DOI: 10.1126/science.841332. Enzyme Polymorphisms as Genetic Signatures in Human Cell Cultures

Enzyme Polymorphisms as Genetic Signatures in Human Cell Cultures

10.1126/science.841332

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The electrophoretic resolution of seven relatively polymorphic human gene-enzyme systems expressed in tissue culture cells can be used as a sensitive genetic monitor for intraspecific cell contamination. An identical genotype at each of the same allozyme loci provides a 95 percent (or greater) confidence estimate of the identity of two cultured lines, on the basis of the allelic frequencies of the seven enzyme loci in natural populations and in populations of independently derived cultured cells. Of 27 commonly used human cell lines examined, only one of 351 pairwise comparisons proved genetically indistinguishable.

Bibliography

OâBrien, S. J., Kleiner, G., Olson, R., & Shannon, J. E. (1977). Enzyme Polymorphisms as Genetic Signatures in Human Cell Cultures. Science, 195(4284), 1345â1348.

Authors 4

Stephen J. O'Brien (first)
Gail Kleiner (additional)
Russell Olson (additional)
John E. Shannon (additional)

References 45 Referenced 78

AUERSPERG, N, ISOENZYME STABILITY IN HUMAN HETEROPLOID CELL LINES, EXPERIMENTAL CELL RESEARCH 61: 465 (1970). (10.1016/0014-4827(70)90474-X) / EXPERIMENTAL CELL RESEARCH (1970)
BENEDICT, W.F., POLYCYCLIC HYDROCARBON-PRODUCED TOXICITY, TRANSFORMATION, AND CHROMOSOMAL-ABERRATIONS AS A FUNCTION OF ARYL HYDROCARBON HYDROXYLASE-ACTIVITY IN CELL-CULTURES, INTERNATIONAL JOURNAL OF CANCER 9: 435 (1972). (10.1002/ijc.2910090223) / INTERNATIONAL JOURNAL OF CANCER (1972)
BREWER G.J. INTRO ISOZYME TECHNI (1970).
DAVIDSON, R.G., ELECTROPHORTIC VARIANTS OF HUMAN 6-PHOSPHOGLUCONATE DHYDROGENASE - POPULATION AND FAMILY STUDIES AND DESCRIPTION OF A NEW VARIANT, ANNALS OF HUMAN GENETICS 30: 355 (1967). (10.1111/j.1469-1809.1967.tb00037.x) / ANNALS OF HUMAN GENETICS (1967)
EDWARDS, Y.H., ADENOSINE DEAMINASE ISOZYMES IN HUMAN TISSUES, ANNALS OF HUMAN GENETICS 35: 207 (1971). (10.1111/j.1469-1809.1956.tb01393.x) / ANNALS OF HUMAN GENETICS (1971)
FILDES, R.A., GENETICALLY DETERMINED VARIATION OF ADENYLATE KINASE IN MAN, NATURE 209: 261 (1966). (10.1038/209261a0) / NATURE (1966)
GARTLER, S.M., NATIONAL CANCER INSTITUTE MONOGRAPHS 26: 167 (1967). / NATIONAL CANCER INSTITUTE MONOGRAPHS (1967)
GARTLER, S.M., APPARENT HELA CELL CONTAMINATION OF HUMAN HETEROPLOID CELL LINES, NATURE 217: 750 (1968). (10.1038/217750a0) / NATURE (1968)
