Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss

Tracy Rankin; Prue Talbot; Eric Lee; Jurrien Dean

doi:10.1242/dev.126.17.3847

journal article Sep 01, 1999

Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss

Tracy Rankin Prue Talbot Eric Lee

Jurrien Dean

Development Vol. 126 No. 17 pp. 3847-3855 · The Company of Biologists

View at Publisher Save 10.1242/dev.126.17.3847

Abstract

Abstract
All vertebrates have an egg shell that surrounds ovulated eggs and plays critical roles in gamete recognition. This extracellular matrix is known as the zona pellucida in eutherian mammals and consists of three glycoproteins, ZP1, ZP2 and ZP3 in the mouse. To investigate the role of ZP1 in fertilization and early development, we have used targeted mutagenesis in embryonic stem cells to create mouse lines (Zp1tm/tm) lacking ZP1. Although a zona pellucida composed of ZP2 and ZP3 was formed around growing Zp1tm/tm oocytes, the matrix was more loosely organized than zonae around normal oocytes. In some Zp1 null follicles, this structural abnormality resulted in ectopic clusters of granulosa cells, lodged between the zona matrix and the oolemma, that perturbed normal folliculogenesis. Comparable numbers of eggs were ovulated from Zp1 null females and normal females following hormonal stimulation. However, after mating with males, fewer two-cell embryos were recovered from Zp1 null females, and their litters were significantly smaller than those produced by normal mice. Therefore, although mouse ZP1 is not essential for sperm binding or fertilization, it is required for the structural integrity of the zona pellucida to minimize precocious hatching and reduced fecundity.

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References

59

[1]

Amanze "The micropyle: A sperm guidance system in teleost fertilization" Development (1990) 10.1242/dev.109.2.495

[2]

Beebe "Recombinant ZP3 inhibits sperm binding and induces the acrosome reaction" Dev. Biol (1992) 10.1016/0012-1606(92)90212-y

[3]

Bleil "Mammalian sperm-egg interaction: Identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm" Cell (1980) 10.1016/0092-8674(80)90334-7

[4]

Bleil "Autoradiographic visualization of the mouse egg’s sperm receptor bound to sperm" J. Cell Biol (1986) 10.1083/jcb.102.4.1363

[5]

Bleil "Galactose at the nonreducing terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoprotein’s sperm receptor activity" Proc. Natl. Acad. Sci. U. S. A (1988) 10.1073/pnas.85.18.6778

[6]

Bleil "Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2" Dev. Biol (1981) 10.1016/0012-1606(81)90329-8

[7]

Bleil "Identification of a secondary sperm receptor in the mouse egg zona pellucida: Role in maintenance of binding of acrosome-reacted sperm to eggs" Dev. Biol (1988) 10.1016/0012-1606(88)90299-0

[8]

Bork "A large domain common to sperm receptors (Zp2 and Zp3) and TGF-beta type III receptor" FEBS Lett (1992) 10.1016/0014-5793(92)80853-9

[9]

Bronson "Transfer to the mouse oviduct of eggs with and without the zona pellucida" J. Reprod. Fertil (1970) 10.1530/jrf.0.0220129

[10]

Burnette "‘Western blotting’: Electrophoretic transfer of proteins from sodium dodecyl sulfate–polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A" Analyt. Biochem (1981) 10.1016/0003-2697(81)90281-5

[11]

Chamberlin "Genomic organization of a sex specific gene: The primary sperm receptor of the mouse zona pellucida" Dev. Biol (1989) 10.1016/s0012-1606(89)80052-1

[12]

Chang "Molecular cloning, structural analysis, and expression of carp ZP2 gene" Mol. Reprod. Dev (1997) 10.1002/(sici)1098-2795(199703)46:3<258::aid-mrd4>3.0.co;2-o

[13]

Chang "Molecular cloning, structural analysis, and expression of carp ZP3 gene" Mol. Reprod. Dev (1996) 10.1002/(sici)1098-2795(199607)44:3<295::aid-mrd3>3.0.co;2-h

[14]

Del Giacco "Identification and spatial distribution of the mRNA encoding the gp49 component of the gilthead sea bream, Sparus aurata, egg envelope" Mol. Reprod. Dev (1998) 10.1002/(sici)1098-2795(199801)49:1<58::aid-mrd7>3.0.co;2-n

[15]

Dietl "Ultrastructural aspects of the developing mammalian zona pellucida" (1989) 10.1007/978-3-642-74048-0_4

[16]

East "Monoclonal antibodies as probes of the distribution of ZP-2, the major sulfated glycoprotein of the murine zona pellucida" J. Cell Biol (1984) 10.1083/jcb.98.3.795

[17]

East "Monoclonal antibodies to the murine zona pellucida protein with sperm receptor activity: Effects on fertilization and early development" Dev. Biol (1985) 10.1016/0012-1606(85)90454-3

[18]

Epifano "Mouse Zp1 encodes a zona pellucida protein homologous to egg envelope proteins in mammals and fish" J. Biol. Chem (1995) 10.1074/jbc.270.45.27254

[19]

Epifano "Coordinate expression of the three zona pellucida genes during mouse oogenesis" Development (1995) 10.1242/dev.121.7.1947

[20]

Eppig "Intercommunication between mammalian oocytes and companion somatic cells" BioEssays (1991) 10.1002/bies.950131105

[21]

Florman "Mouse gamete interactions: The zona pellucida is the site of the acrosome reaction leading to fertilization in vitro" Dev. Biol (1982) 10.1016/0012-1606(82)90015-x

[22]

Green "Three-dimensional structure of the zona pellucida" Rev. Reprod (1997) 10.1530/ror.0.0020147

