Glycines: Role in α-helical membrane protein structures and a potential indicator of native conformation

Biochemistry

Volumn 51, Issue 24, 2012, Pages 4779-4789

  Dong, Hao ^a,b   Sharma, Mukesh ^a,c   Zhou, Huan Xiang ^a,b   Cross, Timothy A ^a,c  

^a FLORIDA STATE UNIVERSITY   (United States)

^b Florida State University   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE RESIDUES; HELICAL MEMBRANE; HELIX-HELIX PACKING; MEMBRANE PROTEIN STRUCTURES; MEMBRANE PROTEINS; MIMETICS; NATIVE CONFORMATION; NATIVE MEMBRANES; PHYSICOCHEMICAL PROPERTY; POTENTIAL INDICATORS; PROTEIN DATA BANK; STRUCTURAL CHARACTERIZATION; TRANS-MEMBRANE DOMAINS; VALIDATION TOOLS;

ACTIVATION ANALYSIS; AMINO ACIDS; BIOLOGICAL MEMBRANES;

PROTEINS;

GLYCINE; LIPID; MEMBRANE PROTEIN;

ALPHA HELIX; NUCLEOTIDE SEQUENCE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW;

CELL MEMBRANE; CONSERVED SEQUENCE; GLYCINE; HUMANS; MEMBRANE PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84862532342     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300090x     Document Type: Review

References (84)

