Insights into Protein Structure and Dynamics by Ultraviolet and Visible Resonance Raman Spectroscopy.

Raman spectroscopy is a form of vibrational spectroscopy based on inelastic scattering of light. In resonance Raman spectroscopy, the wavelength of the incident light falls within an absorption band of a chromophore, and this overlap of excitation and absorption energy greatly enhances the Raman scattering efficiency of the absorbing species. The ability to probe vibrational spectra of select chromophores within a complex mixture of molecules makes resonance Raman spectroscopy an excellent tool for studies of biomolecules. In this Current Topic, we discuss the type of molecular insights obtained from steady-state and time-resolved resonance Raman studies of a prototypical photoactive protein, rhodopsin. We also review recent efforts in ultraviolet resonance Raman investigations of soluble and membrane-associated biomolecules, including integral membrane proteins and antimicrobial peptides. These examples illustrate that resonance Raman is a sensitive, selective, and practical method for studying the structures of biological molecules, and the molecular bonding, geometry, and environments of protein cofactors, the backbone, and side chains.

[1]  M. Tsuboi,et al.  Molecular Geometry in an Excited Electronic State and a Preresonance Raman Effect , 1975, Science.

[2]  P. Hegemann,et al.  Microbial and Animal Rhodopsins: Structures, Functions, and Molecular Mechanisms , 2013, Chemical reviews.

[3]  R. Mathies,et al.  Picosecond time-resolved Raman system for studying photochemical reaction dynamics: application to the primary events in vision , 1999 .

[4]  G. H. Reed,et al.  Optical, EPR, and 1H NMR spectroscopy of serine-ligated [2Fe-2S] ferredoxins produced by site-directed mutagenesis of cysteine residues in recombinant Anabaena 7120 vegetative ferredoxin. , 1994, Biochemistry.

[5]  Royston Goodacre,et al.  The challenge of applying Raman spectroscopy to monitor recombinant antibody production. , 2013, The Analyst.

[6]  A. Oseroff,et al.  Resonance Raman spectroscopy of rhodopsin in retinal disk membranes. , 1974, Biochemistry.

[7]  H. Shafaat,et al.  Ultraviolet resonance Raman spectroscopy of a β‐sheet peptide: a model for membrane protein folding , 2009 .

[8]  T. Spiro,et al.  Ultraviolet resonance Raman spectroscopy of imidazole, histidine, and Cu(imidazole)42+: implications for protein studies , 1986 .

[9]  H. Sussner,et al.  Resonance raman scattering on the haem group of oxy- and deoxyhaemoglobin. , 1972, Journal of molecular biology.

[10]  Richard A. Mathies,et al.  Picosecond time-resolved resonance Raman spectroscopy of bacteriorhodopsin's J, K, and KL intermediates , 1991 .

[11]  R. Mathies,et al.  Mapping GFP structure evolution during proton transfer with femtosecond Raman spectroscopy , 2009, Nature.

[12]  Yang Wang,et al.  UV resonance Raman spectroscopy and hydrogen bonding of the proline peptide bond , 1996 .

[13]  R. Mathies,et al.  Complete assignment of the hydrogen out-of-plane wagging vibrations of bathorhodopsin: chromophore structure and energy storage in the primary photoproduct of vision. , 1989, Biochemistry.

[14]  L. Kay,et al.  The use of 2H, 13C, 15N multidimensional NMR to study the structure and dynamics of proteins. , 1998, Annual review of biophysics and biomolecular structure.

[15]  Stephen H. White,et al.  Experimentally determined hydrophobicity scale for proteins at membrane interfaces , 1996, Nature Structural Biology.

[16]  B. Barry,et al.  Ultraviolet Resonance Raman Microprobe Spectroscopy of Photosystem II , 2008, Photochemistry and photobiology.

[17]  H. Takeuchi,et al.  Pro-oxidant copper-binding mode of the Apo form of ALS-linked SOD1 mutant H43R denatured at physiological temperature. , 2013, Biochemistry.

