DOI: 10.1073/pnas.96.19.10667. Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation

Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation

10.1073/pnas.96.19.10667

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The mechanistic basis of sensory adaptation and gradient sensing in bacterial chemotaxis is reversible covalent modification of transmembrane chemoreceptors, methylation, and demethylation at specific glutamyl residues in their cytoplasmic domains. These reactions are catalyzed by a dedicated methyltransferase CheR and a dedicated methylesterase CheB. The esterase is also a deamidase that creates certain methyl-accepting glutamyls by hydrolysis of glutamine side chains. We investigated the action of CheB and its activated form, phospho-CheB, on a truncated form of the aspartate receptor of Escherichia coli that was missing the last 5 aa of the intact receptor. The deleted pentapeptide is conserved in several chemoreceptors in enteric and related bacteria. The truncated receptor was much less efficiently demethylated and deamidated than intact receptor, but essentially was unperturbed for kinase activation or transmembrane signaling. CheB bound specifically to an affinity column carrying the isolated pentapeptide, implying that in the intact receptor the pentapeptide serves as a docking site for the methylesterase/deamidase and that the truncated receptor was inefficiently modified because the enzyme could not dock. It is striking that the same pentapeptide serves as an activity-enhancing docking site for the methyltransferase CheR, the other enzyme involved in adaptational covalent modification of chemoreceptors. A shared docking site raises the tantalizing possibility that relative rates of methylation and demethylation could be influenced by competition between the two enzymes at that site.

Bibliography

Barnakov, A. N., Barnakova, L. A., & Hazelbauer, G. L. (1999). Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation. Proceedings of the National Academy of Sciences, 96(19), 10667â10672.

Authors 3

Alexander N. Barnakov (first)
Ludmila A. Barnakova (additional)
Gerald L. Hazelbauer (additional)

References 42 Referenced 78

G L Hazelbauer Encyclopedia of Neuroscience, eds G Adelman, B H Smith (Elsevier, Amsterdam), pp. 181–183 (1999). / Encyclopedia of Neuroscience by Hazelbauer G L (1999)
10.1016/0092-8674(93)90267-T
10.1146/annurev.cellbio.13.1.457
10.1016/0092-8674(82)90421-4
10.1073/pnas.80.12.3599
10.1016/S0021-9258(18)92884-X
10.1016/S0021-9258(18)32536-5
10.1016/S0021-9258(18)45534-2
10.1002/prot.340030205
10.1016/S0021-9258(18)67460-5
G L Hazelbauer, R Yaghmai, G G Burrows, J W Baumgartner, D P Dutton, D G Morgan Biology of the Chemotactic Response: Society for General Microbiology Symposium, eds J P Armitage, J M Lackie (Cambridge Univ. Press, Cambridge) 46, 107–134 (1990). / Biology of the Chemotactic Response: Society for General Microbiology Symposium by Hazelbauer G L (1990)
10.1128/jb.172.12.7179-7187.1990
10.1016/S0021-9258(18)52321-8
10.1073/pnas.89.15.6756
10.1016/S0021-9258(18)71497-X
10.1016/S0021-9258(17)39227-X
10.1016/0092-8674(88)90489-8
10.1021/bi980865d
10.1128/jb.171.7.3609-3618.1989
10.1021/bi9530189
10.1021/bi971510h
10.1021/bi9713207
10.1128/JB.180.24.6713-6718.1998
10.1128/JB.181.10.3164-3171.1999
10.1038/283098a0
10.1128/jb.179.21.6714-6720.1997
10.1128/JB.180.4.914-920.1998
10.1128/jb.151.1.106-113.1982
10.1073/pnas.86.4.1208
10.1073/pnas.88.3.750
10.1016/0092-8674(92)90247-A
10.1016/S0006-291X(86)80130-9
10.1016/0003-2697(84)90437-8
10.1021/bi00045a003
10.1016/0076-6879(91)00140-R
10.1038/365343a0
10.1073/pnas.78.10.6051
10.1128/jb.145.1.35-42.1981
10.1128/JB.180.7.1862-1868.1998
10.1016/S0021-9258(20)71286-X
10.1016/0092-8674(81)90051-9
10.1126/science.8456299