1. Tate, C. G. (2006) Comparison of three structures of the multidrug transporter EmrE. Curr. Opin. Struct. Biol. 16, 457-464.
2. Cross, T. A., Sharma, M., Yi, M., and Zhou, H. X. (2011) Influence of solubilizing environments on membrane protein structures. Trends Biochem. Sci. 36, 117-125.
3. Vinothkumar, K. R., and Henderson, R. (2010) Structures of membrane proteins. Q. Rev. Biophys. 43, 65-158.
4. Verardi, R., Shi, L., Traaseth, N. J., Walsh, N., and Veglia, G. (2011) Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method. Proc. Natl. Acad. Sci. U.S.A. 108, 9101-9106.
5. Botelho, A. V., Huber, T., Sakmar, T. P., and Brown, M. F. (2006) Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes. Biophys. J. 91, 4464-4477. (Pubitemid 44911035)
6. Botelho, A. V., Gibson, N. J., Thurmond, R. L., Wang, Y., and Brown, M. F. (2002) Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids. Biochemistry 41, 6354-6368. (Pubitemid 34526000)
7. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains. Science 181, 223-230.
8. Sanders, C. R., and Mittendorf, K. F. (2011) Tolerance to changes in membrane lipid composition as a selected trait of membrane proteins. Biochemistry 50, 7858-7867.
9. Mitsuoka, K., Hirai, T., Murata, K., Miyazawa, A., Kidera, A., Kimura, Y., and Fujiyoshi, Y. (1999) The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: Implication of the charge distribution. J. Mol. Biol. 286, 861-882. (Pubitemid 29106223)
10. Sharma, M., Yi, M., Dong, H., Qin, H., Peterson, E., Busath, D. D., Zhou, H. X., and Cross, T. A. (2010) Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330, 509-512.
11. Ketchem, R. R., Roux, B., and Cross, T. A. (1997) High-Resolution Polypeptide Structure in a Lamellar Phase Lipid Environment from Solid-State NMR Derived Orientational Constraints. Structure 5, 1655-1669. (Pubitemid 28051978)
12. Das, B. B., Ajithkumar, T. G., Sinha, N., Opella, S. J., and Ramanathan, K. V. (2007) Cross- and axial-peak intensities in 2D-SLF experiments based on cross-polarization: The role of the initial density matrix. J. Magn. Reson. 185, 308-317. (Pubitemid 46635237)
13. Park, S. H., Marassi, F. M., Black, D., and Opella, S. J. (2010) Structure and dynamics of the membrane-bound form of Pf1 coat protein: Implications of structural rearrangement for virus assembly. Biophys. J. 99, 1465-1474.
14. Park, S. H., De Angelis, A. A., Nevzorov, A. A., Wu, C. H., and Opella, S. J. (2006) Three-dimensional structure of the transmembrane domain of Vpu from HIV-1 in aligned phospholipid bicelles. Biophys. J. 91, 3032-3042. (Pubitemid 44526493)
15. Grigorieff, N., Ceska, T. A., Downing, K. H., Baldwin, J. M., and Henderson, R. (1996) Electron crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 259, 393-421. (Pubitemid 26179019)
16. Gonen, T., Cheng, Y., Sliz, P., Hiroaki, Y., Fujiyoshi, Y., Harrison, S. C., and Walz, T. (2005) Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438, 633-638. (Pubitemid 41740568)
17. Hite, R. K., Gonen, T., Harrison, S. C., and Walz, T. (2008) Interactions of lipids with aquaporin-0 and other membrane proteins. Pfluegers Arch. 456, 651-661. (Pubitemid 351692134)
18. Popot, J. L., and Engelman, D. M. (2000) Helical Membrane Protein Folding, Stability and Evolution. Annu. Rev. Biochem. 69, 881-922.
19. Hu, J., Asbury, T., Achuthan, S., Li, C., Bertram, R., Quine, J. R., Fu, R., and Cross, T. A. (2007) Backbone structure of the amantadine-blocked trans-membrane domain M2 proton channel from influenza A virus. Biophys. J. 92, 4335-4343. (Pubitemid 46915327)
20. MacKenzie, K. R., and Fleming, K. G. (2008) Association energetics of membrane spanning α-helices. Curr. Opin. Struct. Biol. 18, 412-419.
21. Kim, S., and Cross, T. A. (2002) Uniformity, ideality, and hydrogen bonds in transmembrane α-helices. Biophys. J. 83, 2084-2095.
22. Page, R. C., Li, C., Hu, J., Gao, F. P., and Cross, T. A. (2007) Lipid bilayers: An essential environment for the understanding of membrane proteins. Magn. Reson. Chem. 45, S2-S11.
23. Page, R. C., Kim, S., and Cross, T. A. (2008) Transmembrane helix uniformity examined by spectral mapping of torsion angles. Structure 16, 787-797. (Pubitemid 351626899)
24. Eilers, M., Patel, A. B., Liu, W., and Smith, S. O. (2002) Comparison of helix interactions in membrane and soluble α-bundle proteins. Biophys. J. 82, 2720-2736. (Pubitemid 34441309)
25. Dutzler, R., Campbell, E. B., and MacKinnon, R. (2003) Gating the selectivity filter in ClC chloride channels. Science 300, 108-112. (Pubitemid 36423038)
26. +channel. Nature 423, 33-41.
27. 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 β2-adrenergic G protein-coupled receptor. Science 318, 1258-1265. (Pubitemid 350172884)
28. Serrano-Vega, M. J., Magnani, F., Shibata, Y., and Tate, C. G. (2008) Conformational thermostabilization of the β1-adrenergic receptor in a detergent-resistant form. Proc. Natl. Acad. Sci. U.S.A. 105, 877-882. (Pubitemid 351282049)
