Response of GWALP transmembrane peptides to changes in the tryptophan anchor positions

Biochemistry

Volumn 50, Issue 35, 2011, Pages 7522-7535

  Vostrikov, Vitaly V ^a,b   Koeppe, Roger E ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID COMPOSITIONS; AVERAGE ORIENTATION; C-TERMINUS; CORE REGION; FINE ADJUSTMENTS; HELIX ORIENTATION; INDOLE RINGS; INTERFACIAL INTERACTION; LIPID BILAYER MEMBRANES; PEPTIDE-LIPID INTERACTIONS; PREFERRED ORIENTATIONS; PROTEIN-LIPID INTERACTIONS; RADIAL SEPARATIONS; SECONDARY STRUCTURES; SEQUENCE ISOMERS; SIDE-CHAINS; TORSION ANGLE; TRANSMEMBRANES; TRYPTOPHAN RESIDUES;

AMINO ACIDS; DEUTERIUM; ISOMERS; LIPID BILAYERS; RESONANCE;

PEPTIDES;

ACETYL GLYCYLGLYCYLALANYLLEUCYLTRYPTOPHYLLEUCYLALANYLLEUCYLALANYLLEUCYLALANYLLEUCYLALANYLLEUCYLALANYLLEUCYLALANYLLEUCYLTRYPTOPHYLLEUCYLALANYLGLYCYLALANINE ETHANOLAMIDE; ALANINE; INDOLE; LEUCINE; MEMBRANE PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; HYDROPHOBICITY; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID; THICKNESS;

ACETYLATION; ALANINE; AMINO ACID SEQUENCE; DEUTERIUM EXCHANGE MEASUREMENT; GLYCINE; LIPID BILAYERS; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN ENGINEERING; TRYPTOPHAN;

EID: 80052189197     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2006459     Document Type: Article

References (59)

