DOI: 10.1126/science.7824948. Structural Basis for Sugar Translocation Through Maltoporin Channels at 3.1 Å Resolution

Structural Basis for Sugar Translocation Through Maltoporin Channels at 3.1 Å Resolution

10.1126/science.7824948

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Trimeric maltoporin (LamB protein) facilitates the diffusion of maltodextrins across the outer membrane of Gram-negative bacteria. The crystal structure of maltoporin from Escherichia coli , determined to a resolution of 3.1 angstroms, reveals an 18-stranded, antiparallel β-barrel that forms the framework of the channel. Three inwardly folded loops contribute to a constriction about halfway through the channel. Six contingent aromatic residues line the channel and form a path from the vestibule to the periplasmic outlet. Soaking of a crystal with maltotriose revealed binding of the sugar to this hydrophobic track across the constriction, which suggests that maltose and linear oligosaccharides may be translocated across the membrane by guided diffusion along this path.

Bibliography

Schirmer, T., Keller, T. A., Wang, Y.-F., & Rosenbusch, J. P. (1995). Structural Basis for Sugar Translocation Through Maltoporin Channels at 3.1 Ã Resolution. Science, 267(5197), 512â514.

Authors 4

Tilman Schirmer (first)
Thomas A. Keller (additional)
Yan-Fei Wang (additional)
Jurg P. Rosenbusch (additional)

