Immune regulation at the interface during early steps of murine implantation: Involvement of two new cytokines of the IL-12 family (IL-23 and IL-27) and of TWEAK

American Journal of Reproductive Immunology

Volumn 59, Issue 4, 2008, Pages 323-338

  Mas, Anne Elisabeth ^a,b,c   Petitbarat, Marie ^a,b,c,d   Dubanchet, Sylvie ^a   Fay, Stephanie ^a,b,c   Ledée, Nathalie ^a,d   Chaouat, Gérard ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c HÔPITAL ANTOINE BÉCLÈRE   (France)

^d CENTRE HOSPITALIER INTERCOMMUNAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 23; INTERLEUKIN 27; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DECIDUA; DISEASE PREDISPOSITION; FEMALE; FETUS RESORPTION; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; MALE; MATING; MOUSE; NATURAL KILLER CELL; NIDATION; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPONTANEOUS ABORTION; SURVIVAL RATE;

ANIMALS; ANTIBODIES, MONOCLONAL; EMBRYO IMPLANTATION; EMBRYO LOSS; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-23; INTERLEUKINS; MALE; MICE; MICE, INBRED STRAINS; NEUTRALIZATION TESTS; PLACENTA; REPRODUCIBILITY OF RESULTS; TIME FACTORS; TUMOR NECROSIS FACTORS; UTERUS;

EID: 40949121120     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2007.00567.x     Document Type: Article

References (59)

