Tryptophan-lipid interactions in membrane protein folding probed by ultraviolet resonance Raman and fluorescence spectroscopy

Biophysical Journal

Volumn 100, Issue 9, 2011, Pages 2121-2130

  Sanchez, Katheryn M ^a   Kang, Guipeun ^a   Wu, Beijing ^a   Kim, Judy E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79959731678     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.03.018     Document Type: Article

References (66)

1. White, S. H., and W. C. Wimley. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-365. (Pubitemid 29319262)
2. Popot, J., and D. M. Engelman. 2000. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 69:881-922.
3. Tamm, L. K., H. Hong, and B. Liang. 2004. Folding and assembly of beta-barrel membrane proteins. Biochim. Biophys. Acta. 1666:250-263. (Pubitemid 39425208)
4. Booth, P. J., R. H. Templer,..., M. Lorch. 2001. In vitro studies of membrane protein folding. Crit. Rev. Biochem. Mol. Biol. 36:501-603. (Pubitemid 34056526)
5. Lee, A. G. 2003. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta. 1612:1-40. (Pubitemid 36555684)
6. MacKenzie, K. R. 2006. Folding and stability of alpha-helical integral membrane proteins. Chem. Rev. 106:1931-1977. (Pubitemid 43792787)
7. Wimley, W. C., T. P. Creamer, and S. H. White. 1996. Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry. 35:5109-5124.
8. Hessa, T., H. Kim,..., G. von Heijne. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature. 433:377-381. (Pubitemid 40203311)
9. Roseman, M. A. 1988. Hydrophobicity of the peptide C=O. H-N hydrogen-bonded group. J. Mol. Biol. 201:621-623.
10. Ben-Tal, N., D. Sitkoff,..., B. Honig. 1997. Free energy of amide hydrogen bond formation in vacuum, in water, and in liquid alkane solution. J. Phys. Chem. B. 101:450-457. (Pubitemid 127617329)
11. Lee, A. G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta. 1666:62-87. (Pubitemid 39425199)
12. Babakhani, A., A. A. Gorfe,..., J. A. McCammon. 2007. Peptide insertion, positioning, and stabilization in a membrane: insight from an allatom molecular dynamics simulation. Biopolymers. 85:490-497. (Pubitemid 46649829)
13. Yau, W.-M., W. C. Wimley,..., S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry. 37:14713-14718. (Pubitemid 28487579)
14. Killian, J. A., and G. von Heijne. 2000. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 25:429-434. (Pubitemid 30662410)
15. Reithmeier, R. A. F. 1995. Characterization and modeling of membrane proteins using sequence analysis. Curr. Opin. Struct. Biol. 5:491-500.
16. Gallivan, J. P., and D. A. Dougherty. 1999. Cation-pi interactions in structural biology. Proc. Natl. Acad. Sci. USA. 96:9459-9464.
17. Millefiori, S., A. Alparone,..., A. Vanella. 2008. Electronic and vibrational polarizabilities of the twenty naturally occurring amino acids. Biophys. Chem. 132:139-147. (Pubitemid 350251886)
18. Dornmair, K., H. Kiefer, and F. Jahnig. 1990. Refolding of an integral membrane protein. J. Biol. Chem. 265:18907-18911.
19. Kleinschmidt, J. H., and L. K. Tamm. 1999. Time-resolved distance determination by tryptophan fluorescence quenching: probing intermediates in membrane protein folding. Biochemistry. 38:4996-5005.
20. Hong, H., and L. K. Tamm. 2004. Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc. Natl. Acad. Sci. USA. 101:4065-4070. (Pubitemid 38405884)
21. Ramakrishnan, M., J. Qu,..., D. Marsh. 2005. Orientation of betabarrel proteins OmpA and FhuA in lipid membranes. Chain length dependence from infrared dichroism. Biochemistry. 44:3515-3523. (Pubitemid 40322021)
22. Kleinschmidt, J. H. 2006. Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers. Chem. Phys. Lipids. 141:30-47. (Pubitemid 43744430)
23. Kim, J. E., G. Arjara,..., J. R. Winkler. 2006. Probing folded and unfolded states of outer membrane protein A using steady-state and time-resolved tryptophan fluorescence. J. Phys. Chem. B. 110:17656-17662. (Pubitemid 44412516)
24. Hong, H., S. Park,..., L. K. Tamm. 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)
