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Cited by 140Reproductive Biology and FertilitySperm and Testicular FunctionReproductive biology and impacts on aquatic species

Sperm-borne phospholipase C zeta-1 ensures monospermic fertilization in mice

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Nozawa, Kaori, Satouh, Yuhkoh, Fujimoto, Takao, Oji, Asami, Ikawa, Masahito·2018·Scientific Reports
DOI 10.1038/s41598-018-19497-6PMC PMC5778054
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Abstract

Sperm entry in mammalian oocytes triggers intracellular Ca 2+ oscillations that initiate resumption of the meiotic cell cycle and subsequent activations. Here, we show that phospholipase C zeta 1 (PLCζ1) is the long-sought sperm-borne oocyte activation factor (SOAF). Plcz1 gene knockout (KO) mouse spermatozoa fail to induce Ca 2+ changes in intracytoplasmic sperm injection (ICSI). In contrast to ICSI, Plcz1 KO spermatozoa induced atypical patterns of Ca 2+ changes in normal fertilizations, and most of the fertilized oocytes ceased development at the 1–2-cell stage because of oocyte activation failure or polyspermy. We further discovered that both zona pellucida block to polyspermy (ZPBP) and plasma membrane block to polyspermy (PMBP) were delayed in oocytes fertilized with Plcz1 KO spermatozoa. With the observation that polyspermy is rare in astacin-like metalloendopeptidase (Astl) KO female oocytes that lack ZPBP, we conclude that PMPB plays more critical role than ZPBP in vivo . Finally, we obtained healthy pups from male mice carrying human infertile PLCZ1 mutation by single sperm ICSI supplemented with Plcz1 mRNA injection. These results suggest that mammalian spermatozoa have a primitive oocyte activation mechanism and that PLCζ1 is a SOAF that ensures oocyte activation steps for monospermic fertilization in mammals.

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  • PLCζ1 is sperm-specific and is the physiological trigger responsible for generating IP3-mediated Ca2+ oscillations that induce oocyte activation during mammalian fertilisation.

    “This PLC is sperm-specific and is the physiological trigger responsible for generating I(1,4,5)P3-mediated Ca2+ oscillations that induces oocyte activation during mammalian fertilisation [43,44].”

    From Phosphatidylinositol(4,5)bisphosphate: diverse functions at the plasma membrane (2020) · cites this paper as [44]

    The Introduction identifies PLCζ1 as sperm-specific and says it can induce Ca2+ oscillations in oocytes; the Discussion identifies it as a sperm-borne oocyte activation factor in mice. But the paper also reports PLCζ1-independent Ca2+ oscillations and oocyte activation during normal fertilization, so it does not support presenting PLCζ1 as the sole physiological trigger. Its explicit account of IP3 generation describes PLC in somatic cells, rather than directly establishing that mechanism for PLCζ1 here. (LLM, conf=0.87)

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Research works printed but not linked: 41

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Cited by

Sorted by citations

Authors
Nozawa, K., Satouh, Y., Fujimoto, T., Oji, A., & Ikawa, M.
Affiliations
  • Research Institute for Microbial Diseases, The University of Osaka (JP)
  • Institute of Medical Science, The University of Tokyo (JP)
Corresponding author
Ikawa, Masahito
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2018-01-22
Volume
8
Issue
1
Pages
1315-1315
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-018-19497-6
PMC
PMC5778054
OpenAlex
W2783911624
Cited by
140
References
0
Citations by year
2026: 10 · 2025: 13 · 2024: 21 · 2023: 24 · 2022: 14 · 2021: 10 · 2020: 26 · 2019: 9 · 2018: 12 · 2012: 1
FWCI
13.59
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • OUKA (Osaka University Knowledge Archive) (Osaka University) (submittedVersion, cc-by)
Funders
  • National Institutes of Health
  • Japan Society for the Promotion of Science (17K15126, 15J03870, 17H01394)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD087157, R01HD088412)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords
PLC1, oocyte activation, monospermy, polyspermy, intracytoplasmic sperm injection, calcium oscillations, mouse oocytes
MeSH terms
Animals, Female, Fertilization, Male, Mice, Inbred C57BL, Mice, Inbred DBA, Mutation, Oocytes, Spermatozoa, Metalloproteases, Mice, Phosphoinositide Phospholipase C

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