Skip to main content
SpringerLink
Log in

H-type 1 carbohydrate antigen expression by ovine endometrial cells

  • Articles
  • Cytokines/Growth Factors/Adhesion Factors
  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Summary

Our objective was to determine whether H-Type 1 carbohydrate antigen is expressed by ovine endometrial epithelial cells. Endometrium was obtained from sheep on days (D) 1, 5, 11, 13, and 15 of the estrous cycle or pregnancy and D17 and D19 of pregnancy. Immunofluorescence microscopy of frozen tissue sections revealed intense staining on the apical surface of glandular uterine epithelial (GE) cells from D11 to D17 of pregnancy. Light punctate staining of luminal uterine epithelial (LE) cells was present from D15 to D19 of pregnancy, with isolated areas of intense staining observed only on D15 of pregnancy. There were no noticeable differences in staining patterns on equivalent d of the estrous cycle. Immortalized sheep LE and GE cells were used to determine whether estradiol (E), progesterone (P), or E+P, with or without interferon tau (IFNτ), regulates H-Type 1 antigen expression in vitro. Intermittent punctate surface staining was observed on both cell lines independent of steroid treatment. Treatment with P or IFNτ increased H-Type 1 antigen expression (P<0.01) and resulted in large aggregates of punctate staining. Domain-specific biotinylation and Western blotting of cell lysates from LE and GE cells were used to identify proteins carrying the H-Type 1 antigen. For both cell types, major immunoreactive apical membrane proteins were detected at 31, 33, 42, 55, 60, and 70 kDa. Therefore, the H-type 1 antigen is expressed mainly on GE cells during pregnancy recognition in utero and up-regulated by P and IFNτ on LE and GE cells in vitro.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aplin, J. D. Adhesion molecules in implantation. Rev. Reprod. 2:84–93; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Asselin, E.; Lacroix, D.; Fortier, M. A. Interferon-tau increases PGE2 production and COX-2 gene expression in the bovine endometrium in vitro. Mol. Cell. Endocrinol. 132:117–126; 1997.

    Article  PubMed  CAS  Google Scholar 

  • Austin, K. J.; Ward, S. K.; Teixeira, M. G.; Dean, V. C.; Moore, D. W.; Hansen, T. R. Ubiquitin cross reactive protein is released by the bovine uterus in response to interferon during early pregnancy. Biol. Reprod. 54:600–606; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Bell, A. W. Factors controlling placental and fetal growth and their effects on future production. In: Lindsay, D. H.; Pierce, D. T., ed. Reproduction in sheep. London: Cambridge University Press; 1984;144–152.

    Google Scholar 

  • Bell, A. W. The whole animal—pregnancy and fetal metabolism. In: Forbes, J. M.; France, J., ed., Quantitative aspects of ruminant digestion and metabolism London: Butterworths; 1991:100–145.

    Google Scholar 

  • Bowen, J. A.; Bazer, F. W.; Burghardt, R. C. Spatial and temporal analysis of integrin and MucI expression in porcine uterine epithelium and trophectoderm in vivo. Biol. Reprod. 55:1098–1106; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Burghardt, R. C.; Bowen, J. A.; Newton, G. R.; Bazer, F. W. Extracellular matrix and the implantation cascade in pigs. J. Reprod. Fertil. 52 (Suppl.):151–164; 1997.

    CAS  Google Scholar 

  • Carson, D. D.; DeSouza, M. M.; Regisford, E. G. Mucin and proteoglycan functions in embryo implantation. Bioessays 20:577–583; 1998.

    Article  PubMed  CAS  Google Scholar 

  • DeSousa, M. M.; Mani, S. K.; Julian, J.; Carson, D. D. Reduction in mucin-1 expression during the receptive phase in the rat uterus. Biol. Reprod. 58:1503–1507; 1998.

    Article  Google Scholar 

  • DeSousa, M. M.; Surveyor, G. A.; Price, R. E., et al. MUC1/episialin: a critical barrier in the female reproductive tract. J. Reprod. Immunol. 45:127–158; 1999.

    Article  Google Scholar 

  • Domino, S. E.; Hiraiwa N.; Lowe, J. B. Molecular cloning, chromosomal assignment and tissue specific expression of a murine α(1–2)fucosyltransferase expressed in thymic and epididymal epithelial cells. Biochem. J. 327:105–115; 1997.

