DOI: 10.1242/dev.110.4.1295. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs

A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs

10.1242/dev.110.4.1295

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

Abstract Microinjection of cytosolic sperm extracts into unfertilized golden hamster eggs caused a series of increases in cytoplasmic free calcium, Ca2+i, and membrane hyperpolarizing responses, HRs. These HRs and Ca2+i, transients are similar to those seen during in vitro fertilization of hamster eggs. The sperm factor that is responsible for causing these effects appears to be of high molecular weight and protein based. Injection of sperm factor activated eggs and mimicked fertilization in causing repetitive HRs in the presence of phorbol esters and in sensitizing the egg to calcium-induced calcium release. Since these effects cannot be mimicked by injecting G-protein agonists or calcium-containing solutions, it seems unlikely that a receptor-G-protein signalling system is involved at fertilization. These data instead suggest a novel signal transduction system operates during mammalian fertilization in which a protein factor is transferred from the sperm into the egg cytoplasm after gamete membrane fusion.

Bibliography

Swann, K. (1990). A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development, 110(4), 1295â1302.

Authors 1

Karl Swann (first)

References 40 Referenced 328

10.1002/mrd.1120230202 / Gamete Res. / A consistently successful procedure for in vitro fertilization of golden hamster eggs by Bavister (1989)
10.1096/fasebj.2.15.2847949 / FASEB J. / Cytosolic calcium oscillators by Berridge (1988)
10.1038/316541a0 / Nature / Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell Ca2+ by Cuthbertson (1985)
10.1016/0014-4827(88)90038-9 / Expl Cell Res. / Primary and secondary messengers in the activation of ascidian eggs by Dale (1988)
10.1007/BF01952148 / Experimentia / Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction by Dale (1985)
10.1038/228034a0 / Nature / Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres by Endo (1970)
10.1016/0012-1606(83)90176-8 / Devi Biol. / An electrophysiological study of parthenogenetic activation in mammalian eggs by Eusebi (1983)
10.1038/273149a0 / Nature / Activation of mammalian eggs by intracellular injection of calcium by Fulton (1978)
10.1126/science.3823908 / Science / Electrical responses of eggs to acrosomal protein similar to those induced by sperm by Gould (1987)
10.1016/S0021-9258(19)83641-4 / J. biol. Chem. / A new generation of calcium indicators with greatly improved fluorescent properties by Grykiewicz (1985)
10.1146/annurev.bb.08.060179.002125 / A. Rev. Biophys. Bioeng. / Electrical properties of egg cell membranes by Hagiwara (1979)
10.1093/biolreprod/6.2.300 / Biol. Reprod. / Penetration of zona free eggs by spermatozoa of different species by Hanada (1972)
10.1113/jphysiol.1983.sp014783 / J. Physiol. / Effects of altered extracelluar and intracellular calcium concentration on hyperpolarizing responses of hamster egg by Igusa (1983)
10.1113/jphysiol.1986.sp016181 / J. Physiol. / Period increase of cytoplasmic free calcium in fertilized hamster eggs measured with calciumsensitive electrodes by Igusa (1986)
10.1113/jphysiol.1983.sp014784 / J. Physiol. / Periodic hyperpolarizing responses in hamster and mouse eggs fertilized with mouse sperm by Igusa (1983)
10.1016/0922-3371(88)90094-9 / Cell. Differ. Dev. / G-proteins and egg activation by Jaffe (1988)
10.1016/0012-1606(83)90276-2 / Devi Biol. / Sources of calcium in egg activation; a review and hypothesis by Jaffe (1983)
10.1113/jphysiol.1980.sp013079 / J. Physiol. / Release of calcium linked to the activation of potassium conductance in a caffeine-treated sympathetic neuron by Kuba (1980)
10.1242/jcs.94.3.443 / J. Cell Sci. / Measurement of volume injected into individual cells by quantitative fluorescent microscopy by Lee (1989)
{'key': '2023050312124716700_DEVELOP_110_4_1295C20', 'volume-title': 'Artificial Parthenogenesis and Fertilization.', 'author': 'Loeb', 'year': '1913'} / Artificial Parthenogenesis and Fertilization. by Loeb (1913)
