DOI: 10.1110/ps.04773204. A mobile loop order–disorder transition modulates the speed of chaperonin cycling

A mobile loop order–disorder transition modulates the speed of chaperonin cycling

10.1110/ps.04773204

Crossref journal-article

Wiley

Protein Science (311)

Abstract

AbstractMolecular machines order and disorder polypeptides as they form and dissolve large intermolecular interfaces, but the biological significance of coupled ordering and binding has been established in few, if any, macromolecular systems. The ordering and binding of GroES co‐chaperonin mobile loops accompany an ATP‐dependent conformational change in the GroEL chaperonin that promotes client protein folding. Following ATP hydrolysis, disordering of the mobile loops accompanies co‐chaperonin dissociation, reversal of the GroEL conformational change, and release of the client protein. “High‐affinity” GroEL mutants were identified by their compatibility with “low‐affinity” co‐chaperonin mutants and incompatibility with high‐affinity co‐chaperonin mutants. Analysis of binding kinetics using the intrinsic fluorescence of tryptophan‐containing co‐chaperonin variants revealed that excessive affinity causes the chaperonin to stall in a conformation that forms in the presence of ATP. Destabilizing the β‐hairpins formed by the mobile loops restores the normal rate of dissociation. Thus, the free energy of mobile‐loop ordering and disordering acts like the inertia of an engine's flywheel by modulating the speed of chaperonin conformational changes.

Bibliography

Shewmaker, F., Kerner, M. J., HayerâHartl, M., Klein, G., Georgopoulos, C., & Landry, S. J. (2004). A mobile loop orderâdisorder transition modulates the speed of chaperonin cycling. Protein Science, 13(8), 2139â2148. Portico.

Authors 6

Frank Shewmaker (first)
Michael J. Kerner (additional)
Manajit Hayer‐Hartl (additional)
Gracjana Klein (additional)
Costa Georgopoulos (additional)
Samuel J. Landry (additional)

References 50 Referenced 17

10.1016/0960-9822(93)90268-S
10.1074/jbc.273.51.34075
10.1146/annurev.genet.34.1.439
10.1074/jbc.M008477200
10.1016/0022-2364(85)90018-6
10.1073/pnas.90.9.3978
10.1038/371578a0
10.1016/S0092-8674(01)00517-7
10.1021/bi00220a020
10.1093/emboj/cdg477
10.1038/90443
10.1038/10735
10.1021/bi012159
10.1016/S0959-440X(02)00289-0
10.1016/S0092-8674(00)80692-3
10.1038/371614a0
10.1016/0092-8674(91)90378-C
10.1021/bi020117v
10.1126/science.7638601
10.1038/379037a0
10.1016/S0092-8674(00)80343-8
10.1016/S0021-9258(19)39009-X / J. Biol. Chem. / Enhanced operator binding by trp superrepressors of Escherichia coli by Hurlburt B.K. (1990)
10.1016/S0022-2836(02)00969-5
10.1063/1.438208
10.1093/embo-reports/kvf176
10.1093/genetics/158.2.507 / Genetics / Identification of important amino acid residues that modulate binding of Escherichia coli GroEL to its various cochaperones by Klein G. (2001)
10.1038/364255a0
10.1073/pnas.93.21.11622
10.1021/bi971141p
{'key': 'e_1_2_12_31_1', 'first-page': '520', 'volume-title': "acific Symposium on Biocomputing '99", 'author': 'Landry S.J.', 'year': '1999'} / acific Symposium on Biocomputing '99 by Landry S.J. (1999)
10.1006/jmbi.1998.2439
10.1038/41892
10.1038/371264a0
10.1016/S0022-2836(02)01281-0
10.1002/bip.10286
10.1007/BF02192855
10.1074/jbc.274.1.52
10.1016/0960-9822(93)90176-O
10.1074/jbc.M102765200
10.1073/pnas.160259697
10.1126/science.284.5415.822
10.1006/jmra.1993.1098
10.1021/bi00084a024
10.1126/science.7913555
10.1038/368654a0
10.1016/0022-2836(91)90214-Q
10.1006/jmbi.1999.3110
10.1038/41944
10.1021/bi00016a001
10.1128/jb.176.21.6558-6565.1994 / J. Bacteriol. / Two classes of extragenic suppressor mutations identify functionally distinct regions of the GroEL chaperone of Escherichia coli by Zeilstra‐Ryalls J. (1994)

