Skip to main content
SpringerLink
Log in

Eutopic Endometrium From Women With Endometriosis Shows Altered Ultrastructure and Glycosylation Compared to That From Healthy Controls—A Pilot Observational Study

  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

Endometrial curettings from a cohort of 24 women with endometriosis were compared with matched biopsies from 14 healthy, fertile women and examined for ultrastructural changes and the secretion of glycans bound by the lectin from Dolichos biflorus. Ultrastructural analysis of glandular endometrial tissue from women with stages I to III endometriosis showed heterogeneous responses to the disease, biopsies often showing a mixture of features, combining delays in the maturation sequence with characteristics of later phenotypes particularly in the mid-late secretory phase of the menstrual cycle. Expression of glycans bound by Dolichos biflorus agglutinin was very variable in these cases but generally matched the observed ultrastructure. Biopsies from women with stage IV endometriosis showed immature gland morphology later in the cycle and also failed to express Dolichos biflorus agglutinin—binding glycans, suggesting an association between histological and biochemical function in advanced disease states. These findings may explain in part endometriosis-associated subfertility as blastocyst attachment is intimately associated with appropriate glycosylation and gland morphology.

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

  1. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. 1997;24:235–258.

    Article  CAS  PubMed  Google Scholar 

  2. Gruppo Italiano Per lo Studio Dell’endometriosi. Prevalence and anatomical distribution of endometriosis in women with selected gynecological conditions: results from a multicentric Italian study. Hum Reprod. 1994;9:1158–1162.

    Article  Google Scholar 

  3. Awwad JT, Sayegh RA, Tao XJ, Hassan T, Awwas ST, Isaacson K. The SCID mouse: an experimental model for endometriosis. Hum Reprod. 1999;14:3107–3111.

    Article  CAS  PubMed  Google Scholar 

  4. Rossi G, Somigliana E, Moschetta M, et al. Dynamic aspects of endometriosis in a mouse model through analysis of implantation and progression. Arch Gynecol Obstet. 2000;263:102–107.

    Article  CAS  PubMed  Google Scholar 

  5. D’Hooghe TM. Clinical relevance of the baboon as a model for the study of endometriosis. Fertil Steril. 1997;68:613–625.

    Article  PubMed  Google Scholar 

  6. Fazleabas AT, Brudney A, Gurates B, Chai D, Bulun S. A modified baboon model for endometriosis. Ann N Y Acad Sci USA. 2002;55:308–317.

    Article  Google Scholar 

  7. D’Hooghe TM, Bambra CS, Raeymaekers SCM, De Jonge I, Lauweryns JM, Koninckx PR. Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus and Papio anubis). Am J Obstet Gynecol. 1995;173:125–134.

    Article  PubMed  Google Scholar 

  8. D’Hooghe TM, Riday AM, Bambra CS, Suleman MA, Raeymaekers SCM, Koninckx PR. The cycle pregnancy rate is normal in baboons with stage I endometriosis but decreased in primates with stage II and III-IV disease. Fertil Steril. 1996;66:809–813.

    Article  PubMed  Google Scholar 

  9. Gashaw I, Hastings JM, Jackson K, Winterhager E, Fazleabas AT. Induced endometriosis in baboons (Papio anu-bis) increases the expression of the proangiogenic factor Cyr61 (CCN1) in the eutopic and ectopic endometria. Biol Reprod. 2006;74:1060–1066.

    Article  CAS  PubMed  Google Scholar 

  10. Hastings JM, Jackson KS, Mavrogianis PA, Fazleabas AT. The estrogen early response gene, FOS, is altered in a baboon model of endometriosis. Biol Reprod. 2006;75:176–182.

    Article  CAS  PubMed  Google Scholar 

  11. Kim JJ, Taylor HS, Lu Z, et al. Alterations in HOXA10 expression in endometriosis: potential role in decidualization. Mol Hum Reprod. 2007;13:323–332.

    Article  CAS  PubMed  Google Scholar 

  12. Jones CJP, Denton J, Fazleabas AT. Morphological and glyco-sylation changes associated with the endometrium and ectopic lesions in a baboon model of endometriosis. Hum Reprod. 2006;21:3068–3080.

