Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T16:49:56.943Z Has data issue: false hasContentIssue false
  • English
  • Français

Autologous embryo–cumulus cells co-culture and blastocyst transfer in repeated implantation failures: a collaborative prospective randomized study

Published online by Cambridge University Press:  07 April 2011

M. Benkhalifa ,
A. Demirol ,
T. Sari ,
E. Balashova ,
M. Tsouroupaki ,
Y. Giakoumakis  and
T. Gurgan
M. Benkhalifa*
Affiliation:
ATL R&D Reproductive Biology & Genetics Laboratory, 4 Rue Louis Lormand, 78320 La Verriere, France. Eylau/UNILABS Laboratories, Paris, France.
A. Demirol
Affiliation:
Women's Health Clinic, IVF & Genetics, Ankara, Turkey.
T. Sari
Affiliation:
Women's Health Clinic, IVF & Genetics, Ankara, Turkey.
E. Balashova
Affiliation:
IVF Dept. National Institute of Surgery and Rehabilitation, Moscow, Russia.
M. Tsouroupaki
Affiliation:
Mediterranean Fertility Centre & Genetics Services, Chania, Greece.
Y. Giakoumakis
Affiliation:
Mediterranean Fertility Centre & Genetics Services, Chania, Greece.
T. Gurgan
Affiliation:
Women's Health Clinic, IVF & Genetics, Ankara, Turkey.
*
All correspondence to: Moncef Benkhalifa. ATL R&D Reproductive Biology & Genetics Laboratory, 4 Rue Louis Lormand, 78320 La Verriere, France. Tel: +33 1 30480178. Fax: +33 1 30571934. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In repeated implantation failure, the co-culture of human embryos with somatic cells has been reported to promote the improvement of embryos quality, implantation and pregnancy rate. It was reported that feeder cells can be more beneficial to the oocyte and embryo by detoxifying the culture medium and supporting embryo development via different pathways. In this study, 432 patients, each with a minimum of three repeated implantation failures, were accepted for a prospective randomized study with or without autologous cumulus cell embryo co-culture and transfer at day 3 or day 5–6. We also investigated the expression of leukaemia inhibitor factor (LIF) and platelet activating factor receptor (PAF-R) on day 3 confluent cumulus cells. The statistic analysis of the data showed significant difference of implantation and clinical pregnancy rates between classical culture and day 3 compared with co-culture and day 5–6 transfer. The molecular analysis showed that cumulus cells express the LIF and the PAF-R genes and confirmed the possible positive role of growth factors and cytokines in early embryo development. Embryo co-culture systems with autologous cells can be beneficial in routine in vitro fertilization for embryo selection and implantation improvement. More molecular investigations need to be done to improve elucidation of the complex dialogue between the embryo and feeder cells prior to implantation and to understand the involved biological function and molecular process during embryo development.

