Galectin-I influences trophoblast immune evasion and emerges as a predictive factor for the outcome of pregnancy

Molecular Human Reproduction

Volumn 19, Issue 1, 2013, Pages 43-53

  Tirado gonzález, Irene ^a   Freitag, Nancy ^a   Barrientos, Gabriela ^a   Shaikly, Valerie ^b,c   Nagaeva, Olga ^d   Strand, Magnus ^d   Kjellberg, Lennart ^d   Klapp, Burghard F ^a   Mincheva nilsson, Lucia ^d   Cohen, Marie ^e   Blois, Sandra M ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF ESSEX   (United Kingdom)

^c Assisted Reproduction and Gynaecology Centre   (United Kingdom)

^d UMEÅ UNIVERSITY   (Sweden)

^e Laboratoire d'Hormonologie   (Switzerland)

Author keywords

Gal I; HLA G; Human embryo; Spontaneous abortion

Indexed keywords

GALECTIN 1; HLA G ANTIGEN; LECTIN; ALLOANTIGEN; BIOLOGICAL MARKER; ISOPROTEIN;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTROPHOBLAST; DECIDUA; EMBRYO; FEMALE; FIRST TRIMESTER PREGNANCY; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE EVASION; IMMUNOREGULATION; IN VITRO STUDY; INNER CELL MASS; PHYSIOLOGY; PREDICTION; PREGNANCY; PREGNANCY OUTCOME; PREGNANT WOMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SPONTANEOUS ABORTION; TROPHOBLAST; BLASTOCYST; BLOOD; CELL ADHESION; CELL LINE; GENE EXPRESSION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; NIDATION; PLACENTA; PROGNOSIS;

ABORTION, SPONTANEOUS; ADULT; BIOLOGICAL MARKERS; BLASTOCYST; CELL ADHESION; CELL LINE; DECIDUA; EMBRYO IMPLANTATION; FEMALE; GALECTIN 1; GENE EXPRESSION; HLA-G ANTIGENS; HUMANS; IMMUNE EVASION; IMMUNE TOLERANCE; ISOANTIGENS; PLACENTA; PREGNANCY; PREGNANCY TRIMESTER, FIRST; PROGNOSIS; PROTEIN ISOFORMS; TROPHOBLASTS;

EID: 84871162939     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gas043     Document Type: Article

References (60)

