Immune system cooperatively supports endocrine system-primed embryo implantation

Journal of Mammalian Ova Research

Volumn 26, Issue 3, 2009, Pages 122-128

  Fujiwara, Hiroshi ^a   Ideta, Atsushi ^b   Araki, Yoshihiko ^c   Takao, Yumi ^a   Sato, Yukiyasu ^a   Tsunoda, Noboru ^d   Aoyagi, Yoshito ^b   Konishi, Ikuo ^a  

^a KYOTO UNIVERSITY   (Japan)

^b Zen noh Embryo Transfer Center   (Japan)

^c JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d Shadai Corporation   (Japan)

Author keywords

Embryo implantation; Immune system; Maternal recognition; PBMC; Zona pellucida

Indexed keywords

EID: 77749291939     PISSN: 13417738     EISSN: 13475878     Source Type: Journal    
DOI: 10.1274/jmor.26.122     Document Type: Review

References (33)

1. Achache, H. and Revel, A. (2006): Endometrial receptivity markers, the journey to successful embryo implantation. Hum. Reprod. Update., 12, 731-746.
2. Horcajadas, J.A., Pellicer, A. and Simón, C. (2007): Wide genomic analysis of human endometrial receptivity: new times, new opportunities. Hum. Reprod. Update., 13, 77-86.
3. Boyd, J.D. and Hamilton, W.J. (1970): The Human Placenta, W. Heffer & Sons Ltd, Cambridge, UK.
4. Sugihara, K., Sugiyama, D., Byrne, J., Wolf, D.P., Lowitz, K.P., Kobayashi, Y., Kabir-Salmam, M., Nadano, D., Aoki, D., Nozawa, S., Nakayama, J., Mustelin, T., Ruoslahti, E., Yamaguchi, N. and Fukuda, M.N. (2007): Trophoblast cell activation by trophinin ligation is implicated in human embryo implantation. Proc. Natl. Acad. Sci. USA, 104, 3799-3804.
5. Fujiwara, H., Tatsumi, K., Kosaka, K., Sato, Y., Higuchi, T., Yoshioka, S., Maeda, M., Ueda, M. and Fujii, S. (2003): Human blastocysts and endometrial epithelial cells express activated leukocyte cell adhesion molecule (ALCAM/ CD166). J. Clin. Endocrinol. Metab., 88, 3437-3443.
6. Norman, R.J., Buck, R.H., Kemp, M.A. and Joubert, S.M. (1988): Impaired corpus luteum function in ectopic pregnancy cannot be explained by altered human chorionic gonadotropin. J. Clin. Endocrinol. Metab., 66, 1166-1170.
7. Quagliarello, J., Goldsmith, L., Steinetz, B., Lustig, D.S. and Weiss, G. (1980): Induction of relaxin secretion in nonpregnant women by human chorionic gonadotropin. J. Clin. Endocrinol. Metab., 51, 74-77.
8. Kratzer, P.G. and Taylor, R.N. (1990): Corpus luteum function in early pregnancies is primarily determined by the rate of change of human chorionic gonadotropin levels. Am. J. Obstet. Gynecol., 163,1497-1502.
9. Johnson, M.R., Bolton, V.N., Riddle, A.F., Sharma, V., Nicolaides, K., Grudzinskas, J.G. and Collins, W.P. (1993): Interactions between the embryo and corpus luteum. Hum. Reprod., 8, 1496-1501.
10. Hattori, N., Ueda, M., Fujiwara, H., Fukuoka, M., Maeda, M. and Mori, T. (1995): Human luteal cells express leukocyte functional antigen (LFA)-3. J. Clin. Endocrinol. Metab., 80, 78-84.
11. Hashii, K., Fujiwara, H., Yoshioka, S., Kataoka, N., Yamada, S., Hirano, T., Mori, T., Fuju, S. and Maeda, M. (1998): Peripheral blood mononuclear cells stimulate progesterone production by luteal cells derived from pregnant and non-pregnant women: possible involvement of interleukin-4 and interleukin-10 in corpus luteum function and differentiation. Hum. Reprod., 13, 2738-2744.
12. Fujiwara, H. (2006): Hypothesis: immune cells contribute to systemic cross-talk between the embryo and mother during early pregnancy in cooperation with the endocrine system. Reprod. Med. Biol., 5, 19-29.
13. Takabatake, K., Fujiwara, H., Goto, Y., Nakayama, T., Higuchi, T., Fujita, J., Maeda, M. and Mori, T. (1997): Splenocytes in early pregnancy promote embryo implantation by regulating endometrial differentiation in mice. Hum. Reprod., 12,2102-2107.
14. Dey, S.K. (1996): Implantation. In: Reproductive Endocrinology, Surgery, and Technology (Adashi, E.Y., et al., eds.), pp. 421-134, Lippincott-Raven, Philadelphia.
15. Takabatake, K., Fujiwara, H., Goto, Y., Nakayama, T., Higuchi, T., Maeda, M. and Mori, T. (1997): Intravenous administration of splenocytes in early pregnancy changes the implantation window in mice. Hum. Reprod., 12, 583-585.
16. Wakuda, K., Takakura, K., Nakamshi, K., Kita, N., Shi, H., Hirose, M. and Noda, Y. (1999): Embryo-dependent induction of embryo receptivity in the mouse endometrium. J. Reprod. Fertil., 115, 315-324.
