DOI: 10.1002/bip.10105. New structural insights from Raman spectroscopy of proteins and their assemblies

New structural insights from Raman spectroscopy of proteins and their assemblies

10.1002/bip.10105

Crossref journal-article

Wiley

Biopolymers (311)

Abstract

AbstractProtein structure and stability are sensitive to and dependent on the local interactions of amino acid side chains. A diverse and important type of side‐chain interaction is the hydrogen bond. Although numerous hydrogen bonds are resolved in protein 3‐dimensional structures, those of the cysteine sulfhydryl group (S H) are elusive to high‐resolution X‐ray and NMR methods. However, the nature and strength of sulfhydryl hydrogen bonds (SH…X) are amenable to investigation by Raman spectroscopy. The power of the Raman method for characterizing SH…X interactions is illustrated by resolving the Raman SH stretching band for each of the eight cysteines per 666‐residue subunit in the trimeric tailspike of icosahedral bacteriophage P22. The Raman sulfhydryl signatures of the wild‐type tailspike and eight single‐site cysteine to serine mutants reveal a heretofore unrecognized diversity of SH hydrogen bonds in a native protein. The use of Raman spectroscopy to identify the non‐hydrogen‐bonded state of the tyrosine phenoxyl group is also described. This unusual and unexpected state occurs for all tyrosines in the assembled capsids of filamentous viruses Ff and Pf1. The Raman spectral signature of the non‐hydrogen‐bonded tyrosine phenoxyl, which is characterized by an extraordinary Raman Fermi doublet intensity ratio (I850/I830 = 6.7), extends and refines the existing correlation for hydrogen‐bonded tyrosines. Finally, a novel Raman signature for tryptophan in the Pf3 filamentous virus is identified, which is proposed as diagnostic of “cation–π interaction” involving the guanidinium group of Arg 37 as a cation donor and the indolyl ring of Trp 38 as a π‐electron acceptor. These studies demonstrate the power of Raman spectroscopy for investigating the interactions of key side chains in native protein assemblies. © 2002 Wiley Periodicals, Inc. Biopolymers (Biospectroscopy) 67: 214–225, 2002

Bibliography

Thomas, G. J. (2002). New structural insights from Raman spectroscopy of proteins and their assemblies. Biopolymers, 67(4â5), 214â225. Portico.

Authors 1

George J. Thomas (first)

References 49 Referenced 76

{'key': 'e_1_2_6_2_2', 'series-title': 'Subcellular Biochemistry. Proteins: Structure, Function and Engineering', 'first-page': '55', 'author': 'Miura T.', 'year': '1993'} / Subcellular Biochemistry. Proteins: Structure, Function and Engineering by Miura T. (1993)
10.1021/ja00002a012
10.1146/annurev.biophys.28.1.1
{'key': 'e_1_2_6_5_2', 'series-title': 'Handbook of Vibrational Spectroscopy. Applications of Vibrational Spectroscopy in Biochemistry, Biomedicine and Pharmaceutical Science', 'author': 'Tuma R.', 'year': '2001'} / Handbook of Vibrational Spectroscopy. Applications of Vibrational Spectroscopy in Biochemistry, Biomedicine and Pharmaceutical Science by Tuma R. (2001)
10.1110/ps.34701
10.1006/jmbi.2001.4476
10.1021/bi00171a001
10.1021/bi0023753
10.1021/bi992018w
10.1021/bi0018887
10.1016/S0021-9258(19)57320-3
10.1021/bi00266a014
10.1016/S0022-2836(83)80260-5
10.1021/bi982901e
10.1021/bi00016a015
10.1016/S0006-3495(95)80334-6
{'key': 'e_1_2_6_18_2', 'volume-title': 'Proteins', 'author': 'Creighton T. E.', 'year': '2001'} / Proteins by Creighton T. E. (2001)
10.1016/S0065-3233(08)60376-9
10.1021/ja00045a019
10.1016/S0006-3495(93)81172-X
10.1021/bi00073a012
10.1002/pro.5560070120
10.1073/pnas.95.17.9885
10.1016/0003-9861(89)90106-9
10.1126/science.8023158
10.1006/jmbi.1997.0922
10.1016/0022-2836(88)90620-1
10.1016/S0021-9258(18)47242-0 / J Biol Chem by Sather S. K. (1994)
10.1021/bi00469a022
10.1038/nsb0697-450
10.1016/S0969-2126(99)80078-1
10.1021/bi00693a014
10.1016/0584-8539(88)80138-7
10.1006/jmbi.1994.0009
10.1016/S0959-440X(98)80032-8
10.1021/bi9527707
10.1006/jmbi.1996.0323
10.1021/bi001936n
10.1021/bi970342q
10.1021/bi972339c
10.1021/bi981965m
10.1002/jrs.1250201007
10.1126/science.271.5246.163
10.1021/bi982201
10.1021/cr9603744
10.1073/pnas.95.11.5976
10.1006/jmbi.1998.2081
10.1021/bi9622130
10.1002/pro.5560050613