1. Almkvist J, Karlsson A. Galectins as inflammatory mediators. Glycoconj J 2004;19:575-581.
2. Aplin JD. Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro. J Cell Sci 1991; 99(Pt 4):681-692.
3. Arck PC, Rucke M, Rose M, Szekeres-Bartho J, Douglas AJ, Pritsch M, Blois SM, Pincus MK, Barenstrauch N, Dudenhausen JW et al. Early risk factors for miscarriage: a prospective cohort study in pregnant women. Reprod Biomed Online 2008;17:101-113.
4. Bamberger AM, Jenatschke S, Schulte HM, Loning T, Bamberger MC. Leukemia inhibitory factor (LIF) stimulates the human HLA-G promoter in JEG3 choriocarcinoma cells. J Clin Endocrinol Metab 2000; 85:3932-3936.
5. Belanis L, Plowman SJ, Rotblat B, Hancock JF, Kloog Y. Galectin-1 is a novel structural component and a major regulator of h-ras nanoclusters. Mol Biol Cell 2008;19:1404-1414.
6. Bevan BH, Kilpatrick DC, Liston WA, Hirabayashi J, Kasai K. Immunohistochemical localization of a beta-D-galactoside-binding lectin at the human maternofetal interface. Histochem J 1994; 26:582-586.
7. Bischof P, Haenggeli L, Campana A. Gelatinase and oncofetal fibronectin secretion is dependent on integrin expression on human cytotrophoblasts. Hum Reprod 1995;10:734-742.
8. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B et al. A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 2007;13:1450-1457.
9. Boivin J, Bunting L, Collins JA, Nygren KG. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod 2007;22:1506-1512.
10. Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: a small protein with major functions. Glycobiology 2006;16:137R-157R.
11. Choe YS, Shim C, Choi D, Lee CS, Lee KK, Kim K. Expression of galectin-1 mRNA in the mouse uterus is under the control of ovarian steroids during blastocyst implantation. Mol Reprod Dev 1997; 48:261-266.
12. Contini P, Ghio M, Poggi A, Filaci G, Indiveri F, Ferrone S, Puppo F. Soluble HLA-A,-B,-C and -G molecules induce apoptosis in T and NK CD8+ cells and inhibit cytotoxic T cell activity through CD8 ligation. Eur J Immunol 2003;33:125-134.
13. Donadi EA, Castelli EC, Arnaiz-Villena A, Roger M, Rey D, Moreau P. Implications of the polymorphism of HLA-G on its function, regulation, evolution and disease association. Cell Mol Life Sci 2011; 68:369-395.
14. Fischer C, Sanchez-Ruderisch H, Welzel M, Wiedenmann B, Sakai T, Andre S, Gabius HJ, Khachigian L, Detjen KM, Rosewicz S. Galectin-1 interacts with the {alpha}5{beta}1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J Biol Chem 2005; 280:37266-37277.
15. Fischer I, Redel S, Hofmann S, Kuhn C, Friese K, Walzel H, Jeschke U. Stimulation of syncytium formation in vitro in human trophoblast cells by galectin-1. Placenta 2010;31:825-832.
16. Flajollet S, Poras I, Carosella ED, Moreau P. RREB-1 is a transcriptional repressor of HLA-G. J Immunol 2009;183:6948-6959.
17. Fons P, Chabot S, Cartwright JE, Lenfant F, L'Faqihi F, Giustiniani J, Herault JP, Gueguen G, Bono F, Savi P et al. Soluble HLA-G1 inhibits angiogenesis through an apoptotic pathway and by direct binding to CD160 receptor expressed by endothelial cells. Blood 2006; 108:2608-2615.
18. Harvey S, Zhang Y, Landry F, Miller C, Smith JW. Insights into a plasma membrane signature. Physiol Genomics 2001;5:129-136.
19. Hirabayashi J, Kasai K. Human placenta beta-galactoside-binding lectin. Purification and some properties. Biochem Biophys Res Commun 1984; 122:938-944.
20. Hirota Y, Burnum KE, Acar N, Rabinovich GA, Daikoku T, Dey SK. Galectin-1 markedly reduces the incidence of resorptions in mice missing immunophilin FKBP52. Endocrinology 2012;153:2486-2493.
21. Hunt JS, Petroff MG, McIntire RH, Ober C. HLA-G and immune tolerance in pregnancy. Faseb J 2005;19:681-693.
22. Hunter T. Anti-phosphatases take the stage. Nat Genet 1998;18: 303-305.
23. James JL, Stone PR, Chamley LW. Cytotrophoblast differentiation in the first trimester of pregnancy: evidence for separate progenitors of extravillous trophoblasts and syncytiotrophoblast. Reproduction 2005; 130:95-103.
24. Jeschke U, Toth B, Scholz C, Friese K, Makrigiannakis A. Glycoprotein and carbohydrate binding protein expression in the placenta in early pregnancy loss. J Reprod Immunol 2010;85:99-105.
25. Kapasi K, Albert SE, Yie S, Zavazava N, Librach CL. HLA-G has a concentration-dependent effect on the generation of an allo-CTL response. Immunology 2000;101:191-200.
26. King A, Hiby SE, Gardner L, Joseph S, Bowen JM, Verma S, Burrows TD, Loke YW. Recognition of trophoblast HLA class I molecules by decidual NK cell receptors-a review. Placenta 2000;21(Suppl A):S81-S85.
27. Kolundzic N, Bojic-Trbojevic Z, Kovacevic T, Stefanoska I, Kadoya T, Vicovac L. Galectin-1 is part of human trophoblast invasion machinery-a functional study in vitro. PLoS One 2011;6:e28514.
28. Kopcow HD, Rosetti F, Leung Y, Allan DS, Kutok JL, Strominger JL. T cell apoptosis at the maternal-fetal interface in early human pregnancy, involvement of galectin-1. Proc Natl Acad Sci USA 2008; 105:18472-18477.
29. 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.
30. Lefebvre S, Berrih-Aknin S, Adrian F, Moreau P, Poea S, Gourand L, Dausset J, Carosella ED, Paul P. A specific interferon (IFN)-stimulated response element of the distal HLA-G promoter binds IFN-regulatory factor 1 and mediates enhancement of this nonclassical class I gene by IFN-beta. J Biol Chem 2001;276:6133-6139.