29. Butterwick, J. A., and MacKinnon, R. (2010) Solution structure and phospholipid interactions of the isolated voltage-sensor domain from KvAP. J. Mol. Biol. 403, 591-606.
30. + channel and its dependence on the lipid membrane. Proc. Natl. Acad. Sci. U.S.A. 102, 15441-15446.
31. Vargas, E., Bezanilla, F., and Roux, B. (2011) In search of a consensus model of the resting state of a voltage-sensing domain. Neuron 72, 713-720.
32. Rosenberg, M. F., O'Ryan, L. P., Hughes, G., Zhao, Z., Aleksandrov, L. A., Riordan, J. R., and Ford, R. C. (2011) The cystic fibrosis transmembrane conductance regulator (CFTR): Three-dimensional structure and localization of a channel gate. J. Biol. Chem. 286, 42647-42654.
33. +-ATPase induced by an acid suppressant. Nat. Commun. 2, 155.
34. Oshima, A., Tani, K., Toloue, M. M., Hiroaki, Y., Smock, A., Inukai, S., Cone, A., Nicholson, B. J., Sosinsky, G. E., and Fujiyoshi, Y. (2011) Asymmetric configurations and N-terminal rearrangements in connexin26 gap junction channels. J. Mol. Biol. 405, 724-735.
35. Fleishman, S. J., Harrington, S. E., Enosh, A., Halperin, D., Tate, C. G., and Ben-Tal, N. (2006) Quasi-symmetry in the cryo-EM structure of EmrE provides the key to modeling its transmembrane domain. J. Mol. Biol. 364, 54-67. (Pubitemid 44634527)
36. Hessa, T., White, S. H., and von Heijne, G. (2005) Membrane insertion of a potassium-channel voltage sensor. Science 307, 1427. (Pubitemid 40321932)
37. Bond, P. J., Wee, C. L., and Sansom, M. S. (2008) Coarse-grained molecular dynamics simulations of the energetics of helix insertion into a lipid bilayer. Biochemistry 47, 11321-11331.
38. Gray, T. M., and Matthews, B. W. (1984) Intrahelical hydrogen bonding of serine, threonine and cysteine residues within α-helices and its relevance to membrane-bound proteins. J. Mol. Biol. 175, 75-81.
39. Adamian, L., Nanda, V., DeGrado, W. F., and Liang, J. (2005) Empirical lipid propensities of amino acid residues in multispan αhelical membrane proteins. Proteins 59, 496-509. (Pubitemid 40594293)
40. Parton, D. L., Klingelhoefer, J. W., and Sansom, M. S. (2011) Aggregation of model membrane proteins, modulated by hydrophobic mismatch, membrane curvature, and protein class. Biophys. J. 101, 691-699.
41. Schafer, L. V., de Jong, D. H., Holt, A., Rzepiela, A. J., de Vries, A. H., Poolman, B., Killian, J. A., and Marrink, S. J. (2011) Lipid packing drives the segregation of transmembrane helices into disordered lipid domains in model membranes. Proc. Natl. Acad. Sci. U.S.A. 108, 1343-1348.
42. 2H NMR and ESR study using designed transmembrane α-helical peptides and gramicidin A. Biochemistry 37, 9333-9345.
43. Engelman, D. M. (2005) Membranes are more mosaic than fluid. Nature 438, 578-580.
44. Phillips, R., Ursell, T., Wiggins, P., and Sens, P. (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459, 379-385.
45. Cantor, R. S. (1999) Lipid composition and the lateral pressure profile in bilayers. Biophys. J. 76, 2625-2639.
46. Chou, J. J., Kaufman, J. D., Stahl, S. J., Wingfield, P. T., and Bax, A. (2002) Micelle-Induced Curvature in a Water-Insoluble HIV-1 Env Peptide Revealed by NMR Dipolar Coupling Measurement in Stretched Polyacrylamide Gel. J. Am. Chem. Soc. 124, 2450-2451. (Pubitemid 34251754)
47. Kalyanasundaram, K., and Thomas, J. K. (1977) Environmental Effects on Vibronic Band Intensities in Pyrene Monomer Flourescence and Their Application in Studies of Micellar Systems. J. Am. Chem. Soc. 99, 2039-2044.
48. Fendler, J. H., and Fendler, E. J. (1975) Catalysis in Micellar and Macromolecular Systems, Academic Press, New York.
49. Podo, F., Ray, A., and Nemethy, G. (1973) Structure and Hydration of Nonionic Detergent Micelles. High Resolution Nucelar Magnetic Resonance Study. J. Am. Chem. Soc. 95, 6164-6171.
50. Landau, E. M., and Rosenbusch, J. P. (1996) Lipidic cubic phases: A novel concept for the crystallization of membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 93, 14532-14535. (Pubitemid 26419001)
51. Cevc, G., and Marsh, D. (1987) Phospholipid Bilayers: Physical Principles and Models, Vol. 5, John Wiley & Sons, New York.
52. Higman, V. A., Varga, K., Aslimovska, L., Judge, P. J., Sperling, L. J., Rienstra, C. M., and Watts, A. (2011) The Conformation of Bacteriorhodopsin Loops in Purple Membranes Resolved by Solid-State MAS NMR Spectroscopy. Angew. Chem., Int. Ed. 50, 8432-8435.
53. Maslennikov, I., Klammt, C., Hwang, E., Kefala, G., Okamura, M., Esquivies, L., Mors, K., Glaubitz, C., Kwiatkowski, W., Jeon, Y. H., and Choe, S. (2010) Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc. Natl. Acad. Sci. U.S.A. 107, 10902-10907.
54. Ferguson, A. D., McKeever, B. M., Xu, S., Wisniewski, D., Miller, D. K., Yamin, T. T., Spencer, R. H., Chu, L., Ujjainwalla, F., Cunningham, B. R., Evans, J. F., and Becker, J. W. (2007) Crystal structure of inhibitor-bound human 5-lipoxygenase-activating protein. Science 317, 510-512. (Pubitemid 47196114)