References 31 Referenced 491

BENZ, R, MECHANISM OF SUGAR-TRANSPORT THROUGH THE SUGAR-SPECIFIC LAMB CHANNEL OF ESCHERICHIA-COLI OUTER-MEMBRANE, JOURNAL OF MEMBRANE BIOLOGY 100: 21 (1987). (10.1007/BF02209137) / JOURNAL OF MEMBRANE BIOLOGY (1987)
Brunger A. T. X-PLOR Version 2.1 (1990).
BUEHLER, L.K., PLASTICITY OF ESCHERICHIA-COLI PORIN CHANNELS - DEPENDENCE OF THEIR CONDUCTANCE ON STRAIN AND LIPID ENVIRONMENT, JOURNAL OF BIOLOGICAL CHEMISTRY 266: 24446 (1991). (10.1016/S0021-9258(18)54249-6) / JOURNAL OF BIOLOGICAL CHEMISTRY (1991)
CHARBIT, A, PERMISSIVE SITES AND TOPOLOGY OF AN OUTER-MEMBRANE PROTEIN WITH A REPORTER EPITOPE, JOURNAL OF BACTERIOLOGY 173: 262 (1991). (10.1128/jb.173.1.262-275.1991) / JOURNAL OF BACTERIOLOGY (1991)
CHARBIT, A, MALTOSE TRANSPORT AND STARCH BINDING IN PHAGE-RESISTANT POINT MUTANTS OF MALTOPORIN - FUNCTIONAL AND TOPOLOGICAL IMPLICATIONS, JOURNAL OF MOLECULAR BIOLOGY 201: 487 (1988). (10.1016/0022-2836(88)90630-4) / JOURNAL OF MOLECULAR BIOLOGY (1988)
CLEMENT, J.M., GENE SEQUENCE OF THE LAMBDA RECEPTOR, AN OUTER-MEMBRANE PROTEIN OF ESCHERICHIA-COLI-K12, CELL 27: 507 (1981). (10.1016/0092-8674(81)90392-5) / CELL (1981)
COWAN, S.W., CRYSTAL-STRUCTURES EXPLAIN FUNCTIONAL-PROPERTIES OF 2 ESCHERICHIA-COLI PORINS, NATURE 358: 727 (1992). (10.1038/358727a0) / NATURE (1992)
DARGENT, B, SELECTIVITY FOR MALTOSE AND MALTODEXTRINS OF MALTOPORIN, A PORE-FORMING PROTEIN OF ESCHERICHIA-COLI OUTER-MEMBRANE, FEBS LETTERS 220: 136 (1987). (10.1016/0014-5793(87)80891-8) / FEBS LETTERS (1987)
FERENCI, T, SELECTIVITY IN SOLUTE TRANSPORT - BINDING-SITES AND CHANNEL STRUCTURE IN MALTOPORIN AND OTHER BACTERIAL SUGAR-TRANSPORT PROTEINS, BIOESSAYS 10: 3 (1989). / BIOESSAYS (1989)
FERENCI, T, DIRECTED EVOLUTION OF THE LAMBDA RECEPTOR OF ESCHERICHIA-COLI THROUGH AFFINITY CHROMATOGRAPHIC SELECTION, JOURNAL OF MOLECULAR BIOLOGY 160: 431 (1982). (10.1016/0022-2836(82)90306-0) / JOURNAL OF MOLECULAR BIOLOGY (1982)
FREUNDLIEB, S, FACILITATED DIFFUSION OF PARA-NITROPHENYL-ALPHA-D-MALTOHEXAOSIDE THROUGH THE OUTER-MEMBRANE OF ESCHERICHIA-COLI - CHARACTERIZATION OF LAMB AS A SPECIFIC AND SATURABLE CHANNEL FOR MALTOOLIGOSACCHARIDES, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 314 (1988). (10.1016/S0021-9258(19)57394-X) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
GARAVITO, R.M., THE CRYSTALLIZATION OF OUTER-MEMBRANE PROTEINS FROM ESCHERICHIA-COLI - STUDIES ON LAMB AND OMPA GENE-PRODUCTS, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 4254 (1984). (10.1016/S0021-9258(17)43037-7) / JOURNAL OF BIOLOGICAL CHEMISTRY (1984)
GEHRING, K, STOICHIOMETRY OF MALTODEXTRIN-BINDING SITES IN LAMB, AN OUTER-MEMBRANE PROTEIN FROM ESCHERICHIA-COLI, JOURNAL OF BACTERIOLOGY 173: 1873 (1991). (10.1128/jb.173.6.1873-1878.1991) / JOURNAL OF BACTERIOLOGY (1991)
GOLDSMITH, E, STRUCTURE OF MALTOHEPTAOSE BY DIFFERENCE FOURIER METHODS AND A MODEL FOR GLYCOGEN, JOURNAL OF MOLECULAR BIOLOGY 156: 411 (1982). (10.1016/0022-2836(82)90336-9) / JOURNAL OF MOLECULAR BIOLOGY (1982)
