606.
2. Sanders, C. R., and Sönnichsen, F. (2006) Solution NMR of membrane proteins: Practice and challenges. Magn. Reson. Chem. 44, S24-S40. (Pubitemid 44090388)
3. McDermott, A. (2009) Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Ann. Rev. Biophys. 38, 385-403.
4. Ketchem, R. R., Hu, W., and Cross, T. A. (1993) High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science 261, 1457-1460. (Pubitemid 23334269)
5. Andronesi, O. C., Becker, S., Seidel, K., Heise, H., Young, H. S., and Baldus, M. (2005) Determination of membrane protein structure and dynamics by magic-angle-spinning solidstate NMR spectroscopy. J. Am. Chem. Soc. 127, 12965-12974. (Pubitemid 41339181)
6. Cady, S. D., Schmidt-Rohr, K., Wang, J., Soto, C. S., DeGrado, W. F., and Hong, M. (2010) Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463, 689-692.
7. Chu, S. D., Coey, A. T., and Lorigan, G. A. (2010) Solid-state 2H and 15N NMR studies of side-chain and backbone dynamics of phospholamban in lipid bilayers: Investigation of the N27A mutation. Biochim. Biophys. Acta-Biomembr. 1798, 210-215.
8. Etzkorn, M., Martell, S., Andronesi, O. C., Seidel, K., Engelhard, M., and Baldus, M. (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew. Chem. Int. Ed. Engl. 46, 459-462. (Pubitemid 46142261)
9. Liu, W., Crocker, E., Constantinescu, S. N., and Smith, S. O. (2005) Helix packing and orientation in the transmembrane dimer of gp55-P of the spleen focus forming virus. Biophys. J. 89, 1194-1202. (Pubitemid 41099001)
10. Smith, S. O., Song, D., Shekar, S., Groesbeek, M., Ziliox, M., and Aimoto, S. (2001) Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry 40, 6553-6558. (Pubitemid 32552780)
11. Smith, S. O., Smith, C. S., and Bormann, B. J. (1996) Strong hydrogen bonding interactions involving a buried glutamic acid in the transmembrane sequence of the neu/erbB-2 receptor. Nat. Struct. Biol. 3, 252-258. (Pubitemid 26081708)
12. Ramamoorthy, A., and Opella, S. J. (1995) Two-dimensional chemical shift/heteronuclear dipolar coupling spectra obtained with polarization inversion spin exchange at the magic angle and magic-angle sample spinning (PISEMAMAS). Solid State Nucl. Magn. Reson. 4, 387-392.
13. Wang, J. F., Kim, S., Kovacs, F., and Cross, T. A. (2001) Structure of the transmembrane region of the M2 protein H + channel. Protein Sci. 10, 2241-2250. (Pubitemid 32988641)
14. Kim, M. J., Park, S. H., Opella, S. J., Marsilje, T. H., Michellys, P. Y., Seidel, H. M., and Tian, S. S. (2007) NMR structural studies of interactions of a small, nonpeptidyl Tpo mimic with the thrombopoietin receptor extracellular juxtamembrane and transmembrane domains. J. Biol. Chem. 282, 14253-14261. (Pubitemid 47100429)
15. Bocharov, E. V., Pustovalova, Y. E., Pavlov, K. V., Volynsky, P. E., Goncharuk, M. V., Ermolyuk, Y. S., Karpunin, D. V., Schulga, A. A., Kirpichnikov, M. P., Efremov, R. G., et al. (2007) Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger. J. Biol. Chem. 282, 16256-16266. (Pubitemid 47100372)
16. Bocharov, E. V., Mineev, K. S., Volynsky, P. E., Ermolyuk, Y. S., Tkach, E. N., Sobol, A. G., Chupin, V. V., Kirpichnikov, M. P., Efremov, R. G., and Arseniev, A. S. (2008) Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state. J. Biol. Chem. 283, 6950-6956.
17. Roosild, T. P., Greenwald, J., Vega, M., Castronovo, S., Riek, R., and Choe, S. (2005) NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307, 1317-1321. (Pubitemid 40299982)
18. MacKenzie, K. R., Prestegard, J. H., and Engelman, D. M. (1997) A transmembrane helix dimer: Structure and implications. Science 276, 131-133. (Pubitemid 27161261)
19. Sulistijo, E. S., and MacKenzie, K. R. (2009) Structural basis for dimerization of the BNIP3 transmembrane domain. Biochemistry 48, 5106-5120.