10.1002/mrd.1120150308 / Gamete Res. / Examination of living and fixed gametes and early embryos stained with supravital fluorochromes (Hoechst 33342 and 3,3′-dihexyloxacarbocyanine iodide) by Luttmer (1986)
{'key': '2023050312124716700_DEVELOP_110_4_1295C22', 'first-page': '38', 'article-title': 'When does the sperm fuse with the egg?', 'volume': '88', 'author': 'Mcculloh', 'year': '1986', 'journal-title': 'J. gen. Physiol.'} / J. gen. Physiol. / When does the sperm fuse with the egg? by Mcculloh (1986)
10.1007/BF01907568 / Pflügers Arch. / A delayed hyperpolarisation induced by a single Ca action potential in hamster eggs by Mcniven (1988)
10.1083/jcb.106.2.345 / J. Cell Biol. / Inositol 1,4,5-trisphosphate-induced calcium release and guanine nucleotide-binding protein-mediated period calcium rises in golden hamster eggs by Miyazaki (1988)
10.1111/j.1440-169X.1988.00603.x / Dev. Growth and Diff. / Fertilization potential and calcium transients in mammalian eggs by Miyazaki (1988)
10.1038/290702a0 / Nature / Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations by Miyazaki (1981)
10.1113/jphysiol.1990.sp018134 / J. Physiol. / Synergistic activation by serotonin and GTP analogue and inhibition by phorbol ester of cyclic Ca2+ rises in hamster eggs by Miyazaki (1990)
10.1242/dev.109.1.117 / Development / The parthenogenetic development of rabbit oocytes after repetitive pulsatile stimulation by Ozil (1990)
{'key': '2023050312124716700_DEVELOP_110_4_1295C29', 'first-page': '101', 'article-title': 'Penetration of hamster and pig zona-free eggs by boar ejaculated spermatozoa preincubated in vitro', 'volume': '26', 'author': 'Pavlok', 'year': '1981', 'journal-title': 'Int. J. Fert.'} / Int. J. Fert. / Penetration of hamster and pig zona-free eggs by boar ejaculated spermatozoa preincubated in vitro by Pavlok (1981)
10.1038/315147a0 / Nature / Changes in free calcium with stages of the cell division cycle by Poenie (1985)
10.1530/jrf.0.0660161 / J. Reprod. Fert. / Preservation of hamster oocytes to assay the fertilizing capacity of hamster spermatozoa by Quinn (1982)
10.1002/mrd.1080250309 / Mol. Reprod. and Dev. / Activation of mammalian oocytes by a factor obtained from rabbit sperm by Stice (1990)
10.1002/j.1460-2075.1989.tb08546.x / EMBO J. / Evidence for an inhibitory effect of protein kinase C on G-protein-mediated repetitive calcium transients in hamster eggs by Swann (1989)
{'key': '2023050312124716700_DEVELOP_110_4_1295C34', 'article-title': 'Second messengers at fertilization in sea urchin eggs', 'volume': '42', 'author': 'Swann', 'year': '1990', 'journal-title': 'J. Reprod. Fert. Suppl.'} / J. Reprod. Fert. Suppl. / Second messengers at fertilization in sea urchin eggs by Swann (1990)
10.1083/jcb.102.1.70 / J. Cell Biol. / Regulation of cortical vesicle exocytosis by inositol 1,4,5 trisphosphate and GTP binding protein by Turner (1986)
{'key': '2023050312124716700_DEVELOP_110_4_1295C36', 'first-page': '459', 'article-title': 'Phosphoinositide second messengers in eggs and oocytes', 'volume-title': 'Inositol Lipids in Cell Signalling', 'author': 'Whitaker', 'year': '1989'} / Inositol Lipids in Cell Signalling / Phosphoinositide second messengers in eggs and oocytes by Whitaker (1989)
10.1242/dev.108.4.525 / Development / Calcium and cell cycle control by Whitaker (1990)
10.1016/B978-0-12-492603-5.50011-6 / Biology of Fertilization / Ionic signalling in sea urchin egg fertilization by Whitaker (1985)
10.1007/978-1-4757-0881-3_8 / Mechanisms of Egg Activation / I. What happens during the latent period at fertilization? by Whitaker (1989)
{'key': '2023050312124716700_DEVELOP_110_4_1295C40', 'article-title': 'Parthenogenesis in mammals', 'volume-title': 'Oxford Reviews of Reproductive Biology pp. 205-231 Oxford: Oxford University Press', 'author': 'Whittingham', 'year': '1980'} / Oxford Reviews of Reproductive Biology pp. 205-231 Oxford: Oxford University Press / Parthenogenesis in mammals by Whittingham (1980)

