Do circulating blood cells contribute to maternal tissue remodeling and embryo-maternal cross-talk around the implantation period?

Molecular Human Reproduction

Volumn 15, Issue 6, 2009, Pages 335-343

  Fujiwara, Hiroshi ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Corpus luteum; Cross talk; Embryo implantation; Endometrial differentiation; Trophoblast invasion

Indexed keywords

CHEMOKINE; CHORIONIC GONADOTROPIN; GLYCAN; LECTIN; PROGESTERONE; RECOMBINANT CHORIONIC GONADOTROPIN;

ANGIOGENESIS; BLOOD CELL; CELL FUNCTION; CIRCULATION; CORPUS LUTEUM; CYTOKINE PRODUCTION; EMBRYO DEVELOPMENT; ENDOCRINE SYSTEM; FERTILIZATION IN VITRO; FETOPLACENTAL UNIT; HUMAN; IMMUNOREGULATION; LIVE BIRTH; LUTEAL CELL; MOLECULAR INTERACTION; NIDATION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; PROGESTERONE SYNTHESIS; REVIEW; THROMBOCYTE FUNCTION; TROPHOBLAST;

CORPUS LUTEUM; EMBRYO IMPLANTATION; ENDOMETRIUM; FEMALE; HUMANS; LEUKOCYTES, MONONUCLEAR; MODELS, BIOLOGICAL; PREGNANCY; TROPHOBLASTS;

EID: 65549131436     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gap027     Document Type: Review

References (68)