1. 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)
2. A stabilized by intermolecular hydrogen bonding Biochim. Biophys. Acta 1788, 686-695
3. Schick, S., Chen, L., Li, E., Lin, J., Koper, I., and Hristova, K. (2010) Assembly of the M2 tetramer is strongly modulated by lipid chain length Biophys. J. 99, 1810-1817
4. Brown, M. F. (1994) Modulation of rhodopsin function by properties of the membrane bilayer Chem. Phys. Lipids 73, 159-180 (Pubitemid 24299194)
5. Landolt-Marticorena, C., Williams, K. A., Deber, C. M., and Reithmeier, R. A. (1993) Non-random distribution of amino acids in the transmembrane segments of human type I single span membrane proteins J. Mol. Biol. 229, 602-608 (Pubitemid 23068038)
6. Ulmschneider, M. B. and Sansom, M. S. P. (2001) Amino acid distributions in integral membrane protein structures Biochim. Biophys. Acta 1512, 1-14 (Pubitemid 32378779)
7. de Planque, M. R., Kruijtzer, J. A., Liskamp, R. M., Marsh, D., Greathouse, D. V., Koeppe, R. E., II, de Kruijff, B., and Killian, J. A. (1999) Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane α-helical peptides J. Biol. Chem. 274, 20839-20846
8. Davis, J. H., Clare, D. M., Hodges, R. S., and Bloom, M. (1983) Interaction of a synthetic amphiphilic polypeptide and lipids in a bilayer structure Biochemistry 22, 5298-5305
9. Killian, J. A., Salemink, I., de Planque, M. R., Lindblom, G., Koeppe, R. E., II, and Greathouse, D. V. (1996) Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane α-helical peptides: Importance of hydrophobic mismatch and proposed role of tryptophans Biochemistry 35, 1037-1045 (Pubitemid 26034591)
10. 31P solid-state NMR spectroscopy investigation Biochemistry 39, 13106-13114
11. Krishnakumar, S. S. and London, E. (2007) Effect of sequence hydrophobicity and bilayer width upon the minimum length required for the formation of transmembrane helices in membranes J. Mol. Biol. 374, 671-687 (Pubitemid 350018764)
12. 2H NMR Biophys. J. 83, 1479-1488 (Pubitemid 34977721)
13. 2H solid-state NMR Biophys. J. 86, 3709-3721 (Pubitemid 38780249)
14. de Planque, M. R., Bonev, B. B., Demmers, J. A., Greathouse, D. V., Koeppe, R. E., II, Separovic, F., Watts, A., and Killian, J. A. (2003) Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions Biochemistry 42, 5341-5348 (Pubitemid 36560430)
15. Hong, H., Park, S., Jimenez, R. H., Rinehart, D., and Tamm, L. K. (2007) Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins J. Am. Chem. Soc. 129, 8320-8327 (Pubitemid 47035142)
16. Binder, H. and Gawrisch, K. (2001) Effect of unsaturated lipid chains on dimensions, molecular order and hydration of membranes J. Phys. Chem. B 105, 12378-12390 (Pubitemid 35338340)
17. Vostrikov, V. V., Daily, A. E., Greathouse, D. V., and Koeppe, R. E., II (2010) Charged or aromatic anchor residue dependence of transmembrane peptide tilt J. Biol. Chem. 285, 31723-31730
18. Petrache, H. I., Zuckerman, D. M., Sachs, J. N., Killian, J. A., Koeppe, R. E., II, and Woolf, T. B. (2002) Hydrophobic matching mechanism investigated by molecular dynamics simulations Langmuir 18, 1340-1351 (Pubitemid 35384066)
19. Liu, J., Wang, D., Zheng, Q., Lu, M., and Arora, P. S. (2008) Atomic structure of a short α-helix stabilized by a main chain hydrogen-bond surrogate J. Am. Chem. Soc. 130, 4334-4337 (Pubitemid 351466428)
20. Froyd-Rankenberg, J. M., Greathouse, D. V., and Koeppe, R. E., II (2009) Half-anchored WALP peptides: Effect of anchor position on peptide orientation Biophys. J. 96, 455a-456a
21. Vostrikov, V. V., Grant, C. V., Daily, A. E., Opella, S. J., and Koeppe, R. E., II (2008) Comparison of "Polarization Inversion with Spin Exchange at Magic Angle" and "Geometric Analysis of Labeled Alanines" methods for transmembrane helix alignment J. Am. Chem. Soc. 130, 12584-12585
22. 2H-NMR data Biophys. J. 96, 3223-3232
23. Holt, A., Rougier, L., Reat, V., Jolibois, F., Saurel, O., Czaplicki, J., Killian, J. A., and Milon, A. (2010) Order parameters of a transmembrane helix in a fluid bilayer: Case study of a WALP peptide Biophys. J. 98, 1864-1872
24. 2H NMR study Biochemistry 44, 1004-1012 (Pubitemid 40129660)
25. Vostrikov, V. V., Hall, B. A., Greathouse, D. V., Koeppe, R. E., II, and Sansom, M. S. P. (2010) Changes in transmembrane helix alignment by arginine residues revealed by solid-state NMR experiments and coarse-grained MD simulations J. Am. Chem. Soc. 132, 5803-5811
26. OConnell, A. M., Koeppe, R. E., II, and Andersen, O. S. (1990) Kinetics of gramicidin channel formation in lipid bilayers: Transmembrane monomer association Science 250, 1256-1259 (Pubitemid 120031838)
27. Yau, W. M., Wimley, W. C., Gawrisch, K., and White, S. H. (1998) The preference of tryptophan for membrane interfaces Biochemistry 37, 14713-14718 (Pubitemid 28487579)
28. van der Wel, P. C., Reed, N. D., Greathouse, D. V., and Koeppe, R. E., II (2007) Orientation and motion of tryptophan interfacial anchors in membrane-spanning peptides Biochemistry 46, 7514-7524 (Pubitemid 46986378)
29. ten Kortenaar, P. B. W., Van Dijk, B. G., Peeters, J. M., Raaben, B. J., Adams, P. J. H. M., and Tesser, G. I. (1986) Rapid and efficient method for the preparation of Fmoc-amino acids starting from 9-fluorenylmethanol Int. J. Pept. Protein Res. 27, 398-400
