Feto-maternal immune regulation by TIM-3/galectin-9 pathway and PD-1 molecule in mice at day 14.5 of pregnancy

Placenta

Volumn 36, Issue 10, 2015, Pages 1153-1160

  Meggyes, Matyas ^a,b   Lajko, Adrienn ^a   Palkovics, Tamas ^a,b   Totsimon, Anett ^a   Illes, Zsolt ^c,d   Szereday, Laszlo ^a,b   Miko, Eva ^a,b  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Feto maternal interface; Gal 9; Immunity; PD 1; Pregnancy; TIM 3

Indexed keywords

ECALECTIN; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN; TIM 3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; GALECTIN; GALECTIN 9, MOUSE; HAVCR2 PROTEIN, MOUSE; PDCD1 PROTEIN, MOUSE; VIRUS RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DECIDUA; FEMALE; FETOMATERNAL INTERFACE; GESTATIONAL AGE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; MONONUCLEAR CELL; MOUSE; NATURAL KILLER CELL; NATURAL KILLER T CELL; NONHUMAN; PLACENTA TISSUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; RNA ISOLATION; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; BREEDING; IMMUNOLOGY; IMMUNOPHENOTYPING; MALE; METABOLISM; PLACENTA; PREGNANCY; SPLEEN;

ANIMALS; FEMALE; GALECTINS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; KILLER CELLS, NATURAL; MALE; MICE, INBRED BALB C; PLACENTA; PREGNANCY; PREGNANCY, ANIMAL; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTORS, VIRUS; SPLEEN; T-LYMPHOCYTES;

EID: 84944279190     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2015.07.124     Document Type: Article

References (36)

