Alterations of PLCbeta1 in Mouse Eggs Change Calcium Oscillatory Behavior Following Fertilization

Overview

Journal Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2007 Oct 27

PMID 17961538

Citations 45

Authors

Hideki Igarashi

Jason G Knott

Richard M Schultz

Carmen J Williams

Affiliations

Soon will be listed here.

Abstract

Inositol 1,4,5-trisphosphate generated by the action of a phospholipase C (PLC) mediates release of intracellular Ca2+ that is essential for sperm-induced activation of mammalian eggs. Much attention currently focuses on the role of sperm-derived PLCzeta in generating changes in egg intracellular Ca2+ despite the fact that PLCzeta constitutes a very small fraction of the total amount of PLC in a fertilized egg. Eggs express several isoforms of PLC, but a role for an egg-derived PLC in sperm-induced Ca2+ oscillations has not been examined. Reducing egg PLCbeta1 by a transgenic RNAi approach resulted in a significant decrease in Ca2+ transient amplitude, but not duration or frequency, following insemination. Furthermore, overexpressing PLCbeta1 by microinjecting a Plcb1 cRNA significantly perturbed the duration and frequency of Ca2+ transients and disrupted the characteristic shape of the first transient. These results provide the first evidence for a role of an egg-derived PLC acting in conjunction with a sperm-derived PLCzeta in egg activation.

Citing Articles

Hybrid female sterility due to cohesin protection errors in oocytes.

El Yakoubi W, Pan B, Akera T bioRxiv. 2025; .

PMID: 40027736 PMC: 11870456. DOI: 10.1101/2025.02.16.638358.

Maternal genetic variants in kinesin motor domains prematurely increase egg aneuploidy.

Biswas L, Tyc K, Aboelenain M, Sun S, Dundovic I, Vukusic K Proc Natl Acad Sci U S A. 2024; 121(45):e2414963121.

PMID: 39475646 PMC: 11551467. DOI: 10.1073/pnas.2414963121.

Deoxyhypusine synthase deficiency syndrome zebrafish model: aberrant morphology, epileptiform activity, and reduced arborization of inhibitory interneurons.

Shojaeinia E, Mastracci T, Soliman R, Devinsky O, Esguerra C, Crawford A Mol Brain. 2024; 17(1):68.

PMID: 39334388 PMC: 11429087. DOI: 10.1186/s13041-024-01139-w.

An oocyte meiotic midbody cap is required for developmental competence in mice.

Jung G, Londono-Vasquez D, Park S, Skop A, Balboula A, Schindler K Nat Commun. 2023; 14(1):7419.

PMID: 37973997 PMC: 10654508. DOI: 10.1038/s41467-023-43288-x.

Condensin dysfunction is a reproductive isolating barrier in mice.

El Yakoubi W, Akera T Nature. 2023; 623(7986):347-355.

PMID: 37914934 PMC: 11379054. DOI: 10.1038/s41586-023-06700-6.

References

Ma J, Zeng F, Schultz R, Tseng H . Basonuclin: a novel mammalian maternal-effect gene. Development. 2006; 133(10):2053-62. DOI: 10.1242/dev.02371. View

Toth S, Huneau D, Banrezes B, Ozil J . Egg activation is the result of calcium signal summation in the mouse. Reproduction. 2006; 131(1):27-34. DOI: 10.1530/rep.1.00764. View

Xu Z, Williams C, Kopf G, Schultz R . Maturation-associated increase in IP3 receptor type 1: role in conferring increased IP3 sensitivity and Ca2+ oscillatory behavior in mouse eggs. Dev Biol. 2003; 254(2):163-71. DOI: 10.1016/s0012-1606(02)00049-0. View

Bornslaeger E, Schultz R . Adenylate cyclase activity in zona-free mouse oocytes. Exp Cell Res. 1985; 156(1):277-81. DOI: 10.1016/0014-4827(85)90282-4. View

Dupont G, McGuinness O, Johnson M, Berridge M, Borgese F . Phospholipase C in mouse oocytes: characterization of beta and gamma isoforms and their possible involvement in sperm-induced Ca2+ spiking. Biochem J. 1996; 316 ( Pt 2):583-91. PMC: 1217388. DOI: 10.1042/bj3160583. View