Dates

Type	When
Created	23 years ago (July 26, 2002, 10:35 a.m.)
Deposited	3 years, 4 months ago (April 13, 2022, 3:27 p.m.)
Indexed	2 weeks, 2 days ago (Aug. 6, 2025, 8:09 a.m.)
Issued	25 years, 11 months ago (Sept. 14, 1999)
Published	25 years, 11 months ago (Sept. 14, 1999)
Published Online	25 years, 11 months ago (Sept. 14, 1999)
Published Print	25 years, 11 months ago (Sept. 14, 1999)

Funders 0

None

BibTeX

@article{Barnakov_1999, title={Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation}, volume={96}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.96.19.10667}, DOI={10.1073/pnas.96.19.10667}, number={19}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Barnakov, Alexander N. and Barnakova, Ludmila A. and Hazelbauer, Gerald L.}, year={1999}, month=sep, pages={10667–10672} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        6
      ]
    ],
    "date-time": "2025-08-06T12:09:10Z",
    "timestamp": 1754482150292
  },
  "reference-count": 42,
  "publisher": "Proceedings of the National Academy of Sciences",
  "issue": "19",
  "content-domain": {
    "domain": [
      "www.pnas.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        9,
        14
      ]
    ]
  },
  "abstract": "<jats:p>\n            The mechanistic basis of sensory adaptation and gradient sensing in bacterial chemotaxis is reversible covalent modification of transmembrane chemoreceptors, methylation, and demethylation at specific glutamyl residues in their cytoplasmic domains. These reactions are catalyzed by a dedicated methyltransferase CheR and a dedicated methylesterase CheB. The esterase is also a deamidase that creates certain methyl-accepting glutamyls by hydrolysis of glutamine side chains. We investigated the action of CheB and its activated form, phospho-CheB, on a truncated form of the aspartate receptor of\n            <jats:italic>Escherichia coli</jats:italic>\n            that was missing the last 5 aa of the intact receptor. The deleted pentapeptide is conserved in several chemoreceptors in enteric and related bacteria. The truncated receptor was much less efficiently demethylated and deamidated than intact receptor, but essentially was unperturbed for kinase activation or transmembrane signaling. CheB bound specifically to an affinity column carrying the isolated pentapeptide, implying that in the intact receptor the pentapeptide serves as a docking site for the methylesterase/deamidase and that the truncated receptor was inefficiently modified because the enzyme could not dock. It is striking that the same pentapeptide serves as an activity-enhancing docking site for the methyltransferase CheR, the other enzyme involved in adaptational covalent modification of chemoreceptors. A shared docking site raises the tantalizing possibility that relative rates of methylation and demethylation could be influenced by competition between the two enzymes at that site.\n          </jats:p>",
  "DOI": "10.1073/pnas.96.19.10667",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T14:35:07Z",
    "timestamp": 1027694107000
  },
  "page": "10667-10672",
  "update-policy": "http://dx.doi.org/10.1073/pnas.cm10313",
  "source": "Crossref",
  "is-referenced-by-count": 78,
  "title": "Efficient adaptational demethylation of chemoreceptors requires the same enzyme-docking site as efficient methylation",
  "prefix": "10.1073",
  "volume": "96",
  "author": [
    {
      "given": "Alexander N.",
      "family": "Barnakov",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Biochemistry and Biophysics, Washington State University, Pullman, WA 99164-4660"
        }
      ]
    },
    {
      "given": "Ludmila A.",
      "family": "Barnakova",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry and Biophysics, Washington State University, Pullman, WA 99164-4660"
        }
      ]
    },
    {
      "given": "Gerald L.",
      "family": "Hazelbauer",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biochemistry and Biophysics, Washington State University, Pullman, WA 99164-4660"
        }
      ]
    }
  ],
  "member": "341",
  "published-online": {
    "date-parts": [
      [
        1999,
        9,
        14
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_3_3_1_2",
      "first-page": "181",
      "volume-title": "Encyclopedia of Neuroscience",
      "author": "Hazelbauer G L",
      "year": "1999",
      "unstructured": "G L Hazelbauer Encyclopedia of Neuroscience, eds G Adelman, B H Smith (Elsevier, Amsterdam), pp. 181\u2013183 (1999)."
    },
    {
      "key": "e_1_3_3_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(93)90267-T"
    },
    {
      "key": "e_1_3_3_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.cellbio.13.1.457"
    },
    {
      "key": "e_1_3_3_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(82)90421-4"
    },
    {
      "key": "e_1_3_3_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.80.12.3599"
    },
    {
      "key": "e_1_3_3_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)92884-X"
    },
    {
      "key": "e_1_3_3_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)32536-5"
    },
    {