1. Adashi EY. The potential relevance of cytokines to ovarian physiology: the emerging role of resident ovarian cells of the white blood cell series. Endocr Rev 1990;11:454-464.
2. Adcock EW III, Teasdale T, August CS, Cox S, Meschia G, Ballaglia TC, Naughton MA. Human chorionic gonadotropin: Its possible role in maternal lymphocyte suppression. Science 1973;181:845-847.
3. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004;5:266-712.
4. Auletta FJ, Flint APF. Mechanisms controlling corpus luteum function in sheep, cows, nonhuman primates, and women especially in relation to the time of luteolysis. Endocr Rev 1988;9:88-105.
5. Bhatt H, Brunet LJ, Stewart CL. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci USA 1991;88:11408-11412.
6. Bischof P, Campana A. A putative role for oncogenes in trophoblast invasion? Hum Reprod 2000;15(Suppl. 6):51-58.
7. Blois SM, Kammerer U, Alba Soto C, Tometten MC, Shaikly V, Barrientos G, Jurd R, Rukavina D, Thomson AW, Klapp BF et al. Dendritic cells: key to fetal tolerance? Biol Reprod 2007;277:590-598.
8. Boyd JD, Hamilton WJ. The Human Placenta. Cambridge: W. Heffer & Sons Ltd, 1970.
9. Brewer JI. Studies of the human corpus luteum. Am J Obstet Gynecol 1942; 44:1048-1062.
10. Bulmer JN. Cellular constituents of human endometrium in the menstrual cycle and early pregnancy. In: Bronson RA, Alexander NJ, Anderson D, Branch DW, Kutteh WH (eds). Reproductive Immunology. Cambridge: Blackwell Science, 1996, 212-239.
11. Chaouat G, Assal Meliani A, Martal J, Raghupathy R, Elliot J, Mosmann T, Wegmann TG. IL-10 prevents naturally occurring fetal loss in the CBA x DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-τ. J Immunol 1995;154:4261-4268.
12. Chaouat G, Zourbas S, Ostojic S, Lappree-Delage G, Dubanchet S, Ledee N, Martal J. A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy. J Reprod Immunol 2002;53:241-256.
13. Cole LA. Hyperglycosylated hCG. Placenta 2007;28:977-986.
14. Corner GW. The histological dating of the human corpus luteum of menstruation. Am J Anat 1956;98:377-401.
15. Dey SK. Implantation. In: Adashi EY, Rock JA, Rosenwaks Z. (eds). Reproductive Endocrinology, Surgery, and Technology. Philadelphia: Lippincott-Raven, 1996, 421-434.
16. Egawa H, Fujiwara H, Hirano T, Nakayama T, Higuchi T, Tatsumi K, Mori T, Fujii S. Peripheral blood mononuclear cells in early pregnancy promote invasion of human choriocarcinoma cell line, BeWo cells. Hum Reprod 2002;17:473-480.
17. Emi N, Kanzaki H, Yoshida M, Takakura K, Kariya M, Okamoto N, Imai K, Mori T. Lymphocytes stimulate progesterone production by cultured human granulosa luteal cells. Am J Obstet Gynecol 1991;165: 1469-1474.
18. Fujita K, Nakayama T, Takabatake K, Higuchi T, Fujita J, Maeda M, Fujiwara H, Mori T. Administration of thymocytes derived from non-pregnant mice induces an endometrial receptive stage and leukaemia inhibitory factor expression in the uterus. Hum Reprod 1998;13 2888-2894.
19. Fujiwara H. 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 2006;5:19-29.
20. Fujiwara H, Ueda M, Imai K, Fukuoka M, Yasuda K, Takakura K, Suginami H, Kanzaki H, Inoko H, Mori T et al. Human leukocyte antigen-DR is a differentiation antigen for human granulosa cells. Biol Reprod 1993;49:705-715.
21. Fujiwara H, Kataoka N, Honda T, Ueda M, Yamada S, Nakamura K, Suginami H, Mori T, Maeda M. Physiological roles of integrin a6β1 in ovarian functions. Horm Res 1998;50(Suppl. 2):25-29.
22. Fujiwara H, Imai K, Inoue T, Maeda M, Fujii S. Membrane-bound cell surface peptidases in reproductive organs. Endocr J 1999;46 11-25.
23. Fujiwara H, Tatsumi K, Kosaka K, Sato Y, Higuchi T, Yoshioka S, Maeda M, Ueda M, Fujii S. Human blastocysts and endometrial epithelial cells express activated leukocyte cell adhesion molecule (ALCAM/CD166). J Clin Endocrinol Metab 2003;88:3437-3443.
24. Furukawa K, Fujiwara H, Sato Y, Zeng BX, Fujii H, Yoshioka S, Nishi E, Nishio T. Platelet is a novel regulator for neovascularization and luteinization during human corpus luteum formation. Endocrinology 2007;148:3056-3064.