[18]  T. Spiro,et al.  Protein secondary structure from deep-UV resonance Raman spectroscopy† , 2006 .

[19]  I. Harada,et al.  Structure and ligand-binding modes of human serum albumin studied by UV resonance raman spectroscopy , 1995 .

[20]  C. Santamaria,et al.  Bactericidal and Antiendotoxic Properties of Short Cationic Peptides Derived from a Snake Venom Lys49 Phospholipase A2 , 2005, Antimicrobial Agents and Chemotherapy.

[21]  G. Thomas,et al.  Ultraviolet-resonance raman spectroscopy of the filamentous virus Pf3: interactions of Trp 38 specific to the assembled virion subunit. , 2000, Biochemistry.

[22]  R A Mathies,et al.  Ultraviolet resonance Raman examination of the light-induced protein structural changes in rhodopsin activation. , 1997, Biochemistry.

[23]  R. Mathies,et al.  Interpretation of the resonance Raman spectrum of bathorhodopsin based on visual pigment analogues. , 1980, Biochemistry.

[24]  I. Harada,et al.  Effects of hydrogen bonding on the tyrosine Raman bands in the 1300-1150 cm-1 region , 1989 .

[25]  L. Tamm,et al.  Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. , 2007, Journal of the American Chemical Society.

[26]  Cathy H. Wu,et al.  The Universal Protein Resource (UniProt) , 2004, Nucleic Acids Res..

[27]  Alan J. Waring,et al.  Activities of LL-37, a Cathelin-Associated Antimicrobial Peptide of Human Neutrophils , 1998, Antimicrobial Agents and Chemotherapy.

[28]  D. Klenerman,et al.  Ultraviolet resonance Raman study of drug binding in dihydrofolate reductase, gyrase, and catechol O-methyltransferase. , 1998, Biophysical journal.

[29]  I. Lednev,et al.  Structural variations in the cross-beta core of amyloid beta fibrils revealed by deep UV resonance Raman spectroscopy. , 2010, Journal of the American Chemical Society.

[30]  I. Harada,et al.  Origin of the doublet at 1360 and 1340 cm -1 in the Raman spectra of tryptophan and related compounds , 1986 .

[31]  D. Houde,et al.  Time-resolved Raman spectroscopy with subpicosecond resolution: vibrational cooling and delocalization of strain energy in photodissociated (carbonmonoxy)hemoglobin. , 1987, Biochemistry.

[32]  J. Mccammon,et al.  Spectroscopic and Computational Study of Melittin, Cecropin A, and the Hybrid Peptide CM15 , 2012, The journal of physical chemistry. B.

[33]  R. Houghten,et al.  Probing the relationships between the structure and hemolytic activity of melittin with a complete set of leucine substitution analogs. , 1991, Peptide research.

[34]  S. Asher,et al.  Critical role of the solvent environment in galectin-1 binding to the disaccharide lactose. , 2009, Biochemistry.

[35]  Hideo Takeuchi,et al.  Tryptophan Raman bands sensitive to hydrogen bonding and side-chain conformation , 1989 .

[36]  Rajinder Singh.  C. V. Raman and the Discovery of the Raman Effect , 2002 .

[37]  R. Mathies,et al.  Temperature dependence of the Qy resonance Raman spectra of bacteriochlorophylls, the primary electron donor, and bacteriopheophytins in the bacterial photosynthetic reaction center. , 1997, Biochemistry.

[38]  S. Asher,et al.  Ultraviolet resonance Raman excitation profiles of tyrosine: dependence of Raman cross sections on excited-state intermediates , 1988 .

[39]  T. Kitagawa,et al.  A Novel Idea for Practical UV Resonance Raman Measurement with a Double Monochromator and its Application to Protein Structural Studies , 1992 .