25. Kleinschmidt, J. H., T. den Blaauwen,..., L. K. Tamm. 1999. Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism. Biochemistry. 38:5006-5016.
26. Sanchez, K. M., J. E. Gable,..., J. E. Kim. 2008. Effects of tryptophan microenvironment, soluble domain, and vesicle size on the thermodynamics of membrane protein folding: Lessons from the transmembrane protein OmpA. Biochemistry. 47:12844-12852.
27. Sanchez, K. M., T. J. Neary, and J. E. Kim. 2008. UV resonance Raman spectroscopy of folded and unfolded states of an integral membrane protein. J. Phys. Chem. B. 112:9507-9511.
28. Shafaat, H. S., K. M. Sanchez,..., J. E. Kim. 2008. Ultraviolet resonance Raman spectroscopy of a membrane-bound beta-sheet peptide as a model for membrane protein folding. J. Raman Spectrosc. 40:1060-1064.
29. Huang, C.-Y., G. Balakrishnana, and T. G. Spiro. 2005. Early events in apomyoglobin unfolding probed by laser T-jump/UV resonance Raman spectroscopy. Biochemistry. 44:15734-15742. (Pubitemid 41746904)
30. Ahmed, A., I. A. Beta,..., S. A. Asher. 2005. UV-resonance Raman thermal unfolding study of trp-cage shows that it is not a simple twostate miniprotein. J. Am. Chem. Soc. 127:10943-10950. (Pubitemid 41129869)
31. Rodriguez-Mendieta, I. R., G. R. Spence,..., D. A. Smith. 2005. Ultraviolet resonance Raman studies reveal the environment of tryptophan and tyrosine residues in the native and partially unfolded states of the E colicin-binding immunity protein Im7. Biochemistry. 44:3306-3315. (Pubitemid 40322001)
32. Harada, I., and H. Takeuchi. 1986. Raman and ultraviolet resonance Raman spectra of proteins and related compounds. In Spectroscopy of Biological Systems. R. J. H. Clark and R. E. Hester, editors. John Wiley & Sons, Chichester. 113-175.
33. Schlamadinger, D. E., J. E. Gable, and J. E. Kim. 2009. Hydrogenbonding and solvent polarity markers in the UV resonance Raman spectrum of tryptophan: application to membrane proteins. J. Phys. Chem. B. 113:14769-14778.
34. Chi, Z., and S. A. Asher. 1998. UV Raman determination of the environment and solvent exposure of tyr and trp residues. J. Phys. Chem. B. 102:9595-9602. (Pubitemid 128611879)
35. Austin, J. C., T. Jordan, and T. G. Spiro. 1993. Ultraviolet resonance Raman studies of proteins and related model compounds. In Biomolecular Spectroscopy, Part. A. R. J. H. Clark and R. E. Hester, editors. John Wiley and Sons, New York. 55-127.
36. Surrey, T., and F. Jahnig. 1992. Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc. Natl. Acad. Sci. USA. 89:7457-7461.
37. Miura, T., H. Takeuchi, and I. Harada. 1988. Characterization of individual tryptophan side chains in proteins using Raman spectroscopy and hydrogen-deuterium exchange kinetics. Biochemistry. 27:88-94.
38. Harada, I., T. Miura, and H. Takeuchi. 1986. Origin of the doublet at 1360 and 1340 cm-1 in the Raman spectra of tryptophan and related compounds. Spectrochim. Acta [A]. 42 A: 307-312.
39. Miura, T., H. Takeuchi, and I. Harada. 1989. Tryptophan Raman bands sensitive to hydrogen bonding and side-chain conformation. J. Raman Spectrosc. 20:667-671.
40. Kleinschmidt, J. H., and L. K. Tamm. 2002. Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is syncrhonized and depends on membrane thickness. J. Mol. Biol. 324:319-330. (Pubitemid 35379031)
41. Surrey, T., and F. Jahnig. 1995. Kinetics of folding and membrane insertion of a beta-barrel membrane protein. J. Biol. Chem. 270:28199-28203.
42. Miller, D., K. Charalambous,..., P. J. Booth. 2009. In vitro unfolding and refolding of the small multidrug transporter EmrE. J. Mol. Biol. 393:815-832.
43. Allen, S. J., A. R. Curran,..., P. J. Booth. 2004. Controlling the folding efficiency of an integral membrane protein. J. Mol. Biol. 342:1293-1304. (Pubitemid 39207903)
44. Clark, E. H., J. M. East, and A. G. Lee. 2003. The role of tryptophan residues in an integral membrane protein: diacylglycerol kinase. Biochemistry. 42:11065-11073. (Pubitemid 37174399)
45. White, S. H., A. S. Ladokhin,..., K. Hristova. 2001. How membranes shape protein structure. J. Biol. Chem. 276:32395-32398.