    PubMed  CAS  Google Scholar 

  • Domino, S. E.; Zhang, L.; Lowe, J. B. Molecular cloning, genomic mapping, and expression of two Secretor blood group α(1–2)fucosyltransferase genes differentially regulated in the mouse uterine epithelium and gastrointestinal tract. J. Biol. Chem. 276:23748–23756; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Flieger, D.; Hoff, A. S.; Sauerbruch, T.; Schmidt-Wolf, I. G. Influence of cytokines, monoclonal antibodies and chemotherapeutic drugs on epithelial cell adhesion molecule (EpCAM) and Lewis Y antigen expression. Clin. Exp. Immunol. 123:9–14; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Giudice, L. C. Potential biochemical markers of uterine receptivity. Hum. Reprod. 14 (Suppl. 2):3–16; 1999.

    PubMed  CAS  Google Scholar 

  • Gottardi, C. J.; Caplan, M. J. Cell surface biotinylation in the determination of epithelial membrane polarity. J. Tiss. Cult. Methods 14:173–180; 1992.

    Article  Google Scholar 

  • Guillomot, M.; Flechon, J.-E.; Wintenberger-Torres, S. Conceptus attachment in the ewe: an ultrastructural study. Placenta 2:169–182; 1981.

    PubMed  CAS  Google Scholar 

  • Johnson, G. A.; Bazer, F. W.; Jaeger, L. A.; Ka, H.; Pfarrer, C.; Spencer, T. E.; Burghardt, R. C. Muc-1, integrin, and osteopontin expression during the implantation cascade in sheep. Biol. Reprod. 65:820–828; 2001b.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, G. A.; Burghardt, R. C.; Newton, G. R.; Bazer, F. W.; Spencer, T. E. Development and characterization of immortalized ovine endometrial cell lines. Biol. Reprod. 61:1324–1330; 1999a.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, G. A.; Spencer, T. E.; Burghardt, R. C.; Bazer, F. W. Ovine osteopontin. I. Cloning and expression of messenger ribonucleic acid in the uterus during the periimplantation period. Biol. Reprod. 61:884–891; 1999b.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, G. A.; Spencer, T. E.; Burghardt, R. C.; Joyce, M. M.; Bazer, F. W. Interferon-tau and progesterone regulate ubiquitin cross-reactive protein expression in the ovine uterus. Biol. Reprod. 62:622–627; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, G. A.; Stewart, M. D.; Gray, C. A.; Choi, Y.; Burghardt, R. C.; YuLee, L. Y.; Bazer, F. W.; Spencer, T. E. Effects of the estrous cycle, pregnancy, and interferon tau on 2′,5′-oligoadenylate synthetase expression in the ovine uterus. Biol. Reprod. 64:1392–1399; 2001a

    Article  PubMed  CAS  Google Scholar 

  • Jones, C. J. P.; Fazleabas, A. T.; McGinlay, P. B.; Aplin, J. D. Cyclic modulation of epithelial glycosylation in human and baboon (Papio anubis) endometrium demonstrated by the binding of the agglutinin from Dolichos biflorus. Biol. Reprod. 58:20–27; 1999.

    Article  Google Scholar 

  • Kelly, R. J.; Rouquier, S.; Giorgi, D.; Lennon, G. G.; Lowe, J. B. Sequence and expression of a candidate for the human Secretor blood group alpha(1,2)-fucosyltransferase gene (FUT2): homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J. Biol. Chem. 270:4640–4649; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Kimber, S. J. Carbohydrates as low affinity binding agents involved in initial attachment of mammalian embryos at implantation. In: Ward, R. H. T.; Smith, S. K.; Donnai, D., ed. Early fetal growth and development. London: Royal College of Obstetricians and Gynaecologists Press; 1994;75–102.

    Google Scholar 

  • Kimber, S. J.; Illingworth, I. M.; Glasser, S. R. Expression of carbohydrate antigens in the rat uterus during early pregnancy and after ovariectomy and steroid replacement therapy. J. Reprod. Fertil. 103:75–87; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Kimber, S. J.; Lindenberg, S. Hormonal control of a carbohydrate epitope involved in implantation in mice. J. Reprod. Immunol. 89:13–21; 1990.

    CAS  Google Scholar 

  • King, G. J.; Atkinson, B. A.; Robertson, H. A. Implantation and early placentation in domestic ungulates. J. Reprod. Fertil. 31 (Suppl.):17–30; 1982.

