Galectin-1 confers immune privilege to human trophoblast: Implications in recurrent fetal loss

Glycobiology

Volumn 22, Issue 10, 2012, Pages 1374-1386

  Ramhorst, Rosanna E ^a   Giribaldi, Laura ^a,b   Fraccaroli, Laura ^a   Toscano, Marta A ^b   Stupirski, Juan C ^b   Romero, Marta D ^c   Durand, Edith S ^d   Rubinstein, Natalia ^a   Blaschitz, Astrid ^e   Sedlmayr, Peter ^e   Genti Raimondi, Susana ^d   Fainboim, Leonardo ^f   Rabinovich, Gabriel A ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c LIIDO   (United States)

^d UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^e MEDICAL UNIVERSITY OF GRAZ   (Austria)

^f HOSPITAL DE CLÍNICAS JOSÉ DE SAN MARTÍN   (Argentina)

Author keywords

fetal loss; fetomaternal tolerance; galectin 1; pregnancy; progesterone

Indexed keywords

GALECTIN 1; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 5; LACTOSE; PROGESTERONE; SMALL INTERFERING RNA;

ARTICLE; CANCER CELL CULTURE; CD4+ CD25+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; FEMALE; FEMALE FERTILITY; FETUS WASTAGE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOMODULATION; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; RECURRENT ABORTION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 CELL; TROPHOBLAST;

ABORTION, HABITUAL; CELL LINE; CELL SURVIVAL; CYTOKINES; GALECTIN 1; HUMANS; PROGESTERONE; T-LYMPHOCYTES; TROPHOBLASTS;

EID: 84865449176     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws104     Document Type: Article

References (82)