Dates

Type	When
Created	4 years, 4 months ago (April 25, 2021, 9:45 p.m.)
Deposited	2 years, 4 months ago (May 3, 2023, 8:27 a.m.)
Indexed	2 months, 1 week ago (June 21, 2025, 3:26 a.m.)
Issued	34 years, 9 months ago (Dec. 1, 1990)
Published	34 years, 9 months ago (Dec. 1, 1990)
Published Online	34 years, 9 months ago (Dec. 1, 1990)
Published Print	34 years, 9 months ago (Dec. 1, 1990)

Funders 0

None

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        21
      ]
    ],
    "date-time": "2025-06-21T07:26:06Z",
    "timestamp": 1750490766616
  },
  "reference-count": 40,
  "publisher": "The Company of Biologists",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1990,
            12,
            1
          ]
        ],
        "date-time": "1990-12-01T00:00:00Z",
        "timestamp": 660009600000
      },
      "content-version": "vor",
      "delay-in-days": 0,
      "URL": "http://www.biologists.com/user-licence-1-1/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1990,
        12,
        1
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>Microinjection of cytosolic sperm extracts into unfertilized golden hamster eggs caused a series of increases in cytoplasmic free calcium, Ca2+i, and membrane hyperpolarizing responses, HRs. These HRs and Ca2+i, transients are similar to those seen during in vitro fertilization of hamster eggs. The sperm factor that is responsible for causing these effects appears to be of high molecular weight and protein based. Injection of sperm factor activated eggs and mimicked fertilization in causing repetitive HRs in the presence of phorbol esters and in sensitizing the egg to calcium-induced calcium release. Since these effects cannot be mimicked by injecting G-protein agonists or calcium-containing solutions, it seems unlikely that a receptor-G-protein signalling system is involved at fertilization. These data instead suggest a novel signal transduction system operates during mammalian fertilization in which a protein factor is transferred from the sperm into the egg cytoplasm after gamete membrane fusion.</jats:p>",
  "DOI": "10.1242/dev.110.4.1295",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2021,
        4,
        26
      ]
    ],
    "date-time": "2021-04-26T01:45:29Z",
    "timestamp": 1619401529000
  },
  "page": "1295-1302",
  "source": "Crossref",
  "is-referenced-by-count": 328,
  "title": "A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs",
  "prefix": "10.1242",
  "volume": "110",
  "author": [
    {
      "given": "Karl",
      "family": "Swann",
      "sequence": "first",
      "affiliation": [
        {
          "name": "MRC Experimental Embryology and Teratology Unit, St George\u2019s Hospital Medical School, Cranmer Terrace, London SW17 ORE, UK"
        }
      ]
    }
  ],
  "member": "237",
  "published-online": {
    "date-parts": [
      [
        1990,
        12,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C1",
      "doi-asserted-by": "publisher",
      "first-page": "139",
      "DOI": "10.1002/mrd.1120230202",
      "article-title": "A consistently successful procedure for in vitro fertilization of golden hamster eggs",
      "volume": "23",
      "author": "Bavister",
      "year": "1989",
      "journal-title": "Gamete Res."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C2",
      "doi-asserted-by": "publisher",
      "first-page": "3074",
      "DOI": "10.1096/fasebj.2.15.2847949",
      "article-title": "Cytosolic calcium oscillators",
      "volume": "2",
      "author": "Berridge",
      "year": "1988",
      "journal-title": "FASEB J."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C3",
      "doi-asserted-by": "publisher",
      "first-page": "541",
      "DOI": "10.1038/316541a0",
      "article-title": "Phorbol ester and sperm activate mouse oocytes by inducing sustained oscillations in cell Ca2+",
      "volume": "316",
      "author": "Cuthbertson",
      "year": "1985",
      "journal-title": "Nature"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C4",
      "doi-asserted-by": "publisher",
      "first-page": "205",
      "DOI": "10.1016/0014-4827(88)90038-9",
      "article-title": "Primary and secondary messengers in the activation of ascidian eggs",
      "volume": "207",
      "author": "Dale",
      "year": "1988",
      "journal-title": "Expl Cell Res."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C5",
      "doi-asserted-by": "publisher",
      "first-page": "1068",
      "DOI": "10.1007/BF01952148",
