DOI: 10.1002/jez.1401770202. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes

Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes

10.1002/jez.1401770202

Crossref journal-article

Wiley

Journal of Experimental Zoology (311)

Abstract

AbstractFully grown oocytes of the frog (Rana pipiens) undergo cytoplasmic and nuclear maturation when treated with progesterone after the follicular envelopes have been removed. The mechanism of this maturation was investigated by injection of cytoplasm from progesterone‐treated oocytes at various stages of maturation into fully grown but immature oocytes. The injected cytoplasm becomes effective in inducing maturation by 12 hours after progesterone administration, reaches a maximum effectiveness around 20 hours, and then declines after the donor oocytes complete maturation. However, even cytoplasm from early embryos retains some capacity to induce oocyte maturation. The frequency with which maturation is induced is proportional to the volume of the injected cytoplasm. Progesterone itself is not directly responsible for the maturation‐producing effect of injected cytoplasm since injected progesterone does not promote maturation. However, externally applied progesterone does induce the completion of the first meiotic division, presumably by releasing a cytoplasmic “maturation promoting factor.” The production of this cytoplasmic factor was not affected by removal of the nucleus.After completion of the first meiotic division, oocytes cease further development at the metaphase of the second meiotic division, where they remain until fertilized or activated to develop. Cytoplasm from such secondary oocytes when injected into one of the blastomeres at the two‐cell stage of development suppresses mitosis as well as cleavage. Mitosis is usually arrested at metaphase. No such inhibition was brought about by injection of cytoplasm from cleaving blastomeres. Thus, the arrest of mitosis and cleavage can be attributed to a specific “cytostatic factor” in the cytoplasm of the secondary oocyte. Activation of donor secondary oocytes by insemination or pricking with a glass needle soon destroys the cytostatic factor. Likewise, addition of cortical cytoplasm to endoplasm from the secondary oocyte rapidly destroys the cytostatic capacity. This result implies that cortical material is involved in the process of removing the cytostatic factor at the time of normal activation or fertilization. Enucleation of oocytes demonstrated that production and removal of the cytostatic factor is independent of the nucleus.

Bibliography

Masui, Y., & Markert, C. L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. Journal of Experimental Zoology, 177(2), 129â145. Portico.

Authors 2

Yoshio Masui (first)
Clement L. Markert (additional)

