24
Views
77
CrossRef citations to date
0
Altmetric
Cell Growth and Development

Inactivation of the Mgat1 Gene in Oocytes Impairs Oogenesis, but Embryos Lacking Complex and Hybrid N-Glycans Develop and Implant

, , , , , , & show all
Pages 9920-9929 | Received 10 Jun 2004, Accepted 24 Aug 2004, Published online: 27 Mar 2023

REFERENCES

  • Alfieri, J. A., Martin A. D., Takeda J., Kondoh G., Myles D. G., and Primakoff P.. 2003. Infertility in female mice with an oocyte-specific knockout of GPI-anchored proteins. J. Cell Sci. 116:2149–2155.
  • Armant, D. R., Kaplan H. A., and Lennarz W. J.. 1986. N-linked glycoprotein biosynthesis in the developing mouse embryo. Dev. Biol. 113:228–237.
  • Atienza-Samols, S. B., Pine P. R., and Sherman M. I.. 1980. Effects of tunicamycin upon glycoprotein synthesis and development of early mouse embryos. Dev. Biol. 79:19–32.
  • Aviles, M., El-Mestrah M., Jaber L., Castells M. T., Ballesta J., and Kan F. W.. 2000. Cytochemical demonstration of modification of carbohydrates in the mouse zona pellucida during folliculogenesis. Histochem. Cell Biol. 113:207–219.
  • Bird, J. M., and Kimber S. J.. 1984. Oligosaccharides containing fucose linked alpha(1-3) and alpha(1-4) to N-acetylglucosamine cause decompaction of mouse morulae. Dev. Biol. 104:449–460.
  • Bleil, J. D., and Wassarman P. M.. 1988. 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. USA 85:6778–6782. (Erratum, 85:9600.)
  • Bleil, J. D., and Wassarman P. M.. 1980. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20:873–882.
  • Bleil, J. D., and Wassarman P. M.. 1980. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. Dev. Biol. 76:185–202.
  • Boja, E. S., Hoodbhoy T., Fales H. M., and Dean J.. 2003. Structural characterization of native mouse zona pellucida proteins using mass spectrometry. J. Biol. Chem. 278:34189–34202.
  • Campbell, R. M., Metzler M., Granovsky M., Dennis J. W., and Marth J. D.. 1995. Complex asparagine-linked oligosaccharides in Mgat1-null embryos. Glycobiology 5:535–543.
  • Chen, J., Litscher E. S., and Wassarman P. M.. 1998. Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm. Proc. Natl. Acad. Sci. USA 95:6193–61977.
  • Chen, W., and Stanley P.. 2003. Five Lec1 CHO cell mutants have distinct Mgat1 gene mutations that encode truncated N-acetylglucosaminyltransferase I. Glycobiology 13:43–50.
  • Cummings, R. D., and Kornfeld S.. 1982. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J. Biol. Chem. 257:11230–11234.
  • Dean, J. 2004. Reassessing the molecular biology of sperm-egg recognition with mouse genetics. Bioessays 26:29–38.
  • Dell, A., Chalabi S., Easton R. L., Haslam S. M., Sutton-Smith M., Patankar M. S., Lattanzio F., Panico M., Morris H. R., and Clark G. F.. 2003. Murine and human zona pellucida 3 derived from mouse eggs express identical O-glycans. Proc. Natl. Acad. Sci. USA 100:15631–15636.
  • Domino, S. E., Zhang L., Gillespie P. J., Saunders T. L., and Lowe J. B.. 2001. Deficiency of reproductive tract α(1,2)fucosylated glycans and normal fertility in mice with targeted deletions of the FUT1 or FUT2 α(1,2)fucosyltransferase locus. Mol. Cell. Biol. 21:8336–8345.
  • East, I. J., and Dean J.. 1984. Monoclonal antibodies as probes of the distribution of ZP-2, the major sulfated glycoprotein of the murine zona pellucida. J. Cell Biol. 98:795–800.
  • East, I. J., Gulyas B. J., and Dean J.. 1985. Monoclonal antibodies to the murine zona pellucida protein with sperm receptor activity: effects on fertilization and early development. Dev. Biol. 109:268–273.
  • Easton, R. L., Patankar M. S., Lattanzio F. A., Leaven T. H., Morris H. R., Clark G. F., and Dell A.. 2000. 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. 275:7731–7742.
  • Ellgaard, L., and Helenius A.. 2003. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4:181–191.
  • Epifano, O., Liang L. F., Familari M., Moos M. C., Jr., and Dean J.. 1995. Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development 121:1947–1956.
  • Fenderson, B. A., Zehavi U., and Hakomori S.. 1984. A multivalent lacto-N-fucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J. Exp. Med. 160:1591–1596.