1. L. Monney, C.A. Sabatos, J.L. Gaglia, A. Ryu, H. Waldner, T. Chernova, and et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease [Internet] [cited 2013 Mar 12] Nature 415 6871 2002 Jan 31 536 541 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11823861
2. A.C. Anderson, D.E. Anderson, L. Bregoli, W.D. Hastings, N. Kassam, C. Lei, and et al. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells [Internet] [cited 2013 Mar 12] Science 318 5853 2007 Nov 16 1141 1143 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18006747
3. S. Nakae, M. Iikura, H. Suto, H. Akiba, D.T. Umetsu, R.H. Dekruyff, and et al. TIM-1 and TIM-3 enhancement of Th2 cytokine production by mast cells [Internet] [cited 2014 Feb 4] Blood 110 7 2007 Oct 1 2565 2568 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1988955&tool=pmcentrez&rendertype=abstract
4. J. Lee, E.W. Su, C. Zhu, S. Hainline, J. Phuah, J.A. Moroco, and et al. Phosphotyrosine-dependent coupling of Tim-3 to T-cell receptor signaling pathways [Internet] [cited 2013 Mar 6] Mol. Cell Biol. 31 19 2011 Oct 3963 3974 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3187355&tool=pmcentrez&rendertype=abstract
5. L. Chabtini, B. Mfarrej, M. Mounayar, B. Zhu, I. Batal, P.J. Dakle, and et al. TIM-3 regulates innate immune cells to induce fetomaternal tolerance J. Immunol. 190 1 2013 Jan 88 96
6. N.G. Than, R. Romero, C.J. Kim, M.R. McGowen, Z. Papp, and D.E. Wildman Galectins: guardians of eutherian pregnancy at the maternal-fetal interface [Internet] [cited 2015 Feb 18] Trends Endocrinol. Metab. 23 1 2012 Jan 23 31 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3640805&tool=pmcentrez&rendertype=abstract
7. E.L. Naka, V.C. Ponciano, M.A. Cenedeze, A. Pacheco-Silva, and N.O.S. Câmara Detection of the Tim-3 ligand, galectin-9, inside the allograft during a rejection episode [Internet] [cited 2013 Mar 12] Int. Immunopharmacol. 9 6 2009 Jun 658 662 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19100864
8. M. Moritoki, T. Kadowaki, T. Niki, D. Nakano, G. Soma, H. Mori, and et al. Galectin-9 ameliorates clinical severity of MRL/lpr lupus-prone mice by inducing plasma cell apoptosis independently of Tim-3 [Internet] [cited 2014 Feb 4] PLoS One 8 4 2013 Jan e60807 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3621869&tool=pmcentrez&rendertype=abstract
9. C.A. Sabatos, S. Chakravarti, E. Cha, A. Schubart, A. Sánchez-Fueyo, X.X. Zheng, and et al. Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance [Internet] [cited 2013 Mar 12] Nat. Immunol. 4 11 2003 Nov 1102 1110 Available from: http://www.ncbi.nlm.nih.gov/pubmed/14556006
10. C. Zhu, A.C. Anderson, A. Schubart, H. Xiong, J. Imitola, S.J. Khoury, and et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity [Internet] [cited 2014 Feb 4] Nat. Immunol. 6 12 2005 Dec 1245 1252 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16286920
11. M. Seki, S. Oomizu, K.-M. Sakata, A. Sakata, T. Arikawa, K. Watanabe, and et al. Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis [Internet] [cited 2013 Mar 12] Clin. Immunol. 127 1 2008 Apr 78 88 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18282810
12. Z.-H. Tang, S. Liang, J. Potter, X. Jiang, H.-Q. Mao, and Z. Li Tim-3/galectin-9 regulate the homeostasis of hepatic NKT cells in a murine model of nonalcoholic fatty liver disease [Internet] [cited 2014 Feb 4] J. Immunol. 190 4 2013 Feb 15 1788 1796 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3563933&tool=pmcentrez&rendertype=abstract
13. W.D. Hastings, D.E. Anderson, N. Kassam, K. Koguchi, E.A. Greenfield, S.C. Kent, and et al. TIM-3 is expressed on activated human CD4+ T cells and regulates Th1 and Th17 cytokines [Internet] [cited 2015 Jan 30] Eur. J. Immunol. 39 9 2009 Sep 2492 2501 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2759376&tool=pmcentrez&rendertype=abstract
14. Y. Ju, N. Hou, J. Meng, X. Wang, X. Zhang, D. Zhao, and et al. T cell immunoglobulin- and mucin-domain-containing molecule-3 (Tim-3) mediates natural killer cell suppression in chronic hepatitis B [Internet] [cited 2015 Feb 9] J. Hepatol. 52 3 2010 Mar 322 329 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20133006
15. L.C. Ndhlovu, S. Lopez-Vergès, J.D. Barbour, R.B. Jones, A.R. Jha, B.R. Long, and et al. Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity [Internet] [cited 2015 Feb 9] Blood 119 16 2012 Apr 19 3734 3743 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3335380&tool=pmcentrez&rendertype=abstract
16. M.K. Gleason, T.R. Lenvik, V. McCullar, M. Felices, M.S. O'Brien, S.A. Cooley, and et al. Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9 [Internet] [cited 2015 Feb 9] Blood 119 13 2012 Mar 29 3064 3072 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3321868&tool=pmcentrez&rendertype=abstract
17. C.A.M. Finney, K. Ayi, J.D. Wasmuth, P.M. Sheth, R. Kaul, M.R. Loutfy, and et al. HIV infection deregulates innate immunity to malaria despite combination antiretroviral therapy [Internet] [cited 2015 Feb 9] AIDS 27 3 2013 Jan 28 325 335 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23291537