References 48 Referenced 1,145

{'key': 'e_1_2_1_2_1', 'first-page': '132', 'article-title': 'Changes in the ultrastructure of amphibian eggs following fertilization', 'volume': '9', 'author': 'Balinsky B. I.', 'year': '1966', 'journal-title': 'Acta Embryol. Morph. Exptl.'} / Acta Embryol. Morph. Exptl. / Changes in the ultrastructure of amphibian eggs following fertilization by Balinsky B. I. (1966)
10.1007/BF02272327
{'key': 'e_1_2_1_4_1', 'first-page': '439', 'article-title': "Etudes analytiques et experimentales sur les rythmes cinétique dans l'oeuf (Hyla arborea, Paracentrotus lividus, Bombyx mori)", 'volume': '40', 'author': 'Bataillon E.', 'year': '1930', 'journal-title': 'Archs. Biol.'} / Archs. Biol. / Etudes analytiques et experimentales sur les rythmes cinétique dans l'oeuf (Hyla arborea, Paracentrotus lividus, Bombyx mori) by Bataillon E. (1930)
{'key': 'e_1_2_1_5_1', 'first-page': '205', 'article-title': "Recherches sur la fécondation prématuréee de l'oeuf d'oursin (Paracentrotus lividus)", 'volume': '32', 'author': 'Brachet A.', 'year': '1922', 'journal-title': 'Arch. Biol.'} / Arch. Biol. / Recherches sur la fécondation prématuréee de l'oeuf d'oursin (Paracentrotus lividus) by Brachet A. (1922)
10.1016/0014-4827(67)90312-6
10.1073/pnas.55.5.1103
{'key': 'e_1_2_1_8_1', 'first-page': '284', 'article-title': 'Etude expérimentales sur la maturation cytoplasmique et sur la parthenogénèse artificielle chez les Echinodermes', 'volume': '9', 'author': 'Delage Y.', 'year': '1901', 'journal-title': 'Arch. Zool. exp. gén. (Ser 3)'} / Arch. Zool. exp. gén. (Ser 3) / Etude expérimentales sur la maturation cytoplasmique et sur la parthenogénèse artificielle chez les Echinodermes by Delage Y. (1901)
10.1016/0014-4827(60)90345-1
10.1073/pnas.57.3.607
{'key': 'e_1_2_1_11_1', 'first-page': '183', 'article-title': 'Action of actinomycin and puromycin upon frog oöcyte maturation', 'volume': '16', 'author': 'Detlaff T. A.', 'year': '1966', 'journal-title': 'J. Embryol. exp. Morphol.'} / J. Embryol. exp. Morphol. / Action of actinomycin and puromycin upon frog oöcyte maturation by Detlaff T. A. (1966)
{'key': 'e_1_2_1_12_1', 'first-page': '851', 'article-title': 'The role of the germinal vesicle in oöcyte Saturation in anurans as revealed by the removal and transplantation of nuclei', 'volume': '12', 'author': 'Detlaff T. A.', 'year': '1964', 'journal-title': 'J. Embryol. exp. Morph.'} / J. Embryol. exp. Morph. / The role of the germinal vesicle in oöcyte Saturation in anurans as revealed by the removal and transplantation of nuclei by Detlaff T. A. (1964)
10.3109/10520294109106190 / Stain Tech. / Amylacetate as a clearing agent for embryonic material by Drury H. F. (1941)
10.1016/0014-4827(61)90347-0
{'key': 'e_1_2_1_15_1', 'first-page': '3', 'volume-title': 'The Control of Nuclear Activity', 'author': 'Goldstein L.', 'year': '1967'} / The Control of Nuclear Activity by Goldstein L. (1967)
10.1242/jcs.1.3.363 / J. Cell. Sci. / The regulation of DNA synthesis and mitosis in multinucleate frog eggs by Graham C. F. (1966)
10.1016/0012-1606(66)90020-0
10.1073/pnas.58.2.545
{'key': 'e_1_2_1_19_1', 'first-page': '401', 'article-title': 'Changes in somatic cell nuclei inserted into growing and maturing amphibian oöcytes', 'volume': '20', 'author': 'Gurdon J. B.', 'year': '1968', 'journal-title': 'J. Embryol. exp. Morphol.'} / J. Embryol. exp. Morphol. / Changes in somatic cell nuclei inserted into growing and maturing amphibian oöcytes by Gurdon J. B. (1968)