  • Florman, H. M., and Wassarman P. M.. 1985. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41:313–324.
  • Green, E. D., Brodbeck R. M., and Baenziger J. U.. 1987. Lectin affinity high-performance liquid chromatography: interactions of N-glycanase-released oligosaccharides with leukoagglutinating phytohemagglutinin, concanavalin A, Datura stramonium agglutinin, and Vicia villosa agglutinin. Anal. Biochem. 167:62–75.
  • Ioffe, E., Liu Y., and Stanley P.. 1997. Complex N-glycans in Mgat1 null preimplantation embryos arise from maternal Mgat1 RNA. Glycobiology 7:913–919.
  • Ioffe, E., Liu Y., and Stanley P.. 1996. Essential role for complex N-glycans in forming an organized layer of bronchial epithelium. Proc. Natl. Acad. Sci. USA 93:11041–11046.
  • Ioffe, E., and Stanley P.. 1994. Mice lacking N-acetylglucosaminyltransferase I activity die at mid-gestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc. Natl. Acad. Sci. USA 91:728–732.
  • Johnston, D. S., Shaper J. H., Shaper N. L., Joziasse D. H., and Wright W. W.. 1995. The gene encoding murine alpha 1,3-galactosyltransferase is expressed in female germ cells but not in male germ cells. Dev. Biol. 171:224–232.
  • Johnston, D. S., Wright W. W., Shaper J. H., Hokke C. H., Van den Eijnden D. H., and Joziasse D. H.. 1998. Murine sperm-zona binding, a fucosyl residue is required for a high affinity sperm-binding ligand. A second site on sperm binds a nonfucosylated, beta-galactosyl-capped oligosaccharide. J. Biol. Chem. 273:1888–1895.
  • Kimber, S. J. 2000. Molecular interactions at the maternal-embryonic interface during the early phase of implantation. Semin. Reprod. Med. 18:237–253.
  • Kornfeld, R., and Kornfeld S.. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631–664.
  • Kudo, T., Kaneko M., Iwasaki H., Togayachi A., Nishihara S., Abe K., and Narimatsu H.. 2004. Normal embryonic and germ cell development in mice lacking alpha 1,3-fucosyltransferase IX (Fut9) which show disappearance of stage-specific embryonic antigen 1. Mol. Cell. Biol. 24:4221–4228.
  • Kumar, R., Yang J., Eddy R. L., Byers M. G., Shows T. B., and Stanley P.. 1992. Cloning and expression of the murine gene and chromosomal location of the human gene encoding N-acetylglucosaminyltransferase I Glycobiology 2:383–393. (Erratum, 9:ix, 1999.)
  • Lewandoski, M., Wassarman K. M., and Martin G. R.. 1997. Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line. Curr. Biol. 7:148–151.
  • Liu, C., Litscher E. S., and Wassarman P. M.. 1995. Transgenic mice with reduced numbers of functional sperm receptors on their eggs reproduce normally. Mol. Biol. Cell 6:577–585.
  • Lopez, L. C., Bayna E. M., Litoff D., Shaper N. L., Shaper J. H., and Shur B. D.. 1985. Receptor function of mouse sperm surface galactosyltransferase during fertilization. J. Cell Biol. 101:1501–1510.
  • Lowe, J. B., and Marth J. D.. 2003. A genetic approach to mammalian glycan function. Annu. Rev. Biochem. 72:643–691.
  • Metzler, M., Gertz A., Sarkar M., Schachter H., Schrader J. W., and Marth J. D.. 1994. Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J. 13:2056–2065.
  • Miller, D. J., Macek M. B., and Shur B. D.. 1992. Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding. Nature 357:589–593.
  • Noguchi, S., and Nakano M.. 1993. Structural characterization of the N-linked carbohydrate chains from mouse zona pellucida glycoproteins ZP2 and ZP3. Biochim. Biophys. Acta 1158:217–226.
  • O'Donnell, N., Zachara N. E., Hart G. W., and Marth J. D.. 2004. Ogt-dependent X-chromosome-linked protein glycosylation is a requisite modification in somatic cell function and embryo viability. Mol. Cell. Biol. 24:1680–1690.
  • Pedersen, T., and Peters H.. 1968. Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17:555–557.
  • Poirier, F., and Kimber S.. 1997. Cell surface carbohydrates and lectins in early development. Mol. Hum. Reprod. 3:907–918.
  • Pownall, S., Kozak C. A., Schappert K., Sarkar M., Hull E., Schachter H., and Marth J. D.. 1992. Molecular cloning and characterization of the mouseUDP-N-acetylglucosamine:alpha-3-D-mannoside beta-1,2-N-acetylglucos-aminyltransferase I gene. Genomics 12:699–704.