GIARD, D.J., IN-VITRO CULTIVATION OF HUMAN TUMORS - ESTABLISHMENT OF CELL LINES DERIVED FROM A SERIES OF SOLID TUMORS, JOURNAL OF THE NATIONAL CANCER INSTITUTE 51: 1417 (1973). (10.1093/jnci/51.5.1417) / JOURNAL OF THE NATIONAL CANCER INSTITUTE (1973)
HARRIS, H, AVERAGE HETEROZYGOSITY PER LOCUS IN MAN - AN ESTIMATE BASED ON INCIDENCE OF ENZYME POLYMORPHISMS, ANNALS OF HUMAN GENETICS 36: 9 (1972). (10.1111/j.1469-1809.1972.tb00578.x) / ANNALS OF HUMAN GENETICS (1972)
HARRIS H HDB ENZYME ELECTROPH (1976).
HARRIS, H, ISOZYMES 4: 131 (1975). / ISOZYMES (1975)
HIRSCHHORN, R, CONVERSION OF HUMAN ERYTHROCYTE-ADENOSINE DEAMINASE ACTIVITY TO DIFFERENT TISSUE-SPECIFIC ISOENZYMES - EVIDENCE FOR A COMMON CATALYTIC UNIT, JOURNAL OF CLINICAL INVESTIGATION 55: 661 (1975). (10.1172/JCI107974) / JOURNAL OF CLINICAL INVESTIGATION (1975)
HOPKINSON, D.A., RARE PHOSPHOGLUCOMUTASE PHENOTYPES, ANNALS OF HUMAN GENETICS 30: 167 (1966). (10.1111/j.1469-1809.1966.tb00016.x) / ANNALS OF HUMAN GENETICS (1966)
HOPKINSON, D.A., A THIRD PHOSPHOGLUCOMUTASE LOCUS IN MAN, ANNALS OF HUMAN GENETICS 31: 359 (1968). (10.1111/j.1469-1809.1968.tb00567.x) / ANNALS OF HUMAN GENETICS (1968)
HOPKINSON, D.A., ESTERASE-D - NEW HUMAN POLYMORPHISM, ANNALS OF HUMAN GENETICS 37: 119 (1973). (10.1111/j.1469-1809.1973.tb01820.x) / ANNALS OF HUMAN GENETICS (1973)
10.1126/science.1246620
HSU T.C. ATLAS MAMMALIAN CHRO (1967).
KERSEY, J.H., HL-A ANTIGENS OF HUMAN TUMOR-DERIVED CELL LINES AND VIRAL TRANSFORMED FIBROBLASTS IN CULTURE, PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 143: 453 (1973). (10.3181/00379727-143-37341) / PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE (1973)
KIRKMAN, H.N., ADV HUM GENET 2: 1 (1971). / ADV HUM GENET (1971)
10.1038/259211a0
LEWIS, WHP, PEPTIDASE D (PROLIDASE) VARIANTS IN MAN, ANNALS OF HUMAN GENETICS 32: 317 (1969). (10.1111/j.1469-1809.1969.tb00081.x) / ANNALS OF HUMAN GENETICS (1969)
LEWIS, WHP, EXCERPTA MED INT 233: 111 (1971). / EXCERPTA MED INT 233 (1971)
LEWONTIN, R.C., POPULATION GENETICS, ANNUAL REVIEW OF GENETICS 7: 1 (1973). (10.1146/annurev.ge.07.120173.000245) / ANNUAL REVIEW OF GENETICS (1973)
MONTESDEOCA, F, PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 132: 462 (1969). (10.3181/00379727-132-34238) / PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE (1969)
NEI, M, GENETIC DISTANCE BETWEEN POPULATIONS, AMERICAN NATURALIST 106: 283 (1972). (10.1086/282771) / AMERICAN NATURALIST (1972)