    CAS  Google Scholar 

  • Labarca, C.; Paigen, K. A simple, rapid and sensitive DNA assay procedure. Anal. Biochem. 102:344–352; 1980.

    Article  PubMed  CAS  Google Scholar 

  • Larsen, R. D.; Ernst, L. K.; Nair, R. P.; Lowe, J. B. Molecular cloning sequence, and expression of a human GDP-l-fucose: beta-d-galactoside 2-alpha-l-fucosyltransferase cDNA that can form the H blood group antigen. Proc. Natl. Acad. Sci. USA 87:6674–6678; 1990.

    Article  PubMed  CAS  Google Scholar 

  • Lindenberg, S.; Pedersen, B.; Hamberger, H.; Kimber, S. Models for human implantation derived from implantation in vitro. Reprod. Fertil. Dev. 4:653–670; 1992.

    Article  Google Scholar 

  • Lindenberg, S.; Sundberg, K.; Kimber, S. J.; Lundblad, A. The milk oligosaccharide lacto-N fuctopentose I inhibits attachment of mouse blastocysts on endometrial monolayers. J. Reprod. Fertil. 83:149–158; 1988.

    Article  PubMed  CAS  Google Scholar 

  • Masuda, T.; Saito, H.; Kaneko, F., et al. Up-regulation of E-cadherin and I-catenin in human hepatocellular carcinoma cell lines by sodium butyrate and interferon-alpha. In Vitro Cell. Dev. Biol. 36A:387–394; 2000.

    Article  Google Scholar 

  • Newton, G. R.; Weise, D. W.; Bowen, J. A.; Woldesenbet, S.; Burghardt, R. C. Regulation of protein and prostaglandin secretion in polarized primary cultures of caprine uterine epithelial cells. In Vitro Cell. Dev. Biol. 34A:578–584; 1998.

    Google Scholar 

  • Ott, T. L.; Yin, J.; Wiley, A. A., et al. Effects of the estrous cycle and early pregnancy on uterine expression of Mx protein in sheep (Ovis aries). Biol. Reprod. 59:784–794; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Poirer, F.; Kimber, S. J. Cell surface carbohydrates and lectins in early development. Mol. Hum. Reprod. 3:907–918; 1997.

    Article  Google Scholar 

  • Powell, J. K.; Glasser, S. R.; Woldesenbet, S.; Burghardt, R. C.; Newton, G. R. Expression of carbohydrate antigens in the goat uterus during early pregnancy and on steroid treated polarized uterine epithelial cells in vitro. Biol. Reprod. 62:277–284; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Pru, J. K.; Austin, K. J.; Hass, A. L.; Hansen, T. R. Pregnancy and interferon-τ upregulate gene expression of members of the 1–8 family in the bovine uterus. Biol. Reprod. 65:1471–1480; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Ravn, V.; Teglbjaerg, C. S.; Mandel, U.; Dabelsteen, E. The distribution of type-1 chain ABO and related histo-blood group antigens in the normal cycling human endometrium. Int. J. Gynecol. Pathol. 12:70–79; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Riccioli, A.; Filippini, A.; De Cesaris, P.; Barbacci, E.; Stefanini, M.; Starace, G.; Ziparo, E. Inflammatory mediators increase surface expression of integrin ligands, adhesion to lymphocytes, and secretion of interleukin 6 in mouse sertoli cells. Proc. Natl. Acad. Sci. USA 92:5808–5812; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Rouquier, S.; Lowe, J. B.; Kelly, R. J.; Fertitta, A. L.; Lennon, G. G.; Giorgi, D. Molecular cloning of a human genomic region containing the H blood group alpha(1,2)-fucosyltransferase gene and two H locus-related DNA restriction fragments. Isolation of a candidate for the human Secretor blood group locus. J. Biol. Chem. 270:4632–4639; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Sidhu, S. S.; Kimber, S. J. Hormonal control of H-type α(1–2)fucosyltransferase messenger ribonucleic acid in the mouse uterus. Biol. Reprod. 60:147–157; 1999.

    Article  PubMed  CAS  Google Scholar 

  • Spencer, T. E.; Bazer, F. W. Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in ovine endometrium. Endocrinology 137:1144–1147; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Staggs, K. L.; Austin, K. J.; Johnson, G. A.; Teixeira, M. G.; Talbott, C. T.; Dooley, V. A.; Hansen, T. R. Complex induction of bovine uterine proteins by interferon-tau. Biol. Reprod. 59:293–297:1998.

