Activation of Toll-like receptor 5 decreases the attachment of human trophoblast cells to endometrial cells in vitro

Human Reproduction

Volumn 25, Issue 9, 2010, Pages 2217-2228

  Aboussahoud, Wedad ^a   Bruce, Chris ^a   Elliott, Sarah ^a   Fazeli, Alireza ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

flagellin; implantation; innate immune system; TLR5; trophoblast attachment

Indexed keywords

FLAGELLIN; TOLL LIKE RECEPTOR 5;

ARTICLE; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; ENDOMETRIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; INNATE IMMUNITY; INTRAUTERINE INFECTION; NIDATION; RECEPTOR UPREGULATION; TROPHOBLAST;

BACTERIA (MICROORGANISMS);

EID: 77955957366     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deq185     Document Type: Article

References (53)

1. Aboussahoud W, Aflatoonian R, Bruce C, Elliott S, Ward J, Newton S, Hombach-Klonisch S, Klonisch T, Fazeli A. Expression and function of Toll-like receptors in human endometrial epithelial cell lines. J Reprod Immunol 2010;84:41-51.
2. Abrahams VM, Bole-Aldo P, Kim YM, Straszewski-Chavez SL, Chaiworapongsa T, Romero R, Mor G. Divergent trophoblast responses to bacterial products mediated by TLRs. J Immunol 2004; 173:4286-4296.
3. Abrahams VM, Visintin I, Aldo PB, Guller S, Romero R, Mor G. A role for TLRs in the regulation of immune cell migration by first trimester trophoblast cells. J Immunol 2005;175:8096-8104.
4. Acosta AA, Oehninger S, Hammer J, Muasher SJ, Liang HM, Jones DL. Preclinical abortions: incidence and significance in the Norfolk in vitro fertilization program. Fertil Steril 1990;53:673-676.
5. Aflatoonian R, Fazeli A. Toll-like receptors in female reproductive tract and their menstrual cycle dependent expression. J Reprod Immunol 2008;77:7-13.
6. Aflatoonian R, Tuckerman E, Elliott SL, Bruce C, Aflatoonian A, Li TC, Fazeli A. Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum Reprod 2007;22:586-593.
7. Aplin JD. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991; 99:681-692.
8. Arechavaleta-Velasco F, Koi H, Strauss JF 3rd, Parry S. Viral infection of the trophoblast: time to take a serious look at its role in abnormal implantation and placentation? J Reprod Immunol 2002;55:113-121.
9. Barlow P, Lejeune B, Puissant F, Englert Y, Van Rysselberge M, Degueldre M, Vekemans M, Leroy F. Early pregnancy loss and obstetrical risk after in-vitro fertilization and embryo replacement. Hum Reprod 1988;3:671-675.
10. Bergh PA, Navot D. The impact of embryonic development and endometrial maturity on the timing of implantation. Fertil Steril 1992;58:537-542.
11. Caballero-Campo P, Dominguez F, Coloma J, Meseguer M, Remohi J, Pellicer A, Simon C. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod 2002;8:375-384.
12. Carney SA, Tahara H, Swartz CD, Risinger JI, He H, Moore AB, Haseman JK, Barrett JC, Dixon D. Immortalization of human uterine leiomyoma and myometrial cell lines after induction of telomerase activity: molecular and phenotypic characteristics. Lab Invest 2002; 82:719-728.
13. Chard T. Frequency of implantation and early pregnancy loss in natural cycles. Baillieres Clin Obstet Gynaecol 1991;5:179-189.
14. Chen YX, Lv WG, Chen HZ, Ye F, Xie X. Methotrexate induces apoptosis of human choriocarcinoma cell line JAR via a mitochondrial pathway. Eur J Obstet Gynecol Reprod Biol 2009;143:107-111.
15. Croxatto HB, Ortiz ME, Diaz S, Hess R, Balmaceda J, Croxatto HD. Studies on the duration of egg transport by the human oviduct. II. Ovum location at various intervals following luteinizing hormone peak. Am J Obstet Gynecol 1978;132:629-634.
16. De los Santos MJ, Mercader A, Galan A, Albert C, Romero JL, Pellicer A. Implantation rates after two, three, or five days of embryo culture. Placenta 2003;24 (Suppl. B):S13-S19.
17. De Mouzon J, Rossin-Amar B, Bachelot A, Renon C, Devecchi A. FIVNAT. Influence of attempt rank in in vitro fertilization. Contracept Fertil Sex 1998;26:466-472.
18. Diedrich K, Fauser BC, Devroey P, Griesinger G. The role of the endometrium and embryo in human implantation. Hum Reprod Update 2007;13:365-377.
19. Dominguez F, Pellicer A, Simon C. Paracrine dialogue in implantation. Mol Cell Endocrinol 2002;186:175-181.
20. Edwards RG. Implantation, interception and contraception. Hum Reprod 1994;9:985-995.
21. Enders AC, Schlafke S, Hendrickx AG. Differentiation of the embryonic disc, amnion, and yolk sac in the rhesus monkey. Am J Anat 1986; 177:161-185.
22. Ezra Y, Schenker JG. Abortion rate in assisted reproduction\true increase? Early Pregnancy 1995;1:171-175.
23. Fazeli A, Bruce C, Anumba DO. Characterization of Toll-like receptors in the female reproductive tract in humans. Hum Reprod 2005; 20:1372-1378.
24. Grummer R, Hohn HP, Mareel MM, Denker HW. Adhesion and invasion of three human choriocarcinoma cell lines into human endometrium in a three-dimensional organ culture system. Placenta 1994;15:411-429.