30. Koeppe, R. E., II, Sun, H., van der Wel, P. C., Scherer, E. M., Pulay, P., and Greathouse, D. V. (2003) Combined experimental/theoretical refinement of indole ring geometry using deuterium magnetic resonance and ab initio calculations J. Am. Chem. Soc. 125, 12268-12276 (Pubitemid 37238859)
31. Greathouse, D. V., Koeppe, R. E., II, Providence, L. L., Shobana, S., and Andersen, O. S. (1999) Design and characterization of gramicidin channels Methods Enzymol. 294, 525-550 (Pubitemid 28483378)
32. Davis, J. H., Jeffrey, K. R., Bloom, M., Valic, M. I., and Higgs, T. P. (1976) Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains Chem. Phys. Lett. 42, 390-394
33. 2H NMR spectra from deuterated aromatic rings J. Am. Chem. Soc. 127, 17488-17493 (Pubitemid 41791069)
34. Sun, H., Greathouse, D. V., Andersen, O. S., and Koeppe, R. E., II (2008) The preference of tryptophan for membrane interfaces: Insights from N-methylation of tryptophans in gramicidin channels J. Biol. Chem. 283, 22233-22243
35. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
36. Monera, O. D., Sereda, T. J., Zhou, N. E., Kay, C. M., and Hodges, R. S. (1995) Relationship of sidechain hydrophobicity and α-helical propensity on the stability of the single-stranded amphipathic α-helix J. Pept. Sci. 1, 319-329
37. White, S. H. and von Heijne, G. (2008) How translocons select transmembrane helices Annu. Rev. Biophys. 37, 23-42
38. Granseth, E., von Heijne, G., and Elofsson, A. (2005) A study of the membrane-water interface region of membrane proteins J. Mol. Biol. 346, 377-385 (Pubitemid 40128328)
39. 2H solid-state NMR spectroscopy Biochemistry 43, 10502-10512 (Pubitemid 39079321)
40. Hessa, T., Kim, H., Bihlmaier, K., Lundin, C., Boekel, J., Andersson, H., Nilsson, I., White, S. H., and von Heijne, G. (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon Nature 433, 377-381 (Pubitemid 40203311)
41. 31P solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes Biochemistry 40, 9428-9437 (Pubitemid 32730067)
42. 31P solid-state NMR spectroscopy Biophys. J. 96, 86-100
43. Salnikov, E. S. and Bechinger, B. (2011) Lipid-controlled peptide topology and interactions in bilayers: Structural insights into the synergistic enhancement of the antimicrobial activities of PGLa and magainin 2 Biophys. J. 100, 1473-1480
44. Vostrikov, V. V. (2011) Protein-lipid interactions: Influence of anchoring groups and buried arginine on the properties of membrane-spanning peptides, Ph.D. Thesis, University of Arkansas, Fayetteville, AR.
45. Lee, J. and Im, W. (2008) Transmembrane helix tilting: Insights from calculating the potential of mean force Phys. Rev. Lett. 100, 018103
46. Ozdirekcan, S., Etchebest, C., Killian, J. A., and Fuchs, P. F. J. (2007) On the orientation of a designed transmembrane peptide: Toward the right tilt angle? J. Am. Chem. Soc. 129, 15174-15181 (Pubitemid 350247801)
47. Esteban-Martin, S. and Salgado, J. (2007) The dynamic orientation of membrane-bound peptides: Bridging simulations and experiments Biophys. J. 93, 4278-4288 (Pubitemid 350294475)
48. MacCallum, J. L., Bennett, W. F., and Tieleman, D. P. (2008) Distribution of amino acids in a lipid bilayer from computer simulations Biophys. J. 94, 3393-3404
49. Hessa, T., Meindl-Beinker, N. M., Bernsel, A., Kim, H., Sato, Y., Lerch-Bader, M., Nilsson, I., White, S. H., and von Heijne, G. (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon Nature 450, 1026-1030 (Pubitemid 350273612)
50. Wiener, M. C. and White, S. H. (1992) Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. III. Complete structure Biophys. J. 61, 434-447
51. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd ed., Springer, Berlin.
52. Kim, T. and Im, W. (2010) Revisiting hydrophobic mismatch with free energy simulation studies of transmembrane helix tilt and rotation Biophys. J. 99, 175-183
53. Sengupta, D., Smith, J. C., and Ullmann, G. M. (2008) Partitioning of amino-acid analogues in a five-slab membrane model Biochim. Biophys. Acta 1778, 2234-2243
54. Bechinger, B., Resende, J. M., and Aisenbrey, C. (2011) The structural and topological analysis of membrane-associated polypeptides by oriented solid-state NMR spectroscopy: Established concepts and novel developments Biophys. Chem. 153, 115-125
55. Marsh, D. (2008) Energetics of hydrophobic matching in lipid-protein interactions Biophys. J. 94, 3996-4013
56. Samuli Ollila, O. H., Louhivuori, M., Marrink, S. J., and Vattulainen, I. (2011) Protein shape change has a major effect on the gating energy of a mechanosensitive channel Biophys. J. 100, 1651-1659
57. Koeppe, R. E., II, Killian, J. A., and Greathouse, D. V. (1994) Orientations of the tryptophan 9 and 11 side chains of the gramicidin channel based on deuterium nuclear magnetic resonance spectroscopy Biophys. J. 66, 14-24 (Pubitemid 24016479)
58. Hu, W., Lazo, N. D., and Cross, T. A. (1995) Tryptophan dynamics and structural refinement in a lipid bilayer environment: Solid state NMR of the gramicidin channel Biochemistry 34, 14138-14146
59. de Planque, M. R. and Killian, J. A. (2003) Protein-lipid interactions studied with designed transmembrane peptides: Role of hydrophobic matching and interfacial anchoring Mol. Membr. Biol. 20, 271-284 (Pubitemid 37406619)