[40]  H. Takeuchi,et al.  Indole ring orientations of Trp189 in the ground and M intermediate states of bacteriorhodopsin as studied by polarized UV resonance Raman spectroscopy , 2006 .

[41]  R. Mathies,et al.  Femtosecond Time-Resolved Stimulated Raman Spectroscopy: Application to the Ultrafast Internal Conversion in β-Carotene† , 2003 .

[42]  Zhenmin Hong,et al.  Elucidating Peptide and Protein Structure and Dynamics: UV Resonance Raman Spectroscopy. , 2011, The journal of physical chemistry letters.

[43]  R. Jiji,et al.  Bilayer surface association of the pHLIP peptide promotes extensive backbone desolvation and helically-constrained structures. , 2014, Biophysical chemistry.

[44]  S. Asher,et al.  UV Raman Determination of the Environment and Solvent Exposure of Tyr and Trp Residues , 1998 .

[45]  W. Peticolas,et al.  Resonance and preresonance Raman spectra of nucleotides using ultraviolet lasers , 1975 .

[46]  Hiroto Takahashi,et al.  Ultraviolet resonance Raman evidence for utilization of the heme 6-propionate hydrogen-bond network in signal transmission from heme to protein in Ec DOS protein. , 2007, Journal of the American Chemical Society.

[47]  R. Mathies,et al.  Resonance Raman analysis of the mechanism of energy storage and chromophore distortion in the primary visual photoproduct. , 2004, Biochemistry.

[48]  S H White,et al.  Folding of beta-sheet membrane proteins: a hydrophobic hexapeptide model. , 1998, Journal of molecular biology.

[49]  R. B. Merrifield,et al.  N-terminal analogues of cecropin A: synthesis, antibacterial activity, and conformational properties. , 1985, Biochemistry.

[50]  M. El-Sayed,et al.  Resonance Raman spectroscopy in the picosecond time scale: the carboxyhemoglobin photointermediate , 1980 .

[51]  R. Copeland,et al.  Ultraviolet resonance Raman spectroscopy of flavin mononucleotide and flavin adenine dinucleotide , 1986 .

[52]  K. Shinzawa-Itoh,et al.  A New Measurement System for UV Resonance Raman Spectra of Large Proteins and Its Application to Cytochrome c Oxidase , 2000 .

[53]  Pavel Matousek,et al.  Efficient Rejection of Fluorescence from Raman Spectra Using Picosecond Kerr Gating , 1999 .

[54]  A. Ianoul,et al.  The effects of L‐ to D‐isomerization and C‐terminus deamidation on the secondary structure of antimicrobial peptide Anoplin in aqueous and membrane mimicking environment , 2010 .

[55]  A. Warshel.  Interpretation of resonance Raman spectra of biological molecules. , 1977, Annual review of biophysics and bioengineering.

[56]  H. Kano,et al.  Spectroscopy and Structure Determination , 2006 .

[57]  R. McCreery,et al.  Raman Spectroscopy for Chemical Analysis: McCreery/Raman Spectroscopy , 2005 .

[58]  R. Woody,et al.  Theory of Circular Dichroism of Proteins , 1996 .

[59]  J. Lanyi,et al.  Changes in hydrogen bonding and environment of tryptophan residues on helix F of bacteriorhodopsin during the photocycle: a time-resolved ultraviolet resonance Raman study. , 2002, Biochemistry.

[60]  R. Mathies,et al.  High-Throughput Large-Aperture Prism Prefilter for Ultraviolet Resonance Raman Spectroscopy , 1998 .

[61]  K. Imai,et al.  Near-UV circular dichroism and UV resonance Raman spectra of individual tryptophan residues in human hemoglobin and their changes upon the quaternary structure transition. , 2012, Biochemistry.

[62]  M Laskowski,et al.  Tyrosine hydrogen-bonding and environmental effects in proteins probed by ultraviolet resonance Raman spectroscopy. , 1988, Biochemistry.

[63]  K. Brogden.  Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? , 2005, Nature Reviews Microbiology.