20. Oxenoid, K., and Chou, J. J. (2005) The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc. Natl. Acad. Sci. USA 102, 10870-10875. (Pubitemid 41105959)
21. Hu, J., Qin, H., Li, C., Sharma, M., Cross, T. A., and Gao, F. P. (2007) Structural biology of transmembrane domains: Efficient production and characterization of transmembrane peptides by NMR. Protein Sci. 16, 2153-2165. (Pubitemid 47481650)
22. Tamm, L. K., and Liang, B. Y. (2006) NMR of membrane proteins in solution. Prog. Nucl. Magn. Reson. Spectrosc. 48, 201-210. (Pubitemid 44304459)
23. Mineev, K. S., Bocharov, E. V., Pustovalova, Y. E., Bocharova, O. V., Chupin, V. V., and Arseniev, A. S. (2010) Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases. J. Mol. Biol. 400, 231-243.
24. White, S. H. (2009) Biophysical dissection of membrane proteins. Nature 459, 344-346.\
25. Ruscetti, S. K., Janesch, N. J., Chakraborti, A., Sawyer, S. T., and Hankins, W. D. (1990) Friend spleen focus-forming virus induces factor independence in an erythropoietin-dependent erythroleukemia cell line. J. Virol. 64, 1057-1062. (Pubitemid 20087741)
26. Hoatlin, M. E., Kozak, S. L., Lilly, F., Chakraborti, A., Kozak, C. A., and Kabat, D. (1990) Activation of erythropoietin receptors by Friend viral gp55 and by erythropoietin and down-modulation by the murine Fv-2r resistance gene. Proc. Natl. Acad. Sci. USA 87, 9985-9989. (Pubitemid 120016569)
27. Li, J. P., D'Andrea, A. D., Lodish, H. F., and Baltimore, D. (1990) Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature 343, 762-764.
28. Constantinescu, S. N., Keren, T., Socolovsky, M., Nam, H. S., Henis, Y. I., and Lodish, H. F. (2001) Ligand-independent oligomerization of cell-surface erythropoietin receptor is mediated by the transmembrane domain. Proc. Natl. Acad. Sci. USA 98, 4379-4384. (Pubitemid 32294985)
29. Gurezka, R., Laage, R., Brosig, B., and Langosch, D. (1999) A heptad motif of leucine residues found in membrane proteins can drive self-assembly of artificial transmembrane segments. J. Biol. Chem. 274, 9265-9270.
30. Constantinescu, S. N., Keren, T., Russ, W. P., Ubarretxena-Belandia, I., Malka, Y., Kubatzky, K. F., Engelman, D. M., Lodish, H. F., and Henis, Y. I. (2003) The erythropoietin receptor transmembrane domain mediates complex formation with viral anemic and polycythemic gp55 proteins. J. Biol. Chem. 278, 43755-43763. (Pubitemid 37346003)
31. Constantinescu, S. N., Huang, L. J. S., Nam, H. S., and Lodish, H. F. (2001) The erythropoietin receptor cytosolic juxtamembrane domain contains an essential, precisely oriented, hydrophobic motif. Mol. Cell 7, 377-385. (Pubitemid 32206505)
32. Witthuhn, B. A., Quelle, F. W., Silvennoinen, O., Yi, T. L., Tang, B., Miura, O., and Ihle, J. N. (1993) Jak2 associates with the erythropoietin receptor and is tyrosine-phosphorylated and activated following stimulation with erythropoietin. Cell 74, 227-236. (Pubitemid 23221699)
33. Dawson, P. E., and Kent, S. B. H. (2000) Synthesis of native proteins by chemical ligation. Annu. Rev. Biochem. 69, 923-960.
34. Loll, P. J. (2003) Membrane protein structural biology: the high throughput challenge. J. Struct. Biol. 142, 144-153. (Pubitemid 36457896)
35. Wang, D. N., Safferling, M., Lemieux, M. J., Griffith, H., Chen, Y., and Li, X. D. (2003) Practical aspects of overexpressing bacterial secondary membrane transporters for structural studies. Biochim. Biophys. Acta-Biomembr. 1610, 23-36. (Pubitemid 36173993)
36. Klammt, C., Löhr, F., Schäfer, B., Haase, W., Dötsch, V., Rüterjans, H., Glaubitz, C., and Bernhard, F. (2004) High level cell-free expression and specific labeling of integral membrane proteins. Eur. J. Biochem. 271, 568-580. (Pubitemid 38183631)
37. Laage, R., and Langosch, D. (2001) Strategies for prokaryotic expression of eukaryotic membrane proteins. Traffic 2, 99-104. (Pubitemid 32219862)
38. Bormann, B. J., Knowles, W. J., and Marchesi, V. T. (1989) Synthetic peptides mimic the assembly of transmembrane glycoproteins. J. Biol. Chem. 264, 4033-4037. (Pubitemid 19072294)
39. Kochendoerfer, G. G., Salom, D., Lear, J. D., Wilk-Orescan, R., Kent, S. B. H., and DeGrado, W. F. (1999) Total chemical synthesis of the integral membrane protein influenza A virus M2: Role of its C-terminal domain in tetramer. Biochemistry 38, 11905-11913.
