Bilayer surface association of the pHLIP peptide promotes extensive backbone desolvation and helically-constrained structures

Biophysical Chemistry

Volumn 187-188, Issue , 2014, Pages 1-6

  Brown, Mia C ^a   Yakubu, Rauta A ^a   Taylor, Jay ^a   Halsey, Christopher M ^a   Xiong, Jian ^a   Jiji, Renee D ^a   Cooley, Jason W ^a  

^a UNIVERSITY OF MISSOURI   (United States)

Author keywords

Amide I; Deep UV resonance Raman spectroscopy; Membrane protein; pHLIP; Structural transition

Indexed keywords

MEMBRANE PROTEIN; PHLIP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; LIPID BILAYER; LIPID VESICLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SURFACE PROPERTY; ULTRAVIOLET RADIATION;

AMIDE I; DEEP-UV RESONANCE RAMAN SPECTROSCOPY; MEMBRANE PROTEIN; PHLIP; STRUCTURAL TRANSITION;

LIPID BILAYERS; MEMBRANE PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; SURFACE PROPERTIES;

EID: 84892404480     PISSN: 03014622     EISSN: 18734200     Source Type: Journal    
DOI: 10.1016/j.bpc.2013.12.004     Document Type: Article

References (54)

1. A. Badou, M.K. Jha, D. Matza, and R.A. Flavell Emerging roles of L-type voltage-gated and other calcium channels in T lymphocytes Front. Immunol. 4 2013
2. E.L. Eskelinen, Y. Tanaka, and P. Saftig At the acidic edge: emerging functions for lysosomal membrane proteins Trends Cell Biol. 13 2003 137 145
3. J.D. Muller, N. Wu, and K. Palczewski Vertebrate membrane proteins: structure, function, and insights from biophysical approaches Pharmacol. Rev. 60 2008 43 78
4. J.N. Sachs, and D.M. Engelman Introduction to the membrane protein reviews: the interplay of structure, dynamics, and environment in membrane protein function Annu. Rev. Biochem. 75 2006 707 712
5. S. Urban, and S.W. Dickey The rhomboid protease family: a decade of progress on function and mechanism Genome Biol. 12 2011
6. S.H. White Biophysical dissection of membrane proteins Nature 459 2009 344 346
7. L.D. Barron, L. Hecht, and G. Wilsn The lubricant of life: a proposal that solvent water promotes extremely fast conformational fluctuations in mobile heteropolypeptide structure Biochemistry 36 1997 13143 13147
8. R.H. Callender, R.B. Dyer, R. Gilmanshin, and W.H. Woodruff Fast events in protein folding: the time evolution of primary processes Annu. Rev. Phys. Chem. 49 1998 173 202
9. I.K. Lednev, A.S. Karnoup, M.C. Sparrow, and S.A. Asher Nanosecond UV resonance Raman examination of initial steps in alpha-helix secondary structure evolution J. Am. Chem. Soc. 121 1999 4076 4077
10. R.B. Dyer, F. Gai, and W.H. Woodruff Infrared studies of fast events in protein folding Acc. Chem. Res. 31 1998 709 716
11. C.M. Phillips, Y. Mizutani, and R.M. Hochstrasser Ultrafast thermally-induced unfolding of RNase-A Proc. Natl. Acad. Sci. U. S. A. 92 1995 7292 7296
12. C.Y. Huang, Z. Getahun, Y. Zhu, J.W. Klemke, W.F. DeGrado, and F. Gai Helix formation via conformation diffused search Proc. Natl. Acad. Sci. U. S. A. 99 2002 2788 2793
13. C.Y. Huang, G. Balakrishnan, and T.G. Spiro Early events in apomyoglobin unfolding probed by laser T-jump/UV resonance Raman spectroscopy Biochemistry 44 2005 15734 15742
14. M.C. Chen, and R.C. Lord Laser-excited Raman-spectroscopy of biomolecules. IV. Some polypeptides as conformational models J. Am. Chem. Soc. 96 1974 4750 4752
15. P.C. Painter, and J.L. Koenig Solution conformation of poly(L-lysine) - Raman and infrared spectroscopic study Biopolymers 15 1976 229 240
16. M. Jackson, P.I. Haris, and D. Chapman Conformational transitions of poly(L-lysine): studies using Fourier transform infrared spectroscopy Biochim. Biophys. Acta Protein Struct. Mol. Enzymol. 998 1989 75 79