HEINE, H.G., SEQUENCE DETERMINANTS IN THE LAMB GENE OF ESCHERICHIA-COLI INFLUENCING THE BINDING AND PORE SELECTIVITY OF MALTOPORIN, GENE 53: 287 (1987). (10.1016/0378-1119(87)90018-7) / GENE (1987)
Jones T. A. O: The Manual (1991).
KELLER, T.A., CRYSTALLIZATION OF MONODISPERSE MALTOPORIN FROM WILDTYPE AND MUTANT STRAINS OF VARIOUS ENTEROBACTERIACEAE, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 199: 767 (1994). (10.1006/bbrc.1994.1295) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS (1994)
Kleywegt, G. J., Halloween ... Masks and Bones, From First Map to Final Model: 59 (1994). / From First Map to Final Model / Halloween ... Masks and Bones (1994)
KREUSCH, A, STRUCTURE OF THE MEMBRANE CHANNEL PORIN FROM RHODOPSEUDOMONAS-BLASTICA AT 2.0 ANGSTROM RESOLUTION, PROTEIN SCIENCE 3: 58 (1994). (10.1002/pro.5560030108) / PROTEIN SCIENCE (1994)
LESK, A.M., STRUCTURAL PRINCIPLES OF ALPHA-BETA-BARREL PROTEINS - THE PACKING OF THE INTERIOR OF THE SHEET, PROTEINS-STRUCTURE FUNCTION AND GENETICS 5: 139 (1989). (10.1002/prot.340050208) / PROTEINS-STRUCTURE FUNCTION AND GENETICS (1989)
LUCKEY, M, SPECIFICITY OF DIFFUSION CHANNELS PRODUCED BY LAMBDA-PHAGE RECEPTOR PROTEIN OF ESCHERICHIA-COLI, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 167 (1980). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1980)
NEUHAUS, J.M., THE PERIPLASMIC MALTOSE-BINDING PROTEIN MODIFIES THE CHANNEL-FORMING CHARACTERISTICS OF MALTOPORIN, EMBO JOURNAL 2: 1987 (1983). (10.1002/j.1460-2075.1983.tb01689.x) / EMBO JOURNAL (1983)
PAUPTIT, R.A., A COMMON CHANNEL-FORMING MOTIF IN EVOLUTIONARILY DISTANT PORINS, JOURNAL OF STRUCTURAL BIOLOGY 107: 136 (1991). (10.1016/1047-8477(91)90017-Q) / JOURNAL OF STRUCTURAL BIOLOGY (1991)
RANDALLHAZELBAU.L, J BACTERIOL 116: 1436 (1973). (10.1128/jb.116.3.1436-1446.1973) / J BACTERIOL (1973)
ROSSMANN, M.G., RELATIVE POSITIONS OF INDEPENDENT MOLECULES WITHIN SAME ASYMMETRIC UNIT, ACTA CRYSTALLOGRAPHICA 17: 338 (1964). (10.1107/S0365110X64000822) / ACTA CRYSTALLOGRAPHICA (1964)
SCHIRMER, T, PREDICTION OF MEMBRANE-SPANNING BETA-STRANDS AND ITS APPLICATION TO MALTOPORIN, PROTEIN SCIENCE 2: 1361 (1993). (10.1002/pro.5560020820) / PROTEIN SCIENCE (1993)
Schwartz, M., Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology: 1482 (1987). / Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology (1987)
SPURLINO, J.C., THE 2.3-A RESOLUTION STRUCTURE OF THE MALTOSE-BINDING OR MALTODEXTRIN-BINDING PROTEIN, A PRIMARY RECEPTOR OF BACTERIAL ACTIVE-TRANSPORT AND CHEMOTAXIS, JOURNAL OF BIOLOGICAL CHEMISTRY 266: 5202 (1991). (10.1016/S0021-9258(19)67774-4) / JOURNAL OF BIOLOGICAL CHEMISTRY (1991)
STAUFFER, K.A., CRYSTALLIZATION AND PRELIMINARY-X-RAY CHARACTERIZATION OF MALTOPORIN FROM ESCHERICHIA-COLI, JOURNAL OF MOLECULAR BIOLOGY 211: 297 (1990). (10.1016/0022-2836(90)90351-L) / JOURNAL OF MOLECULAR BIOLOGY (1990)
WANDERSMAN, C, ESCHERICHIA-COLI MUTANTS IMPAIRED IN MALTODEXTRIN TRANSPORT, JOURNAL OF BACTERIOLOGY 140: 1 (1979). (10.1128/jb.140.1.1-13.1979) / JOURNAL OF BACTERIOLOGY (1979)
10.1126/science.1721242