1. Aluvihare VR, Kallikourdis M, Betz AG. 2004. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol. 5:266-271. (Pubitemid 38332123)
2. Arck P, Hansen PJ, Mulac Jericevic B, Piccinni MP, Szekeres-Bartho J. 2007. Progesterone during pregnancy: Endocrine-immune cross talk in mammalian species and the role of stress. Am J Reprod Immunol. 58:268-279. (Pubitemid 47249065)
3. Arruvito L, Giulianelli S, Flores AC, Paladino N, Barboza M, Lanari C, Fainboim L. 2008. NK cells expressing a progesterone receptor are susceptible to progesterone-induced apoptosis. J Immunol. 180:5746-5753.
4. Arruvito L, Sanz M, Banham A, Fainboim L. 2007. Expansion of CD4 +CD25+and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: Implications for human reproduction. J Immunol. 178:2572-2578. (Pubitemid 46233460)
5. Baek KH, Lee EJ, Kim YS. 2007. Recurrent pregnancy loss: The key potential mechanisms. Trends Mol Med. 13:310-317.
6. Banh A, Zhang J, Cao H, Bouley DM, Kwok S, Kong C, Giaccia AJ, Koong AC, Le QT. 2011. Tumor galectin-1 mediates tumor growth and metastasis through regulation of T-cell apoptosis. Cancer Res. 71:4423-4431.
7. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobet P, Handjiski B, et al. 2007. A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med. 13:1450-1457. (Pubitemid 350224248)
8. Blois SM, Joachim R, Kandil J, Margni R, Tometten M, Klapp BF, Arck PC. 2004. Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J Immunol. 172:5893-5899. (Pubitemid 38621187)
9. Bozic M, Petronijevic M, Milenkovic S, Atanackovic J, Lazic J, Vicovac L. 2004. Galectin-1 and galectin-3 in the trophoblast of the gestational trophoblastic disease. Placenta. 25:797-802. (Pubitemid 39276945)
10. Cedeno-Laurent F, Opperman M, Barthel SR, Kuchroo VK, Dimitroff CJ. 2012. Galectin-1 triggers an immunoregulatory signature in Th cells functionally defined by IL-10 expression. J Immunol. 188:3127-3137.
11. Cedeno-Laurent F, Watanabe R, Teague JE, Kupper TS, Clark RA, Dimitroff CJ. 2012. Galectin-1 inhibits the viability, proliferation, and Th1 cytokine production of nonmalignant T cells in patients with leukemic cutaneous T-cell lymphoma. Blood. 119:3534-3548.
12. Chaouat G. 2007. The Th1/Th2 paradigm: Still important in pregnancy? Semin Immunopathol. 29:95-113. (Pubitemid 47603024)
13. Dong M, Ding G, Zhou J, Wang H, Zhao Y, Huang H. 2008. The effect of trophoblasts on T lymphocytes: Possible regulatory effector molecules-a proteomic analysis. Cell Physiol Biochem. 21:463-472. (Pubitemid 351620300)
14. Eliçabe RJ, Cargnelutti E, Serer MI, Stege PW, Valdez SR, Toscano MA, Rabinovich GA, Di Genaro MS. 2010. Lack of TNFR p55 results in heightened expression of IFN-γ and IL-17 during the development of reactive arthritis. J Immunol. 185:4485-4495.
15. Fainboim L, Arruvito L. 2011. Mechanisms involved in the expansion of Tregs during pregnancy: Role of IL-2/STAT5 signalling. J Reprod Immunol. 88:93-98.
16. Fischer I, Weber M, Kuhn C, Fitzgerald JS, Schulze S, Friese K, Walzel H, Markert UR, Jeschke U.2011, Is galectin-1 a trigger for trophoblast cell fusion?: The MAP-kinase pathway and syncytium formation in trophoblast tumour cells BeWo, Mol Hum Reprod.17, 747-757
17. Fraccaroli L, Alfieri J, Larocca L, Calafat M, Mor G, Perez Leirós CP, Ramhorst R. 2009. A potential tolerogenic immune mechanism in a trophoblast cell line through the activation of chemokine-induced T cell death and regulatory T cell modulation. Hum Reprod. 24:166-175.
18. Fraccaroli L, Alfieri J, Larocca L, Calafat M, Roca V, Lombardi E, Ramhorst R, Perez Leirós C. 2009. VIP modulates the pro-inflammatory maternal response, inducing tolerance to trophoblast cells. Br J Pharmacol. 156:116-126.
19. Garín MI, Chu CC, Golshayan D, Cernuda-Morollón E, Wait R, Lechler RI. 2007. Galectin-1: A key effector of regulation mediated by CD4+CD25+ T cells. Blood. 109:2058-2065. (Pubitemid 46348206)
20. Giordanengo L, Gea S, Barbieri G, Rabinovich GA. 2001. Anti-galectin-1 autoantibodies in human Trypanosoma cruzi infection: Differential expression of this beta-galactoside-binding protein in cardiac Chagas' disease. Clin Exp Immunol. 124:266-273. (Pubitemid 32587611)