17. R.A. Copeland, and T.G. Spiro Secondary structure determination in proteins from deep (192-223 nm) ultraviolet resonance Raman-spectroscopy Biochemistry 26 1987 2134 2139
18. S.H. Song, and S.A. Asher UV resonance Raman studies of peptide conformation in poly(L-lysine), poly(L-glutamic acid), and model complexes - the basis for protein secondary structure determinations J. Am. Chem. Soc. 111 1989 4295 4305
19. V.A. Shashilov, V. Sikirzhytski, L.A. Popova, and I.K. Lednev Quantitative methods for structural characterization of proteins based on deep UV resonance Raman spectroscopy Methods 52 2010 23 37
20. S.A. Asher, A.V. Mikhonin, and S. Bykov UV Raman demonstrates that alpha-helical polyalanine peptides melt to polyproline II conformations J. Am. Chem. Soc. 126 2004 8433 88440
21. G. Balakrishnan, Y. Hu, G.M. Bender, Z. Getahun, W.F. DeGrado, and T.G. Spiro Enthalpic and entropic stages in α-helical peptide unfolding, from laser T-jump/UV Raman spectroscopy J. Am. Chem. Soc. 129 2007 12801 12808
22. G. Balakrishnan, C.L. Weeks, M. Ibrahim, A.V. Soldatova, and T.G. Spiro Proteins dynamics from time resolved UV Raman spectroscopy Curr. Opin. Struct. Biol. 18 2008 623 629
23. R.D. JiJi, G. Balakrishnan, Y. Hu, and T.G. Spiro Intermediacy of poly(L-proline) II and β-strand conformations in poly(L-lysine) β-sheet formation, probed by temperature-jump/UV resonance Raman spectroscopy Biochemistry 45 2006 34 41
24. I.K. Lednev, A.S. Karnoup, M.C. Sparrow, and S.A. Asher Transient UV Raman spectroscopy finds no crossing barrier between the peptide alpha-helix and fully random coil conformation J. Am. Chem. Soc. 123 2001 2388 2392
25. V.A. Shashilov, and I.K. Lednev 2D correlation deep UV resonance Raman spectroscopy of early events of lysozyme fibrillation: kinetic mechanism and potential interpretation pitfalls J. Am. Chem. Soc. 130 2008 309 317
26. N.I. Topilina, V.V. Ermolenkov, V. Sikirzhytski, S. Higashiya, I.K. Lednev, and J.T. Welch A de novo designed 11 kDa polypeptide: a model for amyloidogenic intrinsically disordered proteins Biopolymers 93 2010 607 618
27. Z. Chi, X.G. Chen, J.S.W. Holtz, and S.A. Asher UV resonance Raman-selective amide vibrational enhancement: quantitative methodology for determining protein secondary structure Biochemistry 37 1998 2854 2864
28. C.Y. Huang, G. Balakrishnan, and T.G. Spiro Protein secondary structure from deep-UV resonance Raman spectroscopy J. Raman Spectrosc. 37 2006 277 282
29. V.A. Shashilov, M. Xu, V.V. Ermolenkov, and I.K. Lednev Latent variable analysis of Raman spectra for structural characterization of proteins J. Quant. Spectrosc. Radiat. Transf. 102 2006 46 61
30. J.V. Simpson, G. Balakrishnan, and R.D. JiJi MCR-ALS analysis of two-way UV resonance Raman spectra to resolve discrete protein secondary structural motifs Analyst 134 2009 138 147
31. J.V. Simpson, O. Oshokoya, N. Wagner, J. Liu, and R.D. JiJi Pre-processing of ultraviolet Raman spectra Analyst 136 2011 1239 1247
32. A.L. Rucker, and T.P. Creamer Polyproline II helical structure in protein unfolded states: lysine peptides revisited Protein Sci. 11 2002 980 985
33. M.L. Tiffany, and S. Krimm New chain conformations of poly(glutamic acid) and polylysine Biopolymers 6 1968 1379 1382
34. M.L. Tiffany, and S. Krimm Extended conformations of polypeptides and proteins in urea and guanidine hydrochloride Biopolymers 12 1973 575 587
35. A.V. Mikhonin, N.S. Myshakina, S.V. Bykov, and S.A. Asher UV resonance Raman determination of polyproline II, extended 2.51-helix, and β-sheet ψ angle energy landscape in poly-L-lysine and poly-L-glutamic acid J. Am. Chem. Soc. 127 2005 7712 7720