17. Fujita, K., Nakayama, T., Takabatake, K., Higuchi, T., Fujita, J., Maeda, M., Fujiwara, H. and Mori, T. (1998): Administration of thymocytes derived from non-pregnant mice induces an endometrial receptive stage and leukaemia inhibitory factor expression in the uterus. Hum. Reprod., 13, 2888-2894.
18. Blois, S.M., Kammerer, U., Alba Soto, C., Tometten, M.C., Shaikly, V., Barnentos, G., Jurd, R., Rukavina, D., Thomson, A.W., Klapp, B.F., Fernández, N. and Arck, P.C. (2007): Dendritic cells: key to fetal tolerance? Biol. Reprod., 277, 590-598.
19. Florman, H.M. and Ducibella, T. (2006): Fertilization in mammals. In: Knobil and Neill's Physiology of Reproduction (Neill, J.D., ed.), pp. 55-112, Elsevier Academic Press, St Louis.
20. Monné, M., Han, L. and Jovine, L. (2006): Tracking down the ZP domain: from the mammalian zona pellucida to the molluscan vitelline envelope. Semin. Reprod. Med., 24, 204-216.
21. Fujiwara, H., Araki, Y. and Toshimori, K. (2009): Is the zona pellucida an intrinsic source of signals activating maternal recognition of the developing mammalian embryo? J. Reprod. Immunol., 81, 1-8.
22. Nakayama, T., Fujiwara, H., Maeda, M., Inoue, T., Yoshioka, S., Mori, T. and Fujii, S. (2002): Human peripheral blood mononuclear cells (PBMC) in early pregnancy promote embryo invasion in vitro: HCG enhances the effects of PBMC. Hum. Reprod., 17, 207-212.
23. Egawa, H., Fujiwara, H., Hirano, T., Nakayama, T., Higuchi, T., Tatsumi, K., Mori, T. and Fujii, S. (2002): Peripheral blood mononuclear cells in early pregnancy promote invasion of human choriocarcinoma cell line, BeWo cells. Hum. Reprod., 17, 473-180.
24. Adcock, Ew. 3d., Teasdale, T., August, C.S., Cox, S., Meschia, G., Ballaglia, T.C. and Naughton, M.A. (1973): Human chorionic gonadotropin: its possible role in maternal lymphocyte suppression. Science, 181, 845-847.
25. Muchmore, A.V. and Blaese, R.M. (1977): Immunoregulatory properties of fractions from human pregnancy urine: evidence that human chorionic gonadotropin is not responsible. J. Immunol., 118, 881-886.
26. Morse, J.H., Ehrlich, P.H. and Canfield, R.E. (1982): Extracts of pregnancy urine contain a mitogen for human peripheral blood lymphocytes (PBL). J. Immunol., 128, 2187-2193.
27. Kosaka, K., Fujiwara, H., Tatsumi, K., Yoshioka, S., Sato, Y., Egawa, H., Higuchi, T., Nakayama, T., Ueda, M., Maeda, M. and Fujii, S. (2002): Human chorionic gonadotropin (HCG) activates monocytes to produce interleukin-8 via a different pathway from luteinizing hormone/HCG receptor system. J. Clin. Endocrinol. Metab., 87, 5199-5208.
28. Rockwell, L.C., Pillai, S., Olson, C.E. and Koos, R.D. (2002): Inhibition of vascular endothelial growth factor/ vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol. Reprod., 67, 1804-1810.
29. Rowe, A.J., Wulff, C. and Fraser, H.M. (2003): Localization of mRNA for vascular endothelial growth factor (VEGF), angiopoietins and their receptors during the pen-implantation period and early pregnancy in marmosets (Callithnx jacchus). Reproduction, 126, 227-238.
30. McMaster, M.T., Dey, S.K. and Andrews, G.K. (1993): Association of monocytes and neutrophils with early events of blastocyst implantation in mice. J. Reprod. Fertil., 99, 561-569.
31. Handschuh, K., Guibourdenche, J., Tsatsaris, V., Guesnon, M., Laurendeau, I., Evain-Brion, D. and Fournier, T. (2007): Human chorionic gonadotropin produced by the invasive trophoblast but not the villous trophoblast promotes cell invasion and is down-regulated by peroxisome proliferator-activated receptor-γ. Endocrinology, 148, 5011-5019.
32. Kosaka, K., Fujiwara, H., Tatsumi, K., Yoshioka, S., Higuchi, T., Sato, Y., Nakayama, T. and Fujii, S. (2003): Human peripheral blood mononuclear cells enhance cell-cell interaction between human endometrial epithelial cells and BeWo-cell spheroids. Hum. Reprod., 18, 19-25.
33. Yoshioka, S., Fujiwara, H., Nakayama, T., Kosaka, K., Mori, T. and Fujii, S. (2006): Intrauterine administration of autologous peripheral blood mononuclear cells promotes implantation rates in patients with repeated failure of IVF-embryo transfer. Hum. Reprod., 21, 3290-3294.