25. Hannan NJ, Salamonsen LA. Role of chemokines in the endometrium and in embryo implantation. Curr Opin Obstet Gynecol 2007;19:266-272.
26. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001; 410:1099-1103.
27. Heneweer C, Kruse LH, Kindhauser F, Schmidt M, Jakobs KH, Denker HW, Thie M. Adhesiveness of human uterine epithelial RL95-2 cells to trophoblast: rho protein regulation. Mol Hum Reprod 2002;8:1014-1022.
28. Heneweer C, Schmidt M, Denker HW, Thie M. Molecular mechanisms in uterine epithelium during trophoblast binding: the role of small GTPase RhoA in human uterine Ishikawa cells. J Exp Clin Assist Reprod 2005;2:4.
29. Hohn HP, Denker HW. The role of cell shape for differentiation of choriocarcinoma cells on extracellular matrix. Exp Cell Res 1994; 215:40-50.
30. Hohn HP, Linke M, Ugele B, Denker HW. Differentiation markers and invasiveness: discordant regulation in normal trophoblast and choriocarcinoma cells. Exp Cell Res 1998;244:249-258.
31. Hohn HP, Linke M, Denker HW. Adhesion of trophoblast to uterine epithelium as related to the state of trophoblast differentiation: in vitro studies using cell lines. Mol Reprod Dev 2000;57:135-145.
32. Hombach-Klonisch S, Kehlen A, Fowler PA, Huppertz B, Jugert JF, Bischoff G, Schluter E, Buchmann J, Klonisch T. Regulation of functional steroid receptors and ligand-induced responses in telomerase-immortalized human endometrial epithelial cells. J Mol Endocrinol 2005;34:517-534.
33. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 1999;162:3749-3752.
34. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002;20:197-216.
35. John NJ, Linke M, Denker HW. Quantitation of human choriocarcinoma spheroid attachment to uterine epithelial cell monolayers. In Vitro Cell Dev Biol Anim 1993;29A:461-468.
36. Klaffenbach D, Rascher W, Rollinghoff M, Dotsch J, Meissner U, Schnare M. Regulation and signal transduction of toll-like receptors in human chorioncarcinoma cell lines. Am J Reprod Immunol 2005; 53:77-84.
37. Koga K, Cardenas I, Aldo P, Abrahams VM, Peng B, Fill S, Romero R, Mor G. Activation of TLR3 in the trophoblast is associated with preterm delivery. Am J Reprod Immunol 2009;61:196-212.
38. Ledee-Bataille N, Lapree-Delage G, Taupin JL, Dubanchet S, Frydman R, Chaouat G. Concentration of leukaemia inhibitory factor (LIF) in uterine flushing fluid is highly predictive of embryo implantation. Hum Reprod 2002;17:213-218.
39. Medzhitov R, Janeway CA Jr. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 1997;9:4-9.
40. Meter RA, Horton M. Decreased implantation rate after cervicovaginal exposure to lipopolysaccharide, a potential pathway of decreased uterine receptivity by Toll-Like receptor activation. Fertil Steril 2007; 88:S40-S41.
41. Miao EA, Ernst RK, Dors M, Mao DP, Aderem A. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc Natl Acad Sci USA 2008;105:2562-2567.
42. Mulla MJ, Brosens JJ, Chamley LW, Giles I, Pericleous C, Rahman A, Joyce SK, Panda B, Paidas MJ, Abrahams VM. Antiphospholipid antibodies induce a pro-inflammatory response in first trimester trophoblast via the TLR4/MyD88 pathway. Am J Reprod Immunol 2009;62:96-111.
43. Nishida M. The Ishikawa cells from birth to the present. Hum Cell 2002; 15:104-117.
44. Perrier D'hauterive S, Charlet-Renard C, Goffin F, Foidart M, Geenen V. The implantation window. J Gynecol Obstet Biol Reprod (Paris) 2002; 31:440-455.
45. Shaykhiev R, Behr J, Bals R. Microbial patterns signaling via Toll-Like receptors 2 and 5 contribute to epithelial repair, growth and survival. PLoS ONE 2008;3:e1393.
46. Simon C, Landeras J, Zuzuarregui JL, Martin JC, Remohi J, Pellicer A. Early pregnancy losses in in vitro fertilization and oocyte donation. Fertil Steril 1999;72:1061-1065.
47. Tinel H, Denker HW, Thie M. Calcium influx in human uterine epithelial RL95-2 cells triggers adhesiveness for trophoblast-like cells. Model studies on signalling events during embryo implantation. Mol Hum Reprod 2000;6:1119-1130.
48. Uchida H, Maruyama T, Ohta K, Ono M, Arase T, Kagami M, Oda H, Kajitani T, Asada H, Yoshimura Y. Histone deacetylase inhibitor-induced glycodelin enhances the initial step of implantation. Hum Reprod 2007;22:2615-2622.
49. Way DL, Grosso DS, Davis JR, Surwit EA, Christian CD. Characterization of a new human endometrial carcinoma (RL95-2) established in tissue culture. In Vitro 1983;19:147-158.
50. White TE, Saltzman RA, Di Sant'Agnese PA, Keng PC, Sutherland RM, Miller RK. Human choriocarcinoma (JAr) cells grown as multicellular spheroids. Placenta 1988;9:583-598.
51. Wilcox AJ, Weinberg CR, O'Connor JF, Baird DD, Schlatterer JP, Canfield RE, Armstrong EG, Nisula BC. Incidence of early loss of pregnancy. N Engl J Med 1988;319:189-194.
52. Zhang J, Wei H, Wu D, Tian Z. Toll-like receptor 3 agonist induces impairment of uterine vascular remodeling and fetal losses in CBA x DBA/2 mice. J Reprod Immunol 2007;74:61-67.
53. Zinaman MJ, Clegg ED, Brown CC, O'Connor J, Selevan SG. Estimates of human fertility and pregnancy loss. Fertil Steril 1996;65:503-509.