[64]  G. Wald.  The Molecular Basis of Visual Excitation , 1968, Nature.

[65]  Diana E. Schlamadinger,et al.  Hydrogen bonding and solvent polarity markers in the uv resonance raman spectrum of tryptophan: application to membrane proteins. , 2009, The journal of physical chemistry. B.

[66]  H. Takeuchi.  UV Raman Markers for Structural Analysis of Aromatic Side Chains in Proteins , 2011, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[67]  S. Radford,et al.  Ultraviolet resonance Raman studies reveal the environment of tryptophan and tyrosine residues in the native and partially folded states of the E colicin-binding immunity protein Im7. , 2005, Biochemistry.

[68]  Thomas G. Spiro,et al.  Solid-State Tunable kHz Ultraviolet Laser for Raman Applications , 1999 .

[69]  I. Harada,et al.  Raman spectroscopic characterization of tryptophan side chains in lysozyme bound to inhibitors: role of the hydrophobic box in the enzymatic function. , 1991, Biochemistry.

[70]  J. Oelze.  9 Analysis of Bacteriochlorophylls , 1985 .

[71]  Judy E. Kim,et al.  Ultraviolet resonance Raman spectroscopy of folded and unfolded states of an integral membrane protein. , 2008, The journal of physical chemistry. B.

[72]  R. Efremov,et al.  Effect of hydrophobic environment on the resonance Raman spectra of tryptophan residues in proteins , 1992 .

[73]  R. Callender,et al.  Raman spectroscopic studies of the structures, energetics, and bond distortions of substrates bound to enzymes. , 1999, Methods in enzymology.

[74]  S. P. Fodor,et al.  Deep-ultraviolet Raman excitation profiles and vibronic scattering mechanisms of phenylalanine, tyrosine, and tryptophan , 1989 .

[75]  Kobayashi,et al.  Femtosecond time-resolved resonance Raman gain spectroscopy in polydiacetylene. , 1994, Physical review. B, Condensed matter.

[76]  Richard A Mathies,et al.  Femtosecond Broadband Stimulated Raman: A New Approach for High-Performance Vibrational Spectroscopy , 2003, Applied spectroscopy.

[77]  D. M. Roberts,et al.  Picosecond transient Raman spectroscopy: The photoisomerization of trans‐stilbene , 1983 .

[78]  L. Stryer,et al.  Retinal chromophore of rhodopsin photoisomerizes within picoseconds. , 1981, Science.

[79]  R. Mathies,et al.  Femtosecond stimulated Raman spectroscopy. , 2007 .

[80]  S. Asher,et al.  UV resonance Raman determination of protein acid denaturation: selective unfolding of helical segments of horse myoglobin. , 1998, Biochemistry.

[81]  H. Shafaat,et al.  Resonance Raman Analysis of the Tryptophan Cation Radical. , 2014, The journal of physical chemistry letters.

[82]  A. Alparone,et al.  Electronic and vibrational polarizabilities of the twenty naturally occurring amino acids. , 2008, Biophysical chemistry.

[83]  Beijing Wu,et al.  Tryptophan-lipid interactions in membrane protein folding probed by ultraviolet resonance Raman and fluorescence spectroscopy. , 2011, Biophysical journal.

[84]  John T. Welch,et al.  Genetic engineering combined with deep UV resonance Raman spectroscopy for structural characterization of amyloid-like fibrils. , 2008, Journal of the American Chemical Society.

[85]  J. Lugtenburg,et al.  Structure of the chromophoric group in bathorhodopsin , 1976, Nature.

[86]  R. Riek,et al.  3D structure of Alzheimer's amyloid-β(1–42) fibrils , 2005 .

[87]  Teizo Kitagawa,et al.  Primary protein response after ligand photodissociation in carbonmonoxy myoglobin , 2007, Proceedings of the National Academy of Sciences.