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 2:19 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 10:55 p.m.)
Indexed	1 hour, 7 minutes ago (Aug. 29, 2025, 6:10 a.m.)
Issued	30 years, 7 months ago (Jan. 27, 1995)
Published	30 years, 7 months ago (Jan. 27, 1995)
Published Print	30 years, 7 months ago (Jan. 27, 1995)

Funders 0

None

BibTeX

@article{Schirmer_1995, title={Structural Basis for Sugar Translocation Through Maltoporin Channels at 3.1 Å Resolution}, volume={267}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.7824948}, DOI={10.1126/science.7824948}, number={5197}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Schirmer, Tilman and Keller, Thomas A. and Wang, Yan-Fei and Rosenbusch, Jurg P.}, year={1995}, month=jan, pages={512–514} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        29
      ]
    ],
    "date-time": "2025-08-29T10:10:29Z",
    "timestamp": 1756462229913
  },
  "reference-count": 31,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "5197",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1995,
        1,
        27
      ]
    ]
  },
  "abstract": "<jats:p>\n            Trimeric maltoporin (LamB protein) facilitates the diffusion of maltodextrins across the outer membrane of Gram-negative bacteria. The crystal structure of maltoporin from\n            <jats:italic>Escherichia coli</jats:italic>\n            , determined to a resolution of 3.1 angstroms, reveals an 18-stranded, antiparallel \u03b2-barrel that forms the framework of the channel. Three inwardly folded loops contribute to a constriction about halfway through the channel. Six contingent aromatic residues line the channel and form a path from the vestibule to the periplasmic outlet. Soaking of a crystal with maltotriose revealed binding of the sugar to this hydrophobic track across the constriction, which suggests that maltose and linear oligosaccharides may be translocated across the membrane by guided diffusion along this path.\n          </jats:p>",
  "DOI": "10.1126/science.7824948",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        27
      ]
    ],
    "date-time": "2006-10-27T18:19:42Z",
    "timestamp": 1161973182000
  },
  "page": "512-514",
  "source": "Crossref",
  "is-referenced-by-count": 491,
  "title": "Structural Basis for Sugar Translocation Through Maltoporin Channels at 3.1 \u00c5 Resolution",
  "prefix": "10.1126",
  "volume": "267",
  "author": [
    {
      "given": "Tilman",
      "family": "Schirmer",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Structural Biology, Biozentrum, University of Basel, CH-4056 Basel, Switzerland."
        }
      ]
    },
    {
      "given": "Thomas A.",
      "family": "Keller",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, Biozentrum, University of Basel, CH-4056 Basel, Switzerland."
        }
      ]
    },
    {
      "given": "Yan-Fei",
      "family": "Wang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, Biozentrum, University of Basel, CH-4056 Basel, Switzerland."
        }
      ]
    },
    {
      "given": "Jurg P.",
      "family": "Rosenbusch",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Microbiology, Biozentrum, University of Basel, CH-4056 Basel, Switzerland."
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "21",
      "DOI": "10.1007/BF02209137",
      "volume": "100",
      "year": "1987",
      "unstructured": "BENZ, R, MECHANISM OF SUGAR-TRANSPORT THROUGH THE SUGAR-SPECIFIC LAMB CHANNEL OF ESCHERICHIA-COLI OUTER-MEMBRANE, JOURNAL OF MEMBRANE BIOLOGY 100: 21 (1987).",