21. Guleria I, Khosroshanhi A, Ansari MJ, Habicht A, Azuma M, Yagita H, Noelle RJ, Coyle A, Mellor AL, Khoury SJ, et al. 2005. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med. 202:231-237. (Pubitemid 41043819)
22. He J, Baum LG. 2006. Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration. Lab Invest. 86:578-590. (Pubitemid 43780439)
23. Hirota Y, Burnum KE, Acar N, Rabinovich GA, Daikoku T, Dey SK. 2012. Galectin-1 markedly reduces the incidence of resorptions in mice missing immunophilin FKBP52. Endocrinology. 153:2486-2493.
24. Hoyer KK, Dooms H, Barron L, Abbas AK. 2008. Interleukin-2 in the development and control of inflammatory disease. Immunol Rev. 226:19-28.
25. Iglesias MM, Rabinovich GA, Ivanovic V, Sotomayor C, Wolfenstein-Todel C. 1998. Galectin-1 from ovine placenta-amino-acid sequence, physicochemical properties and implications in T-cell death. Eur J Biochem. 252:400-407. (Pubitemid 28156864)
26. Ilarregui JM, Croci DO, Bianco GA, Toscano MA, Salatino M, Vermeulen ME, Geffner JR, Rabinovich GA. 2009. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat Immunol. 10:981-991.
27. Jasper MJ, Tremellen KP, Robertson SA. 2006. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod. 12:301-308. (Pubitemid 43821793)
28. Jeschke U, Reimer T, Bergemann C, Wiest I, Schulze S, Friese K, Walzel H. 2004. Binding of galectin-1 (gal-1) on trophoblast cells and inhibition of hormone production of trophoblast tumor cells in vitro by gal-1. Histochem Cell Biol. 121:501-508. (Pubitemid 38916438)
29. Juszczynski P, Ouyang J, Monti S, Rodig SJ, Takeyama K, Abramson J, Chen W, Kutok JL, Rabinovich GA, Shipp MA. 2007. The AP1-dependent secretion of Galectin-1 by Reed Sternberg cells fosters immune privilege in classical Hodgkin lymphoma. Proc Natl Acad Sci USA. 104: 13134-13139. (Pubitemid 351737605)
30. Kallikourdis M, Andersen KG, Welch KA, Betz AG. 2007. Alloantigenenhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc Natl Acad Sci USA. 104:594-599. (Pubitemid 46123070)
31. Kayisli UA, Selam B, Guzeloglu-Kayisli O, Demir R, Arici A. 2003. Human chorionic gonadotropin contributes to maternal immunotolerance and endometrial apoptosis by regulating Fas-Fas ligand system. J Immunol. 171:2305-2313. (Pubitemid 37025535)
32. Kolundži? N, Boji?-Trbojevi? Ž, Kova?evi? T, Stefanoska I, Kadoya T, Vi?ovac L. 2011. Galectin-1 is part of human trophoblast invasion machinery-a functional study in vitro. PLoS One. 6:e28514.
33. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, Masch R, Lockwood CJ, Schachter AD, Park PJ, et al. 2003. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med. 198:1201-1212. (Pubitemid 37323385)
34. Kopcow HD, Rosetti F, Leung Y, Allan DS, Kutok JL, Strominger JL. 2008. T cell apoptosis at the maternal-fetal interface in early human pregnancy, involvement of galectin-1. Proc Natl Acad Sci USA. 26:3017-3022.
35. Kreisman LS, Cobb BA. 2012. Infection, inflammation and host carbohydrates: A glyco-evasion hypothesis. Glycobiology 22:1019-1030.
36. Kuo PL, Hung JY, Huang SK, Chou SH, Cheng DE, Jong YJ, Hung CH, Yang CJ, Tsai YM, Hsu YL, et al. 2011. Lung cancer-derived galectin-1 mediates dendritic cell energy through inhibitor of DNA binding 3/IL-10 signaling pathway. J Immunol. 186:1521-1530.
37. Kwak-Kim J, Yang KM, Gilman-Sachs A. 2009. Recurrent pregnancy loss: A disease of inflammation and coagulation. J Obstet Gynaecol Res. 35:609-622.
38. Leber A, Teles A, Zenclussen AC. 2010. Regulatory T cells and their role in pregnancy. Am J Reprod Immunol. 63:445-459.
39. Ledee-Bataille N, Dubanchet S, Coulomb-L'hermine A, Durand-Gasselin I, Frydman R, Chaouat G. 2004. A new role for natural killer cells, interleukin (IL)-12, and IL-18 in repeated implantation failure after in vitro fertilization. Fertil Steril. 81:59-65. (Pubitemid 38058328)
40. Ledeen RW, Wu G, André S, Bleich D, Huet G, Kaltner H, Kopitz J, Gabius HJ. 2012. Beyond glycoproteins as galectin counterreceptors: Effector T cell growth control of tumors via ganglioside GM1. Ann N Y Acad Sci. 1253:206-221.