    Article  PubMed  CAS  Google Scholar 

  • Steel, R. G. D.; Torrie, J. H. Principles and procedures of statistics, a biometrical approach. New York: McGraw-Hill; 1980.

    Google Scholar 

  • Stewart, D. M.; Johnson, G. A.; Vyhlidal, C. A.; Burghardt, R. C.; Safe, S. H.; Yu-Lee, L. Y.; Bazer, F. W.; Spencer, T. E. Interferon-tau activates multiple signal transducer and activator of transcription proteins and has complex effects on interferon-responsive gene transcription in ovine endometrial epithelial cells. Endocrinology 142:98–107; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Surveyor, G. A.; Gendler, S. J.; Pemberton, L., et al. Expression and steroid hormonal control of Muc 1 in the mouse uterus. Endocrinology 136:3639–3647; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, A. J.; Greer, M. R.; Young, A.; Boswell, J. F.; Telfer, J. F.; Cameron, I. T.; Norman, J. E.; Campbell, S. Expression of intracellular adhesion molecules ICAM-1 and ICAM-2 in human endometrium: regulation by interferon-γ. Mol. Human Reprod. 5:64–70; 1999.

    Article  Google Scholar 

  • Todd, I.; McElveen, J. E.; Lamming, G. E. Ovine trophoblast interferon enhances MHC class I expression by sheep endometrial cells. J. Reprod. Immunol. 37:117–123; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Wango, E. O.; Wooding, F. B. P.; Heap, R. B. The role of trophoblast binucleate cells in implantation in the goat: a morphological study. J. Anat. 171:241–257; 1990.

    PubMed  CAS  Google Scholar 

  • Watkins, W. M. Biochemistry and genetics of the ABO, Lewis, and P blood group systems. In: Harris, H; Hirschhorn, K., ed. Advances in human genetics, vol. 10. New York: Plenum Press; 1986:1–136.

    Google Scholar 

  • Weitlauf, H. M. Biology of implantation. In: Knobile, E.; Neill, J. D., ed. The physiology of reproduction, vol. 1. New York: Raven Press; 1994:391–440.

    Google Scholar 

  • White, S.; Kimber, S. J. changes in α(1–2)-fucosyltransfersase activity in the murine endometrial epithelium during the estrous cycle, early pregnancy, and after ovariectomy and hormone replacement. Biol. Reprod. 50:73–81; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Woldesenbet, S.; Garcia, R.; Newton, G. R. Potential lectin-like receptors for endometrial H-type 1 antigen on goat conceptuses. Biol. Reprod. 64 (Suppl. 1):183; 2001.

    Google Scholar 

  • Wooding, F. B. Current topic: the synepitheliochorial placenta of ruminants: binucleate cell fusion and hormone production. Placenta 13:101–113; 1992.

    PubMed  CAS  Google Scholar 

  • Wooding, F. B. P.; Staples, L. D. Functions of the trophoblast papillae and binucleate cells in implantation in the sheep. J. Anat. 133:110–112; 1981.

    Google Scholar 

  • Yamagata, T.; Yamakazi K. Implanting mouse blastocysts stain with LNF-1 bearing fluorescent probe at their mural trophectoderm side. Biochem. Biophys. Res. Commun. 181:1004–1009; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, M. Z.; Kojima, N.; Stroud, M. R.; Hacomori, S.; Fenderson, B. A. Monoclonal antibody directed to Ley oligosaccharide inhibits implantation in the mouse. Biol. Reprod. 52:903–912; 1995.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cooperative Agricultural Research Center, Prairie View A&M University, P.O. Box 4079, 7446-4079, Prairie View, Texas

    S. Woldesenbet, T. Green & G. R. Newton

Authors
  1. S. Woldesenbet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G. R. Newton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. R. Newton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Woldesenbet, S., Green, T. & Newton, G.R. H-type 1 carbohydrate antigen expression by ovine endometrial cells. In Vitro Cell.Dev.Biol.-Animal 38, 358–364 (2002). https://doi.org/10.1290/1071-2690(2002)038<0358:HTCAEB>2.0.CO;2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1290/1071-2690(2002)038<0358:HTCAEB>2.0.CO;2

Key words

Search

Navigation