Dates

Type	When
Created	23 years ago (Aug. 25, 2002, 7:27 p.m.)
Deposited	2 years ago (Aug. 30, 2023, 10:37 a.m.)
Indexed	2 months, 4 weeks ago (June 6, 2025, 5:08 a.m.)
Issued	23 years, 8 months ago (Jan. 1, 2002)
Published	23 years, 8 months ago (Jan. 1, 2002)
Published Online	23 years, 3 months ago (May 9, 2002)
Published Print	23 years, 8 months ago (Jan. 1, 2002)

Funders 0

None

BibTeX

@article{Thomas_2002, title={New structural insights from Raman spectroscopy of proteins and their assemblies}, volume={67}, ISSN={1097-0282}, url={http://dx.doi.org/10.1002/bip.10105}, DOI={10.1002/bip.10105}, number={4–5}, journal={Biopolymers}, publisher={Wiley}, author={Thomas, George J.}, year={2002}, month=jan, pages={214–225} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        6
      ]
    ],
    "date-time": "2025-06-06T09:08:01Z",
    "timestamp": 1749200881920
  },
  "reference-count": 49,
  "publisher": "Wiley",
  "issue": "4-5",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2002,
            5,
            9
          ]
        ],
        "date-time": "2002-05-09T00:00:00Z",
        "timestamp": 1020902400000
      },
      "content-version": "vor",
      "delay-in-days": 128,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2002,
        1
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Protein structure and stability are sensitive to and dependent on the local interactions of amino acid side chains. A diverse and important type of side\u2010chain interaction is the hydrogen bond. Although numerous hydrogen bonds are resolved in protein 3\u2010dimensional structures, those of the cysteine sulfhydryl group (S\uf8ff H) are elusive to high\u2010resolution X\u2010ray and NMR methods. However, the nature and strength of sulfhydryl hydrogen bonds (S\uf8ffH\u2026X) are amenable to investigation by Raman spectroscopy. The power of the Raman method for characterizing S\uf8ffH\u2026X interactions is illustrated by resolving the Raman S\uf8ffH stretching band for each of the eight cysteines per 666\u2010residue subunit in the trimeric tailspike of icosahedral bacteriophage P22. The Raman sulfhydryl signatures of the wild\u2010type tailspike and eight single\u2010site cysteine to serine mutants reveal a heretofore unrecognized diversity of S\uf8ffH hydrogen bonds in a native protein. The use of Raman spectroscopy to identify the non\u2010hydrogen\u2010bonded state of the tyrosine phenoxyl group is also described. This unusual and unexpected state occurs for all tyrosines in the assembled capsids of filamentous viruses Ff and Pf1. The Raman spectral signature of the non\u2010hydrogen\u2010bonded tyrosine phenoxyl, which is characterized by an extraordinary Raman Fermi doublet intensity ratio (<jats:italic>I</jats:italic><jats:sub>850</jats:sub>/<jats:italic>I</jats:italic><jats:sub>830</jats:sub> = 6.7), extends and refines the existing correlation for hydrogen\u2010bonded tyrosines. Finally, a novel Raman signature for tryptophan in the Pf3 filamentous virus is identified, which is proposed as diagnostic of \u201ccation\u2013\u03c0 interaction\u201d involving the guanidinium group of Arg 37 as a cation donor and the indolyl ring of Trp 38 as a \u03c0\u2010electron acceptor. These studies demonstrate the power of Raman spectroscopy for investigating the interactions of key side chains in native protein assemblies. \u00a9 2002 Wiley Periodicals, Inc. Biopolymers (Biospectroscopy) 67: 214\u2013225, 2002</jats:p>",
  "DOI": "10.1002/bip.10105",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        8,
        25
      ]
    ],
    "date-time": "2002-08-25T23:27:00Z",
    "timestamp": 1030318020000
  },
  "page": "214-225",
  "source": "Crossref",
  "is-referenced-by-count": 76,
  "title": "New structural insights from Raman spectroscopy of proteins and their assemblies",
  "prefix": "10.1002",
  "volume": "67",
  "author": [
    {
      "suffix": "Jr.",
      "given": "George J.",
      "family": "Thomas",
      "sequence": "first",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2002,
        5,
        9
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_6_2_2",
      "series-title": "Subcellular Biochemistry. Proteins: Structure, Function and Engineering",
      "first-page": "55",
      "author": "Miura T.",
      "year": "1993"
    },
    {
      "key": "e_1_2_6_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja00002a012"
    },
    {
      "key": "e_1_2_6_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.biophys.28.1.1"
    },
    {
      "key": "e_1_2_6_5_2",
      "series-title": "Handbook of Vibrational Spectroscopy. Applications of Vibrational Spectroscopy in Biochemistry, Biomedicine and Pharmaceutical Science",
      "author": "Tuma R.",
      "year": "2001"
    },
    {
      "key": "e_1_2_6_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1110/ps.34701"
    },
    {
      "key": "e_1_2_6_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.2001.4476"
    },
    {
      "key": "e_1_2_6_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00171a001"
    },
    {
      "key": "e_1_2_6_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi0023753"
    },
    {
      "key": "e_1_2_6_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi992018w"