25. Guimond MJ, Wang B, Croy BA. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med 1998;187:217-223.
26. Hamatani T, Daikoku T, Wang H, Matsumoto H, Carter MG, Ko MS, Dey SK. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc Natl Acad Sci USA 2004;101:10326-10331.
27. Handschuh K, Guibourdenche J, Tsatsaris V, Guesnon M, Laurendeau I, Evain-Brion D, Fournier T. 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 2007;148:5011-5019.
28. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I et al Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006;12:1065-1074.
29. Hannan NJ, Jones RL, White CA, Salamonsen LA. The chemokines, CX3CL1, CCL14, and CCL4, promote human trophoblast migration at the feto-maternal interface. Biol Reprod 2006;74:896-904.
30. Hashii K, Fujiwara H, Yoshioka S, Kataoka N, Yamada S, Hirano T, Mori T, Fujii S, Maeda M. 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 1998;13:2738-2744.
31. Hattori N, Ueda M, Fujiwara H, Fukuoka M, Maeda M, Mori T. Human luteal cells express leukocyte functional antigen (LFA)-3. J Clin Endocrinol Metab 1995;80:78-84.
32. Johnson MR, Bolton VN, Riddle AF, Sharma V, Nicolaides K, Grudzinskas JG, Collins WP. Interactions between the embryo and corpus luteum. Hum Reprod 1993;8:1496-1501.
33. Kosaka K, Fujiwara H, Tatsumi K, Yoshioka S, Sato Y, Egawa H, Higuchi T, Nakayama T, Ueda M, Maeda M et al. Human chorionic gonadotropin (HCG) activates monocytes to produce interleukin-8 via a different pathway from luteinizing hormone/HCG receptor system. J Clin Endocrinol Metab 2002;87:5199-5208.
34. Kosaka K, Fujiwara H, Tatsumi K, Yoshioka S, Higuchi T, Sato Y, Nakayama T, Fujii S. Human peripheral blood mononuclear cells enhance cell-cell interaction between human endometrial epithelial cells and BeWo-cell spheroids. Hum Reprod 2003;18:19-25.
35. Kosaka K, Fujiwara H, Yoshioka S, Fujii S. Vascular endothelial growth factor production by circulating immune cells is elevated in ovarian hyperstimulation syndrome. Hum Reprod 2007;22:1647-1651.
36. Kratzer PG, Taylor RN. Corpus luteum function in early pregnancies is primarily determined by the rate of change of human chorionic gonadotropin levels. Am J Obstet Gynecol 1990;163:1497-1502.
37. Krey G, Frank P, Shaikly V, Barrientos G, Cordo-Russo R, Ringel F, Moschansky P, Chernukhin IV, Metodiev M, Fernández N et al. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J Mol Med 2008;86:999-1011.
38. Lea RG, Sandra O. Immunoendocrine aspects of endometrial function and implantation. Reproduction 2007;134:389-404.
39. Matsuyama S, Ohta M, Takahashi M. The critical period in which splenectomy causes functional disorder of the ovary in adult rats. Endocrinol Jpn 1987;34:849-855.
40. McMaster MT, Dey SK, Andrews GK. Association of monocytes and neutrophils with early events of blastocyst implantation in mice. J Reprod Fertil 1993;99:561-569.
41. Morse JH, Ehrlich PH, Canfield RE. Extracts of pregnancy urine contain a mitogen for human peripheral blood lymphocytes (PBL). J Immunol 1982;128:2187-2193.
42. Muchmore AV, Blaese RM. Immunoregulatory properties of fractions from human pregnancy urine: Evidence that human chorionic gonadotropin is not responsible. J Immunol 1977;118:881-886.
43. Murphy BD, Martinuk SD. Equine chorionic gonadotropin. Endocr Rev 1991;12:27-44.
44. Nakayama T, Fujiwara H, Maeda M, Inoue T, Yoshioka S, Mori T, Fujii S. Human peripheral blood mononuclear cells (PBMC) in early pregnancy promote embryo invasion in vitro: HCG enhances the effects of PBMC. Hum Reprod 2002;17:207-212.
45. Nurden AT. Platelets and tissue remodeling: Extending the role of the blood clotting system. Endocrinology 2007;148:3053-3055.
46. Pate JL, Keyes PL. Immune cells in the corpus luteum: Friends or foes? Reproduction 2001;122:665-676.
47. Psychoyos A. The implantation window: Basic and clinical aspects. In: Mori T et al. (eds). Perspectives in Assisted Reproduction. In: Ares Serono Symposia, Rome, 1993, pp. 57-62.
48. Quagliarello J, Goldsmith L, Steinetz B, Lustig DS, Weiss G. Induction of relaxin secretion in nonpregnant women by human chorionic gonadotropin. J Clin Endocrinol Metab 1980;51:74-77.
