Placental Galectins Are Key Players in Regulating the Maternal Adaptive Immune Response.
Abortion, Spontaneous
/ immunology
Adaptive Immunity
/ immunology
Adult
Apoptosis
/ immunology
Biomarkers
/ metabolism
Cytokines
/ immunology
Female
Galectins
/ immunology
Humans
Immunohistochemistry
/ methods
Placenta
/ immunology
Pregnancy
Pregnancy Trimester, First
/ immunology
T-Lymphocytes
/ immunology
Young Adult
PP13
angiogenesis
glycomics
immune privilege
trophoblast differentiation
trophoblast invasion
Journal
Frontiers in immunology
ISSN: 1664-3224
Titre abrégé: Front Immunol
Pays: Switzerland
ID NLM: 101560960
Informations de publication
Date de publication:
2019
2019
Historique:
received:
11
02
2019
accepted:
16
05
2019
entrez:
6
7
2019
pubmed:
6
7
2019
medline:
23
10
2020
Statut:
epublish
Résumé
Galectins are potent immunomodulators that regulate maternal immune responses in pregnancy and prevent the rejection of the semi-allogeneic fetus that also occurs in miscarriages. We previously identified a gene cluster on Chromosome 19 that expresses a subfamily of galectins, including galectin-13 (Gal-13) and galectin-14 (Gal-14), which emerged in anthropoid primates. These galectins are expressed only by the placenta and induce the apoptosis of activated T lymphocytes, possibly contributing to a shifted maternal immune balance in pregnancy. The placental expression of Gal-13 and Gal-14 is decreased in preeclampsia, a life-threatening obstetrical syndrome partly attributed to maternal anti-fetal rejection. This study is aimed at revealing the effects of Gal-13 and Gal-14 on T cell functions and comparing the expression of these galectins in placentas from healthy pregnancies and miscarriages. First-trimester placentas were collected from miscarriages and elective termination of pregnancies, tissue microarrays were constructed, and then the expression of Gal-13 and Gal-14 was analyzed by immunohistochemistry and immunoscoring. Recombinant Gal-13 and Gal-14 were expressed and purified, and their effects were investigated on primary peripheral blood T cells. The binding of Gal-13 and Gal-14 to T cells and the effects of these galectins on apoptosis, activation marker (CD25, CD71, CD95, HLA-DR) expression and cytokine (IL-1β, IL-6, IL-8, IL-10, IFNγ) production of T cells were examined by flow cytometry. Gal-13 and Gal-14 are primarily expressed by the syncytiotrophoblast at the maternal-fetal interface in the first trimester, and their placental expression is decreased in miscarriages compared to first-trimester controls. Recombinant Gal-13 and Gal-14 bind to T cells in a population- and activation-dependent manner. Gal-13 and Gal-14 induce apoptosis of Th and Tc cell populations, regardless of their activation status. Out of the investigated activation markers, Gal-14 decreases the cell surface expression of CD71, Gal-13 increases the expression of CD25, and both galectins increase the expression of CD95 on T cells. Non-activated T cells produce larger amounts of IL-8 in the presence of Gal-13 or Gal-14. In conclusion, these results show that Gal-13 and Gal-14 already provide an immunoprivileged environment at the maternal-fetal interface during early pregnancy, and their reduced expression is related to miscarriages.
