DOI: 10.1126/science.1079605. Architecture of Succinate Dehydrogenase and Reactive Oxygen Species Generation

Architecture of Succinate Dehydrogenase and Reactive Oxygen Species Generation

10.1126/science.1079605

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The structure of Escherichia coli succinate dehydrogenase (SQR), analogous to the mitochondrial respiratory complex II, has been determined, revealing the electron transport pathway from the electron donor, succinate, to the terminal electron acceptor, ubiquinone. It was found that the SQR redox centers are arranged in a manner that aids the prevention of reactive oxygen species (ROS) formation at the flavin adenine dinucleotide. This is likely to be the main reason SQR is expressed during aerobic respiration rather than the related enzyme fumarate reductase, which produces high levels of ROS. Furthermore, symptoms of genetic disorders associated with mitochondrial SQR mutations may be a result of ROS formation resulting from impaired electron transport in the enzyme.

Bibliography

Yankovskaya, V., Horsefield, R., ToÌrnroth, S., Luna-Chavez, C., Miyoshi, H., LeÌger, C., Byrne, B., Cecchini, G., & Iwata, S. (2003). Architecture of Succinate Dehydrogenase and Reactive Oxygen Species Generation. Science, 299(5607), 700â704.

Authors 9

Victoria Yankovskaya (first)
Rob Horsefield (additional)
Susanna Törnroth (additional)
César Luna-Chavez (additional)
Hideto Miyoshi (additional)
Christophe Léger (additional)
Bernadette Byrne (additional)
Gary Cecchini (additional)
So Iwata (additional)

References 36 Referenced 789

For a review see
10.1016/S0005-2728(01)00238-9
For a review see
10.1016/S0005-2728(01)00228-6
10.1038/ng1095-144
10.1126/science.287.5454.848
10.1038/81551
10.1038/29331
10.1074/jbc.M104718200
10.1007/BF00245358
For a review see
10.1126/science.284.5422.1941
Guest J. R., J. Gen. Microbiol. 122, 171 (1981). / J. Gen. Microbiol. by Guest J. R. (1981)
10.1128/JB.180.22.5989-5996.1998
10.1126/science.284.5422.1961
10.1038/46483
10.1016/S0005-2728(01)00237-7
10.1042/bj3040321
Materials and methods are available as supporting material on Science Online.
10.1107/S0108767390010224
10.1016/0003-9861(89)90561-4
10.1016/S0005-2728(97)00019-4
10.1016/0014-5793(92)80086-V
10.1007/PL00021452
10.1038/46972
10.1074/jbc.M011270200
10.1074/jbc.271.35.21020
10.1006/jmbi.2000.3509
10.1126/science.1068186
10.1086/321282
10.1136/jmg.39.9.617
10.1074/jbc.M204958200
10.1016/S0021-9258(19)75761-5
10.1074/jbc.274.37.26157
10.1073/pnas.72.8.2886
Supported by Biotechnology and Biological Sciences Research Council of the UK Structural Biology Network of Sweden Syngenta and the Department of Veterans Affairs and NIH grant GM61606. We thank E. Mitchell and A. Thompson at ESRF Grenoble and T. Tomizakiand C. Schulze-Briese at SLS for technical assistance. We also thank J. Abramson and T. Iverson for critically reading the manuscript. The coordinates for the native SQR and the DNP-17 complex are deposited with PDB (entries 1NEK and 1NEN respectively).