    Article  CAS  PubMed  Google Scholar 

  13. Baker DA, Sugii S, Kabat EA, Ratcliffe RM, Hermentin P, Lemieux RU. Immunochemical studies on the combining sites of Forssman hapten reactive hemagglutinins from Dolichos biflorus, Helix pomatia and Wistaria floribunda. Biochemistry. 1983;22:2741–2750.

    CAS  PubMed  Google Scholar 

  14. American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis. Fertil Steril. 1996;67:817–821.

    Article  Google Scholar 

  15. Weibel ER. Stereological Methods. Vol 1: Practical Methods for Biological Morphometry. London: Academic Press; 1979.

  16. Reed MG, Howard CV. Surface weighted star-volume: concept and estimation. J Microsc. 1998;190:350–356.

    Article  CAS  PubMed  Google Scholar 

  17. Gundersen HJG, Jensen EB. Stereological estimation of the volume-weighted mean volume of arbitrary particles observed on random sections. J Microsc. 1985;138:27–142.

    Article  Google Scholar 

  18. Maddox PH, Jenkins D. 3’Aminopropyltriethoxysilane (APES): a new advance in section adhesion. J Clin Pathol. 1987;40:1256–1260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jones CJP, Mosley S, Jeffrey IJM, Stoddart RW. Elimination of the non-specific binding of avidin to tissue sections. Histo-chem J. 1987;19:264–268.

    CAS  Google Scholar 

  20. Armstrong EM, More IAR, McSeveney D, Chatfield WR. Reappraisal of the ultrastructure of the human endometrial gland cell. J Obs Gyn Brit Comm. 1973;80:446–460.

    Article  CAS  Google Scholar 

  21. Gordon M. Cyclic changes in the fine structure of the epithelial cells of human endometrium. Int Rev Cytol. 1975;42:127–172.

    Article  CAS  PubMed  Google Scholar 

  22. Cornillie FJ, Lauweryns JM, Brosens IA. Normal human endometrium—an ultrastructural survey. Gynecol Obstet Invest. 1985;20:113–129.

    Article  CAS  PubMed  Google Scholar 

  23. Dockery P, Li TC, Rogers AW, Cooke ID, Lenton EA. The ultrastructure of the glandular epithelium in the timed endo-metrial biopsy. Hum Reprod. 1988;3:826–834.

    Article  CAS  PubMed  Google Scholar 

  24. Dockery P, Burke MJ. The fine structure of the mature human endometrium. In: Aplin JD, Fazleabas AT, Glasser SR, Guidice LC, eds. The Endometrium. 2nd ed. London: Informa Healthcare; 2008:46–65.

    Chapter  Google Scholar 

  25. Burney RO, Talbi S, Hamilton AE, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007;148:3814–3826.

    Article  CAS  PubMed  Google Scholar 

  26. Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE. Progesterone receptor isoform A but not B is expressed in endo-metriosis. J Clin Endocrinol Metab. 2000;85:2897–2902.

    CAS  PubMed  Google Scholar 

  27. Zeitoun KM, Takayama K, Sasano H, et al. Deficient 17ß-hydroxysteroid dehydrogenase type 2 expression in endometriosis: failure to metabolize 17ß-estradiol. J Clin Endocrinol Metab. 1998;83:4474–4480.

    CAS  PubMed  Google Scholar 

  28. Hudelist G, Czerwenka K, Keckstein J, et al. Expression of aromatase and estrogen sulfotransferase in eutopic and ectopic endometrium: evidence for unbalanced estradiol production in endometriosis. Reprod Sci. 2007;14:798–805.

    Article  CAS  PubMed  Google Scholar 

  29. Cooke PS, Buchanan DL, Lubahn DB, Cunha GR. Mechanism of estrogen action: lessons from the estrogen receptor-α knockout mouse. Biol Reprod. 1998;59:470–475.

    Article  CAS  PubMed  Google Scholar 

  30. Matsuzaki S, Murakami T, Uehara S, Canis M, Sasano H, Okamura K. Expression of estrogen receptor alpha and beta in peritoneal and ovarian endometriosis. Fertil Steril. 2001;75:1198–1205.