41. Liu AX, Jin F, Zhang WW, Zhou TH, Zhou CY, Yao WM, Qian YL, Huang HF. 2006. Proteomic analysis on the alteration of protein expression in the placental villous tissue of early pregnancy loss. Biol Reprod. 75:414-420. (Pubitemid 44268076)
42. Maquoi E, van den Brule FA, Castronovo V, Foidart JM. 1997. Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts. Placenta. 18:433-439. (Pubitemid 27326313)
43. Molvarec A, Blois SM, Stenczer B, Toldi G, Tirado-Gonzalez I, Ito M, Shima T, Yoneda S, Vásárhelyi B, Rigó J, Jr, et al. 2011. Peripheral blood galectin-1-expressing T and natural killer cells in normal pregnancy and preeclampsia. Clin Immunol. 139:48-56.
44. Montiel JL, Monsiváis-Urenda A, Figueroa-Vega N, Moctezuma JF, Burgos-Vargas R, González-Amaro R, Rosenstein Y. 2010. Anti-CD43 and anti-galectin-1 autoantibodies in patients with systemic lupus erythematosus. Scand J Rheumatol. 39:50-57.
45. Mor G. 2008. Inflammation and pregnancy. The role of Toll-like receptors in trophoblast-immune interaction. Ann NY Acad Sci. 1127:121-128. (Pubitemid 351563099)
46. Mor G, Cardenas I. 2010. The immune system in pregnancy: A unique complexity. Am J Reprod Immunol. 63:425-433.
47. Motran CC, Molinder KM, Liu SD, Poirier F, Miceli MC. 2008. Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function. Eur J Immunol. 38:3015-3027.
48. Norling LV, Sampaio AL, Cooper D, Perretti M. 2008. Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking. FASEB J. 22:682-690. (Pubitemid 351348121)
49. Ohshima K, Nakashima M, Sonoda K, Kikuchi M, Watanabe T. 2001. Expression of RCAS1 and FasL in human trophoblasts and uterine glands during pregnancy: The possible role in immune privilege. Clin Exp Immunol. 123:481-486. (Pubitemid 32289969)
50. Pace KE, Lee C, Stewart PL, Baum LG. 1999. Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. J Immunol. 163:3801-3811. (Pubitemid 29450905)
51. Perillo NL, Pace KE, Seilhamer JJ, Baum LG. 1995. Apoptosis of T cells mediated by galectin-1. Nature. 378:736-739. (Pubitemid 126647279)
52. Perone MJ, Bertera S, Shufesky WJ, Divito SJ, Montecalvo A, Mathers AR, Larregina AT, Pang M, Seth N, Wucherpfennig KW, et al. 2009. Suppression of autoimmune diabetes by soluble galectin-1. J Immunol. 182:2641-2653.
53. Phillips B, Knisley K, Weitlauf KD, Dorsett J, Lee V, Weitlauf H. 1996. Differential expression of two β-galactoside-binding lectins in the reproductive tracts of pregnant mice. Biol Reprod. 55:548-558. (Pubitemid 26295053)
54. Phillips TA, Ni J, Pan G, Ruben SM, Wei YF, Pace JL, Hunt JS. 1999. TRAIL (Apo-2L) and TRAIL receptors in human placentas. Implications for immune privilege. J Immunol. 162:6053-6059. (Pubitemid 29314964)
55. Poirier F, Robertson EJ. 1993. Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development. 119:1229-1236. (Pubitemid 23358589)
56. Rabinovich GA, Croci DO. 2012. Regulatory circuits mediated by lectinglycan interactions in autoimmunity and cancer. Immunity. 23:322-335.
57. Rabinovich GA, Daly G, Dreja H, Tailor H, Riera CM, Hirabayashi J, Chernajovsky Y. 1999. Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J Exp Med. 190:385-398.
58. Rabinovich GA, Ramhorst R, Corigliano A, Daroqui C, Rubistein N, Bal de Kier E, Fainboim L. 2002. Induction of allogeneic T-cell hyporesponsiveness by galectin-1-mediated apoptotic and non-apoptotic mechanisms. Cell Death Differ. 9:661-670. (Pubitemid 34618872)
59. Rabinovich GA, Rubinstein N, Fainboim L. 2002. Unlocking the secrets of galectins: A challenge at the frontier of glyco-immunology. J Leukoc Biol. 71:741-752.
60. Rabinovich GA, van Kooyk Y, Cobb BA. 2012. Glycobiology of immune responses. Ann NY Acad Sci. 1253:1-15.
61. Rajasagi NK, Suryawanshi A, Sehrawat S, Reddy PB, Mulik S, Hirashima M, Rouse BT. 2012. Galectin-1 reduces the severity of herpes simplex virus-induced ocular immunopathological lesions. J Immunol. 188: 4631-4643.
62. Ramhorst R, Fraccaroli L, Aldo P, Alvero AB, Cardenas I, Perez Leirós C, Mor G. 2012. Modulation and recruitment of inducible regulatory T cells by first trimester trophoblast cells. Am J Reprod Immunol. 67:17-27.