Dates

Type	When
Created	22 years, 6 months ago (Jan. 30, 2003, 4:37 p.m.)
Deposited	1 year, 7 months ago (Jan. 9, 2024, 11:43 p.m.)
Indexed	2 hours, 10 minutes ago (Aug. 27, 2025, 12:30 p.m.)
Issued	22 years, 6 months ago (Jan. 31, 2003)
Published	22 years, 6 months ago (Jan. 31, 2003)
Published Print	22 years, 6 months ago (Jan. 31, 2003)

Funders 0

None

BibTeX

@article{Yankovskaya_2003, title={Architecture of Succinate Dehydrogenase and Reactive Oxygen Species Generation}, volume={299}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.1079605}, DOI={10.1126/science.1079605}, number={5607}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Yankovskaya, Victoria and Horsefield, Rob and Törnroth, Susanna and Luna-Chavez, César and Miyoshi, Hideto and Léger, Christophe and Byrne, Bernadette and Cecchini, Gary and Iwata, So}, year={2003}, month=jan, pages={700–704} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        27
      ]
    ],
    "date-time": "2025-08-27T16:30:18Z",
    "timestamp": 1756312218169
  },
  "reference-count": 36,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5607",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2003,
        1,
        31
      ]
    ]
  },
  "abstract": "<jats:p>\n            The structure of\n            <jats:italic>Escherichia coli</jats:italic>\n            succinate dehydrogenase (SQR), analogous to the mitochondrial respiratory complex II, has been determined, revealing the electron transport pathway from the electron donor, succinate, to the terminal electron acceptor, ubiquinone. It was found that the SQR redox centers are arranged in a manner that aids the prevention of reactive oxygen species (ROS) formation at the flavin adenine dinucleotide. This is likely to be the main reason SQR is expressed during aerobic respiration rather than the related enzyme fumarate reductase, which produces high levels of ROS. Furthermore, symptoms of genetic disorders associated with mitochondrial SQR mutations may be a result of ROS formation resulting from impaired electron transport in the enzyme.\n          </jats:p>",
  "DOI": "10.1126/science.1079605",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2003,
        1,
        30
      ]
    ],
    "date-time": "2003-01-30T21:37:47Z",
    "timestamp": 1043962667000
  },
  "page": "700-704",
  "source": "Crossref",
  "is-referenced-by-count": 789,
  "title": "Architecture of Succinate Dehydrogenase and Reactive Oxygen Species Generation",
  "prefix": "10.1126",
  "volume": "299",
  "author": [
    {
      "given": "Victoria",
      "family": "Yankovskaya",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Molecular Biology Division, VA Medical Center, San Francisco, CA 94121, USA."
        }
      ]
    },
    {
      "given": "Rob",
      "family": "Horsefield",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biological Sciences, Imperial College London, London SW7 2AY, UK."
        }
      ]
    },
    {
      "given": "Susanna",
      "family": "To\u0308rnroth",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry, Uppsala University, BMC Box 576, S-75123 Uppsala, Sweden."
        }
      ]
    },
    {
      "given": "Ce\u0301sar",
      "family": "Luna-Chavez",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Biology Division, VA Medical Center, San Francisco, CA 94121, USA."
        },
        {
          "name": "Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94143, USA."
        }
      ]
    },
    {
      "given": "Hideto",
      "family": "Miyoshi",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan."
        }
      ]
    },
    {
      "given": "Christophe",
      "family": "Le\u0301ger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Inorganic Chemistry Laboratory, Oxford University, South Parks Road, Oxford OX1 3QR, UK."
        }
      ]
    },
    {
      "given": "Bernadette",
      "family": "Byrne",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biological Sciences, Imperial College London, London SW7 2AY, UK."
        }
      ]
    },
    {
      "given": "Gary",
      "family": "Cecchini",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Molecular Biology Division, VA Medical Center, San Francisco, CA 94121, USA."
        },
        {
          "name": "Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94143, USA."
        }
      ]
    },
    {
      "given": "So",
      "family": "Iwata",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biological Sciences, Imperial College London, London SW7 2AY, UK."
        },
        {
          "name": "Department of Biochemistry, Uppsala University, BMC Box 576, S-75123 Uppsala, Sweden."
        },
        {
          "name": "Division of Biomedical Sciences, Imperial College London, London SW7 2AZ, UK."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_3_1_2_2",
      "unstructured": "For a review see"
    },
    {
      "key": "e_1_3_1_2_3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0005-2728(01)00238-9"
    },
    {
      "key": "e_1_3_1_3_2",