10.1111/j.1469-185X.1968.tb00960.x
10.1242/jcs.2.1.23 / J. Cell Sci. / The reactivation of the red cell nucleus by Harris H. (1967)
10.2307/1538709
10.1086/physzool.12.2.30151487
{'key': 'e_1_2_1_24_1', 'first-page': '505', 'article-title': 'Etude sur les bases cytologiques du mécanisme de la parthenogénèse expérimentale chez les Amphibiens', 'volume': '28', 'author': 'Herlant M.', 'year': '1913', 'journal-title': 'Arch. Biol.'} / Arch. Biol. / Etude sur les bases cytologiques du mécanisme de la parthenogénèse expérimentale chez les Amphibiens by Herlant M. (1913)
10.1002/jez.1400930205
{'key': 'e_1_2_1_26_1', 'first-page': '166', 'article-title': 'Cortical change at fertilization in the egg of the grass frog, Rana temporaria', 'volume': '14', 'author': 'Katagiri C.', 'year': '1959', 'journal-title': 'J. Fac. Sci. Hokkaido Univ.'} / J. Fac. Sci. Hokkaido Univ. / Cortical change at fertilization in the egg of the grass frog, Rana temporaria by Katagiri C. (1959)
10.1083/jcb.34.1.111
10.1002/jez.1401570308
10.1016/0022-2836(69)90282-4
10.1002/jez.1401660309
10.1016/0012-1606(65)90032-1
10.1002/jez.1401640304
10.1242/jcs.5.2.333 / J. Cell Sci. / Movement of cytoplasmic proteins into nuclei induced to enlarge and initiate DNA or RNA synthesis by Merriam R. W. (1969)
{'key': 'e_1_2_1_34_1', 'first-page': '73', 'volume-title': 'The Biochemistry of Animal Development 1', 'author': 'Monroy A.', 'year': '1965'} / The Biochemistry of Animal Development 1 by Monroy A. (1965)
10.1073/pnas.54.1.107
{'issue': '122', 'key': 'e_1_2_1_36_1', 'article-title': 'Chromosomes of frog eggs and embryos stained by Feulgen method to avoid excessive staining of yolk granules', 'volume': '78', 'author': 'Moore B.', 'year': '1940', 'journal-title': 'Anat. Rec.'} / Anat. Rec. / Chromosomes of frog eggs and embryos stained by Feulgen method to avoid excessive staining of yolk granules by Moore B. (1940)
{'key': 'e_1_2_1_37_1', 'first-page': '129', 'article-title': 'Inhibition of development with the extract from the unfertilized eggs of the Japanese Palolo', 'volume': '33', 'author': 'Osanai K.', 'year': '1967', 'journal-title': 'Sci. Rep. Tohoku Unic. Ser. IV (Biol.)'} / Sci. Rep. Tohoku Unic. Ser. IV (Biol.) / Inhibition of development with the extract from the unfertilized eggs of the Japanese Palolo by Osanai K. (1967)
10.3181/00379727-124-31993
10.1002/jez.1401660307
10.1002/jmor.1050230106
10.1016/0012-1606(66)90019-4
10.1016/0012-1606(69)90065-7
10.1016/0012-1606(70)90172-7
10.1016/0012-1606(68)90010-9
10.1016/0014-4827(69)90472-8
{'key': 'e_1_2_1_46_1', 'first-page': '203', 'article-title': 'Fertílízation of artificially ovulated premature eggs of Bufo', 'volume': '1', 'author': 'Tchou‐Su', 'year': '1942', 'journal-title': 'Sci. Rec.'} / Sci. Rec. / Fertílízation of artificially ovulated premature eggs of Bufo by Tchou‐Su (1942)
{'key': 'e_1_2_1_47_1', 'first-page': '129', 'article-title': "Etude comparative sur l'ovulation et la maturation in vivo et in vitro chez le Crapaud asiatique (Bufo bufo asiaticus)", 'volume': '6', 'author': 'Tchou‐Su', 'year': '1958', 'journal-title': 'Acta exp. Biol. Sin.'} / Acta exp. Biol. Sin. / Etude comparative sur l'ovulation et la maturation in vivo et in vitro chez le Crapaud asiatique (Bufo bufo asiaticus) by Tchou‐Su (1958)
10.3181/00379727-106-26333
10.1002/jez.1400020206