46. Persson, S., J. A. Killian, and G. Lindblom. 1998. Molecular ordering of interfacially localized tryptophan analogs in ester-and ether-lipid bilayers studied by H-2-NMR. Biophys. J. 75:1365-1371. (Pubitemid 28397605)
47. Gaede, H. C., W.-M. Yau, and K. Gawrisch. 2005. Electrostatic contributions to indole-lipid interactions. J. Phys. Chem. B. 109:13014-13023. (Pubitemid 40999829)
48. Sanderson, J. M. 2007. Refined models for the preferential interactions of tryptophan with phosphocholines. Org. Biomol. Chem. 5:3276-3286. (Pubitemid 47519065)
49. Huysmans, G. H. M., S. A. Baldwin,..., S. E. Radford. 2010. The transition state for folding of an outer membrane protein. Proc. Natl. Acad. Sci. USA. 107:4099-4104.
50. Gao, J., D. A. Bosco,..., J. W. Kelly. 2009. Localized thermodynamic coupling between hydrogen bonding and microenvironment polarity substantially stabilizes proteins. Nat. Struct. Biol. 16:684-691.
51. Joh, N. H., A. Min,..., J. U. Bowie. 2008. Modest stabilization by most hydrogen-bonded side-chain interactions in membrane proteins. Nature. 453:1266-1270. (Pubitemid 351913594)
52. Shan, S., and D. Herschlag. 1996. The change in hydrogen bond strength accompanying charge rearrangement: Implications for enzymatic catalysis. Proc. Natl. Acad. Sci. USA. 93:14474-14479. (Pubitemid 26418991)
53. Takano, K., J. M. Scholtz,..., C. N. Pace. 2003. The contribution of polar group burial to protein stability is strongly context-dependent. J. Biol. Chem. 278:31790-31795. (Pubitemid 37048360)
54. Sun, H., D. V. Greathouse,..., R. E. Koeppe. 2008. The preference of tryptophan for membrane interfaces: insights from N-methylation of tryptophans in gramicidin channels. J. Biol. Chem. 283:22233-22243.
55. van der Wel, P. C. A., N. D. Reed,..., R. E. Koeppe. 2007. Orientation and motion of tryptophan interfacial anchors in membrane-spanning peptides. Biochemistry. 46:7514-7524. (Pubitemid 46986378)
56. Petersen, F. N. R., M. O. Jensen, and C. H. Nielsen. 2005. Interfacial tryptophan residues: a role of the cation-pi effect? Biophys. J. 89:3985-3996. (Pubitemid 41725619)
57. Norman, K. E., and H. Nymeyer. 2006. Indole localization in lipid membranes revealed by molecular simulations. Biophys. J. 91:2046-2054. (Pubitemid 44354753)
58. Burley, S. K., and G. A. Petsko. 1985. Aromatic-aromatic interaction: a mechanism of protein structural stabilization. Science. 229:23-28.
59. Guvench, O., and C. L. Brooks, III. 2005. Tryptophan side chain electrostatic interactions determine edge-to-face vs parallel-displaced tryptophan side chain geometries in the designed beta-hairpin "trpzip2". J. Am. Chem. Soc. 127:4668-4674. (Pubitemid 40489623)
60. Bunte, S. W., G. M. Jensen,..., K. J. Jalkanen. 2001. Theoretical determination of the vibrational absorption and Raman spectra of 3-methylindole and 3-methylindole radicals. Chem. Phys. 265:13-25. (Pubitemid 32230198)
61. Jensen, G. M., D. B. Goodin, and S. W. Bunte. 1996. Density functional and MP2 calculations of spin densities of oxidized 3-methylindole: models for tryptophan radicals. J. Phys. Chem. 100:954-959. (Pubitemid 126789244)
62. Okada, A., T. Miura, and H. Takeuchi. 2001. Protonation of histidine and histidine-tryptophan interactions in the activation of the M2 ion channel from influenza A virus. Biochemistry. 40:6053-6060. (Pubitemid 32466308)
63. Wen, Z. Q., and G. J. Thomas, Jr. 2000. Ultraviolet-resonance Raman spectroscopy of the filamentous virus Pf3: interactions of Trp-38 specific to the assembled virion subunit. Biochemistry. 39:146-152. (Pubitemid 30033329)
64. Schlamadinger, D. E., M. M. Daschbach,..., J. E. Kim. 2010. UV resonance Raman study of cation-pi interactions in an indole crown ether. J. Raman Spectrosc., accepted.
65. Xue, Y., A. V. Davis,..., T. V. O'Halloran. 2008. Cu (I) recognition via cation-pi and methionine interactions in CusF. Nat. Chem. Biol. 4:107-109.
66. Sanderson, J. M., and E. J. Whelan. 2004. Characterization of the interactions of aromatic amino acids with diacetyl phosphatidylcholine. Phys. Chem. Chem. Phys. 6:1012-1017.