18. C.A.M. Finney, K. Ayi, J.D. Wasmuth, P.M. Sheth, R. Kaul, M. Loutfy, and et al. HIV infection deregulates Tim-3 expression on innate cells: combination antiretroviral therapy results in partial restoration [Internet] [cited 2015 Feb 9] J. Acquir Immune Defic. Syndr. 63 2 2013 Jun 1 161 167 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23314411
19. M.E. Keir, M.J. Butte, G.J. Freeman, and A.H. Sharpe PD-1 and its ligands in tolerance and immunity [Internet] [cited 2014 May 27] Annu. Rev. Immunol. 26 2008 Jan 677 704 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18173375
20. M.N. Wykes, J.M. Horne-Debets, C.-Y. Leow, and D.S. Karunarathne Malaria drives T cells to exhaustion [Internet] [cited 2014 Jun 10] Front. Microbiol. 5 2014 Jan 249 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4034037&tool=pmcentrez&rendertype=abstract
21. H. Dong, G. Zhu, K. Tamada, and L. Chen B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion [Internet] [cited 2014 Jun 10] Nat. Med. 5 12 1999 Dec 1365 1369 Available from: http://www.ncbi.nlm.nih.gov/pubmed/10581077
22. G.J. Freeman, A.J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, and et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation [Internet] [cited 2014 Jun 3] J. Exp. Med. 192 7 2000 Oct 2 1027 1034 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2193311&tool=pmcentrez&rendertype=abstract
23. Y. Latchman, C.R. Wood, T. Chernova, D. Chaudhary, M. Borde, I. Chernova, and et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation [Internet] [cited 2014 Jun 3] Nat. Immunol. 2 3 2001 Mar 261 268 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11224527
24. A.H. Sharpe, E.J. Wherry, R. Ahmed, and G.J. Freeman The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection [Internet] [cited 2014 Jun 4] Nat. Immunol. 8 3 2007 Mar 239 245 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17304234
25. E.J. Wherry T cell exhaustion [Internet] [cited 2015 Jan 14] Nat. Immunol. 12 6 2011 Jun 492 499 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21739672
26. J. Leitner, A. Rieger, W.F. Pickl, G. Zlabinger, K. Grabmeier-Pfistershammer, and P. Steinberger TIM-3 does not act as a receptor for galectin-9 [Internet] [cited 2015 Feb 9] PLoS Pathog. 9 3 2013 Mar e1003253 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3605152&tool=pmcentrez&rendertype=abstract
27. M.W. Pfaffl, G.W. Horgan, and L. Dempfle Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR [Internet] [cited 2014 Feb 4] Nucleic Acids Res. 30 9 2002 May 1 e36 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=113859&tool=pmcentrez&rendertype=abstract
28. I. Guleria, A. Khosroshahi, M.J. Ansari, A. Habicht, M. Azuma, H. Yagita, and et al. A critical role for the programmed death ligand 1 in fetomaternal tolerance [Internet] [cited 2015 Feb 10] J. Exp. Med. 202 2 2005 Jul 18 231 237 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2213002&tool=pmcentrez&rendertype=abstract
29. R.W. Redline, and C.Y. Lu Localization of fetal major histocompatibility complex antigens and maternal leukocytes in murine placenta. Implications for maternal-fetal immunological relationship [Internet] [cited 2015 Feb 10] Lab. Invest 61 1 1989 Jul 27 36 Available from: http://www.ncbi.nlm.nih.gov/pubmed/2473277
30. A. Moffett, and C. Loke Immunology of placentation in eutherian mammals [Internet] [cited 2015 Feb 10] Nat. Rev. Immunol. 6 8 2006 Aug 584 594 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16868549
31. F.A. Zuckermann, and J.R. Head Expression of MHC antigens on murine trophoblast and their modulation by interferon [Internet] [cited 2015 Feb 10] J. Immunol. 137 3 1986 Aug 1 846 853 Available from: http://www.ncbi.nlm.nih.gov/pubmed/2424987
32. F. Wang, L. Wan, C. Zhang, X. Zheng, J. Li, and Z.K. Chen Tim-3-Galectin-9 pathway involves the suppression induced by CD4+CD25+ regulatory T cells [Internet] [cited 2015 Jan 29] Immunobiology 214 5 2009 Jan 342 349 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19362679
33. S. Oomizu, T. Arikawa, T. Niki, T. Kadowaki, M. Ueno, N. Nishi, and et al. Cell surface galectin-9 expressing Th cells regulate Th17 and Foxp3+ Treg development by galectin-9 secretion [Internet] [cited 2014 Dec 9] PLoS One 7 11 2012 Jan e48574 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3492452&tool=pmcentrez&rendertype=abstract
34. L. Mincheva-Nilsson Pregnancy and gamma/delta T cells: taking on the hard questions [Internet] [cited 2015 Feb 10] Reprod. Biol. Endocrinol. 1 2003 Dec 2 120 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=305336&tool=pmcentrez&rendertype=abstract
35. S.M. Blois, B.F. Klapp, and G. Barrientos Decidualization and angiogenesis in early pregnancy: unravelling the functions of DC and NK cells [Internet] [cited 2015 Feb 10] J. Reprod. Immunol. 88 2 2011 Mar 86 92 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21227511
36. K. Ito, M. Karasawa, T. Kawano, T. Akasaka, H. Koseki, Y. Akutsu, and et al. Involvement of decidual Valpha14 NKT cells in abortion [Internet] [cited 2015 Feb 10] Proc. Natl. Acad. Sci. U. S. A. 97 2 2000 Jan 18 740 744 Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=15400&tool=pmcentrez&rendertype=abstract