[88]  W. Schreier,et al.  The photochemistry of o-nitrobenzaldehyde as seen by femtosecond vibrational spectroscopy. , 2005, Angewandte Chemie.

[89]  J. Merlin.  Resonance Raman spectroscopy of carotenoids and carotenoid-containing systems , 1985 .

[90]  I. Harada,et al.  Utilization of a Prism Monochromator as a Sharp-Cut Bandpass Filter in Ultraviolet Raman Spectroscopy , 1993 .

[91]  J. Svendsen,et al.  Antibacterial activity of 15-residue lactoferricin derivatives. , 2000, The journal of peptide research : official journal of the American Peptide Society.

[92]  T. Spiro,et al.  Hemoglobin: resonance Raman spectra. , 1972, Biochimica et biophysica acta.

[93]  Resonance Raman spectroscopy in the picosecond time scale: the carboxyhemoglobin photointermediate , 1980 .

[94]  Steen Brøndsted Nielsen,et al.  Tunable kHz Deep Ultraviolet (193–210 nm) Laser for Raman Applications , 2005, Applied spectroscopy.

[95]  T. Kitagawa,et al.  Near-UV circular dichroism and UV resonance Raman spectra of tryptophan residues as a structural marker of proteins. , 2013, The journal of physical chemistry. B.

[96]  X. G. Chen,et al.  UV resonance Raman-selective amide vibrational enhancement: quantitative methodology for determining protein secondary structure. , 1998, Biochemistry.

[97]  Hideo Takeuchi,et al.  Raman structural markers of tryptophan and histidine side chains in proteins. , 2003, Biopolymers.

[98]  S. White,et al.  Membrane protein folding and stability: physical principles. , 1999, Annual review of biophysics and biomolecular structure.

[99]  I. Lednev,et al.  Deep-UV Raman spectrometer tunable between 193 and 205 nm for structural characterization of proteins , 2005, Analytical and bioanalytical chemistry.

[100]  K. Moffat.  Time-Resolved Biochemical Crystallography: A Mechanistic Perspective , 2010 .

[101]  D. McCamant.  Re-evaluation of rhodopsin's relaxation kinetics determined from femtosecond stimulated Raman lineshapes. , 2011, The journal of physical chemistry. B.

[102]  I. Harada,et al.  Ultraviolet resonance Raman spectra of bacteriorhodopsin in the light-adapted and dark-adapted states , 1990 .

[103]  R. L. Baldwin,et al.  Circular dichroism spectra of short, fixed-nucleus alanine helices , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[104]  A. Pevsner,et al.  Time-resolved absorption and UV resonance Raman spectra reveal stepwise formation of T quaternary contacts in the allosteric pathway of hemoglobin. , 2004, Journal of molecular biology.

[105]  Blondelle Se,et al.  Probing the relationships between the structure and hemolytic activity of melittin with a complete set of leucine substitution analogs. , 1991 .

[106]  R. Woody,et al.  Circular dichroism. , 1995, Methods in enzymology.

[107]  P. Rentzepis,et al.  Primary photochemical event in vision: proton translocation. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[108]  R. Mathies,et al.  Structural Observation of the Primary Isomerization in Vision with Femtosecond-Stimulated Raman , 2005, Science.

[109]  H. Vogel,et al.  Diversity of antimicrobial peptides and their mechanisms of action. , 1999, Biochimica et biophysica acta.

[110]  H. Takeuchi,et al.  Ultraviolet resonance Raman evidence for the absence of tyrosinate in octopus rhodopsin and the participation of Trp residues in the transition to acid metarhodopsin , 1996, FEBS letters.

[111]  Sanford A. Asher,et al.  Tryptophan UV Resonance Raman Excitation Profiles , 1990 .

[112]  E. H. Strickland,et al.  Aromatic contributions to circular dichroism spectra of proteins. , 1974, CRC critical reviews in biochemistry.

[113]  Richard A. Mathies,et al.  Effective Rejection of Fluorescence Interference in Raman Spectroscopy Using a Shifted Excitation Difference Technique , 1992 .