49. Red-Horse K, Kapidzic M, Zhou Y, Feng KT, Singh H, Fisher SJ. EPHB4 regulates chemokine-evoked trophoblast responses: A mechanism for incorporating the human placenta into the maternal circulation. Development 2005;132:4097-4106.
50. Rockwell LC, Pillai S, Olson CE, Koos RD. Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biol Reprod 2002;67:1804-1810.
51. Rowe AJ, Wulff C, Fraser HM. Localization of mRNA for vascular endothelial growth factor (VEGF), angiopoietins and their receptors during the peri-implantation period and early pregnancy in marmosets (Callithrix jacchus). Reproduction 2003;126:227-238.
52. Saito S. Cytokine cross-talk between mother and the embryo/placenta. J Reprod Immunol 2001;52:15-33.
53. Saito S, Shiozaki A, Sasaki Y, Nakashima A, Shima T, Ito M. Regulatory T cells and regulatory natural killer (NK) cells play important roles in feto-maternal tolerance. Semin Immunopathol 2007;29:115-122.
54. Saito S, Nakashima A, Myojo-Higuma S, Shiozaki A. The balance between cytotoxic NK cells and regulatory NK cells in human pregnancy. J Reprod Immunol 2008;77:14-22.
55. Sato Y, Fujiwara H, Higuchi T, Yoshioka S, Tatsumi K, Maeda M, Fujii S. Involvement of dipeptidyl peptidase IV in extravillous trophoblast invasion and differentiation. J Clin Endocrinol Metab 2002;87 4287-4296.
56. Sato Y, Higuchi T, Yoshioka S, Tatsumi K, Fujiwara H, Fujii S. Trophoblasts acquire a chemokine receptor, CCR1, as they differentiate towards invasive phenotype. Development 2003;130:5519-5532.
57. Sato Y, Fujiwara H, Zeng B-X, Higuchi T, Yoshioka S, Fujii S. Plateletderived soluble factors induce human extravillous trophoblast migration and differentiation: Platelets are a possible regulator of trophoblast infiltration into maternal spiral arteries. Blood 2005;106:428-435.
58. Simón C, Dominguez F, Remohí J, Pellicer A. Embryo effects in human implantation: Embryonic regulation of endometrial molecules in human implantation. Ann NY Acad Sci 2001;943:1-16.
59. Sugino N, Suzuki T, Sakata A, Miwa I, Asada H, Taketani T, Yamagata Y, Tamura H. Angiogenesis in the human corpus luteum: Changes in expression of angiopoietins in the corpus luteum throughout the menstrual cycle and in early pregnancy. J Clin Endocrinol Metab 2005;90 6141-6148.
60. Takabatake K, Fujiwara H, Goto Y, Nakayama T, Higuchi T, Maeda M, Mori T. Intravenous administration of splenocytes in early pregnancy changes the implantation window in mice. Hum Reprod 1997a; 12 583-585.
61. Takabatake K, Fujiwara H, Goto Y, Nakayama T, Higuchi T, Fujita J, Maeda M, Mori T. Splenocytes in early pregnancy promote embryo implantation by regulating endometrial differentiation in mice. Hum Reprod 1997b;12:2102-2107.
62. Vigano P, Gaffuri B, Ragni G, Di Blasio AM, Vignali M. Intercellular adhesion molecule-1 is expressed on human granulosa cells and mediates their binding to lymphoid cells. J Clin Endocrinol Metab 1997; 82:101-105.
63. Wegmann TG. Maternal T cells promote placental growth and prevent spontaneous abortion. Immunol Lett 1988;17:297-302.
64. Woodruff JD, Parmley TH, Kurman RJ. The ovary. In: Woodruff JD, Parmley TH, Kurman RJ (eds), Atlas of Gynecologic Pathology. Philadelphia: Lippincott Co., 1988, 7.1-7.47.
65. Yan Z, Weich HA, Bernart W, Breckwoldt M, Neulen J. Vascular endothelial growth factor (VEGF) messenger ribonucleic acid (mRNA) expression in luteinized human granulosa cells in vitro. J Clin Endocrinol Metab 1993;77:1723-1725.
66. Yen SSC. Endocrine-metabolic adaptations in pregnancy. In: Yen SSC, Jaffe RB (eds). Reproductive Endocrinology, 3rd edn. Philadelphia: Saunders, 1991, 936-981.
67. Yoshinaga K. Review of factors essential for blastocyst implantation for their modulating effects on the maternal immune system. Semin Cell Dev Biol 2008;19:161-169.
68. Yoshioka S, Fujiwara H, Nakayama T, Kosaka K, Mori T, Fujii S. Intrauterine administration of autologous peripheral blood mononuclear cells promotes implantation rates in patients with repeated failure of IVF-embryo transfer. Hum Reprod 2006;21:3290-3294.