10.1126/science.1246601
10.1126/science.557237
10.1126/science.184.4141.1093
OBRIEN S.J. GENETICS BIOLOGY DRO 2:.
O'Brien S. J. Genetics and Biology of Drosophila 2 (1978).
OBRIEN, S.J., ISOZYME BULLETIN 9: 20 (1976). / ISOZYME BULLETIN (1976)
OBRIEN, S.J., ISOZYME BULLETIN 9: 47 (1976). / ISOZYME BULLETIN (1976)
PERUTZ, M.F., MOLECULAR PATHOLOGY OF HUMAN HAEMOGLOBIN, NATURE 219: 902 (1968). (10.1038/219902a0) / NATURE (1968)
POVEY, S, GENETIC STUDIES ON HUMAN LYMPHOBLASTOID LINES - ISOENZYME ANALYSIS ON CELL LINES FROM 41 DIFFERENT INDIVIDUALS AND ON MUTANTS PRODUCED FOLLOWING EXPOSURE TO A CHEMICAL MUTAGEN, ANNALS OF HUMAN GENETICS 36: 247 (1973). (10.1111/j.1469-1809.1973.tb00588.x) / ANNALS OF HUMAN GENETICS (1973)
POVEY, S, CHARACTERIZATION OF HUMAN CELL LINES AND DIFFERENTIATION FROM HELA BY ENZYME TYPING, NATURE 264: 60 (1976). / NATURE (1976)
RAPLEY, S, ANN HUM GENET 31: 237 (1967). / ANN HUM GENET (1967)
RUCKER, N, J NATL CANCER I 54: 157 (1975). (10.1093/jnci/54.1.157) / J NATL CANCER I (1975)
RUDDLE, F.H., STARCH-GEL ELECTROPHORETIC PHENOTYPES OF MOUSE X HUMAN SOMATIC CELL HYBRIDS AND MOUSE ISOENZYME POLYMORPHISMS, IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION 7: 120 (1971). / IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION (1971)
SHAW, C.R., STARCH GEL ELECTROPHORESIS OF ENZYMES - A COMPILATION OF RECIPES, BIOCHEMICAL GENETICS 4: 297 (1970). (10.1007/BF00485780) / BIOCHEMICAL GENETICS (1970)
SPENCER, N, ADENOSINE DEAMINASE POLYMORPHISM IN MAN, ANNALS OF HUMAN GENETICS 32: 9 (1968). (10.1111/j.1469-1809.1968.tb00044.x) / ANNALS OF HUMAN GENETICS (1968)
STEELE, M.W., GLUCOSE 6-PHOSPHATE DEHYDROGENASE IN DROSOPHILA MELANOGASTER - STARCH GEL ELECTROPHORETIC VARIATION DUE TO MOLECULAR INSTABILITY, BIOCHEMICAL GENETICS 2: 159 (1968). (10.1007/BF01458714) / BIOCHEMICAL GENETICS (1968)
TASHIAN, R.E., GENETIC VARIATION AND EVOLUTION OF CARBOXYLIC ESTERASES AND CARBONIC ANHYDRASES OF PRIMATE ERYTHROCYTES, AMERICAN JOURNAL OF HUMAN GENETICS 17: 257 (1965). / AMERICAN JOURNAL OF HUMAN GENETICS (1965)
TASHIAN, R, MULTIPLE FORMS OF ESTERASES FROM HUMAN ERYTHROCYTES, PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 108: 364 (1961). (10.3181/00379727-108-26939) / PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE (1961)
YOSHIDA, A, HUMAN GLUCOSE-6-PHOSPHATE DEHYDROGENASE VARIANTS, BULLETIN OF THE WORLD HEALTH ORGANIZATION 45: 243 (1971). / BULLETIN OF THE WORLD HEALTH ORGANIZATION (1971)