      "journal-title": "JOURNAL OF MEMBRANE BIOLOGY"
    },
    {
      "key": "e_1_2_1_2_1",
      "unstructured": "Brunger A. T. X-PLOR Version 2.1 (1990)."
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "crossref",
      "first-page": "24446",
      "DOI": "10.1016/S0021-9258(18)54249-6",
      "volume": "266",
      "year": "1991",
      "unstructured": "BUEHLER, L.K., PLASTICITY OF ESCHERICHIA-COLI PORIN CHANNELS - DEPENDENCE OF THEIR CONDUCTANCE ON STRAIN AND LIPID ENVIRONMENT, JOURNAL OF BIOLOGICAL CHEMISTRY 266: 24446 (1991).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "262",
      "DOI": "10.1128/jb.173.1.262-275.1991",
      "volume": "173",
      "year": "1991",
      "unstructured": "CHARBIT, A, PERMISSIVE SITES AND TOPOLOGY OF AN OUTER-MEMBRANE PROTEIN WITH A REPORTER EPITOPE, JOURNAL OF BACTERIOLOGY 173: 262 (1991).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "487",
      "DOI": "10.1016/0022-2836(88)90630-4",
      "volume": "201",
      "year": "1988",
      "unstructured": "CHARBIT, A, MALTOSE TRANSPORT AND STARCH BINDING IN PHAGE-RESISTANT POINT MUTANTS OF MALTOPORIN - FUNCTIONAL AND TOPOLOGICAL IMPLICATIONS, JOURNAL OF MOLECULAR BIOLOGY 201: 487 (1988).",
      "journal-title": "JOURNAL OF MOLECULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1016/0092-8674(81)90392-5",
      "volume": "27",
      "year": "1981",
      "unstructured": "CLEMENT, J.M., GENE SEQUENCE OF THE LAMBDA RECEPTOR, AN OUTER-MEMBRANE PROTEIN OF ESCHERICHIA-COLI-K12, CELL 27: 507 (1981).",
      "journal-title": "CELL"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "727",
      "DOI": "10.1038/358727a0",
      "volume": "358",
      "year": "1992",
      "unstructured": "COWAN, S.W., CRYSTAL-STRUCTURES EXPLAIN FUNCTIONAL-PROPERTIES OF 2 ESCHERICHIA-COLI PORINS, NATURE 358: 727 (1992).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "136",
      "DOI": "10.1016/0014-5793(87)80891-8",
      "volume": "220",
      "year": "1987",
      "unstructured": "DARGENT, B, SELECTIVITY FOR MALTOSE AND MALTODEXTRINS OF MALTOPORIN, A PORE-FORMING PROTEIN OF ESCHERICHIA-COLI OUTER-MEMBRANE, FEBS LETTERS 220: 136 (1987).",
      "journal-title": "FEBS LETTERS"
    },
    {
      "key": "e_1_2_1_9_1",
      "first-page": "3",
      "volume": "10",
      "year": "1989",
      "unstructured": "FERENCI, T, SELECTIVITY IN SOLUTE TRANSPORT - BINDING-SITES AND CHANNEL STRUCTURE IN MALTOPORIN AND OTHER BACTERIAL SUGAR-TRANSPORT PROTEINS, BIOESSAYS 10: 3 (1989).",
      "journal-title": "BIOESSAYS"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "431",
      "DOI": "10.1016/0022-2836(82)90306-0",
      "volume": "160",
      "year": "1982",
      "unstructured": "FERENCI, T, DIRECTED EVOLUTION OF THE LAMBDA RECEPTOR OF ESCHERICHIA-COLI THROUGH AFFINITY CHROMATOGRAPHIC SELECTION, JOURNAL OF MOLECULAR BIOLOGY 160: 431 (1982).",
      "journal-title": "JOURNAL OF MOLECULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "314",
      "DOI": "10.1016/S0021-9258(19)57394-X",
      "volume": "263",
      "year": "1988",
      "unstructured": "FREUNDLIEB, S, FACILITATED DIFFUSION OF PARA-NITROPHENYL-ALPHA-D-MALTOHEXAOSIDE THROUGH THE OUTER-MEMBRANE OF ESCHERICHIA-COLI - CHARACTERIZATION OF LAMB AS A SPECIFIC AND SATURABLE CHANNEL FOR MALTOOLIGOSACCHARIDES, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 314 (1988).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_12_1",
      "doi-asserted-by": "crossref",
      "first-page": "4254",
      "DOI": "10.1016/S0021-9258(17)43037-7",