Dates

Type	When
Created	21 years, 1 month ago (July 6, 2004, 9:14 p.m.)
Deposited	1 year, 11 months ago (Sept. 28, 2023, 6:47 p.m.)
Indexed	1 year, 1 month ago (July 2, 2024, 1:08 a.m.)
Issued	21 years ago (Aug. 1, 2004)
Published	21 years ago (Aug. 1, 2004)
Published Online	16 years, 7 months ago (Jan. 1, 2009)
Published Print	21 years ago (Aug. 1, 2004)

Funders 0

None

BibTeX

@article{Shewmaker_2004, title={A mobile loop order–disorder transition modulates the speed of chaperonin cycling}, volume={13}, ISSN={1469-896X}, url={http://dx.doi.org/10.1110/ps.04773204}, DOI={10.1110/ps.04773204}, number={8}, journal={Protein Science}, publisher={Wiley}, author={Shewmaker, Frank and Kerner, Michael J. and Hayer‐Hartl, Manajit and Klein, Gracjana and Georgopoulos, Costa and Landry, Samuel J.}, year={2004}, month=aug, pages={2139–2148} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        7,
        2
      ]
    ],
    "date-time": "2024-07-02T05:08:53Z",
    "timestamp": 1719896933504
  },
  "reference-count": 50,
  "publisher": "Wiley",
  "issue": "8",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2009,
            1,
            1
          ]
        ],
        "date-time": "2009-01-01T00:00:00Z",
        "timestamp": 1230768000000
      },
      "content-version": "vor",
      "delay-in-days": 1614,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2004,
        8
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Molecular machines order and disorder polypeptides as they form and dissolve large intermolecular interfaces, but the biological significance of coupled ordering and binding has been established in few, if any, macromolecular systems. The ordering and binding of GroES co\u2010chaperonin mobile loops accompany an ATP\u2010dependent conformational change in the GroEL chaperonin that promotes client protein folding. Following ATP hydrolysis, disordering of the mobile loops accompanies co\u2010chaperonin dissociation, reversal of the GroEL conformational change, and release of the client protein. \u201cHigh\u2010affinity\u201d GroEL mutants were identified by their compatibility with \u201clow\u2010affinity\u201d co\u2010chaperonin mutants and incompatibility with high\u2010affinity co\u2010chaperonin mutants. Analysis of binding kinetics using the intrinsic fluorescence of tryptophan\u2010containing co\u2010chaperonin variants revealed that excessive affinity causes the chaperonin to stall in a conformation that forms in the presence of ATP. Destabilizing the \u03b2\u2010hairpins formed by the mobile loops restores the normal rate of dissociation. Thus, the free energy of mobile\u2010loop ordering and disordering acts like the inertia of an engine's flywheel by modulating the speed of chaperonin conformational changes.</jats:p>",
  "DOI": "10.1110/ps.04773204",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2004,
        7,
        7
      ]
    ],
    "date-time": "2004-07-07T01:14:27Z",
    "timestamp": 1089162867000
  },
  "page": "2139-2148",
  "source": "Crossref",
  "is-referenced-by-count": 17,
  "title": "A mobile loop order\u2013disorder transition modulates the speed of chaperonin cycling",
  "prefix": "10.1002",
  "volume": "13",
  "author": [
    {
      "given": "Frank",
      "family": "Shewmaker",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Michael J.",
      "family": "Kerner",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Manajit",
      "family": "Hayer\u2010Hartl",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Gracjana",
      "family": "Klein",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Costa",
      "family": "Georgopoulos",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Samuel J.",
      "family": "Landry",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2009,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_12_2_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0960-9822(93)90268-S"
    },
    {
      "key": "e_1_2_12_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.51.34075"
    },
    {
      "key": "e_1_2_12_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.genet.34.1.439"
    },
    {
      "key": "e_1_2_12_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M008477200"
    },
    {
      "key": "e_1_2_12_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2364(85)90018-6"
    },
    {
      "key": "e_1_2_12_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.90.9.3978"
    },
    {
      "key": "e_1_2_12_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/371578a0"
    },
    {
      "key": "e_1_2_12_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(01)00517-7"
    },
    {
      "key": "e_1_2_12_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00220a020"
    },
    {
      "key": "e_1_2_12_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/cdg477"
    },
    {
      "key": "e_1_2_12_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/90443"
    },
    {
      "key": "e_1_2_12_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/10735"
    },
    {
      "key": "e_1_2_12_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi012159"
    },
    {
      "key": "e_1_2_12_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0959-440X(02)00289-0"
    },
    {
      "key": "e_1_2_12_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80692-3"
    },
    {
      "key": "e_1_2_12_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/371614a0"