Dates

Type	When
Created	18 years, 11 months ago (Oct. 5, 2006, 12:03 p.m.)
Deposited	1 year, 7 months ago (Jan. 15, 2024, 6:38 a.m.)
Indexed	1 day, 16 hours ago (Sept. 4, 2025, 9:11 a.m.)
Issued	48 years, 5 months ago (March 25, 1977)
Published	48 years, 5 months ago (March 25, 1977)
Published Print	48 years, 5 months ago (March 25, 1977)

Funders 0

None

BibTeX

@article{O_Brien_1977, title={Enzyme Polymorphisms as Genetic Signatures in Human Cell Cultures}, volume={195}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.841332}, DOI={10.1126/science.841332}, number={4284}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={O’Brien, Stephen J. and Kleiner, Gail and Olson, Russell and Shannon, John E.}, year={1977}, month=mar, pages={1345–1348} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        9,
        4
      ]
    ],
    "date-time": "2025-09-04T13:11:31Z",
    "timestamp": 1756991491719
  },
  "reference-count": 45,
  "publisher": "American Association for the Advancement of Science (AAAS)",
  "issue": "4284",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1977,
        3,
        25
      ]
    ]
  },
  "abstract": "<jats:p>The electrophoretic resolution of seven relatively polymorphic human gene-enzyme systems expressed in tissue culture cells can be used as a sensitive genetic monitor for intraspecific cell contamination. An identical genotype at each of the same allozyme loci provides a 95 percent (or greater) confidence estimate of the identity of two cultured lines, on the basis of the allelic frequencies of the seven enzyme loci in natural populations and in populations of independently derived cultured cells. Of 27 commonly used human cell lines examined, only one of 351 pairwise comparisons proved genetically indistinguishable.</jats:p>",
  "DOI": "10.1126/science.841332",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        5
      ]
    ],
    "date-time": "2006-10-05T16:03:07Z",
    "timestamp": 1160064187000
  },
  "page": "1345-1348",
  "source": "Crossref",
  "is-referenced-by-count": 78,
  "title": "Enzyme Polymorphisms as Genetic Signatures in Human Cell Cultures",
  "prefix": "10.1126",
  "volume": "195",
  "author": [
    {
      "given": "Stephen J.",
      "family": "O'Brien",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Laboratory of Viral Carcinogenesis, National Cancer Institute, Bethesda, Maryland 20014"
        }
      ]
    },
    {
      "given": "Gail",
      "family": "Kleiner",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratory of Viral Carcinogenesis, National Cancer Institute, Bethesda, Maryland 20014"
        }
      ]
    },
    {
      "given": "Russell",
      "family": "Olson",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Flow Laboratories, Rockville, Maryland 20852"
        }
      ]
    },
    {
      "given": "John E.",
      "family": "Shannon",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "American Type Culture Collection, Rockville, 20852"
        }
      ]
    }
  ],
  "member": "221",
  "reference": [
    {
      "key": "e_1_2_1_1_1",
      "doi-asserted-by": "crossref",
      "first-page": "465",
      "DOI": "10.1016/0014-4827(70)90474-X",
      "volume": "61",
      "year": "1970",
      "unstructured": "AUERSPERG, N, ISOENZYME STABILITY IN HUMAN HETEROPLOID CELL LINES, EXPERIMENTAL CELL RESEARCH 61: 465 (1970).",
      "journal-title": "EXPERIMENTAL CELL RESEARCH"
    },
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "435",
      "DOI": "10.1002/ijc.2910090223",
      "volume": "9",
      "year": "1972",
      "unstructured": "BENEDICT, W.F., POLYCYCLIC HYDROCARBON-PRODUCED TOXICITY, TRANSFORMATION, AND CHROMOSOMAL-ABERRATIONS AS A FUNCTION OF ARYL HYDROCARBON HYDROXYLASE-ACTIVITY IN CELL-CULTURES, INTERNATIONAL JOURNAL OF CANCER 9: 435 (1972).",
      "journal-title": "INTERNATIONAL JOURNAL OF CANCER"
    },
    {
      "key": "e_1_2_1_3_1",
      "unstructured": "BREWER G.J. INTRO ISOZYME TECHNI (1970)."