Dates

Type	When
Created	20 years, 2 months ago (June 11, 2005, 7:23 a.m.)
Deposited	1 year, 9 months ago (Nov. 12, 2023, 10:42 a.m.)
Indexed	1 hour, 5 minutes ago (Sept. 2, 2025, 10:32 p.m.)
Issued	54 years, 3 months ago (June 1, 1971)
Published	54 years, 3 months ago (June 1, 1971)
Published Online	20 years, 3 months ago (May 9, 2005)
Published Print	54 years, 3 months ago (June 1, 1971)

Funders 0

None

BibTeX

@article{Masui_1971, title={Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes}, volume={177}, ISSN={1097-010X}, url={http://dx.doi.org/10.1002/jez.1401770202}, DOI={10.1002/jez.1401770202}, number={2}, journal={Journal of Experimental Zoology}, publisher={Wiley}, author={Masui, Yoshio and Markert, Clement L.}, year={1971}, month=jun, pages={129–145} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        9,
        3
      ]
    ],
    "date-time": "2025-09-03T02:32:37Z",
    "timestamp": 1756866757867
  },
  "reference-count": 48,
  "publisher": "Wiley",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2005,
            5,
            9
          ]
        ],
        "date-time": "2005-05-09T00:00:00Z",
        "timestamp": 1115596800000
      },
      "content-version": "vor",
      "delay-in-days": 12396,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1971,
        6
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>Fully grown oocytes of the frog (<jats:italic>Rana pipiens</jats:italic>) undergo cytoplasmic and nuclear maturation when treated with progesterone after the follicular envelopes have been removed. The mechanism of this maturation was investigated by injection of cytoplasm from progesterone\u2010treated oocytes at various stages of maturation into fully grown but immature oocytes. The injected cytoplasm becomes effective in inducing maturation by 12 hours after progesterone administration, reaches a maximum effectiveness around 20 hours, and then declines after the donor oocytes complete maturation. However, even cytoplasm from early embryos retains some capacity to induce oocyte maturation. The frequency with which maturation is induced is proportional to the volume of the injected cytoplasm. Progesterone itself is not directly responsible for the maturation\u2010producing effect of injected cytoplasm since injected progesterone does not promote maturation. However, externally applied progesterone does induce the completion of the first meiotic division, presumably by releasing a cytoplasmic \u201cmaturation promoting factor.\u201d The production of this cytoplasmic factor was not affected by removal of the nucleus.</jats:p><jats:p>After completion of the first meiotic division, oocytes cease further development at the metaphase of the second meiotic division, where they remain until fertilized or activated to develop. Cytoplasm from such secondary oocytes when injected into one of the blastomeres at the two\u2010cell stage of development suppresses mitosis as well as cleavage. Mitosis is usually arrested at metaphase. No such inhibition was brought about by injection of cytoplasm from cleaving blastomeres. Thus, the arrest of mitosis and cleavage can be attributed to a specific \u201ccytostatic factor\u201d in the cytoplasm of the secondary oocyte. Activation of donor secondary oocytes by insemination or pricking with a glass needle soon destroys the cytostatic factor. Likewise, addition of cortical cytoplasm to endoplasm from the secondary oocyte rapidly destroys the cytostatic capacity. This result implies that cortical material is involved in the process of removing the cytostatic factor at the time of normal activation or fertilization. Enucleation of oocytes demonstrated that production and removal of the cytostatic factor is independent of the nucleus.</jats:p>",
  "DOI": "10.1002/jez.1401770202",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2005,
        6,
        11
      ]
    ],
    "date-time": "2005-06-11T11:23:28Z",
    "timestamp": 1118489008000
  },
  "page": "129-145",
  "source": "Crossref",
  "is-referenced-by-count": 1145,
  "title": "Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes",
  "prefix": "10.1002",
  "volume": "177",
  "author": [
    {
      "given": "Yoshio",
      "family": "Masui",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Clement L.",
      "family": "Markert",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2005,
        5,
        9
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_1",
      "first-page": "132",
      "article-title": "Changes in the ultrastructure of amphibian eggs following fertilization",
      "volume": "9",
      "author": "Balinsky B. I.",
      "year": "1966",
      "journal-title": "Acta Embryol. Morph. Exptl."
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF02272327"
    },
    {
      "key": "e_1_2_1_4_1",
      "first-page": "439",
      "article-title": "Etudes analytiques et experimentales sur les rythmes cin\u00e9tique dans l'oeuf (Hyla arborea, Paracentrotus lividus, Bombyx mori)",
      "volume": "40",
      "author": "Bataillon E.",
      "year": "1930",
      "journal-title": "Archs. Biol."
    },
    {
      "key": "e_1_2_1_5_1",
      "first-page": "205",
      "article-title": "Recherches sur la f\u00e9condation pr\u00e9matur\u00e9ee de l'oeuf d'oursin (Paracentrotus lividus)",
      "volume": "32",
      "author": "Brachet A.",
      "year": "1922",
      "journal-title": "Arch. Biol."
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-4827(67)90312-6"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.55.5.1103"
    },
    {
      "key": "e_1_2_1_8_1",
      "first-page": "284",
      "article-title": "Etude exp\u00e9rimentales sur la maturation cytoplasmique et sur la parthenog\u00e9n\u00e8se artificielle chez les Echinodermes",
      "volume": "9",
      "author": "Delage Y.",
      "year": "1901",
      "journal-title": "Arch. Zool. exp. g\u00e9n. (Ser 3)"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-4827(60)90345-1"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.57.3.607"
    },
    {
      "key": "e_1_2_1_11_1",
      "first-page": "183",
      "article-title": "Action of actinomycin and puromycin upon frog o\u00f6cyte maturation",
      "volume": "16",
      "author": "Detlaff T. A.",
      "year": "1966",
      "journal-title": "J. Embryol. exp. Morphol."
    },
    {
      "key": "e_1_2_1_12_1",
      "first-page": "851",
      "article-title": "The role of the germinal vesicle in o\u00f6cyte Saturation in anurans as revealed by the removal and transplantation of nuclei",
      "volume": "12",
      "author": "Detlaff T. A.",
      "year": "1964",
      "journal-title": "J. Embryol. exp. Morph."