      "article-title": "Injection of a soluble sperm extract into sea urchin eggs triggers the cortical reaction",
      "volume": "41",
      "author": "Dale",
      "year": "1985",
      "journal-title": "Experimentia"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C6",
      "doi-asserted-by": "publisher",
      "first-page": "34",
      "DOI": "10.1038/228034a0",
      "article-title": "Calcium induced release of calcium from the sarcoplasmic reticulum of skinned skeletal muscle fibres",
      "volume": "228",
      "author": "Endo",
      "year": "1970",
      "journal-title": "Nature"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C7",
      "doi-asserted-by": "publisher",
      "first-page": "386",
      "DOI": "10.1016/0012-1606(83)90176-8",
      "article-title": "An electrophysiological study of parthenogenetic activation in mammalian eggs",
      "volume": "96",
      "author": "Eusebi",
      "year": "1983",
      "journal-title": "Devi Biol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C8",
      "doi-asserted-by": "publisher",
      "first-page": "149",
      "DOI": "10.1038/273149a0",
      "article-title": "Activation of mammalian eggs by intracellular injection of calcium",
      "volume": "273",
      "author": "Fulton",
      "year": "1978",
      "journal-title": "Nature"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C9",
      "doi-asserted-by": "publisher",
      "first-page": "1654",
      "DOI": "10.1126/science.3823908",
      "article-title": "Electrical responses of eggs to acrosomal protein similar to those induced by sperm",
      "volume": "235",
      "author": "Gould",
      "year": "1987",
      "journal-title": "Science"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C10",
      "doi-asserted-by": "publisher",
      "first-page": "3440",
      "DOI": "10.1016/S0021-9258(19)83641-4",
      "article-title": "A new generation of calcium indicators with greatly improved fluorescent properties",
      "volume": "260",
      "author": "Grykiewicz",
      "year": "1985",
      "journal-title": "J. biol. Chem."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C11",
      "doi-asserted-by": "publisher",
      "first-page": "385",
      "DOI": "10.1146/annurev.bb.08.060179.002125",
      "article-title": "Electrical properties of egg cell membranes",
      "volume": "8",
      "author": "Hagiwara",
      "year": "1979",
      "journal-title": "A. Rev. Biophys. Bioeng."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C12",
      "doi-asserted-by": "publisher",
      "first-page": "363",
      "DOI": "10.1093/biolreprod/6.2.300",
      "article-title": "Penetration of zona free eggs by spermatozoa of different species",
      "volume": "6",
      "author": "Hanada",
      "year": "1972",
      "journal-title": "Biol. Reprod."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C13",
      "doi-asserted-by": "publisher",
      "first-page": "611",
      "DOI": "10.1113/jphysiol.1983.sp014783",
      "article-title": "Effects of altered extracelluar and intracellular calcium concentration on hyperpolarizing responses of hamster egg",
      "volume": "340",
      "author": "Igusa",
      "year": "1983",
      "journal-title": "J. Physiol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C14",
      "doi-asserted-by": "publisher",
      "first-page": "193",
      "DOI": "10.1113/jphysiol.1986.sp016181",
      "article-title": "Period increase of cytoplasmic free calcium in fertilized hamster eggs measured with calciumsensitive electrodes",
      "volume": "377",
      "author": "Igusa",
      "year": "1986",
      "journal-title": "J. Physiol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C15",
      "doi-asserted-by": "crossref",
      "first-page": "643",
      "DOI": "10.1113/jphysiol.1983.sp014784",
      "article-title": "Periodic hyperpolarizing responses in hamster and mouse eggs fertilized with mouse sperm",
      "volume": "340",
      "author": "Igusa",
      "year": "1983",
      "journal-title": "J. Physiol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0922-3371(88)90094-9",
      "article-title": "G-proteins and egg activation",
      "volume": "25",
      "author": "Jaffe",
      "year": "1988",
      "journal-title": "Cell. Differ. Dev."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C17",
      "doi-asserted-by": "publisher",
      "first-page": "265",
      "DOI": "10.1016/0012-1606(83)90276-2",
      "article-title": "Sources of calcium in egg activation; a review and hypothesis",
      "volume": "99",