Keywords

BlastocystClinical pregnancyCo-cultureImplantation failureLIF gene expressionPAF receptor gene expression
Type
Research Article
Information
Zygote , Volume 20 , Issue 2 , May 2012 , pp. 173 - 180
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamson, E.D. (1993). Activities of growth factors in preimplantation embryos. J. Cell. Biochem. 53, 280–7.CrossRefGoogle ScholarPubMed
Ahmed, A., Dearu, S., Shams, M., Li, X., Sangha, R., Rola-Pleszcynski, M. & Jiang, J. (1998). Localization, quantification and activation of platelet-activating factor receptor in human endometrium during the menstrual cycle: PAF stimulate NO, VEGF and FAK. FASEB J. 12, 831–43.Google Scholar
Bamberger, A.M., Erdmann, I., Jenatschke, S., Bamberger, C. & Schulte, H.M. (1997). Regulation of the human leukemia inhibitory factor (LIF) promoter in HEC-1B endometrial adenocarcinoma cells. Mol. Hum. Reprod. 3, 789–93.CrossRefGoogle ScholarPubMed
Barnette, D.K. & Bavisier, B.D. (1992). Hypotaurine requirement for in vitro development of golden hamster one-cell embryos into morulae and blastocysts, and production of term offspring from in-vitro fertilized ova. Biol. Reprod. 47, 297–304.Google Scholar
Benkhalifia, M., Montjean, D., Cohen-Bacrie, P. & Ménézo, Y. (2010). Imprinting: RNA expression for homocysteine recycling in the human oocyte. Fertil Steril. 93, 1585–90.Google Scholar
Bongso, A., Ng, S., Fong, C. & Ratnam, S. (1991). Cocultures: a new lead in embryo quality improvement for assisted reproduction. Fertil. Steril. 56, 179–91.CrossRefGoogle ScholarPubMed
Carrel, D., Peterson, C., Jones, K., Katasaka, H., Udoff, L., Cornwell, C., Thorp, C., Kuneck, P., Erickson, L. & Campbell, B. (1999). A simplified coculture system using homologous, attached cumulus tissue results in improved human embryo morphology and pregnancy rates during in vitro fertilization. J. Assist. Reprod. Genet. 16, 344–9.Google Scholar
Cecconi, S., Mauro, A., Cappachietti, G., Berardenelli, P., Bernabo, N., Di Vencenzo, A., Mattioli, M. & Barboni, B. (2008). Meiotic maturation of incompetent prepubertal sheep oocytes is induced by paracrine factor(s) released by gonadotropin stimulated oocyte cumulus cells complexes and involves mitogen activated protein kinase activation. Endocrinology 149, 100–7.CrossRefGoogle ScholarPubMed
Chia, C.M., Winston, R.M.L. & Handyside, A. (1993). EGF, TGFalpha and EGFR expression in human preimplantation embryos. Development 121, 297–307.Google Scholar
Croteau, S., Menezo, Y. & Benkhalifa, M. (1995). Transforming growth factors expression in fertilized and parthenogenetic pre-implantation mouse embryos: RNA detection with fluorescent in situ hybridization. Dev. Growth Differ. 37, 433–40.CrossRefGoogle ScholarPubMed
Ebner, T., Moser, M., Sommergrube, M., Shebl, O. & Tews, G. (2006). Incomplete denudation of oocytes prior to ICSI enhances embryo quality and blastocyst development. Hum. Reprod. 21, 2972–7.CrossRefGoogle ScholarPubMed
Edwards, R. (1997). Recent scientific and medical advances in assisted human conception. Int. J. Dev. Biol. 41, 255–62.Google Scholar
Eyheremendy, V., Raffo, F., Papayannis, M., Barnes, G., Granados, C. & Blaquier, J. (2010). Beneficial effect of autologous endometrial cell coculture in patients with repeated implantation failure. Fertil. Steril. 93, 769–73.Google Scholar
Fry, R.C., Batt, P.A., Fairclough, R.J. & Parr, R. (1992).Human leukemia inhibitory factor improves the viability of cultured ovine embryos. Biol. Reprod. 46, 470–4.CrossRefGoogle ScholarPubMed
