Soluble HLA-G regulates motility and invasion of the trophoblast-derived cell line SGHPL-4

Human Reproduction

Volumn 24, Issue 6, 2009, Pages 1339-1345

  McCormick, James ^a   Whitley, Guy St J ^a   Le Bouteiller, Philippe ^b   Cartwright, Judith E ^a  

^a ST GEORGE S HOSPITAL   (United Kingdom)

^b INSERM   (France)

Author keywords

HLA G; Invasion; Motility; Placenta; Trophoblast

Indexed keywords

EPIDERMAL GROWTH FACTOR; HLA G ANTIGEN; SCATTER FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CELL CULTURE; CELL INVASION; CELL LINE; CELL MOTILITY; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; MICROCARRIER CULTURE; MICROSCOPY; TROPHOBLAST; WESTERN BLOTTING;

EID: 66249129335     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dep026     Document Type: Article

References (46)

1. Anin SA, Vince G, Quenby S. Trophoblast invasion. Hum Fertil (Camb) 2004;7:169-174.
2. Apps R, Gardner L, Sharkey AM, Holmes N, Moffett A. A homodimeric complex of HLA-G on normal trophoblast cells modulates antigen-presenting cells via LILRB1. EurJ Immunol 2007;37:1924-1937.
3. Ashton SV, Whitley GS, Dash PR, Wareing M, Crocker IP, Baker PN, Cartwright JE. Uterine spiral artery remodeling involves endothelial apoptosis induced by extravillous trophoblasts through Fas/FasL interactions. Arterioscler Thromb Vasc Biol 2005;25:102-108.
4. Bainbridge D, Ellis S, Le Bouteiller P, Sargent I. HLA-G remains a mystery. Trends Immunol 2001;22:548-552.
5. Bass KE, Morrish D, Roth I, Bhardwaj D, Taylor R, Zhou Y, Fisher SJ. Human cytotrophoblast invasion is up-regulated by epidermal growth factor: evidence that paracrine factors modify this process. Dev Bio 1994;164:550-561.
6. Behrendtsen O, Alexander CM, Werb Z. Metalloproteinases mediate extracellular matrix degradation by cells from mouse blastocyst outgrowths. Development 1992; 114:447-456.
7. Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 1967;93:569-579.
8. Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of pre-eclampsia. J Pathol 1970;101: Pvi.
9. Cartwright JE, Holden DP, Whitley GS. Hepatocyte growth facto regulates human trophoblast motility and invasion: a role for nitric oxide. Br J Pharmacol 1999;128:181-189.
10. Chumbley G, King A, Robertson K, Holmes N, Loke YW. Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell Immunol 1994;155:312-322.
11. Dash PR, McCormick J, Thomson MJ, Johnstone AP, Cartwright JE, Whitley GS. Fas ligand-induced apoptosis is regulated by nitric oxide through the inhibition of fas receptor clustering and the nitrosylation of protein kinase Cepsilon. Exp Cell Res 2007;313:3421-3431.
12. Deniz G, Christmas SE, Brew R, Johnson PM. Phenotypic and functional cellular differences between human CD32 decidual and peripheral blood leukocytes. J Immunol 1994;152:4255-4261.
13. Ellis SA, Palmer MS, McMichael AJ. Human trophoblast and the choriocarcinoma cell line BeWo express a truncated HLA Class I molecule. J Immunol 1990;144:731-735.
14. Fons P et al. Soluble HLA-G 1 inhibits angiogenesis through an apoptotic pathway and by direct binding to CD 160 receptor expressed by endothelial cells. Blood 2006;108:2608-2615.
15. Fournel S, Aguerre-Girr M, Campan A, Salauze L, Berrebi A, Lone YC, Lenfant F, Le Bouteiller P. Soluble HLA-G: purification from eukaryotic transfected cells and detection by a specific ELISA. Am J Reprod Immunol 1999;42:22-29.
16. Fujii T, Ishitani A, Geraghty DE. A soluble form of the HLA-G antigen is encoded by a messenger ribonucleic acid containing intron 4. J Immunol 1994;153:5516-5524.
17. Geraghty DE, Koller BH, Orr HT. A human major histocompatibility complex class I gene that encodes a protein with a shortened cytoplasmic segment. Proc Natl Acad Sci USA 1987;84:9145-9149.
18. Harris LK, Keogh RJ, Wareing M, Baker PN, Cartwright JE, Aplin JD, Whitley GS. Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a fas ligand-dependent mechanism. Am J Pathol 2006; 169:1863-1874.
19. Ishitani A, Geraghty DE. Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc Natl Acad Sci USA 1992;89:3947-3951.
20. Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990; 248:220-223.
21. Langat DK, Sue Platt J, Tawfik O, Fazleabas AT, Hunt JS. Differential expression of human leukocyte antigen-G (HLA-G) messenger RNAs and proteins in normal human prostate and prostatic adenocarcinoma. J Reprod Immunol 2006;71:75-86.