      "author": "Jaffe",
      "year": "1983",
      "journal-title": "Devi Biol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C18",
      "doi-asserted-by": "publisher",
      "first-page": "251",
      "DOI": "10.1113/jphysiol.1980.sp013079",
      "article-title": "Release of calcium linked to the activation of potassium conductance in a caffeine-treated sympathetic neuron",
      "volume": "298",
      "author": "Kuba",
      "year": "1980",
      "journal-title": "J. Physiol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C19",
      "doi-asserted-by": "publisher",
      "first-page": "443",
      "DOI": "10.1242/jcs.94.3.443",
      "article-title": "Measurement of volume injected into individual cells by quantitative fluorescent microscopy",
      "volume": "94",
      "author": "Lee",
      "year": "1989",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C20",
      "volume-title": "Artificial Parthenogenesis and Fertilization.",
      "author": "Loeb",
      "year": "1913"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C21",
      "doi-asserted-by": "publisher",
      "first-page": "267",
      "DOI": "10.1002/mrd.1120150308",
      "article-title": "Examination of living and fixed gametes and early embryos stained with supravital fluorochromes (Hoechst 33342 and 3,3\u2032-dihexyloxacarbocyanine iodide)",
      "volume": "21",
      "author": "Luttmer",
      "year": "1986",
      "journal-title": "Gamete Res."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C22",
      "first-page": "38",
      "article-title": "When does the sperm fuse with the egg?",
      "volume": "88",
      "author": "Mcculloh",
      "year": "1986",
      "journal-title": "J. gen. Physiol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C23",
      "doi-asserted-by": "publisher",
      "first-page": "451",
      "DOI": "10.1007/BF01907568",
      "article-title": "A delayed hyperpolarisation induced by a single Ca action potential in hamster eggs",
      "volume": "412",
      "author": "Mcniven",
      "year": "1988",
      "journal-title": "Pfl\u00fcgers Arch."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C24",
      "doi-asserted-by": "publisher",
      "first-page": "345",
      "DOI": "10.1083/jcb.106.2.345",
      "article-title": "Inositol 1,4,5-trisphosphate-induced calcium release and guanine nucleotide-binding protein-mediated period calcium rises in golden hamster eggs",
      "volume": "106",
      "author": "Miyazaki",
      "year": "1988",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C25",
      "doi-asserted-by": "publisher",
      "first-page": "603",
      "DOI": "10.1111/j.1440-169X.1988.00603.x",
      "article-title": "Fertilization potential and calcium transients in mammalian eggs",
      "volume": "30",
      "author": "Miyazaki",
      "year": "1988",
      "journal-title": "Dev. Growth and Diff."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C26",
      "doi-asserted-by": "publisher",
      "first-page": "706",
      "DOI": "10.1038/290702a0",
      "article-title": "Fertilization potential in golden hamster eggs consists of recurring hyperpolarizations",
      "volume": "290",
      "author": "Miyazaki",
      "year": "1981",
      "journal-title": "Nature"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C27",
      "doi-asserted-by": "publisher",
      "first-page": "209",
      "DOI": "10.1113/jphysiol.1990.sp018134",
      "article-title": "Synergistic activation by serotonin and GTP analogue and inhibition by phorbol ester of cyclic Ca2+ rises in hamster eggs",
      "volume": "426",
      "author": "Miyazaki",
      "year": "1990",
      "journal-title": "J. Physiol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C28",
      "doi-asserted-by": "publisher",
      "first-page": "117",
      "DOI": "10.1242/dev.109.1.117",
      "article-title": "The parthenogenetic development of rabbit oocytes after repetitive pulsatile stimulation",
      "volume": "109",
      "author": "Ozil",
      "year": "1990",
      "journal-title": "Development"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C29",
      "first-page": "101",
      "article-title": "Penetration of hamster and pig zona-free eggs by boar ejaculated spermatozoa preincubated in vitro",
      "volume": "26",
      "author": "Pavlok",
      "year": "1981",
      "journal-title": "Int. J. Fert."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C30",
      "doi-asserted-by": "publisher",
      "first-page": "147",
      "DOI": "10.1038/315147a0",