Fukui, Y., Saito, T., Miyamoto, A., Yamashina, H. & Okamoto, Y. (1994). Effect of leukemia inhibitory factor on in vitro development of bovine morulae. Theriogenology 42, 1133–9.Google Scholar
Gardner, D.K. & Lane, M. (1997). Culture and selection of viable blastocysts: a feasible proposition for human IVF. Hum. Reprod. Update 3, 367–82.CrossRefGoogle ScholarPubMed
Godard, N., Pukazhenthi, B., Wildt, D. & Comizzoli, P. (2009). Paracrine factors from cumulus-enclosed oocytes ensure the successful maturation and fertilization in vitro denuded oocytes in the cat model. Fertil. Steril. 91, 2051–60.Google Scholar
Goodeaux, L.L., Voelkel, S.A., Anzalone, C.A., Ménézo, Y. & Graves, K.H. (1989). The effect of rhesus epithelial cell monolayers on in vitro growth of rhesus embryos. Theriogenology 39, 197–202.Google Scholar
Goovaerts, I., Leroy, J., Van Soon, A., De Clerq, J., Andries, S. & Bols, P. (2009). Effect of cumulus cell coculture and oxygen tension on the in vitro developmental competence of bovine zygotes cultured singly. Theriogenology 71, 729–38.CrossRefGoogle ScholarPubMed
Ho, Y., Doherty, A.S. & Schultz, R.M. (1994). Mouse preimplantation embryo development in vitro: effect of sodium concentration in culture media on RNA synthesis and accumulation and gene expression. Mol. Reprod. Dev. 38, 131–41.CrossRefGoogle ScholarPubMed
Ikeda, S., Saeki, K., Imai, H. & Yamada, M. (2006). Abilities of cumulus and granulosa cells to enhance the developmental cumulus of bovine oocytes during in vitro maturation period are promoted by midkine; a possible implication of its apoptosis suppressing effect. Reproduction 132, 549–57.CrossRefGoogle Scholar
Johnson, J., Higdon, H. & Boone, W. (2008). Effect of cumulus cell coculture using standard culture media on the maturation and fertilization potential of immature human oocyte. Fertil. Steril. 90, 1674–9.Google Scholar
Jung, T. (1989). Protein synthesis and degradation in non-cultured and in vitro cultured rabbit blastocysts. J. Reprod. Fertil. 86, 507–512.CrossRefGoogle ScholarPubMed
Kattal, N., Cohen, J. & Barmat, L. (2008). Role of coculture in human in vitro fertilization. Fertil. Steril. 90, 1069–75.CrossRefGoogle ScholarPubMed
Kauna, S.W. & Matt, D.W. (1995). Coculture cells that express leukemia inhibitory factor enhance mouse blastocyst development in vitro. J. Assist. Reprod. Genet. 12, 153–6.CrossRefGoogle Scholar
Larson, R.C., Ignotz, G.G. & Currie, W.B. (1992). Transforming growth factor β and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle. Mol. Reprod. Dev. 33, 432–5.Google Scholar
Leese, H. (1995). Metabolic control during preimplantation mammalian development. Hum. Reprod. Update 1, 63–72.CrossRefGoogle ScholarPubMed
Levitas, E., Lunenfeld, E., Har-Vardi, I., Albotiano, S., Sonnin, Y., Hackman-Ram, R. & Potashnik, G. (2004). Blastocyst stage embryo transfer in patient who failed to conceive in three or more day 2–3 embryo transfer cycles: a prospective randomised study. Fertil. Steril. 81, 567–71.Google Scholar
Lin, Y., Hwang, J., Seow, K., Huang, L., Chen, H. & Tzeng, C. (2009). Effects of growth factors and granulosa cell co-culture on in-vitro maturation of oocytes. Reprod. Biomed. Online 19, 165–70.CrossRefGoogle ScholarPubMed
Mansoor, R., Aboulghar, M., Serour, G. & Abbas, M. (1994). Co-culture of human pronucleate oocytes with their cumulus cells. Hum. Reprod. 9, 1727–9.Google Scholar
Ménézo, Y., Guérin, J.F. & Czyba, J.C. (1990). Improvement of human early embryo development in vitro by co-culture on monolayers of Vero cells. Biol. Reprod. 42, 301–6.CrossRefGoogle Scholar