40. Fisher, L. E., and Engelman, D. M. (2001) High-yield synthesis and purification of an á-helical transmembrane domain. Anal. Biochem. 293, 102-108. (Pubitemid 32500511)
41. Tian, C. L., Karra, M. D., Ellis, C. D., Jacob, J., Oxenoid, K., Sonnichsen, F., and Sanders, C. R. (2005) Membrane protein preparation for TROSY NMR screening. Meth. Enzymol. 394, 321-334. (Pubitemid 40460921)
42. Page, R. C., Moore, J. D., Nguyen, H. B., Sharma, M., Chase, R., Gao, F. P., Mobley, C. K., Sanders, C. R., Ma, L., Sonnichsen, F. D., et al. (2006) Comprehensive evaluation of solution nuclear magnetic resonance spectroscopy sample preparation for helical integral membrane proteins. J. Struct. Funct. Genomics 7, 51-64. (Pubitemid 44273863)
43. Qin, H. J., Hu, J., Hua, Y. Z., Challa, S. V., Cross, T. A., and Gao, F. P. (2008) Construction of a series of vectors for high throughput cloning and expression screening of membrane proteins from Mycobacterium tuberculosis. BMC Biotechnol. 8, 51-59.
44. Kent, S. B. H. (1988) Chemical synthesis of peptides and proteins. Annu. Rev. Biochem. 57, 957-989.
45. Carpino, L. A. (1993) 1-Hydroxy-7-Azabenzotriazole-an efficient peptide coupling additive. J. Am. Chem. Soc. 115, 4397-4398.
46. Glover, K. J., Martini, P. M., Vold, R. R., and Komives, E. A. (1999) Preparation of insoluble transmembrane peptides: Glycophorin-A, prion (110-137), and FGFR (368-397). Anal. Biochem. 272, 270-274. (Pubitemid 29364993)
47. Heukeshoven, J., and Dernick, R. (1982) Reversed-phase high-performance liquid-chromatography of virus proteins and other large hydrophobic proteins in formic-acid containing solvents. J. Chromatogr. 252, 241-254. (Pubitemid 13115650)
48. Mutter, M., Nefzi, A., Sato, T., Sun, X., Wahl, F., and Wohr, T. (1995) Pseudo-prolines (Psi-Pro) for accessing inaccessible peptides. Pept. Res. 8, 145-153.
49. Arnau, J., Lauritzen, C., Petersen, G. E., and Pedersen, J. (2006) Current strategies for the use of affinity tags and tag removal for the purify cation of recombinant proteins. Protein Expr. Purif. 48, 1-13. (Pubitemid 43782626)
50. Kapust, R. B., and Waugh, D. S. (1999) Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci. 8, 1668-1674. (Pubitemid 29379949)
51. Nallamsetty, S., and Waugh, D. S. (2006) Solubility-enhancing proteins MBP and NusA play a passive role in the folding of their fusion partners. Protein Expr. Purif. 45, 175-182. (Pubitemid 41773324)
52. Korepanova, A., Gao, F. P., Hua, Y. Z., Qin, H. J., Nakamoto, R. K., and Cross, T. A. (2005) Cloning and expression of multiple integral membrane proteins from Mycobacterium tuberculosis in Escherichia coli. Protein Sci. 14, 148-158. (Pubitemid 40054126)
53. Amor-Mahjoub, M., Suppini, J. P., Gomez-Vrielyunck, N., and Ladjimi, M. (2006) The effect of the hexahistidine-tag in the oligomerization of HSC70 constructs. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 844, 328-334. (Pubitemid 44792013)
54. Stols, L., Gu, M. Y., Dieckman, L., Raffen, R., Collart, F. R., and Donnelly, M. I. (2002) A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein Expr. Purif. 25, 8-15. (Pubitemid 36034995)
55. Lew, S., and London, E. (1997) Simple procedure for reversed-phase high-performance liquid chromatographic purification of long hydrophobic peptides that form transmembrane helices. Anal. Biochem. 251, 113-116. (Pubitemid 27352152)