Swann K, Lai F . A novel signalling mechanism for generating Ca2+ oscillations at fertilization in mammals. Bioessays. 1997; 19(5):371-8. DOI: 10.1002/bies.950190504. View

Ross E, Mateu D, Gomes A, Arana C, Tran T, Litosch I . Structural determinants for phosphatidic acid regulation of phospholipase C-beta1. J Biol Chem. 2006; 281(44):33087-94. DOI: 10.1074/jbc.M606487200. View

Millar S, Lader E, Liang L, Dean J . Oocyte-specific factors bind a conserved upstream sequence required for mouse zona pellucida promoter activity. Mol Cell Biol. 1991; 11(12):6197-204. PMC: 361804. DOI: 10.1128/mcb.11.12.6197-6204.1991. View

Miyazaki S, Hashimoto N, Yoshimoto Y, Kishimoto T, Igusa Y, Hiramoto Y . Temporal and spatial dynamics of the periodic increase in intracellular free calcium at fertilization of golden hamster eggs. Dev Biol. 1986; 118(1):259-67. DOI: 10.1016/0012-1606(86)90093-x. View

10.

Markoulaki S, Matson S, Abbott A, Ducibella T . Oscillatory CaMKII activity in mouse egg activation. Dev Biol. 2003; 258(2):464-74. DOI: 10.1016/s0012-1606(03)00133-7. View

11.

Chatot C, Ziomek C, Bavister B, Lewis J, Torres I . An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil. 1989; 86(2):679-88. DOI: 10.1530/jrf.0.0860679. View

12.

Ozil J, Huneau D . Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development. Development. 2001; 128(6):917-28. DOI: 10.1242/dev.128.6.917. View

13.

Kimura Y, Yanagimachi R . Intracytoplasmic sperm injection in the mouse. Biol Reprod. 1995; 52(4):709-20. DOI: 10.1095/biolreprod52.4.709. View

14.

Yoda A, Oda S, Shikano T, Kouchi Z, Awaji T, Shirakawa H . Ca2+ oscillation-inducing phospholipase C zeta expressed in mouse eggs is accumulated to the pronucleus during egg activation. Dev Biol. 2004; 268(2):245-57. DOI: 10.1016/j.ydbio.2003.12.028. View

15.

Kouchi Z, Fukami K, Shikano T, Oda S, Nakamura Y, Takenawa T . Recombinant phospholipase Czeta has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs. J Biol Chem. 2004; 279(11):10408-12. DOI: 10.1074/jbc.M313801200. View

16.

Knott J, Kurokawa M, Fissore R, Schultz R, Williams C . Transgenic RNA interference reveals role for mouse sperm phospholipase Czeta in triggering Ca2+ oscillations during fertilization. Biol Reprod. 2004; 72(4):992-6. DOI: 10.1095/biolreprod.104.036244. View

17.

Avazeri N, Courtot A, Pesty A, Duquenne C, Lefevre B . Cytoplasmic and nuclear phospholipase C-beta 1 relocation: role in resumption of meiosis in the mouse oocyte. Mol Biol Cell. 2000; 11(12):4369-80. PMC: 15079. DOI: 10.1091/mbc.11.12.4369. View

18.

Miyazaki S, Yuzaki M, Nakada K, Shirakawa H, Nakanishi S, Nakade S . Block of Ca2+ wave and Ca2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science. 1992; 257(5067):251-5. DOI: 10.1126/science.1321497. View

19.

Lawrence Y, Whitaker M, Swann K . Sperm-egg fusion is the prelude to the initial Ca2+ increase at fertilization in the mouse. Development. 1997; 124(1):233-41. DOI: 10.1242/dev.124.1.233. View

20.

Jones K, Soeller C, Cannell M . The passage of Ca2+ and fluorescent markers between the sperm and egg after fusion in the mouse. Development. 1998; 125(23):4627-35. DOI: 10.1242/dev.125.23.4627. View