  • Rankin, T., Talbot P., Lee E., and Dean J.. 1999. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126:3847–3855.
  • Rankin, T. L., Coleman J. S., Epifano O., Hoodbhoy T., Turner S. G., Castle P. E., Lee E., Gore-Langton R., and Dean J.. 2003. Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs. Dev. Cell 5:33–43.
  • Rankin, T. L., O'Brien M., Lee E., Wigglesworth K., Eppig J., and Dean J.. 2001. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development. Development 128:1119–1126.
  • Rankin, T. L., Tong Z. B., Castle P. E., Lee E., Gore-Langton R., Nelson L. M., and Dean J.. 1998. Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development 125:2415–2424.
  • Riethmacher, D., Brinkmann V., and Birchmeier C.. 1995. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl. Acad. Sci. USA 92:855–859.
  • Robertson, M. A., Etchison J. R., Robertson J. S., Summers D. F., and Stanley P.. 1978. Specific changes in the oligosaccharide moieties of VSV grown in different lectin-resistant CHO cells. Cell 13:515–526.
  • Rodeheffer, C., and Shur B. D.. 2004. Characterization of a novel ZP3-independent sperm-binding ligand that facilitates sperm adhesion to the egg coat. Development 131:503–512.
  • Schachter, H. 2000. The joys of HexNAc. The synthesis and function of N- and O-glycan branches. Glycoconj. J. 17:465–483.
  • Schlesinger, S., Gottlieb C., Feil P., Gelb N., and Kornfeld S.. 1975. Growth of enveloped RNA viruses in a line of Chinese hamster ovary cells with deficient N-acetylglucosaminyltransferase activity. J. Virol. 17:239–246.
  • Shafi, R., Iyer S. P., Ellies L. G., O'Donnell N., Marek K. W., Chui D., Hart G. W., and Marth J. D.. 2000. The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc. Natl. Acad. Sci. USA 97:5735–5739.
  • Shur, B. D., and Hall N. G.. 1982. A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J. Cell Biol. 95:574–579.
  • Stanley, P., Narasimhan S., Siminovitch L., and Schachter H.. 1975. Chinese hamster ovary cells selected for resistance to the cytotoxicity of phytohemagglutinin are deficient in a UDP-N-acetylglucosamine-glycoprotein N-acetylglucosaminyltransferase activity. Proc. Natl. Acad. Sci. USA 72:3323–3327.
  • Su, A. I., Wiltshire T., Batalov S., Lapp H., Ching K. A., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G., Cooke M. P., Walker J. R., and Hogenesch J. B.. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. USA 101:6062–6067.
  • Surani, M. A. 1979. Glycoprotein synthesis and inhibition of glycosylation by tunicamycin in preimplantation mouse embryos: compaction and trophoblast adhesion. Cell 18:217–227.
  • Talbot, P., Shur B. D., and Myles D. G.. 2003. Cell adhesion and fertilization: steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion. Biol. Reprod. 68:1–9.
  • Tarentino, A. L., Trimble R. B., and Plummer T. H., Jr. 1989. Enzymatic approaches for studying the structure, synthesis, and processing of glycoproteins. Methods Cell Biol. 32:111–139.
  • Thall, A. D., Maly P., and Lowe J. B.. 1995. Oocyte Gal alpha 1,3Gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse. J. Biol. Chem. 270:21437–21440.
  • Tulsiani, D. R., Nagdas S. K., Cornwall G. A., and Orgebin-Crist M. C.. 1992. Evidence for the presence of high-mannose/hybrid oligosaccharide chain(s) on the mouse ZP2 and ZP3. Biol. Reprod. 46:93–100.
  • Wang, X. Q., Zhu Z. M., Fenderson B. A., Zeng G. Q., Cao Y. J., and Jiang G. T.. 1998. Effects of monoclonal antibody directed to LeY on implantation in the mouse. Mol. Hum. Reprod. 4:295–300.
  • Wassarman, P. M. 1988. Zona pellucida glycoproteins. Annu. Rev. Biochem. 57:415–442.
  • Watson, A. J., and Barcroft L. C.. 2001. Regulation of blastocyst formation. Front Biosci. 6:D708–730.
  • Ye, Z., and Marth J. D.. 2004. N-glycan branching requirement in neuronal and post-natal viability. Glycobiology 14:547–558.
  • Zhu, Z. M., Kojima N., Stroud M. R., Hakomori S. I., and Fenderson B. A.. 1995. Monoclonal antibody directed to LeY oligosaccharide inhibits implantation in the mouse. Biol. Reprod. 52:903–912.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.