56. Fleming, K. G., Ackerman, A. L., and Engelman, D. M. (1997) The effect of point mutations on the free energy of transmembrane alpha-helix dimerization. J. Mol. Biol. 272, 266-275. (Pubitemid 27397350)
57. Smith, S. O., Eilers, M., Song, D., Crocker, E., Ying, W. W., Groesbeek, M., Metz, G., Ziliox, M., and Aimoto, S. (2002) Implications of threonine hydrogen bonding in the glycophorin A transmembrane helix dimer. Biophys. J. 82, 2476-2486. (Pubitemid 34441286)
58. Tamm, L. K., and Tatulian, S. A. (1997) Infrared spectroscopy of proteins and peptides in lipid bilayers. Q. Rev. Biophys. 30, 365-429. (Pubitemid 28260614)
59. Johnson, W. C. (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins 35, 307-312. (Pubitemid 29200967)
60. Siminovitch, D. J. (1998) Solid-state NMR studies of proteins: the view from static 2H NMR experiments. Biochem. Cell Biol. 76, 411-422. (Pubitemid 29102026)
61. Ying, W. W., Irvine, S. E., Beekman, R. A., Siminovitch, D. J., and Smith, S. O. (2000) Deuterium NMR reveals helix packing interactions in phospholamban. J. Am. Chem. Soc. 122, 11125-11128.
62. Sharpe, S., Barber, K. R., Grant, C. W. M., Goodyear, D., and Morrow, M. R. (2002) Organization of model helical peptides in lipid bilayers: Insight into the behavior of singlespan protein transmembrane domains. Biophys. J. 83, 345-358. (Pubitemid 34700195)
63. Siminovitch, D. J., Ruocco, M. J., Olejniczak, E. T., Das Gupta, S. K., and Griffin, R. G. (1988) Anisotropic 2H-nuclear magnetic resonance spin-lattice relaxation in cerebroside-and phospholipid-cholesterol bilayer membranes. Biophys. J. 54, 373-381.
64. Bloom, M., and Smith, I. C. P. (1985) Manifestations of lipid-protein interactions in deuterium NMR, in Progress in Protein-Lipid Interactions (Watts, A. & De Pont, J. J. H. H. M., Eds.) pp 61-88, Elsevier, Amsterdam.
65. Krueger-Koplin, R. D., Sorgen, P. L., Krueger-Koplin, S. T., Rivera-Torres, A. O., Cahill, S. M., Hicks, D. B., Grinius, L., Krulwich, T. A., and Girvin, M. E. (2004) An evaluation of detergents for NMR structural studies of membrane proteins. J. Biomol. NMR 28, 43-57. (Pubitemid 38220159)
66. Nallamsetty, S., and Waugh, D. S. (2007) A generic protocol for the expression and purifi-cation of recombinant proteins in Escherichia coli using a combinatorial His6-maltose binding protein fusion tag. Nat. Protoc. 2, 383-391. (Pubitemid 47040053)
67. Karas, M., Bachmann, D., Bahr, U., and Hillenkamp, F. (1987) Matrix-assisted ultraviolet laser desorption of non-volatile compounds. Int. J. Mass Spectrom. Ion Process. 78, 53-68.
68. Bollhagen, R., Schmiedberger, M., and Grell, E. (1995) High-Performance Liquid-Chromatographic Purification of Extremely Hydrophobic Peptides-Transmembrane Segments. J. Chromatogr. A 711, 181-186.
69. Sato, T., Kawakami, T., Akaji, K., Konishi, H., Mochizuki, K., Fujiwara, T., Akutsu, H., and Aimoto, S. (2002) Synthesis of a membrane protein with two transmembrane regions. J. Pept. Sci. 8, 172-180. (Pubitemid 34449796)
70. Gardner, K. H., and Kay, L. E. (1998) The use of 2H, 13C, 15N multidimensional NMR to study the structure and dynamics of proteins. Annu. Rev. Biophys. Biomol. Struct. 27, 357-406. (Pubitemid 28286019)
71. Goto, N. K., and Kay, L. E. (2000) New developments in isotope labeling strategies for protein solution NMR spectroscopy. Curr. Opin. Struct. Biol. 10, 585-592.
72. Gennis, R. B. (1989) Membrane Dynamics and Protein-Lipid Interactions, in Biomembranes pp 166-198, Springer-Verlag, New York.