[23]

Greve "Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat" J. Mol. Biol (1985) 10.1016/0022-2836(85)90089-0

[24]

Ho "Preimplantation development of mouse embryos in KSOM: Augmentation by amino acids and analysis of gene expression" Mol. Reprod. Dev (1995) 10.1002/mrd.1080410214

[25]

Killick "Molecular cloning of chick beta-tectorin, an extracellular matrix molecule of the inner ear" J. Cell Biol (1995) 10.1083/jcb.129.2.535

[26]

Kinloch "Embryonal carcinoma cells transfected with ZP3 genes differentially glycosylate similar polypeptides and secrete active mouse sperm receptor" J. Cell Biol (1991) 10.1083/jcb.115.3.655

[27]

Kinloch "Primary structure of the mouse sperm receptor polypeptide determined by genomic cloning" Proc. Natl. Acad. Sci. USA (1988) 10.1073/pnas.85.17.6409

[28]

Kumar "A molecular timescale for vertebrate evolution" Nature (1998) 10.1038/31927

[29]

Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4

U. K. LAEMMLI

Nature 1970 10.1038/227680a0

[30]

Legan "The mouse tectorins. Modular matrix proteins of the inner ear homologous to components of the sperm-egg adhesion system" J. Biol. Chem (1997) 10.1074/jbc.272.13.8791

[31]

Liang "Oocyte-specific expression of mouse Zp-2: Developmental regulation of the zona pellucida genes" Mol. Cell. Biol (1990)

[32]

Liu "Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice" Proc. Natl. Acad. Sci. USA (1996) 10.1073/pnas.93.11.5431

[33]

Lu "Sperm from b1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly" Development (1997) 10.1242/dev.124.20.4121

[34]

Lunsford "Genomic mapping of murine Zp-2 and Zp-3, two oocyte-specific loci encoding zona pellucida proteins" Genomics (1990) 10.1016/0888-7543(90)90465-7

[35]

Lyons "Expression and structural analysis of a teleost homolog of a mammalian zona pellucida gene" J. Biol. Chem (1993) 10.1016/s0021-9258(19)36930-3

[36]

Miller "Egg cortical granule N-acetylglucosaminidase is required for the mouse zona block to polyspermy" J. Cell Biol (1993) 10.1083/jcb.123.6.1431

[37]

Modlinski "The role of the zona pellucida in the development of mouse eggs in vivo" J. Embryol. Exp. Morphol (1970)

[38]

Murata "Cloning of cDNA for precursor protein of a low moleclar weight subunit of the inner layer of the egg envelope (chorion) of the fish, Oryzias latipes" Dev. Biol (1995) 10.1006/dbio.1995.1002

[39]

Murata "Cloning of cDNA and estrogen-induced hepatic gene expression for choriogenin H, a precursor protein of the fish egg envelope (chorion)" Proc. Natl. Acad. Sci. USA (1997) 10.1073/pnas.94.5.2050

[40]

Nagy "Derivation of completely cell culture-derived mice from early-passage embryonic stem cells" Proc. Natl. Acad. Sci. USA (1993) 10.1073/pnas.90.18.8424

[41]

O’Rand "Sperm-egg recognition and barriers to interspecies fertilization" Gamete Res (1988) 10.1002/mrd.1120190402

[42]

Phillips "Surface architecture of the mouse and hamster zona pellucida and oocyte" J. Ultrastruct. Res (1980) 10.1016/s0022-5320(80)90129-x

[43]

Prasad "Evaluating zona-pellucida structure and function using antibodies to rabbit 55 kDa ZP protein expressed in baculovirus expression system" Mol. Reprod. Dev (1996) 10.1002/(sici)1098-2795(199604)43:4<519::aid-mrd15>3.0.co;2-u

[44]

Rankin "Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile" Development (1996) 10.1242/dev.122.9.2903

[45]

Rankin "Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding" Development (1998) 10.1242/dev.125.13.2415

[46]

Sacco "Porcine zona pellucida: Association of sperm receptor activity with the alpha-glycoprotein component of the Mr = 55,000 family" Biol. Reprod (1989) 10.1095/biolreprod41.3.523

[47]

Saling "An ultrastructural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: Sequential relationship to the acrosome reaction" J. Exp. Zool (1979) 10.1002/jez.1402090205

[48]

Sugiyama "The third egg envelope subunit in fish: cDNA cloning and analysis, and gene expression" Dev. Growth Differ (1998) 10.1046/j.1440-169x.1998.t01-5-00005.x

[49]

Talbot "Ultrastructure of opossum oocyte investing coats and their sensitivity to trypsin and hyaluronidase" Dev. Biol (1984) 10.1016/0012-1606(84)90017-4

[50]

Thomas "Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells" Cell (1987) 10.1016/0092-8674(87)90646-5

Showing 50 of 59 references

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References

Details

Published: Sep 01, 1999
Vol/Issue: 126(17)
Pages: 3847-3855
License: View

Authors

T

Tracy Rankin

1 Laboratory of Cellular and Developmental Biology, NIDDK,

P

Prue Talbot

1 Laboratory of Cellular and Developmental Biology, NIDDK,

E

Eric Lee

2 Laboratory of Mammalian Genes, NICHD, National Institutes of Health Bethesda, Maryland 20892, USA

J

Jurrien Dean

1 Laboratory of Cellular and Developmental Biology, NIDDK,

Cite This Article

Tracy Rankin, Prue Talbot, Eric Lee, et al. (1999). Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development, 126(17), 3847-3855. https://doi.org/10.1242/dev.126.17.3847

Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss

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