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "crossref",
      "first-page": "21",
      "DOI": "10.3109/10520294109106190",
      "article-title": "Amylacetate as a clearing agent for embryonic material",
      "volume": "6",
      "author": "Drury H. F.",
      "year": "1941",
      "journal-title": "Stain Tech."
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-4827(61)90347-0"
    },
    {
      "key": "e_1_2_1_15_1",
      "first-page": "3",
      "volume-title": "The Control of Nuclear Activity",
      "author": "Goldstein L.",
      "year": "1967"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "crossref",
      "first-page": "363",
      "DOI": "10.1242/jcs.1.3.363",
      "article-title": "The regulation of DNA synthesis and mitosis in multinucleate frog eggs",
      "volume": "1",
      "author": "Graham C. F.",
      "year": "1966",
      "journal-title": "J. Cell. Sci."
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(66)90020-0"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.58.2.545"
    },
    {
      "key": "e_1_2_1_19_1",
      "first-page": "401",
      "article-title": "Changes in somatic cell nuclei inserted into growing and maturing amphibian o\u00f6cytes",
      "volume": "20",
      "author": "Gurdon J. B.",
      "year": "1968",
      "journal-title": "J. Embryol. exp. Morphol."
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1469-185X.1968.tb00960.x"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1242/jcs.2.1.23",
      "article-title": "The reactivation of the red cell nucleus",
      "volume": "2",
      "author": "Harris H.",
      "year": "1967",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.2307/1538709"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/physzool.12.2.30151487"
    },
    {
      "key": "e_1_2_1_24_1",
      "first-page": "505",
      "article-title": "Etude sur les bases cytologiques du m\u00e9canisme de la parthenog\u00e9n\u00e8se exp\u00e9rimentale chez les Amphibiens",
      "volume": "28",
      "author": "Herlant M.",
      "year": "1913",
      "journal-title": "Arch. Biol."
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1400930205"
    },
    {
      "key": "e_1_2_1_26_1",
      "first-page": "166",
      "article-title": "Cortical change at fertilization in the egg of the grass frog, Rana temporaria",
      "volume": "14",
      "author": "Katagiri C.",
      "year": "1959",
      "journal-title": "J. Fac. Sci. Hokkaido Univ."
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.34.1.111"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1401570308"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(69)90282-4"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1401660309"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(65)90032-1"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1401640304"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "crossref",
      "first-page": "333",
      "DOI": "10.1242/jcs.5.2.333",
      "article-title": "Movement of cytoplasmic proteins into nuclei induced to enlarge and initiate DNA or RNA synthesis",
      "volume": "5",
      "author": "Merriam R. W.",
      "year": "1969",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "e_1_2_1_34_1",
      "first-page": "73",
      "volume-title": "The Biochemistry of Animal Development 1",
      "author": "Monroy A.",
      "year": "1965"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.54.1.107"
    },
    {
      "issue": "122",
      "key": "e_1_2_1_36_1",
      "article-title": "Chromosomes of frog eggs and embryos stained by Feulgen method to avoid excessive staining of yolk granules",
      "volume": "78",
      "author": "Moore B.",
      "year": "1940",
      "journal-title": "Anat. Rec."
    },
    {
      "key": "e_1_2_1_37_1",
      "first-page": "129",
      "article-title": "Inhibition of development with the extract from the unfertilized eggs of the Japanese Palolo",
      "volume": "33",
      "author": "Osanai K.",
      "year": "1967",
      "journal-title": "Sci. Rep. Tohoku Unic. Ser. IV (Biol.)"
    },
    {
      "key": "e_1_2_1_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3181/00379727-124-31993"
    },
    {
      "key": "e_1_2_1_39_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1401660307"
    },
    {
      "key": "e_1_2_1_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jmor.1050230106"
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(66)90019-4"
    },
    {
      "key": "e_1_2_1_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(69)90065-7"
    },
    {
      "key": "e_1_2_1_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(70)90172-7"
    },
    {
      "key": "e_1_2_1_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0012-1606(68)90010-9"
    },
    {
      "key": "e_1_2_1_45_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-4827(69)90472-8"
    },
    {
      "key": "e_1_2_1_46_1",
      "first-page": "203",
      "article-title": "Fert\u00edl\u00edzation of artificially ovulated premature eggs of Bufo",
      "volume": "1",
      "author": "Tchou\u2010Su",
      "year": "1942",
      "journal-title": "Sci. Rec."
    },
    {
      "key": "e_1_2_1_47_1",
      "first-page": "129",
      "article-title": "Etude comparative sur l'ovulation et la maturation in vivo et in vitro chez le Crapaud asiatique (Bufo bufo asiaticus)",
      "volume": "6",
      "author": "Tchou\u2010Su",
      "year": "1958",
      "journal-title": "Acta exp. Biol. Sin."
    },
    {
      "key": "e_1_2_1_48_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.3181/00379727-106-26333"
    },
    {
      "key": "e_1_2_1_49_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jez.1400020206"
    }
  ],
  "container-title": "Journal of Experimental Zoology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1002%2Fjez.1401770202",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1002/jez.1401770202",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        11,
        12
      ]
    ],
    "date-time": "2023-11-12T15:42:49Z",
    "timestamp": 1699803769000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1002/jez.1401770202"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1971,
        6
      ]
    ]
  },
  "references-count": 48,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          1971,
          6
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1002/jez.1401770202"
  ],
  "URL": "http://dx.doi.org/10.1002/jez.1401770202",
  "relation": {},
  "ISSN": [
    "0022-104X",
    "1097-010X"
  ],
  "subject": [],
  "container-title-short": "J. Exp. Zool.",
  "published": {
    "date-parts": [
      [
        1971,
        6
      ]
    ]
  }
}