      "unstructured": "For a review see"
    },
    {
      "key": "e_1_3_1_3_3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0005-2728(01)00228-6"
    },
    {
      "key": "e_1_3_1_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/ng1095-144"
    },
    {
      "key": "e_1_3_1_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.287.5454.848"
    },
    {
      "key": "e_1_3_1_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/81551"
    },
    {
      "key": "e_1_3_1_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/29331"
    },
    {
      "key": "e_1_3_1_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M104718200"
    },
    {
      "key": "e_1_3_1_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00245358"
    },
    {
      "key": "e_1_3_1_10_2",
      "unstructured": "For a review see"
    },
    {
      "key": "e_1_3_1_10_3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.284.5422.1941"
    },
    {
      "key": "e_1_3_1_11_2",
      "first-page": "171",
      "volume": "122",
      "author": "Guest J. R.",
      "year": "1981",
      "unstructured": "Guest J. R., J. Gen. Microbiol. 122, 171 (1981).",
      "journal-title": "J. Gen. Microbiol."
    },
    {
      "key": "e_1_3_1_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.22.5989-5996.1998"
    },
    {
      "key": "e_1_3_1_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.284.5422.1961"
    },
    {
      "key": "e_1_3_1_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/46483"
    },
    {
      "key": "e_1_3_1_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0005-2728(01)00237-7"
    },
    {
      "key": "e_1_3_1_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bj3040321"
    },
    {
      "key": "e_1_3_1_17_2",
      "unstructured": "Materials and methods are available as supporting material on Science Online."
    },
    {
      "key": "e_1_3_1_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1107/S0108767390010224"
    },
    {
      "key": "e_1_3_1_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-9861(89)90561-4"
    },
    {
      "key": "e_1_3_1_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0005-2728(97)00019-4"
    },
    {
      "key": "e_1_3_1_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(92)80086-V"
    },
    {
      "key": "e_1_3_1_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/PL00021452"
    },
    {
      "key": "e_1_3_1_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/46972"
    },
    {
      "key": "e_1_3_1_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M011270200"
    },
    {
      "key": "e_1_3_1_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.35.21020"
    },
    {
      "key": "e_1_3_1_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.2000.3509"
    },
    {
      "key": "e_1_3_1_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1068186"
    },
    {
      "key": "e_1_3_1_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/321282"
    },
    {
      "key": "e_1_3_1_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1136/jmg.39.9.617"
    },
    {
      "key": "e_1_3_1_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M204958200"
    },
    {
      "key": "e_1_3_1_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)75761-5"
    },
    {
      "key": "e_1_3_1_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.274.37.26157"
    },
    {
      "key": "e_1_3_1_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.72.8.2886"
    },
    {
      "key": "e_1_3_1_34_2",
      "unstructured": "Supported by Biotechnology and Biological Sciences Research Council of the UK Structural Biology Network of Sweden Syngenta and the Department of Veterans Affairs and NIH grant GM61606. We thank E. Mitchell and A. Thompson at ESRF Grenoble and  T. Tomizakiand C. Schulze-Briese at SLS for technical assistance. We also thank J. Abramson and T. Iverson for critically reading the manuscript. The coordinates for the native SQR and the DNP-17 complex are deposited with PDB (entries 1NEK and 1NEN respectively)."
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.1079605",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        10
      ]
    ],
    "date-time": "2024-01-10T04:43:44Z",
    "timestamp": 1704861824000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.1079605"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2003,
        1,
        31
      ]
    ]
  },
  "references-count": 36,
  "journal-issue": {
    "issue": "5607",
    "published-print": {
      "date-parts": [
        [
          2003,
          1,
          31
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.1079605"
  ],
  "URL": "http://dx.doi.org/10.1126/science.1079605",
  "relation": {
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.3410/f.1012126.184382",
        "asserted-by": "object"
      },
      {
        "id-type": "doi",
        "id": "10.3410/f.1012126.185766",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        2003,
        1,
        31
      ]
    ]
  }
}