      "article-title": "Changes in free calcium with stages of the cell division cycle",
      "volume": "315",
      "author": "Poenie",
      "year": "1985",
      "journal-title": "Nature"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C31",
      "doi-asserted-by": "publisher",
      "first-page": "161",
      "DOI": "10.1530/jrf.0.0660161",
      "article-title": "Preservation of hamster oocytes to assay the fertilizing capacity of hamster spermatozoa",
      "volume": "66",
      "author": "Quinn",
      "year": "1982",
      "journal-title": "J. Reprod. Fert."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C32",
      "doi-asserted-by": "publisher",
      "first-page": "272",
      "DOI": "10.1002/mrd.1080250309",
      "article-title": "Activation of mammalian oocytes by a factor obtained from rabbit sperm",
      "volume": "25",
      "author": "Stice",
      "year": "1990",
      "journal-title": "Mol. Reprod. and Dev."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C33",
      "doi-asserted-by": "publisher",
      "first-page": "3711",
      "DOI": "10.1002/j.1460-2075.1989.tb08546.x",
      "article-title": "Evidence for an inhibitory effect of protein kinase C on G-protein-mediated repetitive calcium transients in hamster eggs",
      "volume": "8",
      "author": "Swann",
      "year": "1989",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C34",
      "article-title": "Second messengers at fertilization in sea urchin eggs",
      "volume": "42",
      "author": "Swann",
      "year": "1990",
      "journal-title": "J. Reprod. Fert. Suppl."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C35",
      "doi-asserted-by": "publisher",
      "first-page": "70",
      "DOI": "10.1083/jcb.102.1.70",
      "article-title": "Regulation of cortical vesicle exocytosis by inositol 1,4,5 trisphosphate and GTP binding protein",
      "volume": "102",
      "author": "Turner",
      "year": "1986",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C36",
      "first-page": "459",
      "article-title": "Phosphoinositide second messengers in eggs and oocytes",
      "volume-title": "Inositol Lipids in Cell Signalling",
      "author": "Whitaker",
      "year": "1989"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C37",
      "doi-asserted-by": "publisher",
      "first-page": "525",
      "DOI": "10.1242/dev.108.4.525",
      "article-title": "Calcium and cell cycle control",
      "volume": "108",
      "author": "Whitaker",
      "year": "1990",
      "journal-title": "Development"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C38",
      "doi-asserted-by": "crossref",
      "first-page": "167",
      "DOI": "10.1016/B978-0-12-492603-5.50011-6",
      "article-title": "Ionic signalling in sea urchin egg fertilization",
      "volume-title": "Biology of Fertilization",
      "author": "Whitaker",
      "year": "1985"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C39",
      "doi-asserted-by": "crossref",
      "DOI": "10.1007/978-1-4757-0881-3_8",
      "article-title": "I. What happens during the latent period at fertilization?",
      "volume-title": "Mechanisms of Egg Activation",
      "author": "Whitaker",
      "year": "1989"
    },
    {
      "key": "2023050312124716700_DEVELOP_110_4_1295C40",
      "article-title": "Parthenogenesis in mammals",
      "volume-title": "Oxford Reviews of Reproductive Biology pp. 205-231 Oxford: Oxford University Press",
      "author": "Whittingham",
      "year": "1980"
    }
  ],
  "container-title": "Development",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/110/4/1295/2806171/develop_110_4_1295.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://journals.biologists.com/dev/article-pdf/110/4/1295/2806171/develop_110_4_1295.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        5,
        3
      ]
    ],
    "date-time": "2023-05-03T12:27:35Z",
    "timestamp": 1683116855000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.biologists.com/dev/article/110/4/1295/37120/A-cytosolic-sperm-factor-stimulates-repetitive"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1990,
        12,
        1
      ]
    ]
  },
  "references-count": 40,
  "journal-issue": {
    "issue": "4",
    "published-print": {
      "date-parts": [
        [
          1990,
          12,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/dev.110.4.1295",
  "relation": {},
  "ISSN": [
    "0950-1991",
    "1477-9129"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1990,
        12,
        1
      ]
    ]
  }
}