1. Chaouat G, Ledée-Bataille N, Dubanchet S, Zourbas S, Sandra O, Martal J: Th1/Th2 paradigP in pregnancy: paradigm lost? (Cytokines in pregnancy/early abortion: Re-examining the Th1/Th2 paradigm). Int Arch Allergy Immunol 2004; 134:93-119.
2. Tranguch S, Daikoku T, Guo Y, Wang H, Dey SK: Molecular complexity in establishing uterine receptivity and implantation. Cell Mol Life Sci 2005; 62:1964-1973.
3. Hoozemans DA, Schats R, Lambalk CB, Homburg R, Hompes PG: Human embryo implantation: Current knowledge and clinical implications in assisted reproductive technology. Reprod Biomed Online 2004; 9:692-715.
4. Laird SM, Tuckerman EM, Li TC: Cytokine expression in the endometrium of women with implantation failure and recurrent miscarriage. Reprod Biomed Online 2006; 13:13-23.
5. Trowsdale J, BetM AG: Mother's little help: mechanisms of fetomaternalm tolerance. Nat Immunol 2006; 7:241-246.
6. Arck P, Merali FS, Stanicz AM, Stead RH, Chaouat G, Manuel J, Clark DA: Stress induced murine abortion associated with substance P dependent alterations in maternal uterine decidua. Biol Reprod 1995; 53:814-820.
7. Szekeres-Bartho J, Barakonyi A, Par G, Polgar B, Palkovics T, Szereday L: Progesterone as an immunomodulatory molecule. Int Immunopharmacol 2001; 1:1037-1048.
8. Robertson SA, Mau VJ, Hudson SN, Tremellen KP: Cytokine leukocyte networks and the establishment of pregnancy. Am J Reprod Immunol 1997; 37:438-443.
9. Drake BL, Head JR: Murine trophoblast can be killed by lymphokine-activated killer cells. J Immunol 1989; 143:9-14.
10. Kinsky R, Delage G, Rosin N, Thang MN, Hoffman M, Chaouat G: A murine model of NK mediated fetal resorption. Am J Reprod Immunol 1990; 23:73-78.
11. Chaouat G: Placental Infiltration of Resorbing CBA × DBA/2 Embryos. Book of Abstracts. Toronto, 6th International Congress Immunology, 1986.
12. Baines M, Fougerolles R: Modulation of natural killer activity influences resorption rates in CBA × DBA/2 matings. J Reprod Immunol 1988; 11:147-153.
13. Gendron R, Baines M: Infiltrating decidual natural killer cells are associated with spontaneous abortion in mice. Cell Immunol 1988; 113:261-267.
14. Wegmann TG, Lin H, Guilbert L, Mosmann TR: Bidirectional cytokine interactions in the maternal-foetal relationship: Is successful pregnancy a TH2 phenomenon?. Immunol Today 1993; 14:353-356.
15. King A, Loke YW: Uterine largeAgranular lymphocytes: a possible role in embryonic implantation?. Am J Obstet Gynecol 1991; 164:702.
16. Guimond MJ, Wang B, Croy BA: Engraftment of bone marrow from severe combined immunodeficiency (SCID) mice reverses the reproductive deficit in Natural Killer cells deficient TgE26 mice. J Exp Med 1998; 187:217-223.
17. Barber EM, Pollard JW: The uterine NK cell population requires IL-15 but these cells are not required for pregnancy nor the resolution of a Listeria monocytogenes infection. J Immunol 2003; 171:37-46.
18. Ostojic S, Dubanchet S, Chaouat G, Abdelkarim M, Truyens C, Capron F: Demonstration of the presence of IL-16, IL-17 and IL-18 at the murine fetomaternal interface during murine pregnancy. Am J Reprod Immunol 2003; 49:101-112.
19. Ledee-Bataille N, Bonnet-Chea K, Hosny G, Dubanchet S, Frydman R, Chaouat G: Role of the endometrial tripod interleukin-18, -15, and -12 in inadequate uterine receptivity in patients with a history of repeated in vitro fertilization-embryo transfer failure. Fertil Steril 2005; 83:598-605.
20. Hayakawa S, Fujikawa T, Fukuoka H, Chisima F, Karasaki-Suzuki M, Ohkoshi E, Ohi H, Kiyoshi FT, Tochigi M, Satoh K, Shimizu T, Nishinarita S, Nemoto N, Sakurai I: Murine fetal resorption and experimental pre-eclampsia are induced by both excessive Th1 and Th2 activation. J Reprod Immunol 2000; 47:121-138.
21. Kachkache M, Acker GM, Chaouat G, Noun A, Garabedian M: Hormonal and local factors control the immuno histochemical distribution of immunocytes in the rat uterus before conceptus implantation: Effects of ovariectomy, fallopian fallopian tube section and RU 486 injection. Biol Reprod 1991; 45:860-865.
22. Sanford TR, De M, Wood G: Expression of colony stimulating factors and inflammatory cytokines in the uterus if CD1 mice during days 1 to days 3 of pregnancy. J Reprod Fertil 1992; 94:213-220.
23. Mac Master MT, Newton RC, Dey SK, Andrews GK: Activation and distribution of inflammatory cells in the mouse uterus during the preimplantation period. J Immunol 1992; 148:1699-1705.
24. Parand M, Chedid L: Protective effects of chlorpromazine against endotoxin induced abortion. Proc Soc Exp Biol Med 1964; 116:906-915.
25. Chaouat G, Assal MA, Martal J, Raghupathy R, John E, Mossmann T, Wegmann TG: Il-10 prevents inflammatory cytokine-mediated foetal death and is inducible by tau interferon. J Immunol 1995; 152:2411-2420.
26. Clark DA, Chaouat G, Arck PC, Mittruecker HW, Levy GA: Cytokine dependent abortion in CBA × DBA/2 mice is mediated by the procoagulant fgl/2 prothrombinase. J Immunol 1998; 160:550-555.
27. Aluvihare VR, Kallikourdis M, Betz AG: Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5:266-271.
28. Oppmann B, Lesley R, Blom B, Timans JC, Xu Y, Hunte B, Vega F, Yu N, Wang J, Singh K, Zonin F, Vaisberg E, Churakova T, Liu M, Gorman D, Wagner J, Zurawski S, Liu Y, Abrams JS, Moore KW, Rennick D, de Waal-Malefyt R, Hannum C, Bazan JF, Kastelein RA: Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000; 13:715-725.
29. Brombacher F, Kastelein RA, Alber G: Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends Immunol 2003; 24:207-212.
30. Trinchieri G, Pflanz S, Kastelein RA: The IL-12 family of heterodimeric cytokines: New players in the regulation of T cell responses. Immunity 2003; 19:641-644.
31. Bell E: TWEAK and TNF: Yin and Yang in innate immunity. Research Highlights in Nat Rev Immunol 2006; 6:91.
