Home LiteratureArticle Details
PMID: 17047254 Published · ppublish English Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

ZP2 and ZP3 traffic independently within oocytes prior to assembly into the extracellular zona pellucida.

Molecular and cellular biology ·Vol. 26 ·No. 21 ·2006-11-00 ·Pages 7991-8

Hoodbhoy T, Avilés M, Baibakov B, Epifano O, Jiménez-Movilla M, Gauthier L, Dean J

Abstract

The extracellular zona pellucida surrounds mammalian eggs and mediates taxon-specific sperm-egg recognition at fertilization. In mice, the zona pellucida is composed of three glycoproteins, but the presence of ZP2 and ZP3 is sufficient to form a biologically functional structure. Each zona pellucida glycoprotein is synthesized in growing oocytes and traffics through the endomembrane system to the cell surface, where it is released from a transmembrane domain and assembled into the insoluble zona pellucida matrix. ZP2 and ZP3 colocalize in the endoplasmic reticulum and in 1- to 5-microm post-Golgi structures comprising multivesicular aggregates (MVA), but a coimmunoprecipitation assay does not detect physical interactions. In addition, ZP2 traffics normally in growing oocytes in the absence of ZP3 or if ZP3 has been mutated to prevent incorporation into the zona pellucida matrix, complementing earlier studies indicating the independence of ZP3 secretion in Zp2 null mice. N glycosylation has been implicated in correct protein folding and intracellular trafficking of secreted proteins. Although ZP3 contain five N-glycans, enhanced green fluorescent protein-tagged ZP3 lacking N glycosylation sites is present in MVA and is incorporated into the zona pellucida matrix of transgenic mice. Thus, ZP2 secretion is seemingly unaffected by ZP3 lacking N-glycans. Taken together, these observations indicate that ZP2 and ZP3 traffic independently through the oocyte prior to assembly into the zona pellucida.