36. B.W. Chellgren, and T.P. Creamer Short sequences of non-proline residues can adopt the polyproline II helical conformation Biochemistry 43 2004 5864 5869
37. C. Halsey, J. Xiong, O. Oshokoya, J. Johnson, S. Shinde, T.J. Beaty, G. Ghirlanda, R. JiJi, and J. Cooley Simultaneous observation of peptide backbone lipid solvation and α-helical structure by deep-UV resonance Raman spectroscopy Chembiochem 12 2011 2125 2128
38. J.F. Hunt, P. Rath, K.J. Rothschild, and D.M. Engleman Spontaneous, pH-dependent membrane insertion of a transbilayer α-helix Biochemistry 36 1997 15177 15192
39. Y.K. Reshetnyak, M. Segala, O.A. Andreev, and D.M. Engelman A monomeric membrane peptide that lives in three worlds: in solutions, attached to, and inserted across lipid bilayers Biophys. J. 93 2007 2363 2372
40. M. Zoonens, Y.K. Reshetnyak, and D.M. Engelman Bilayer interactions of pHLIP, a peptide that can deliver drugs and target tumors Biophys. J. 95 2008 225 235
41. D. Weerakkody, A. Moshnikova, M.S. Thakur, V. Moshnikova, J. Daniels, D.M. Engelman, O.A. Andreev, and Y.K. Reshetnyak Family of pH (low) insertion peptides for tumor targeting Proc. Natl. Acad. Sci. 110 2013 5834 5839
42. J. Fendos, F.N. Barrera, and D.M. Engelman Aspartate embedding depth affects pHLIP's insertion pKa Biochemistry 52 2013 4595 4604
43. G. Rouser, S. Fleischer, and A. Yamamoto Two dimensional thin-layer chromatographic separation of polar lipids and determination of phospholipids by phosphorous analysis of spots Lipids 5 1970 494 496
44. M. Wang, and R.D. JiJi Resolution of localized small molecule - aβ interactions by deep-ultraviolet resonance Raman spectroscopy Biophys. Chem. 158 2011 96 103
45. J.R. Ferraro, K. Nakamoto, and C.V. Brown Introductory Raman Spectroscopy 2nd ed. 1994 Academic Press San Diego, CA
46. J. Tang, and F. Gai Dissecting the membrane binding and insertion kinetics of a pHLIP peptide Biochemistry 47 2008 8250 8252
47. Y. Wang, R. Purrello, T. Jordan, and T.G. Spiro UVRR spectroscopy of the peptide bond. 1. Amide S, a nonhelical structure marker, is a C.alpha.H bending mode J. Am. Chem. Soc. 113 1991 6359 6368
48. S. Krimm, and J. Bandekar Vibrational spectroscopy and conformation of peptides, polypeptides and proteins C. Anfinson, J.T. Edsall, F.M. Richards, Advances in Protein Chemistry 1986 Academic Press New York 181 365
49. J.C. Austin, T. Jordan, and T.G. Spiro Ultraviolet resonance Raman studies of proteins and related model compounds R.J.H. Clark, R.E. Hester, Biomolecular Spectroscopy, Part A 1993 John Wiley & Sons Ltd. New York 55 127
50. Y. Wang, R. Purrello, S. Georgiou, and T.G. Spiro UVRR spectroscopy of the peptide bond. 2. Carbonyl H-bond effects on the ground- and excited-state structures of N-methylacetamide J. Am. Chem. Soc. 113 1991 6368 6377
51. S.A. Oladepo, K. Xiong, Z. Hong, and S.A. Asher Elucidating peptide and protein structure and dynamics: UV resonance Raman spectroscopy J. Phys. Chem. Lett. 2 2011 334 344
52. A.V. Mikhonin, S.V. Bykov, N.S. Myshakina, and S.A. Asher Peptide secondary structure folding reaction coordinate: correlation between UV Raman amide III frequency, psi Ramachandran angle, and hydrogen bonding J. Phys. Chem. B 110 2006 1928 1943
53. Y. Deng, Z. Qian, Y. Luo, Y. Zhang, Y. Mu, and G. Wei Membrane binding and insertion of a pHLIP peptide studied by all-atom molecular dynamics simulations Int. J. Mol. Sci. 14 2013 14532 14549
54. M. Eagleburger, J.W. Cooley, R. D. JiJi, Effects of fluidity on the ensemble structure of a membrane embedded α-helical peptide, unpublished results, (2013).