      "key": "e_1_3_3_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)45534-2"
    },
    {
      "key": "e_1_3_3_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/prot.340030205"
    },
    {
      "key": "e_1_3_3_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)67460-5"
    },
    {
      "key": "e_1_3_3_11_2",
      "first-page": "107",
      "volume-title": "Biology of the Chemotactic Response: Society for General Microbiology Symposium",
      "author": "Hazelbauer G L",
      "year": "1990",
      "unstructured": "G L Hazelbauer, R Yaghmai, G G Burrows, J W Baumgartner, D P Dutton, D G Morgan Biology of the Chemotactic Response: Society for General Microbiology Symposium, eds J P Armitage, J M Lackie (Cambridge Univ. Press, Cambridge) 46, 107\u2013134 (1990)."
    },
    {
      "key": "e_1_3_3_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.172.12.7179-7187.1990"
    },
    {
      "key": "e_1_3_3_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)52321-8"
    },
    {
      "key": "e_1_3_3_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.15.6756"
    },
    {
      "key": "e_1_3_3_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)71497-X"
    },
    {
      "key": "e_1_3_3_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(17)39227-X"
    },
    {
      "key": "e_1_3_3_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(88)90489-8"
    },
    {
      "key": "e_1_3_3_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi980865d"
    },
    {
      "key": "e_1_3_3_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.171.7.3609-3618.1989"
    },
    {
      "key": "e_1_3_3_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi9530189"
    },
    {
      "key": "e_1_3_3_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi971510h"
    },
    {
      "key": "e_1_3_3_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi9713207"
    },
    {
      "key": "e_1_3_3_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.24.6713-6718.1998"
    },
    {
      "key": "e_1_3_3_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.181.10.3164-3171.1999"
    },
    {
      "key": "e_1_3_3_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/283098a0"
    },
    {
      "key": "e_1_3_3_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.21.6714-6720.1997"
    },
    {
      "key": "e_1_3_3_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.4.914-920.1998"
    },
    {
      "key": "e_1_3_3_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.151.1.106-113.1982"
    },
    {
      "key": "e_1_3_3_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.4.1208"
    },
    {
      "key": "e_1_3_3_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.88.3.750"
    },
    {
      "key": "e_1_3_3_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90247-A"
    },
    {
      "key": "e_1_3_3_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-291X(86)80130-9"
    },
    {
      "key": "e_1_3_3_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-2697(84)90437-8"
    },
    {
      "key": "e_1_3_3_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1021/bi00045a003"
    },
    {
      "key": "e_1_3_3_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0076-6879(91)00140-R"
    },
    {
      "key": "e_1_3_3_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/365343a0"
    },
    {
      "key": "e_1_3_3_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.78.10.6051"
    },
    {
      "key": "e_1_3_3_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.145.1.35-42.1981"
    },
    {
      "key": "e_1_3_3_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.7.1862-1868.1998"
    },
    {
      "key": "e_1_3_3_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(20)71286-X"
    },
    {
      "key": "e_1_3_3_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(81)90051-9"
    },
    {
      "key": "e_1_3_3_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8456299"
    }
  ],
  "container-title": "Proceedings of the National Academy of Sciences",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://pnas.org/doi/pdf/10.1073/pnas.96.19.10667",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        4,
        13
      ]
    ],
    "date-time": "2022-04-13T19:27:12Z",
    "timestamp": 1649878032000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://pnas.org/doi/full/10.1073/pnas.96.19.10667"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        9,
        14
      ]
    ]
  },
  "references-count": 42,
  "journal-issue": {
    "issue": "19",
    "published-print": {
      "date-parts": [
        [
          1999,
          9,
          14
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1073/pnas.96.19.10667"
  ],
  "URL": "http://dx.doi.org/10.1073/pnas.96.19.10667",
  "relation": {},
  "ISSN": [
    "0027-8424",
    "1091-6490"
  ],
  "subject": [],
  "container-title-short": "Proc. Natl. Acad. Sci. U.S.A.",
  "published": {
    "date-parts": [
      [
        1999,
        9,
        14
      ]
    ]
  },
  "assertion": [
    {
      "value": "1999-06-03",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-09-14",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}