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "crossref",
      "first-page": "355",
      "DOI": "10.1111/j.1469-1809.1967.tb00037.x",
      "volume": "30",
      "year": "1967",
      "unstructured": "DAVIDSON, R.G., ELECTROPHORTIC VARIANTS OF HUMAN 6-PHOSPHOGLUCONATE DHYDROGENASE - POPULATION AND FAMILY STUDIES AND DESCRIPTION OF A NEW VARIANT, ANNALS OF HUMAN GENETICS 30: 355 (1967).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "207",
      "DOI": "10.1111/j.1469-1809.1956.tb01393.x",
      "volume": "35",
      "year": "1971",
      "unstructured": "EDWARDS, Y.H., ADENOSINE DEAMINASE ISOZYMES IN HUMAN TISSUES, ANNALS OF HUMAN GENETICS 35: 207 (1971).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "261",
      "DOI": "10.1038/209261a0",
      "volume": "209",
      "year": "1966",
      "unstructured": "FILDES, R.A., GENETICALLY DETERMINED VARIATION OF ADENYLATE KINASE IN MAN, NATURE 209: 261 (1966).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_7_1",
      "first-page": "167",
      "volume": "26",
      "year": "1967",
      "unstructured": "GARTLER, S.M., NATIONAL CANCER INSTITUTE MONOGRAPHS 26: 167 (1967).",
      "journal-title": "NATIONAL CANCER INSTITUTE MONOGRAPHS"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "750",
      "DOI": "10.1038/217750a0",
      "volume": "217",
      "year": "1968",
      "unstructured": "GARTLER, S.M., APPARENT HELA CELL CONTAMINATION OF HUMAN HETEROPLOID CELL LINES, NATURE 217: 750 (1968).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "crossref",
      "first-page": "1417",
      "DOI": "10.1093/jnci/51.5.1417",
      "volume": "51",
      "year": "1973",
      "unstructured": "GIARD, D.J., IN-VITRO CULTIVATION OF HUMAN TUMORS - ESTABLISHMENT OF CELL LINES DERIVED FROM A SERIES OF SOLID TUMORS, JOURNAL OF THE NATIONAL CANCER INSTITUTE 51: 1417 (1973).",
      "journal-title": "JOURNAL OF THE NATIONAL CANCER INSTITUTE"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "9",
      "DOI": "10.1111/j.1469-1809.1972.tb00578.x",
      "volume": "36",
      "year": "1972",
      "unstructured": "HARRIS, H, AVERAGE HETEROZYGOSITY PER LOCUS IN MAN - AN ESTIMATE BASED ON INCIDENCE OF ENZYME POLYMORPHISMS, ANNALS OF HUMAN GENETICS 36: 9 (1972).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_11_1",
      "unstructured": "HARRIS H HDB ENZYME ELECTROPH (1976)."
    },
    {
      "key": "e_1_2_1_12_1",
      "first-page": "131",
      "volume": "4",
      "year": "1975",
      "unstructured": "HARRIS, H, ISOZYMES 4: 131 (1975).",
      "journal-title": "ISOZYMES"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "661",
      "DOI": "10.1172/JCI107974",
      "volume": "55",
      "year": "1975",
      "unstructured": "HIRSCHHORN, R, CONVERSION OF HUMAN ERYTHROCYTE-ADENOSINE DEAMINASE ACTIVITY TO DIFFERENT TISSUE-SPECIFIC ISOENZYMES - EVIDENCE FOR A COMMON CATALYTIC UNIT, JOURNAL OF CLINICAL INVESTIGATION 55: 661 (1975).",
      "journal-title": "JOURNAL OF CLINICAL INVESTIGATION"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "167",
      "DOI": "10.1111/j.1469-1809.1966.tb00016.x",
      "volume": "30",
      "year": "1966",
      "unstructured": "HOPKINSON, D.A., RARE PHOSPHOGLUCOMUTASE PHENOTYPES, ANNALS OF HUMAN GENETICS 30: 167 (1966).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1111/j.1469-1809.1968.tb00567.x",
      "volume": "31",
      "year": "1968",
      "unstructured": "HOPKINSON, D.A., A THIRD PHOSPHOGLUCOMUTASE LOCUS IN MAN, ANNALS OF HUMAN GENETICS 31: 359 (1968).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "crossref",
      "first-page": "119",
      "DOI": "10.1111/j.1469-1809.1973.tb01820.x",
      "volume": "37",
      "year": "1973",
      "unstructured": "HOPKINSON, D.A., ESTERASE-D - NEW HUMAN POLYMORPHISM, ANNALS OF HUMAN GENETICS 37: 119 (1973).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1246620"
    },
    {
      "key": "e_1_2_1_18_1",
      "unstructured": "HSU T.C. ATLAS MAMMALIAN CHRO (1967)."
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "453",