      "volume": "259",
      "year": "1984",
      "unstructured": "GARAVITO, R.M., THE CRYSTALLIZATION OF OUTER-MEMBRANE PROTEINS FROM ESCHERICHIA-COLI - STUDIES ON LAMB AND OMPA GENE-PRODUCTS, JOURNAL OF BIOLOGICAL CHEMISTRY 259: 4254 (1984).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "1873",
      "DOI": "10.1128/jb.173.6.1873-1878.1991",
      "volume": "173",
      "year": "1991",
      "unstructured": "GEHRING, K, STOICHIOMETRY OF MALTODEXTRIN-BINDING SITES IN LAMB, AN OUTER-MEMBRANE PROTEIN FROM ESCHERICHIA-COLI, JOURNAL OF BACTERIOLOGY 173: 1873 (1991).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "DOI": "10.1016/0022-2836(82)90336-9",
      "volume": "156",
      "year": "1982",
      "unstructured": "GOLDSMITH, E, STRUCTURE OF MALTOHEPTAOSE BY DIFFERENCE FOURIER METHODS AND A MODEL FOR GLYCOGEN, JOURNAL OF MOLECULAR BIOLOGY 156: 411 (1982).",
      "journal-title": "JOURNAL OF MOLECULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "287",
      "DOI": "10.1016/0378-1119(87)90018-7",
      "volume": "53",
      "year": "1987",
      "unstructured": "HEINE, H.G., SEQUENCE DETERMINANTS IN THE LAMB GENE OF ESCHERICHIA-COLI INFLUENCING THE BINDING AND PORE SELECTIVITY OF MALTOPORIN, GENE 53: 287 (1987).",
      "journal-title": "GENE"
    },
    {
      "key": "e_1_2_1_16_1",
      "unstructured": "Jones T. A. O: The Manual (1991)."
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "crossref",
      "first-page": "767",
      "DOI": "10.1006/bbrc.1994.1295",
      "volume": "199",
      "year": "1994",
      "unstructured": "KELLER, T.A., CRYSTALLIZATION OF MONODISPERSE MALTOPORIN FROM WILDTYPE AND MUTANT STRAINS OF VARIOUS ENTEROBACTERIACEAE, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 199: 767 (1994).",
      "journal-title": "BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS"
    },
    {
      "key": "e_1_2_1_18_1",
      "first-page": "59",
      "article-title": "Halloween ... Masks and Bones",
      "year": "1994",
      "unstructured": "Kleywegt, G. J., Halloween ... Masks and Bones, From First Map to Final Model: 59 (1994).",
      "journal-title": "From First Map to Final Model"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "58",
      "DOI": "10.1002/pro.5560030108",
      "volume": "3",
      "year": "1994",
      "unstructured": "KREUSCH, A, STRUCTURE OF THE MEMBRANE CHANNEL PORIN FROM RHODOPSEUDOMONAS-BLASTICA AT 2.0 ANGSTROM RESOLUTION, PROTEIN SCIENCE 3: 58 (1994).",
      "journal-title": "PROTEIN SCIENCE"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "139",
      "DOI": "10.1002/prot.340050208",
      "volume": "5",
      "year": "1989",
      "unstructured": "LESK, A.M., STRUCTURAL PRINCIPLES OF ALPHA-BETA-BARREL PROTEINS - THE PACKING OF THE INTERIOR OF THE SHEET, PROTEINS-STRUCTURE FUNCTION AND GENETICS 5: 139 (1989).",
      "journal-title": "PROTEINS-STRUCTURE FUNCTION AND GENETICS"
    },
    {
      "key": "e_1_2_1_21_1",
      "first-page": "167",
      "volume": "77",
      "year": "1980",
      "unstructured": "LUCKEY, M, SPECIFICITY OF DIFFUSION CHANNELS PRODUCED BY LAMBDA-PHAGE RECEPTOR PROTEIN OF ESCHERICHIA-COLI, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 77: 167 (1980).",
      "journal-title": "PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "1987",
      "DOI": "10.1002/j.1460-2075.1983.tb01689.x",
      "volume": "2",
      "year": "1983",
      "unstructured": "NEUHAUS, J.M., THE PERIPLASMIC MALTOSE-BINDING PROTEIN MODIFIES THE CHANNEL-FORMING CHARACTERISTICS OF MALTOPORIN, EMBO JOURNAL 2: 1987 (1983).",