Ménézo, Y., Veiga, A. & Benkhalifa, M. (1998). Improved methods for blastocyst formation and culture. Hum. Reprod. 4, 256–65.Google Scholar
Mercader, A., Garcia Valesco, J., Escudero, E., Remohi, J., Pellicie, A. & Simon, C. (2003). Clinical experiences and perinatal outcome of blastocyst transfer after coculture of human embryos with human endometrial epithelial cells: a 5 years follow up study. Fertil. Steril. 80, 1162–8.CrossRefGoogle Scholar
Moulavi, F., Hosseini, H., Ashtiani, S., Shahverdi, A. & Nasr-Esfahani, M. (2006). Can Vero cell coculture improve in vitro maturation of bovine oocytes? Reprod. Biomed. Online 13, 404–11.CrossRefGoogle ScholarPubMed
Munné, S., Howles, CM. & Wells, D. (2009). The role of preimplantation genetic diagnosing embryo aneuploidy. Curr. Opin. Obstet. Gynecol. 21, 442–9.CrossRefGoogle ScholarPubMed
Omar, F. & Vlad, M. (2008). In vitro development of mouse pronuclear embryos to blastocysts in sequential media with and without coculture of autologous cumulus cells. J. Reprod. Dev. 54, 385–90.CrossRefGoogle Scholar
Ouhibi, N., Hamidi, J., Guillaud, J. & Ménézo, Y. (1990). Co-culture of 1-cell mouse embryos on different cell supports. Hum. Reprod. 5, 737–43.CrossRefGoogle ScholarPubMed
Papanikolaou, E., Camus, M., Kolibianakis, E., Van Landuyt, L., Van Steirtegheim, A. & Devroey, P. (2006). In vitro fertilization with single blastocyst stage versus single cleavage stage embryos. N. Engl. J. Med. 354, 1139–46.CrossRefGoogle ScholarPubMed
Papanikolaou, E., Kolibianakis, E., Tournaye, H., Venetis, C., Fatemi, H., Tarlatsi, B. & Devroey, P. (2008). Live birth rates after transfer of equal number of blastocysts or cleavage-stage embryo in IVF. A systematic review and meta-analysis.Hum. Reprod. 23, 91–9.Google Scholar
Parikh, F., Nadkarni, S., Naik, N., Naik, D. & Uttamchandani, S. (2006). Cumulus coculture and cumulus aided embryo transfer increase pregnancy rates in patients undergoing in vitro fertilization. Fertil. Steril. 86, 839–47.CrossRefGoogle ScholarPubMed
Pink, R., Ryan, J. & O'Neil, C. (1990). Antagonist of embryo-derived platelet activating factor act by inhibiting the ability of the mouse embryo to implant. J. Reprod. Fertil. 88, 241–8.Google Scholar
Quinn, P. & Margualit, R. (1996). Beneficial effect of coculture with cumulus cells on blastocyst formation in prospective trial with supernumerary human embryos. J. Assist. Reprod. Genet. 13, 9–12.Google Scholar
Sapandorfer, S., Pascal, P., Parkas, J., Clark, R., Veek, L., Davis, O. & Rosenwaks, Z. (2004). Autologous endometrial coculture in patients with IVF failure: outcome of the first 1030 case. J. Reprod. Med. 49, 463–7.Google Scholar
Van Blerkom, J. (1993). Development of the human embryo to the hatched blastocyst stage in the presence or absence of a monolayer of Vero cells. Hum. Reprod. 8, 1525–39.CrossRefGoogle ScholarPubMed
Veiga, A., Torello, M., Menezo, Y., Busquets, A., Sarrias, O., Coreleu, B. & Barri, P. (1999). Use of coculture of human embryos on vero cells to improve clinical implantation rate. Hum. Reprod. 14, 112–20.Google Scholar
Vlad, M., Walker, D. & Kennedy, R.C. (1986). Nuclei number in human embryos co-cultured with human ampullary cells. Hum. Reprod. 11, 1678–86.CrossRefGoogle Scholar
Watson, A.J., Hogan, E., Hahnel, A., Wiemer, K. & Schultz, G. (1992). Expression of growth factor ligand and receptor genes in the preimplantation bovine embryo. Mol. Reprod. Dev. 31, 87–95.CrossRefGoogle ScholarPubMed