22. Le Bouteiller P, Legrand-Abravanel F, Solier C. Soluble HLA-G 1 at the materno-foetal interface - a review. Placenta 2003;24(Suppl A):S10-S15.
23. Le Bouteiller P, Fons P, Herault JP, Bono F, Chabot S, Cartwright JE, Bensussan A. Soluble HLA-G and control of angiogenesis. J Reprod Immunol 2007;76:17-22.
24. LeMaoultJ, Zafaranloo K, Le Danff C, Carosella ED. HLA-G up-regulates ILT2, ILT3, ILT4, and KIR2DL4 in antigen presenting cells, NK cells, and T cells. FASEBJ 2005;19:662-664.
25. Lim KH, Zhou Y, Janatpour M, McMaster M, Bass K, Chun SH, Fisher SJ. Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am J Pathol 1997;151:1809-1818.
26. Lindaman A, Dowden A, Zavazava N. Soluble HLA-G molecules induce apoptosis in natural killer cells. Am J Reprod Immunol 2006;56:68-76.
27. Mallet V, Proll J, Solier C, Aguerre-Girr M, DeRossi M, Loke YW, Lenfant F, Le Bouteiller P. The full length HLA-G 1 and no other alternative form of HLA-G is expressed at the cell surface of transfected cells. Hum Immunol 2000;61:212-224.
28. Marchal-Bras-Goncalves R, Rouas-Freiss N, Connan F, Choppin J, Dausset J, Carosella ED, Kirszenbaum M, Guillet J. A soluble HLA-G protein that inhibits natural killer cell-mediated cytotoxicity. Transplant Proc 2001;33:2355-2359.
29. McMaster MT, Librach CL, Zhou Y, Lim KH, Janatpour MJ, DeMars R, Kovats S, Damsky C, Fisher SJ. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol 1995; 154:3771-3778.
30. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, van Asshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994;101:669-674.
31. Moreau P, Carosella E, Teyssier M, Prost S, Gluckman E, Dausset J, Kirszenbaum M. Soluble HLA-G molecule. An alternatively spliced HLA-G mRNA form candidate to encode it in peripheral blood mononuclear cells and human trophoblasts. Hum Immunol 1995; 43:231-236.
32. Nehls V, Drenckhahn D. A novel, microcarrier-based in vitro assay for rapid and reliable quantification of three-dimensional cell migration and angiogenesis. Microvasc Res 1995;50:311-322.
33. Paul P, Cabestre FA, Ibrahim EC, Lefebvre S, Khalil-Daher I, Vazeux G, Quiles RM, Bermond F, Dausset J, Carosella ED. Identification of LA-G7 as a new splice variant of the HLA-G mRNA and expression of soluble HLA-G5, -G6, and -G7 transcripts in human transfected cells. Hum Immunol 2000;61:1138- 1149.
34. Pijnenborg R, Dixon G, Robertson WB, Brosens I. Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980; 1:3-19.
35. Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983;4:397-413.
36. Pijnenborg R, Ball E, Bulmer JN, Hanssens M, Robson SC, Vercruysse L In vivo analysis of trophoblast cell invasion in the human. Methods Mol Med 2006;122:11-44.
37. ; Qiu Q, Yang M, Tsang BK, Gruslin A. EGF-induced trophoblast secretion of MMP-9 and TIMP-1 involves activation of both PI3K and MAPK signalling pathways. Reproduction 2004;128:355-363.
38. Rajagopalan S, Long EO. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 1999;189:1093-1100.
39. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I, Long EO. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol 2006;4:e9.
40. Robertson WB, Brosens IA, Dixon HG. Placental bed vessels. Am J Obstet Gynecol 1973;117:294-295.
41. Rouas-Freiss N, Goncalves RM, Menier C, Dausset J, Carosella ED. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci USA 1997; 94:11520-11525.
42. Shiroishi M et al. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci USA 2003;100:8856- 8861.
43. Whitley GS, Dash PR, Ayling LJ, Prefumo F, Thilaganathan B, Cartwright JE. Increased apoptosis in first trimester extravillous trophoblasts from pregnancies at higher risk of developing preeclampsia. Am J Pathol 2007;170:1903-1909.
44. Yelavarthi KK, Fishback JL, Hunt JS. Analysis of HLA-G mRNA in human placental and extraplacental membrane cells by in situ hybridization. J Immunol 1991;146:2847-2854.
45. Yie SM, Li LH, Li YM, Librach C. HLA-G protein concentrations in maternal serum and placental tissue are decreased in preeclampsia. Am J Obstet Gynecol 2004;191:525-529.
46. Zavazava N, Kronke M. Soluble HLA class I molecules induce apoptosis in alloreactive cytotoxic T lymphocytes. Nat Med1996;2: 1005-1010.