      "journal-title": "EMBO JOURNAL"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "136",
      "DOI": "10.1016/1047-8477(91)90017-Q",
      "volume": "107",
      "year": "1991",
      "unstructured": "PAUPTIT, R.A., A COMMON CHANNEL-FORMING MOTIF IN EVOLUTIONARILY DISTANT PORINS, JOURNAL OF STRUCTURAL BIOLOGY 107: 136 (1991).",
      "journal-title": "JOURNAL OF STRUCTURAL BIOLOGY"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "1436",
      "DOI": "10.1128/jb.116.3.1436-1446.1973",
      "volume": "116",
      "year": "1973",
      "unstructured": "RANDALLHAZELBAU.L, J BACTERIOL 116: 1436 (1973).",
      "journal-title": "J BACTERIOL"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "338",
      "DOI": "10.1107/S0365110X64000822",
      "volume": "17",
      "year": "1964",
      "unstructured": "ROSSMANN, M.G., RELATIVE POSITIONS OF INDEPENDENT MOLECULES WITHIN SAME ASYMMETRIC UNIT, ACTA CRYSTALLOGRAPHICA 17: 338 (1964).",
      "journal-title": "ACTA CRYSTALLOGRAPHICA"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "1361",
      "DOI": "10.1002/pro.5560020820",
      "volume": "2",
      "year": "1993",
      "unstructured": "SCHIRMER, T, PREDICTION OF MEMBRANE-SPANNING BETA-STRANDS AND ITS APPLICATION TO MALTOPORIN, PROTEIN SCIENCE 2: 1361 (1993).",
      "journal-title": "PROTEIN SCIENCE"
    },
    {
      "key": "e_1_2_1_27_1",
      "first-page": "1482",
      "year": "1987",
      "unstructured": "Schwartz, M., Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology: 1482 (1987).",
      "journal-title": "Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "crossref",
      "first-page": "5202",
      "DOI": "10.1016/S0021-9258(19)67774-4",
      "volume": "266",
      "year": "1991",
      "unstructured": "SPURLINO, J.C., THE 2.3-A RESOLUTION STRUCTURE OF THE MALTOSE-BINDING OR MALTODEXTRIN-BINDING PROTEIN, A PRIMARY RECEPTOR OF BACTERIAL ACTIVE-TRANSPORT AND CHEMOTAXIS, JOURNAL OF BIOLOGICAL CHEMISTRY 266: 5202 (1991).",
      "journal-title": "JOURNAL OF BIOLOGICAL CHEMISTRY"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "297",
      "DOI": "10.1016/0022-2836(90)90351-L",
      "volume": "211",
      "year": "1990",
      "unstructured": "STAUFFER, K.A., CRYSTALLIZATION AND PRELIMINARY-X-RAY CHARACTERIZATION OF MALTOPORIN FROM ESCHERICHIA-COLI, JOURNAL OF MOLECULAR BIOLOGY 211: 297 (1990).",
      "journal-title": "JOURNAL OF MOLECULAR BIOLOGY"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1128/jb.140.1.1-13.1979",
      "volume": "140",
      "year": "1979",
      "unstructured": "WANDERSMAN, C, ESCHERICHIA-COLI MUTANTS IMPAIRED IN MALTODEXTRIN TRANSPORT, JOURNAL OF BACTERIOLOGY 140: 1 (1979).",
      "journal-title": "JOURNAL OF BACTERIOLOGY"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1721242"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.7824948",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        15
      ]
    ],
    "date-time": "2024-01-15T03:55:33Z",
    "timestamp": 1705290933000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.7824948"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1995,
        1,
        27
      ]
    ]
  },
  "references-count": 31,
  "journal-issue": {
    "issue": "5197",
    "published-print": {
      "date-parts": [
        [
          1995,
          1,
          27
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.7824948"
  ],
  "URL": "http://dx.doi.org/10.1126/science.7824948",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1995,
        1,
        27
      ]
    ]
  }
}