[114]  T. Spiro,et al.  Cytochrome c: resonance Raman spectra. , 1972, Biochimica et biophysica acta.

[115]  S. White,et al.  How Membranes Shape Protein Structure* , 2001, The Journal of Biological Chemistry.

[116]  I. Harada,et al.  Characterization of individual tryptophan side chains in proteins using Raman spectroscopy and hydrogen-deuterium exchange kinetics. , 1988, Biochemistry.

[117]  R. Jiji,et al.  Simultaneous Observation of Peptide Backbone Lipid Solvation and α‐Helical Structure by Deep‐UV Resonance Raman Spectroscopy , 2011, Chembiochem : a European journal of chemical biology.

[118]  L. Mayne,et al.  Ultraviolet resonance Raman studies of N-methylacetamide , 1985 .

[119]  Sergey Arzhantsev,et al.  Deep-Ultraviolet (UV) Resonance Raman Spectroscopy as a Tool for Quality Control of Formulated Therapeutic Proteins , 2012, Applied spectroscopy.

[120]  S. Asher,et al.  Ultraviolet resonance Raman examination of horse apomyoglobin acid unfolding intermediates. , 1999, Biochemistry.

[121]  D. A. Dougherty,et al.  Cation-π interactions in structural biology , 1999 .

[122]  A. Lewis,et al.  Tunable laser resonance Raman spectroscopy of the visual process. I: The spectrum of rhodopsin , 1973 .

[123]  Ayyalusamy Ramamoorthy,et al.  LL-37, the only human member of the cathelicidin family of antimicrobial peptides. , 2006, Biochimica et biophysica acta.

[124]  R. Mathies,et al.  Anti-stokes Raman study of vibrational cooling dynamics in the primary photochemistry of rhodopsin. , 2002, The journal of physical chemistry. A.

[125]  S. Bykov,et al.  Steady-State and Transient Ultraviolet Resonance Raman Spectrometer for the 193–270 nm Spectral Region , 2005, Applied spectroscopy.

[126]  J. Killian,et al.  How proteins adapt to a membrane-water interface. , 2000, Trends in biochemical sciences.

[127]  Diana E. Schlamadinger,et al.  Effects of tryptophan microenvironment, soluble domain, and vesicle size on the thermodynamics of membrane protein folding: lessons from the transmembrane protein OmpA. , 2008, Biochemistry.

[128]  D. Gill,et al.  Resonance-enhanced Raman spectra of visual pigments in intact bovine retinas at low temperatures. , 1970, Biochemical and biophysical research communications.

[129]  R. Mathies,et al.  Resonance Raman Structural Evidence that the Cis-to-Trans Isomerization in Rhodopsin Occurs in Femtoseconds. , 2001, The journal of physical chemistry. B.

[130]  R. Mathies,et al.  Picosecond dynamics of G-protein coupled receptor activation in rhodopsin from time-resolved UV resonance Raman spectroscopy. , 2003, Biochemistry.

[131]  S. Asher,et al.  Comparison between UV Raman and circular dichroism detection of short alpha helices in bombolitin III. , 2002, Biochemistry.

[132]  S. Kruglik,et al.  Sub-picosecond Raman spectrometer for time-resolved studies of structural dynamics in heme proteins , 2011 .

[133]  R. Houghten,et al.  Hemolytic and antimicrobial activities of the twenty-four individual omission analogues of melittin. , 1991, Biochemistry.

[134]  R. Gallo,et al.  Fluorescence and UV resonance Raman study of peptide-vesicle interactions of human cathelicidin LL-37 and its F6W and F17W mutants. , 2009, Biochemistry.

[135]  D. Gill,et al.  Resonance Raman Scattering of Laser Radiation by Vibrational Modes of Carotenoid Pigment Molecules in Intact Plant Tissues , 1970, Nature.