    Article  CAS  PubMed  Google Scholar 

  31. Kao LC, Germeyer A, Tulac S, et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology. 2003;144:2870–2881.

    Article  CAS  PubMed  Google Scholar 

  32. Wang C, Mavrogianis PA, Fazleabas AT. Endometriosis is associated with progesterone-resistance in the oviduct: evidence based on the localization of oviductal glycoprotein 1 (OVGP1). Biol Reprod. 2009;80:272–278.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Jackson KS, Brudney A, Hastings JM, Mavrogianis PA, Kim JJ, Fazleabas AT. The altered distribution of the steroid hormone receptors and the chaperone immunophilin FKBP52 in a baboon model of endometriosis is associated with progesterone resistance during the window of uterine receptivity. Reprod Sci. 2007;14:137–150.

    Article  CAS  PubMed  Google Scholar 

  34. Bulun SE, Cheng YH, Yin P, et al. Progesterone resistance in endometriosis: link to failure to metabolize estradiol. Mol Cell Endocrinol. 2006;248:94–103.

    Article  CAS  PubMed  Google Scholar 

  35. Meresman GF, Vighi S, Buquet RA, Contreras-Ortiz O, Tesone M, Rumi LS. Apoptosis and expression of bcl–2 and bax in eutopic endometrium from women with endometrio-sis. Fertil Steril. 2000;74:760–766.

    Article  CAS  PubMed  Google Scholar 

  36. Johnson MC, Torres M, Alves A, et al. Augmented cell survival in eutopic endometrium from women with endometriosis: expression of c-myc, TGF-beta1 and bax genes. Reprod Biol Endocrinol. 2005;3:45; doi:10.1186/ 1477–7827–3–45.

    Article  Google Scholar 

  37. Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod. 2003;18:157–161.

    Article  PubMed  Google Scholar 

  38. Abbott JA, Hawe J, Clayton RD, Garry R. The effects and effectiveness of laparoscopic excision of endometriosis: a prospective study with 2–5 year follow-up. Hum Reprod. 2003;18:1922–1927.

    Article  CAS  PubMed  Google Scholar 

  39. Heilier JF, Nackers F, Verougstraete V, Tonglet R, Lison D, Donnez J. Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometrio-tic (adenomyotic) nodules. Fertil Steril. 2005;84:305–312.

    Article  CAS  PubMed  Google Scholar 

  40. Aplin JD, Jones CJP, McGinlay PB, Croxatto HB, Fazleabas AT. Progesterone regulates glycosylation in endometrium. Biochem Soc Trans. 1997;25:1184–1187.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Maternal and Fetal Health Research Centre, School of Clinical and Laboratory Science, University of Manchester, Manchester, United Kingdom

    Carolyn J. P. Jones PhD & Luciano G. Nardo MD

  2. Department of Human and Clinical Anatomy, Sultan Qaboos University Hospital, Sultanate of Oman, United Kingdom

    Ibrahim M. Inuwa PhD

  3. Department of Reproductive Medicine, St Mary’s Hospital, Manchester, United Kingdom

    Luciano G. Nardo MD

  4. Department of Obstetrics and Gynaecology, University of Padua, Italy

    Pietro Litta MD

  5. Department of Obstetrics and Gynecology, University of Illinois at Chicago, Illinois, Chicago, USA

    Asgerally T. Fazleabas

  6. Research Floor, Maternal and Fetal Health Research Group, University of Manchester, St Mary’s Hospital, Hathersage Road, Manchester M13 0JH, United Kingdom

    Carolyn J. P. Jones PhD

Authors
  1. Carolyn J. P. Jones PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ibrahim M. Inuwa PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luciano G. Nardo MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pietro Litta MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asgerally T. Fazleabas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carolyn J. P. Jones PhD.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jones, C.J.P., Inuwa, I.M., Nardo, L.G. et al. Eutopic Endometrium From Women With Endometriosis Shows Altered Ultrastructure and Glycosylation Compared to That From Healthy Controls—A Pilot Observational Study. Reprod. Sci. 16, 559–572 (2009). https://doi.org/10.1177/1933719109332825

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1177/1933719109332825

Key words

Search

Navigation