      "DOI": "10.3181/00379727-143-37341",
      "volume": "143",
      "year": "1973",
      "unstructured": "KERSEY, J.H., HL-A ANTIGENS OF HUMAN TUMOR-DERIVED CELL LINES AND VIRAL TRANSFORMED FIBROBLASTS IN CULTURE, PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 143: 453 (1973).",
      "journal-title": "PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE"
    },
    {
      "key": "e_1_2_1_20_1",
      "first-page": "1",
      "volume": "2",
      "year": "1971",
      "unstructured": "KIRKMAN, H.N., ADV HUM GENET 2: 1 (1971).",
      "journal-title": "ADV HUM GENET"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/259211a0"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "317",
      "DOI": "10.1111/j.1469-1809.1969.tb00081.x",
      "volume": "32",
      "year": "1969",
      "unstructured": "LEWIS, WHP, PEPTIDASE D (PROLIDASE) VARIANTS IN MAN, ANNALS OF HUMAN GENETICS 32: 317 (1969).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_23_1",
      "first-page": "111",
      "year": "1971",
      "unstructured": "LEWIS, WHP, EXCERPTA MED INT 233: 111 (1971).",
      "journal-title": "EXCERPTA MED INT 233"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1146/annurev.ge.07.120173.000245",
      "volume": "7",
      "year": "1973",
      "unstructured": "LEWONTIN, R.C., POPULATION GENETICS, ANNUAL REVIEW OF GENETICS 7: 1 (1973).",
      "journal-title": "ANNUAL REVIEW OF GENETICS"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "462",
      "DOI": "10.3181/00379727-132-34238",
      "volume": "132",
      "year": "1969",
      "unstructured": "MONTESDEOCA, F, PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 132: 462 (1969).",
      "journal-title": "PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1086/282771",
      "volume": "106",
      "year": "1972",
      "unstructured": "NEI, M, GENETIC DISTANCE BETWEEN POPULATIONS, AMERICAN NATURALIST 106: 283 (1972).",
      "journal-title": "AMERICAN NATURALIST"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.1246601"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.557237"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.184.4141.1093"
    },
    {
      "key": "e_1_2_1_30_1",
      "unstructured": "OBRIEN S.J. GENETICS BIOLOGY DRO 2:."
    },
    {
      "key": "e_1_2_1_31_1",
      "unstructured": "O'Brien S. J. Genetics and Biology of Drosophila 2 (1978)."
    },
    {
      "key": "e_1_2_1_32_1",
      "first-page": "20",
      "volume": "9",
      "year": "1976",
      "unstructured": "OBRIEN, S.J., ISOZYME BULLETIN 9: 20 (1976).",
      "journal-title": "ISOZYME BULLETIN"
    },
    {
      "key": "e_1_2_1_33_1",
      "first-page": "47",
      "volume": "9",
      "year": "1976",
      "unstructured": "OBRIEN, S.J., ISOZYME BULLETIN 9: 47 (1976).",
      "journal-title": "ISOZYME BULLETIN"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "902",
      "DOI": "10.1038/219902a0",
      "volume": "219",
      "year": "1968",
      "unstructured": "PERUTZ, M.F., MOLECULAR PATHOLOGY OF HUMAN HAEMOGLOBIN, NATURE 219: 902 (1968).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "247",
      "DOI": "10.1111/j.1469-1809.1973.tb00588.x",
      "volume": "36",
      "year": "1973",
      "unstructured": "POVEY, S, GENETIC STUDIES ON HUMAN LYMPHOBLASTOID LINES - ISOENZYME ANALYSIS ON CELL LINES FROM 41 DIFFERENT INDIVIDUALS AND ON MUTANTS PRODUCED FOLLOWING EXPOSURE TO A CHEMICAL MUTAGEN, ANNALS OF HUMAN GENETICS 36: 247 (1973).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_36_1",
      "first-page": "60",
      "volume": "264",
      "year": "1976",
      "unstructured": "POVEY, S, CHARACTERIZATION OF HUMAN CELL LINES AND DIFFERENTIATION FROM HELA BY ENZYME TYPING, NATURE 264: 60 (1976).",
      "journal-title": "NATURE"
    },
    {
      "key": "e_1_2_1_37_1",
      "first-page": "237",
      "volume": "31",
      "year": "1967",
      "unstructured": "RAPLEY, S, ANN HUM GENET 31: 237 (1967).",
      "journal-title": "ANN HUM GENET"