55. Jegerschold, C., Pawelzik, S. C., Purhonen, P., Bhakat, P., Gheorghe, K. R., Gyobu, N., Mitsuoka, K., Morgenstern, R., Jakobsson, P. J., and Hebert, H. (2008) Structural basis for induced formation of the inflammatory mediator prostaglandin E2. Proc. Natl. Acad. Sci. U.S.A. 105, 11110-11115.
56. Jasti, J., Furukawa, H., Gonzales, E. B., and Gouaux, E. (2007) Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449, 316-323. (Pubitemid 47443482)
57. Gonzales, E. B., Kawate, T., and Gouaux, E. (2009) Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 460, 599-604.
58. von Heijne, G. (1981) Membrane proteins: The amino acid composition of membrane-penetrating segments. Eur. J. Biochem. 120, 275-278.
59. O'Neil, K. T., and DeGrado, W. F. (1990) A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids. Science 250, 646-651. (Pubitemid 120034280)
60. Lyu, P. C., Liff, M. I., Marky, L. A., and Kallenbach, N. R. (1990) Side chain contributions to the stability of α-helical structure in peptides. Science 250, 669-673. (Pubitemid 120034286)
61. Pace, C. N., and Scholtz, J. M. (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 75, 422-427. (Pubitemid 28311831)
62. Chou, P. Y., and Fasman, G. D. (1974) Conformational parameters for amino acids in helical, β-sheet, and random coil regions calculated from proteins. Biochemistry 13, 211-222.
63. Senes, A., Ubarretxena-Belandia, I., and Engelman, D. M. (2001) The Cα-H⋯O hydrogen bond: A determinant of stability and specificity in transmembrane helix interactions. Proc. Natl. Acad. Sci. U.S.A. 98, 9056-9061. (Pubitemid 32743868)
64. Grottesi, A., Domene, C., Hall, B., and Sansom, M. S. (2005) Conformational dynamics of M2 helices in KirBac channels: Helix flexibility in relation to gating via molecular dynamics simulations. Biochemistry 44, 14586-14594. (Pubitemid 41567466)
65. Yi, M., Cross, T. A., and Zhou, H. X. (2009) Conformational heterogeneity of the M2 proton channel and a structural model for channel activation. Proc. Natl. Acad. Sci. U.S.A. 106, 13311-13316.
66. +Conduction and Selectivity. Science 280, 69-77.
67. Xu, F., Wang, A., Vaughn, J. B., Jr., and Cross, T. A. (1996) A Catalytic Role for Protic Solvents in Conformational Interconversion. J. Am. Chem. Soc. 118, 9176-9177. (Pubitemid 26342556)
68. Xu, F., and Cross, T. A. (1999) Water: Foldase activity in catalyzing polypeptide conformational rearrangements. Proc. Natl. Acad. Sci. U.S.A. 96, 9057-9061. (Pubitemid 29374706)
69. Brewer, M. L., Schmitt, U. W., and Voth, G. A. (2001) The formation and dynamics of proton wires in channel environments. Biophys. J. 80, 1691-1702. (Pubitemid 32280985)
70. Pomès, R., and Roux, B. (1996) Structure and dynamics of a proton wire: A theoretical study of H+ translocation along the single-file water chain in the gramicidin A channel. Biophys. J. 71, 19-39. (Pubitemid 26227289)
71. Javadpour, M. M., Eilers, M., Groesbeek, M., and Smith, S. O. (1999) Helix packing in polytopic membrane proteins: Role of glycine in transmembrane helix association. Biophys. J. 77, 1609-1618. (Pubitemid 29407334)
72. MacKenzie, K. R., Prestegard, J. H., and Engelman, D. M. (1997) A Transmembrane Helix Dimer: Structure and Implications. Science 276, 131-133. (Pubitemid 27161261)
73. Yohannan, S., Faham, S., Yang, D., Grosfeld, D., Chamberlain, A. K., and Bowie, J. U. (2004) A Cα-H⋯O hydrogen bond in a membrane protein is not stabilizing. J. Am. Chem. Soc. 126, 2284-2285. (Pubitemid 38295690)
74. Russ, W. P., and Engelman, D. M. (2000) The GxxxG motif: A framework for transmembrane helix-helix association. J. Mol. Biol. 296, 911-919.
75. 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. (Pubitemid 38509359)
76. 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. (Pubitemid 34498904)
77. 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. (Pubitemid 39094354)
78. Kim, S., Jeon, T. J., Oberai, A., Yang, D., Schmidt, J. J., and Bowie, J. U. (2005) Transmembrane glycine zippers: Physiological and pathological roles in membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 14278-14283. (Pubitemid 41429689)
79. Wigley, W. C., Corboy, M. J., Cutler, T. D., Thibodeau, P. H., Oldan, J., Lee, M. G., Rizo, J., Hunt, J. F., and Thomas, P. J. (2002) A protein sequence that can encode native structure by disfavoring alternate conformations. Nat. Struct. Biol. 9, 381-388. (Pubitemid 34462558)
80. Deber, C. M., and Therien, A. G. (2002) Putting the β-breaks on membrane protein misfolding. Nat. Struct. Biol. 9, 318-319. (Pubitemid 34462544)
81. 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. (Pubitemid 44967776)
82. + antiporter from a cyanobacterium. Biochemistry 50, 788-794.
83. Ashkenazy, H., Erez, E., Martz, E., Pupko, T., and Ben-Tal, N. (2010) ConSurf 2010: Calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529-W533.
84. Yin, Y., He, X., Szewczyk, P., Nguyen, T., and Chang, G. (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science 312, 741-744.