31. Liu AX, Jin F, Zhang WW, Zhou TH, Zhou CY, Yao WM, Qian YL, Huang HF. Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss. Biol Reprod 2006; 75:414-420.
32. Lowenstein EJ, Daly RJ, Batzer AG, Li W, Margolis B, Lammers R, Ullrich A, Skolnik EY, Bar-Sagi D, Schlessinger J. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 1992;70:431-442.
33. Maquoi E, van den Brule FA, Castronovo V, Foidart JM. Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts. Placenta 1997;18:433-439.
34. McCormick J, Whitley GS, Le Bouteiller P, Cartwright JE. Soluble HLA-G regulates motility and invasion of the trophoblast-derived cell line SGHPL-4. Hum Reprod 2009;24:1339-1345.
35. 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.
36. Medawar P. Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrate. Symp Soc Exp Biol 1953; 7:320-338.
37. Moreau P, Paul P, Rouas-Freiss N, Kirszenbaum M, Dausset J, Carosella ED. Molecular and immunologic aspects of the nonclassical HLA class I antigen HLA-G: evidence for an important role in the maternal tolerance of the fetal allograft. Am J Reprod Immunol 1998; 40:136-144.
38. Moreau P, Adrian-Cabestre F, Menier C, Guiard V, Gourand L, Dausset J, Carosella ED, Paul P. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int Immunol 1999;11:803-811.
39. Moreau P, Faure O, Lefebvre S, Ibrahim EC, O'Brien M, Gourand L, Dausset J, Carosella ED, Paul P. Glucocorticoid hormones upregulate levels of HLA-G transcripts in trophoblasts. Transplant Proc 2001; 33:2277-2280.
40. Mouillot G, Marcou C, Zidi I, Guillard C, Sangrouber D, Carosella ED, Moreau P. Hypoxia modulates HLA-G gene expression in tumor cells. Hum Immunol 2007;68:277-285.
41. Ombelet W, Cooke I, Dyer S, Serour G, Devroey P. Infertility and the provision of infertility medical services in developing countries. Hum Reprod Update 2008;14:605-621.
42. Pavan L, Tarrade A, Hermouet A, Delouis C, Titeux M, Vidaud M, Therond P, Evain-Brion D, Fournier T. Human invasive trophoblasts transformed with simian virus 40 provide a new tool to study the role of PPARgamma in cell invasion process. Carcinogenesis 2003; 24:1325-1336.
43. Paz A, Haklai R, Elad-Sfadia G, Ballan E, Kloog Y. Galectin-1 binds oncogenic H-Ras to mediate ras membrane anchorage and cell transformation. Oncogene 2001;20:7486-7493.
44. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. Apoptosis of T cells mediated by galectin-1. Nature 1995;378:736-739.
45. Poirier F, Timmons PM, Chan CT, Guenet JL, Rigby PW. Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during pre- and post-implantation development. Development 1992;115: 143-155.
46. Rai R, Regan L. Recurrent miscarriage. Lancet 2006;368:601-611.
47. Ribaux P, Petignat P, Finci V, Nehme FP, Carles D, Irion O, Epiney M, Cohen M. Overexpression of GRP78 in complete hydatidiform moles. Gynecol Oncol 2012;125:580-584.
48. Rubinstein N, Alvarez M, Zwirner NW, Toscano MA, Ilarregui JM, Bravo A, Mordoh J, Fainboim L, Podhajcer OL, Rabinovich GA. Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection; a potential mechanism of tumor-immune privilege. Cancer Cell 2004;5:241-251.
49. Seger R, Krebs EG. The MAPK signaling cascade. Faseb J 1995;9:726-735.
50. Terness P, Kallikourdis M, Betz AG, Rabinovich GA, Saito S, Clark DA. Tolerance signaling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells. Am J Reprod Immunol 2007; 58:238-254.
51. Than NG, Romero R, Erez O, Weckle A, Tarca AL, Hotra J, Abbas A, Han YM, Kim SS, Kusanovic JP et al. Emergence of hormonal and redox regulation of galectin-1 in placental mammals: implication in maternal-fetal immune tolerance. Proc Natl Acad Sci USA 2008; 105:15819-15824.
52. Thijssen VL, Postel R, Brandwijk RJ, Dings RP, Nesmelova I, Satijn S, Verhofstad N, Nakabeppu Y, Baum LG, Bakkers J et al. Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA 2006;103:15975-15980.
53. Thijssen VL, Hulsmans S, Griffioen AW. The galectin profile of the endothelium: altered expression and localization in activated and tumor endothelial cells. Am J Pathol 2008;172:545-553.
54. Vicovac L, Jankovic M, Cuperlovic M. Galectin-1 and -3 in cells of the first trimester placental bed. Hum Reprod 1998;13:730-735.
55. von Wolff M, Wang X, Gabius HJ, Strowitzki T. Galectin fingerprinting in human endometrium and decidua during the menstrual cycle and in early gestation. Mol Hum Reprod 2005;11:189-194.
56. Yang Y, Geraghty DE, Hunt JS. Cytokine regulation of HLA-G expression in human trophoblast cell lines. J Reprod Immunol 1995;29:179-195.
57. Yao YQ, Barlow DH, Sargent IL. Differential expression of alternatively spliced transcripts of HLA-G in human preimplantation embryos and inner cell masses. J Immunol 2005;175:8379-8385.
58. Yie SM, Li LH, Li GM, Xiao R, Librach CL. Progesterone enhances HLA-G gene expression in JEG-3 choriocarcinoma cells and human cytotrophoblasts in vitro. Hum Reprod 2006a;21:46-51.
59. Yie SM, Xiao R, Librach CL. Progesterone regulates HLA-G gene expression through a novel progesterone response element. Hum Reprod 2006b;21:2538-2544.
60. Zhao XY, Chen TT, Xia L, Guo M, Xu Y, Yue F, Jiang Y, Chen GQ, Zhao KW. Hypoxia inducible factor-1 mediates expression of galectin-1: the potential role in migration/invasion of colorectal cancer cells. Carcinogenesis 2010;31:1367-1375.