32. Volumenie JL, Mognetti B, de Smedt D, Menu E, Chaouat G: Induction of transient murine T cell anergy by a low molecular weight compound obtained from supernatants of human placental cultures is linked to defective phosphorylation of TCR CD3ζchain. Am J Reprod Immunol 1997; 38:168-175.
33. Zourbas S, Dubanchet S, Martal J, Chaouat G: Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the feto maternal interface during murine pregnancy. Clin Exp Immunol 2001; 126:519-528.
34. Devergne O, Coulomb-L'Hermine A, Capel F, Moussa M, Capron F: Expression of Epstein-Barr virus-induced gene 3, an interleukin-12 p40-related molecule, throughout human pregnancy: Involvement of syncytio trophoblasts and extra villous trophoblasts. Am J Pathol 2001; 159:1763-1776.
35. Wiekowski M, Leach M, Evans E et.al.. Ubiquitinous transgenic expression of the IL-23 subunit p19 induces multiorgan inflammation, runting, infertility and premature death. J Immunol 2001; 166:7563-7570.
36. Zhang JH, He H, Borzychowski AM, Takeda K, Akira S, Croy BA: Analysis of cytokine regulators inducing interferon production by mouse uterine natural killer cells. Biol Reprod 2003; 69:404-411.
37. Ashkar AA, Black GP, Wei Q, He H, Liang L, Head JR, Croy BA: Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J Immunol. 2003; 171:2937-2944.
38. Leonard S, Murrant C, Tayade C, van den Heuvel M, Watering R, Croy BA: Mechanisms regulating immune cell contributions to spiral artery modification - facts and hypotheses - a review. Placenta 2006; (Epub ahead of print Jan 2006)
39. Drake BL, Head JR, Hedley ML, Tucker P, Forman J: Ontogeny of class I MHC gene expression in the mouse fetus and placenta. Am J Reprod Immunol 1988; 16:111.
40. Chaouat G, Mathieson B, Asofsky RA: Regulatory mechanisms of the mixed lymphocyte reaction: Evidence for the requirement of two T cells to interact in the generation of effective suppression. J Immunol 1982; 129:2502.
41. Kallikourdis M, Betz AG: Periodic accumulation of regulatory T cells in the uterus: Preparation for the implantation of a semi-allogeneic fetus?. PLoS ONE 2007; 2:e382.
42. Jasper MJ, Tremellen KP, Robertson SA: Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod 2006; 12:301-308. Epub 2006 Mar 30.
43. Pflanz S, Timans JC, Cheung J, Rosales R, Kanzler H, Gilbert J, Hibbert L, Churakova T, Travis M, Vaisberg E, Blumenschein WM, Mattson JD, Wagner JL, To W, Zurawski S, McClanahan TK, Gorman DM, Bazan JF, de Waal Malefyt R, Rennick D, Kastelein RA: IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naive CD4(+) T cells. Immunity 2002; 16:779-790.
44. Baines MG, Gendron RL: Natural and experimental animal models of reproductive failure. In Immunology of Pregnancy, G Chaouat (ed). Boca Raton, CRC Press, 1993, pp 173-203.
45. Chaouat G, Clark DA, Wegmann TG: Genetics aspects of the CBA/J × DBA/2J and B10 x B10. In A Models of Murine Spontaneous Abortions and Prevention by Leukocyte Immunisation. 18th R.C.O.G. Study Group. Early Pregnancy Loss. Mechanisms and Treatment. R.C.O.G, WR Allen, DA Clark, TJ Gill III, JF Mowbray, WR Robertson (eds). London, RCOG Press, 1988, pp 89-105.
46. Girardi G, Yarilin D, Thurman JM, Holers VM, Salmon JE: Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006; 203: 2165-2175.
47. Chaouat G, Menu E, Dy M, Minkwoski M, Clark DA, Wegmann TG: Control of fetal survival in CBA × DBA/2 mice by lymphokine therapy. J Reprod Fertil 1990; 89: 447-458.
48. Chicheportiche Y, Bourdon P, Xu H, Hsu YM, Scott H, Hession C, Garcia I, Browning J: TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem 1997; 272: 32401-32410.
49. Wiley SR, Winkles JA: TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev 2003; 14: 241-249.
50. Maecker H, Varfolomeev E, Kischkel F, Lawrence D, LeBlanc H, Lee W, Hurst S, Danilenko D, Li J, Filvaroff E, Yang B, Daniel D, Ashkenazi A: TWEAK attenuates the transition from innate to adaptive immunity. Cell 2005; 123:931-944.
51. Tartakovsky B, Ben-Yair E: Cytokines modulate preimplantation development and pregnancy. Dev Biol 1991; 146:345-352.
52. Tartakowsky B, Goldstein O, Ben YB: In vivo modulation of pre embryonic development by cytokines. In Biologie cellulaire et moléculaire de la relation materno fetale, G Chaouat, J Mowbray (eds). Editions Paris, France, INSERM. John Libbey, 1991; pp 239-245.
53. Du MR, Dong L, Zhou WH, Yan FT, Li DJ: Cyclosporin a improves pregnancy outcome by promoting functions of trophoblasts and inducing maternal tolerance to the allogeneic fetus in abortion-prone matings in the mouse. Biol Reprod 2007; 76:906-14 (Epub ahead of print Jan 2007).
54. Paldi A: Genomic imprinting and feto maternal relationship. In Biologie cellulaire et moléculaire de la relation materno fetale. G Chaouat, J Mowbray (eds). Colloque INSERM 254. Editions INSERM Paris, France. John Libbey, 1991, 61-66.
55. Xu C, Mao D, Holmers M, Palanca B, Cheng AM, Molina H: A critical role for complement regulatory Crry in feto maternal tolerance. Science 2000; 287:498-499.
56. Mohamed OA, Jonnaert M, Labelle-Dumais C, Kuroda K, Clarke HJ, Dufort D: Uterine Wnt/beta-catenin signaling is required for implantation. Proc Natl Acad Sci USA. 2005; 102:8579-8584 [Epub 2005 Jun 1].
57. Tangri S, Raghupathy R: Expression of cytokines in placentas of mice undergoing immunologically mediated spontaneous fetal resorptions. Biol Reprod 1993; 49:850-856.
58. Bobe P, Chaouat G, Stanislwaski M, Kiger N: Immunogenetics of spontaneous abortion in mice. II) anti abortive effects are independent of systemic regulatory mechanisms. Cell Immunol 1986; 98:477-485.
59. Robertson SA, Seamark RF: Granulocyte macrophage colony stimulating factor (GM-CSF) in the murine reproductive tract: Stimulation by seminal factors. Reprod Fertil Dev 1990; 2:359-368.