    },
    {
      "key": "e_1_2_1_38_1",
      "doi-asserted-by": "crossref",
      "first-page": "157",
      "DOI": "10.1093/jnci/54.1.157",
      "volume": "54",
      "year": "1975",
      "unstructured": "RUCKER, N, J NATL CANCER I 54: 157 (1975).",
      "journal-title": "J NATL CANCER I"
    },
    {
      "key": "e_1_2_1_39_1",
      "first-page": "120",
      "volume": "7",
      "year": "1971",
      "unstructured": "RUDDLE, F.H., STARCH-GEL ELECTROPHORETIC PHENOTYPES OF MOUSE X HUMAN SOMATIC CELL HYBRIDS AND MOUSE ISOENZYME POLYMORPHISMS, IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION 7: 120 (1971).",
      "journal-title": "IN VITRO-JOURNAL OF THE TISSUE CULTURE ASSOCIATION"
    },
    {
      "key": "e_1_2_1_40_1",
      "doi-asserted-by": "crossref",
      "first-page": "297",
      "DOI": "10.1007/BF00485780",
      "volume": "4",
      "year": "1970",
      "unstructured": "SHAW, C.R., STARCH GEL ELECTROPHORESIS OF ENZYMES - A COMPILATION OF RECIPES, BIOCHEMICAL GENETICS 4: 297 (1970).",
      "journal-title": "BIOCHEMICAL GENETICS"
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "crossref",
      "first-page": "9",
      "DOI": "10.1111/j.1469-1809.1968.tb00044.x",
      "volume": "32",
      "year": "1968",
      "unstructured": "SPENCER, N, ADENOSINE DEAMINASE POLYMORPHISM IN MAN, ANNALS OF HUMAN GENETICS 32: 9 (1968).",
      "journal-title": "ANNALS OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_42_1",
      "doi-asserted-by": "crossref",
      "first-page": "159",
      "DOI": "10.1007/BF01458714",
      "volume": "2",
      "year": "1968",
      "unstructured": "STEELE, M.W., GLUCOSE 6-PHOSPHATE DEHYDROGENASE IN DROSOPHILA MELANOGASTER - STARCH GEL ELECTROPHORETIC VARIATION DUE TO MOLECULAR INSTABILITY, BIOCHEMICAL GENETICS 2: 159 (1968).",
      "journal-title": "BIOCHEMICAL GENETICS"
    },
    {
      "key": "e_1_2_1_43_1",
      "first-page": "257",
      "volume": "17",
      "year": "1965",
      "unstructured": "TASHIAN, R.E., GENETIC VARIATION AND EVOLUTION OF CARBOXYLIC ESTERASES AND CARBONIC ANHYDRASES OF PRIMATE ERYTHROCYTES, AMERICAN JOURNAL OF HUMAN GENETICS 17: 257 (1965).",
      "journal-title": "AMERICAN JOURNAL OF HUMAN GENETICS"
    },
    {
      "key": "e_1_2_1_44_1",
      "doi-asserted-by": "crossref",
      "first-page": "364",
      "DOI": "10.3181/00379727-108-26939",
      "volume": "108",
      "year": "1961",
      "unstructured": "TASHIAN, R, MULTIPLE FORMS OF ESTERASES FROM HUMAN ERYTHROCYTES, PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE 108: 364 (1961).",
      "journal-title": "PROCEEDINGS OF THE SOCIETY FOR EXPERIMENTAL BIOLOGY AND MEDICINE"
    },
    {
      "key": "e_1_2_1_45_1",
      "first-page": "243",
      "volume": "45",
      "year": "1971",
      "unstructured": "YOSHIDA, A, HUMAN GLUCOSE-6-PHOSPHATE DEHYDROGENASE VARIANTS, BULLETIN OF THE WORLD HEALTH ORGANIZATION 45: 243 (1971).",
      "journal-title": "BULLETIN OF THE WORLD HEALTH ORGANIZATION"
    }
  ],
  "container-title": "Science",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.science.org/doi/pdf/10.1126/science.841332",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2024,
        1,
        15
      ]
    ],
    "date-time": "2024-01-15T11:38:17Z",
    "timestamp": 1705318697000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.science.org/doi/10.1126/science.841332"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1977,
        3,
        25
      ]
    ]
  },
  "references-count": 45,
  "journal-issue": {
    "issue": "4284",
    "published-print": {
      "date-parts": [
        [
          1977,
          3,
          25
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1126/science.841332"
  ],
  "URL": "http://dx.doi.org/10.1126/science.841332",
  "relation": {},
  "ISSN": [
    "0036-8075",
    "1095-9203"
  ],
  "subject": [],
  "container-title-short": "Science",
  "published": {
    "date-parts": [
      [
        1977,
        3,
        25
      ]
    ]
  }
}