    },
    {
      "key": "e_1_2_6_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi0018887"
    },
    {
      "key": "e_1_2_6_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)57320-3"
    },
    {
      "key": "e_1_2_6_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00266a014"
    },
    {
      "key": "e_1_2_6_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-2836(83)80260-5"
    },
    {
      "key": "e_1_2_6_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi982901e"
    },
    {
      "key": "e_1_2_6_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00016a015"
    },
    {
      "key": "e_1_2_6_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-3495(95)80334-6"
    },
    {
      "key": "e_1_2_6_18_2",
      "volume-title": "Proteins",
      "author": "Creighton T. E.",
      "year": "2001"
    },
    {
      "key": "e_1_2_6_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0065-3233(08)60376-9"
    },
    {
      "key": "e_1_2_6_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/ja00045a019"
    },
    {
      "key": "e_1_2_6_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-3495(93)81172-X"
    },
    {
      "key": "e_1_2_6_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00073a012"
    },
    {
      "key": "e_1_2_6_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/pro.5560070120"
    },
    {
      "key": "e_1_2_6_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.95.17.9885"
    },
    {
      "key": "e_1_2_6_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-9861(89)90106-9"
    },
    {
      "key": "e_1_2_6_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8023158"
    },
    {
      "key": "e_1_2_6_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.1997.0922"
    },
    {
      "key": "e_1_2_6_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(88)90620-1"
    },
    {
      "key": "e_1_2_6_29_2",
      "doi-asserted-by": "crossref",
      "first-page": "25268",
      "DOI": "10.1016/S0021-9258(18)47242-0",
      "volume": "269",
      "author": "Sather S. K.",
      "year": "1994",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "e_1_2_6_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00469a022"
    },
    {
      "key": "e_1_2_6_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nsb0697-450"
    },
    {
      "key": "e_1_2_6_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0969-2126(99)80078-1"
    },
    {
      "key": "e_1_2_6_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00693a014"
    },
    {
      "key": "e_1_2_6_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0584-8539(88)80138-7"
    },
    {
      "key": "e_1_2_6_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.1994.0009"
    },
    {
      "key": "e_1_2_6_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0959-440X(98)80032-8"
    },
    {
      "key": "e_1_2_6_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi9527707"
    },
    {
      "key": "e_1_2_6_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.1996.0323"
    },
    {
      "key": "e_1_2_6_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi001936n"
    },
    {
      "key": "e_1_2_6_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi970342q"
    },
    {
      "key": "e_1_2_6_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi972339c"
    },
    {
      "key": "e_1_2_6_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi981965m"
    },
    {
      "key": "e_1_2_6_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jrs.1250201007"
    },
    {
      "key": "e_1_2_6_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.271.5246.163"
    },
    {
      "key": "e_1_2_6_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi982201"
    },
    {
      "key": "e_1_2_6_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/cr9603744"
    },
    {
      "key": "e_1_2_6_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.95.11.5976"
    },
    {
      "key": "e_1_2_6_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.1998.2081"
    },
    {
      "key": "e_1_2_6_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi9622130"
    },
    {
      "key": "e_1_2_6_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/pro.5560050613"
    }
  ],
  "container-title": "Biopolymers",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fbip.10105",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/bip.10105",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        8,
        30
      ]
    ],
    "date-time": "2023-08-30T14:37:24Z",
    "timestamp": 1693406244000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/bip.10105"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2002,
        1
      ]
    ]
  },
  "references-count": 49,
  "journal-issue": {
    "issue": "4-5",
    "published-print": {
      "date-parts": [
        [
          2002,
          1
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/bip.10105"
  ],
  "URL": "http://dx.doi.org/10.1002/bip.10105",
  "relation": {},
  "ISSN": [
    "0006-3525",
    "1097-0282"
  ],
  "subject": [],
  "container-title-short": "Biopolymers",
  "published": {
    "date-parts": [
      [
        2002,
        1
      ]
    ]
  }
}