    },
    {
      "key": "e_1_2_12_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90378-C"
    },
    {
      "key": "e_1_2_12_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi020117v"
    },
    {
      "key": "e_1_2_12_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7638601"
    },
    {
      "key": "e_1_2_12_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/379037a0"
    },
    {
      "key": "e_1_2_12_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)80343-8"
    },
    {
      "key": "e_1_2_12_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "7853",
      "DOI": "10.1016/S0021-9258(19)39009-X",
      "article-title": "Enhanced operator binding by trp superrepressors of Escherichia coli",
      "volume": "265",
      "author": "Hurlburt B.K.",
      "year": "1990",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_12_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-2836(02)00969-5"
    },
    {
      "key": "e_1_2_12_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1063/1.438208"
    },
    {
      "key": "e_1_2_12_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/embo-reports/kvf176"
    },
    {
      "key": "e_1_2_12_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1093/genetics/158.2.507",
      "article-title": "Identification of important amino acid residues that modulate binding of Escherichia coli GroEL to its various cochaperones",
      "volume": "158",
      "author": "Klein G.",
      "year": "2001",
      "journal-title": "Genetics"
    },
    {
      "key": "e_1_2_12_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/364255a0"
    },
    {
      "key": "e_1_2_12_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.21.11622"
    },
    {
      "key": "e_1_2_12_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi971141p"
    },
    {
      "key": "e_1_2_12_31_1",
      "first-page": "520",
      "volume-title": "acific Symposium on Biocomputing '99",
      "author": "Landry S.J.",
      "year": "1999"
    },
    {
      "key": "e_1_2_12_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.1998.2439"
    },
    {
      "key": "e_1_2_12_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/41892"
    },
    {
      "key": "e_1_2_12_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/371264a0"
    },
    {
      "key": "e_1_2_12_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0022-2836(02)01281-0"
    },
    {
      "key": "e_1_2_12_36_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/bip.10286"
    },
    {
      "key": "e_1_2_12_37_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF02192855"
    },
    {
      "key": "e_1_2_12_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.274.1.52"
    },
    {
      "key": "e_1_2_12_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0960-9822(93)90176-O"
    },
    {
      "key": "e_1_2_12_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.M102765200"
    },
    {
      "key": "e_1_2_12_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.160259697"
    },
    {
      "key": "e_1_2_12_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.284.5415.822"
    },
    {
      "key": "e_1_2_12_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmra.1993.1098"
    },
    {
      "key": "e_1_2_12_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00084a024"
    },
    {
      "key": "e_1_2_12_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7913555"
    },
    {
      "key": "e_1_2_12_46_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/368654a0"
    },
    {
      "key": "e_1_2_12_47_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(91)90214-Q"
    },
    {
      "key": "e_1_2_12_48_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/jmbi.1999.3110"
    },
    {
      "key": "e_1_2_12_49_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/41944"
    },
    {
      "key": "e_1_2_12_50_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00016a001"
    },
    {
      "key": "e_1_2_12_51_1",
      "doi-asserted-by": "crossref",
      "first-page": "6558",
      "DOI": "10.1128/jb.176.21.6558-6565.1994",
      "article-title": "Two classes of extragenic suppressor mutations identify functionally distinct regions of the GroEL chaperone of Escherichia coli",
      "volume": "176",
      "author": "Zeilstra\u2010Ryalls J.",
      "year": "1994",
      "journal-title": "J. Bacteriol."
    }
  ],
  "container-title": "Protein Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1110%2Fps.04773204",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1110/ps.04773204",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        9,
        28
      ]
    ],
    "date-time": "2023-09-28T22:47:31Z",
    "timestamp": 1695941251000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1110/ps.04773204"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2004,
        8
      ]
    ]
  },
  "references-count": 50,
  "journal-issue": {
    "issue": "8",
    "published-print": {
      "date-parts": [
        [
          2004,
          8
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1110/ps.04773204"
  ],
  "URL": "http://dx.doi.org/10.1110/ps.04773204",
  "relation": {},
  "ISSN": [
    "0961-8368",
    "1469-896X"
  ],
  "subject": [],
  "container-title-short": "Protein Science",
  "published": {
    "date-parts": [
      [
        2004,
        8
      ]
    ]
  }
}