[136]  Michele Vendruscolo,et al.  Prediction of "aggregation-prone" and "aggregation-susceptible" regions in proteins associated with neurodegenerative diseases. , 2005, Journal of molecular biology.

[137]  K. S. Krishnan,et al.  A New Type of Secondary Radiation , 1928, Nature.

[138]  K. Palczewski,et al.  Crystal Structure of Rhodopsin: A G‐Protein‐Coupled Receptor , 2002, Chembiochem : a European journal of chemical biology.

[139]  S. R. Bolton,et al.  Ultraviolet resonance raman spectroscopy of bacteriorhodopsin : evidence against tyrosinate in the photocycle , 1990 .

[140]  M. Pazgier,et al.  Trp-26 Imparts Functional Versatility to Human , 2010 .

[141]  R. Mathies,et al.  Time-resolved ultraviolet resonance Raman studies of protein structure: application to bacteriorhodopsin. , 1992, Biochemistry.

[142]  T. O’Halloran,et al.  Cu(I) recognition via cation-pi and methionine interactions in CusF. , 2008, Nature chemical biology.

[143]  R. Mathies,et al.  Chromophore structure in lumirhodopsin and metarhodopsin I by time-resolved resonance Raman microchip spectroscopy. , 2001, Biochemistry.

[144]  R. Jiji,et al.  Deep-UV resonance Raman analysis of the Rhodobacter capsulatus cytochrome bc₁complex reveals a potential marker for the transmembrane peptide backbone. , 2011, Biochemistry.

[145]  Y. Mizutani,et al.  Developments of widely tunable light sources for picosecond time-resolved resonance Raman spectroscopy , 1997 .

[146]  W. DeGrado,et al.  Investigation of an unnatural amino acid for use as a resonance Raman probe: Detection limits, solvent and temperature dependence of the νC≡N band of 4-cyanophenylalanine. , 2008, Journal of Raman spectroscopy : JRS.

[147]  M. Zasloff.  Antimicrobial peptides of multicellular organisms , 2002, Nature.

[148]  T. Spiro,et al.  Metal-Bound Histidine Modes in UV Resonance Raman Spectra of Cu, Zn Superoxide Dismutase , 2000 .

[149]  H. Hiramatsu,et al.  Involvement of histidine residues in the pH-dependent β-galactoside binding activity of human galectin-1. , 2013, Biochemistry.

[150]  A. Ianoul,et al.  UV resonance Raman spectroscopy probes the localization of tryptophan‐containing antimicrobial peptides in lipid vesicles , 2009 .

[151]  R. Mathies,et al.  Time-resolved resonance Raman analysis of chromophore structural changes in the formation and decay of rhodopsin's BSI intermediate. , 2002, Journal of the American Chemical Society.

[152]  Jonathan G. Lees,et al.  Analyses of circular dichroism spectra of membrane proteins , 2003, Protein science : a publication of the Protein Society.

[153]  R. Purrello,et al.  UVRR spectroscopy of the peptide bond. 1. Amide S, a nonhelical structure marker, is a C.alpha.H bending mode , 1991 .

[154]  R A Mathies,et al.  The first step in vision: femtosecond isomerization of rhodopsin. , 1991, Science.

[155]  Freek Ariese,et al.  Fluorescence Rejection in Resonance Raman Spectroscopy Using a Picosecond-Gated Intensified Charge-Coupled Device Camera , 2007, Applied spectroscopy.

[156]  Diana E. Schlamadinger,et al.  UV resonance Raman study of TrpZip2 and related peptides: π-π interactions of tryptophan. , 2012, Journal of Raman spectroscopy : JRS.

[157]  R. Jiji,et al.  Resolution of localized small molecule-Aβ interactions by deep-ultraviolet resonance Raman spectroscopy. , 2011, Biophysical chemistry.

[158]  G. Thomas,et al.  Design and performance of an ultraviolet resonance Raman spectrometer for proteins and nucleic acids. , 1995, Biophysical journal.