63. Romero MD, Muiño JC, Bianco GA, Ferrero M, Juarez CP, Luna JD, Rabinovich GA. 2006. Circulating anti-galectin-1 antibodies are associated with the severity of ocular disease in autoimmune and infectious uveitis. Invest Ophthalmol Vis Sci. 47:1550-1556. (Pubitemid 46780764)
64. Rubinstein N, Alvarez M, Zwirner NW, Toscano MA, Ilarregui JM, Bravo A, Mordoh J, Fainboim L, Podhajcer OL, Rabinovich GA. 2004. 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. 5:241-251. (Pubitemid 38402116)
65. Saito S, Nakashima A, Shima T, Ito M. 2010. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol. 63:601-610.
66. Soldati R, Berger E, Zenclussen AC, Jorch G, Lode HN, Salatino M, Rabinovich GA, Fest S. 2011. Neuroblastoma triggers an immunoevasive program involving galectin-1-dependent modulation of T cell and dendritic cell compartments. Int J Cancer. doi:10.1002/ijc.26498.
67. Stowell SR, Qian Y, Karmakar S, Koyama NS, Dias-Baruffi M, Leffler H, McEver RP, Cummings RD. 2008. Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J Immunol. 180:3091-3102.
68. Teklenburg G, Salker M, Heijnen C, Macklon NS, Brosens JJ. 2010. The molecular basis of recurrent pregnancy loss: Impaired natural embryo selection. Mol Hum Reprod. 16:886-895.
69. Terness P, Kallikourdis M, Betz AG, Rabinovich GA, Saito S, Clark DA. 2007. Tolerance signalling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells. Am J Reprod Immunol. 58:238-254. (Pubitemid 47249063)
70. Than NG, Erez O, Wildman DE, Tarca AL, Edwin SS, Abbas A, Hotra J, Kusanovic JP, Gotsch F, Hassan SS, et al. 2008. Severe preeclampsia is characterized by increased placental expression of galectin-1. J Matern Fetal Neonatal Med. 21:429-442. (Pubitemid 352000663)
71. Than NG, Romero R, Erez O, Weckle A, Tarca AL, Hotra J, Abbas A, Han YM, Kim SS, Kusanovic JP, et al. 2008. Emergence of hormonal and redox regulation of galectin-1 in placental mammals: Implication in maternal-fetal immune tolerance. Proc Natl Acad Sci USA. 105: 15819-15824.
72. Than NG, Romero R, Kim CJ, McGowen MR, Papp Z, Wildman DE. 2012. Galectins: Guardians of eutherian pregnancy at the maternal-fetal interface. Trends Endocrinol Metab. 23:23-31.
73. Thijssen VL, Postel R, Brandwijk RJ, Dings RP, Nesmelova I, Satijin S, Verhofstad N, Nakabeppu Y, Baum LG, Bakkers J, et al. 2006. Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA. 103:15975-15980. (Pubitemid 44657577)
74. Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, Hernandez JD, Zwirner NW, Poirier F, Riley EM, Baum LG, et al. 2007. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol. 8:825-834. (Pubitemid 47099035)
75. Toscano MA, Commodaro AG, Ilarregui JM, Bianco GA, Liberman A, Serra HM, Hirabayashi J, Rizzo LV, Rabinovich GA. 2006. Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2-and T regulatory-mediated anti-inflammatory responses. J Immunol. 176: 6323-6332.
76. Toth B, Jeschkec U, Rogenhoferb N, Scholzc C, Würfeld W, Thalerb CJ, Makrigiannakise A. 2010. Recurrent miscarriage: Current concepts in diagnosis and treatment. J Reprod Immunol. 85:25-32.
77. Trowsdale J, Betz AG. 2006. Mother's little helpers: Mechanisms of maternal-fetal tolerance. Nat Immunol. 7:241-246.
78. van der Leij J, van den Berg A, Harms G, Eschbach H, Vos H, Zwiers P, van Weeghel R, Groen H, Poppema S, Visser L. 2007. Strongly enhanced IL-10 production using stable galectin-1 homodimers. Mol Immunol. 44: 506-513. (Pubitemid 44287047)
79. Van Voorhis BJ, Anderson DJ, Hill JA. 1989. The effects of RU 486 on immune function and steroid-induced immunosuppression in vitro. J Clin Endocrinol Metab. 69:1195-1199. (Pubitemid 20010047)
80. Vasta GR. 2012. Galectins as pattern recognition receptors: Structure, function, and evolution. Adv Exp Med Biol. 946:21-36.
81. von Wolff M, Wang X, Gabius HJ, Strowitzki T. 2005. Galectin fingerprinting in human endometrium and decidua during the menstrual cycle and in early gestation. Mol Hum Reprod. 11:189-194. (Pubitemid 40662752)
82. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk HD. 2005. Abnormal T-cell reactivity against paternal antigens in spontaneous abortions: Adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am J Pathol. 166:811-822. (Pubitemid 40315638)