MeSH Terms
Animals Egg Proteins/genetics,metabolism Endoplasmic Reticulum/metabolism,ultrastructure Female Fluorescent Dyes/metabolism Membrane Glycoproteins/genetics,metabolism Mice Mice, Knockout Mice, Transgenic Oocytes/cytology,physiology Polysaccharides/chemistry,metabolism Receptors, Cell Surface/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism Zona Pellucida/chemistry,metabolism Zona Pellucida Glycoproteins
Chemicals
Egg Proteins Fluorescent Dyes Membrane Glycoproteins Polysaccharides Receptors, Cell Surface Recombinant Fusion Proteins Zona Pellucida Glycoproteins Zp2 protein, mouse Zp3 protein, mouse
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Hoodbhoy Tanya
Laboratory of Cellular and Developmental Biology, NIDDK, National Institutes of Health, Bethesda, MD 20892-8028, USA.
Avilés Manuel
Baibakov Boris
Epifano Olga
Jiménez-Movilla María
Gauthier Lyn
Dean Jurrien
References (39)
39 references, click to expand
  1. Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen.
    J Biol Chem. 2000 Mar 17;275(11):7731-42 PMID: 10713085
  2. Role of asparagine-linked oligosaccharides in secretion of glycoproteins of the mouse egg's extracellular coat.
    J Biol Chem. 1983 Nov 10;258(21):13243-9 PMID: 6630229
  3. Lectins and traffic in the secretory pathway.
    FEBS Lett. 2000 Jun 30;476(1-2):32-7 PMID: 10878245
  4. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development.
    Development. 2001 Apr;128(7):1119-26 PMID: 11245577
  5. Secretion and assembly of zona pellucida glycoproteins by growing mouse oocytes microinjected with epitope-tagged cDNAs for mZP2 and mZP3.
    Mol Biol Cell. 2002 Feb;13(2):530-41 PMID: 11854410
  6. Subcellular distribution of ZP1, ZP2, and ZP3 glycoproteins during folliculogenesis and demonstration of their topographical disposition within the zona matrix of mouse ovarian oocytes.
    Biol Reprod. 2002 Apr;66(4):866-76 PMID: 11906903
  7. Conserved furin cleavage site not essential for secretion and integration of ZP3 into the extracellular egg coat of transgenic mice.
    Mol Cell Biol. 2002 May;22(9):3111-20 PMID: 11940668
  8. The ZP domain is a conserved module for polymerization of extracellular proteins.
    Nat Cell Biol. 2002 Jun;4(6):457-61 PMID: 12021773
  9. Constitutive protein secretion from the trans-Golgi network to the plasma membrane.
    Mol Membr Biol. 2003 Apr-Jun;20(2):129-39 PMID: 12851070
  10. Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs.
    Dev Cell. 2003 Jul;5(1):33-43 PMID: 12852850
  11. Structural characterization of native mouse zona pellucida proteins using mass spectrometry.
    J Biol Chem. 2003 Sep 5;278(36):34189-202 PMID: 12799386
  12. Formation of stacked ER cisternae by low affinity protein interactions.
    J Cell Biol. 2003 Oct 27;163(2):257-69 PMID: 14581454
  13. Mutation of a conserved hydrophobic patch prevents incorporation of ZP3 into the zona pellucida surrounding mouse eggs.
    Mol Cell Biol. 2003 Dec;23(24):8982-91 PMID: 14645511
  14. A duplicated motif controls assembly of zona pellucida domain proteins.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):5922-7 PMID: 15079052
  15. Roles of N-linked glycans in the endoplasmic reticulum.
    Annu Rev Biochem. 2004;73:1019-49 PMID: 15189166
  16. Inactivation of the Mgat1 gene in oocytes impairs oogenesis, but embryos lacking complex and hybrid N-glycans develop and implant.
    Mol Cell Biol. 2004 Nov;24(22):9920-9 PMID: 15509794
  17. The structure of the mammalian egg.
    Int Rev Cytol. 1965;18:29-71 PMID: 5337036
  18. Comparison of cytoplasmic lamellae and membranous elements in the oocytes of five mammalian species.
    Z Zellforsch Mikrosk Anat. 1968;85(1):109-23 PMID: 4882486
  19. An electron microscopic study of mouse eggs matured in vivo and in vitro.
    Anat Rec. 1971 Sep;171(1):21-37 PMID: 5095062
  20. Development of the zona pellucida in the rat oocyte.
    Am J Anat. 1974 Apr;139(4):535-65 PMID: 4274178
  21. Oocyte development in the mouse: an ultrastructural comparison of oocytes isolated at various stages of growth and meiotic competence.
    J Morphol. 1978 May;156(2):209-35 PMID: 642015
  22. Monoclonal antibodies as probes of the distribution of ZP-2, the major sulfated glycoprotein of the murine zona pellucida.
    J Cell Biol. 1984 Mar;98(3):795-800 PMID: 6699085
  23. Genomic sequencing.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991-5 PMID: 6326095
  24. Monoclonal antibodies to the major protein of the murine zona pellucida: effects on fertilization and early development.
    Dev Biol. 1984 Jul;104(1):49-56 PMID: 6376213
  25. Monoclonal antibodies to the murine zona pellucida protein with sperm receptor activity: effects on fertilization and early development.
    Dev Biol. 1985 Jun;109(2):268-73 PMID: 3996750
  26. Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida.
    Dev Biol. 1988 Jun;127(2):287-95 PMID: 3378665
  27. Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes.
    Mol Cell Biol. 1990 Apr;10(4):1507-15 PMID: 1690843
  28. A large domain common to sperm receptors (Zp2 and Zp3) and TGF-beta type III receptor.
    FEBS Lett. 1992 Apr 6;300(3):237-40 PMID: 1313375
  29. O-linked trisaccharide and N-linked poly-N-acetyllactosaminyl glycans are present on mouse ZP2 and ZP3.
    Biol Reprod. 1994 Aug;51(2):262-72 PMID: 7948482
  30. Coordinate expression of the three zona pellucida genes during mouse oogenesis.
    Development. 1995 Jul;121(7):1947-56 PMID: 7635043
  31. Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5431-6 PMID: 8643592
  32. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile.
    Development. 1996 Sep;122(9):2903-10 PMID: 8787763
  33. Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding.
    Development. 1998 Jul;125(13):2415-24 PMID: 9609824
  34. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss.
    Development. 1999 Sep;126(17):3847-55 PMID: 10433913
  35. The development of the zona pellucida of the mammalian ovum.
    Am J Anat. 1960 Mar;106:149-69 PMID: 13693138
  36. Synthesis of zona pellucida proteins by denuded and follicle-enclosed mouse oocytes during culture in vitro.
    Proc Natl Acad Sci U S A. 1980 Feb;77(2):1029-33 PMID: 6928658
  37. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida.
    Dev Biol. 1980 Apr;76(1):185-202 PMID: 7380091
  38. In vitro biosynthesis of three sulfated glycoproteins of murine zonae pellucidae by oocytes grown in follicle culture.
    J Biol Chem. 1983 May 10;258(9):5858-63 PMID: 6853551
  39. Cytochemical demonstration of modification of carbohydrates in the mouse zona pellucida during folliculogenesis.
    Histochem Cell Biol. 2000 Mar;113(3):207-19 PMID: 10817675
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2006-11-00
Pages
7991-8
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC1636726
Subset
IM
Grants
Intramural NIH HHS · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]