Identifiants
pubmed: 31275299
doi: 10.3389/fimmu.2019.01240
pmc: PMC6593412
doi:
Substances chimiques
Biomarkers
0
Cytokines
0
Galectins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1240Subventions
Organisme : NICHD NIH HHS
ID : HHSN275201300006C
Pays : United States
Références
Immunol Today. 1999 Mar;20(3):114-8
pubmed: 10203701
Protein Eng. 2001 Dec;14(12):993-1000
pubmed: 11809930
Biochim Biophys Acta. 2002 Apr 12;1574(3):407-11
pubmed: 11997112
Nat Rev Immunol. 2002 Sep;2(9):656-63
pubmed: 12209134
Biochim Biophys Acta. 2002 Sep 19;1572(2-3):209-31
pubmed: 12223271
Biol Reprod. 2002 Oct;67(4):1211-7
pubmed: 12297538
Am J Obstet Gynecol. 2002 Oct;187(4):889-93
pubmed: 12388971
J Immunol. 2003 Mar 15;170(6):3369-76
pubmed: 12626597
Am J Reprod Immunol. 1992 Apr-May;27(3-4):117-23
pubmed: 1418402
N Engl J Med. 2004 Feb 12;350(7):672-83
pubmed: 14764923
Eur J Biochem. 2004 Mar;271(6):1065-78
pubmed: 15009185
J Immunol. 2004 Jun 1;172(11):6709-14
pubmed: 15153487
Am J Reprod Immunol. 2004 Apr;51(4):275-82
pubmed: 15212680
J Clin Pathol. 2004 Aug;57(8):785-92
pubmed: 15280396
J Soc Gynecol Investig. 2004 Sep;11(6):342-52
pubmed: 15350246
J Pathol. 2004 Dec;204(5):511-8
pubmed: 15538736
FASEB J. 2005 May;19(7):681-93
pubmed: 15857883
Am J Obstet Gynecol. 1992 May;166(5):1576-87
pubmed: 1595815
J Matern Fetal Neonatal Med. 2005 Apr;17(4):239-45
pubmed: 16147832
Biochemistry. 2005 Sep 20;44(37):12564-71
pubmed: 16156668
Crit Rev Immunol. 2005;25(5):375-88
pubmed: 16167887
Nat Immunol. 2005 Dec;6(12):1245-52
pubmed: 16286920
J Immunol. 2006 Jan 15;176(2):778-89
pubmed: 16393961
Nat Immunol. 2006 Mar;7(3):241-6
pubmed: 16482172
J Immunol. 2006 Mar 15;176(6):3585-92
pubmed: 16517727
Biol Reprod. 2006 Sep;75(3):414-20
pubmed: 16738225
Immunol Rev. 2006 Aug;212:330-43
pubmed: 16903924
Am J Obstet Gynecol. 2007 Apr;196(4):372-81
pubmed: 17403426
Mol Aspects Med. 2007 Apr;28(2):192-209
pubmed: 17433431
Expert Rev Mol Med. 2007 Apr 27;9(10):1-14
pubmed: 17462112
Cell Tissue Res. 2007 Sep;329(3):559-69
pubmed: 17549520
Nat Immunol. 2007 Aug;8(8):825-34
pubmed: 17589510
Biol Reprod. 2007 Oct;77(4):590-8
pubmed: 17596562
Am J Obstet Gynecol. 2007 Jul;197(1):35.e1-7
pubmed: 17618748
Semin Immunopathol. 2007 Jun;29(2):115-22
pubmed: 17621697
Semin Immunopathol. 2007 Jun;29(2):151-62
pubmed: 17621700
Semin Immunopathol. 2007 Jun;29(2):163-7
pubmed: 17621701
Placenta. 2007 Nov-Dec;28(11-12):1165-73
pubmed: 17664004
Am J Reprod Immunol. 2007 Sep;58(3):238-54
pubmed: 17681041
Am J Reprod Immunol. 2007 Sep;58(3):280-8
pubmed: 17681044
Annu Rev Med. 2008;59:61-78
pubmed: 17937587
J Matern Fetal Neonatal Med. 2007 Nov;20(11):777-92
pubmed: 17943641
Placenta. 2008 Mar;29 Suppl A:S86-91
pubmed: 17950457
Nat Med. 2007 Dec;13(12):1450-7
pubmed: 18026113
J Matern Fetal Neonatal Med. 2008 Jan;21(1):9-23
pubmed: 18175241
Am J Reprod Immunol. 2008 May;59(5):425-32
pubmed: 18405313
Ann N Y Acad Sci. 2008 Apr;1127:121-8
pubmed: 18443339
J Matern Fetal Neonatal Med. 2008 May;21(5):279-87
pubmed: 18446652
Am J Obstet Gynecol. 2008 Aug;199(2):122.e1-122.e11
pubmed: 18539259
J Matern Fetal Neonatal Med. 2008 Jun;21(6):389-402
pubmed: 18570117
J Matern Fetal Neonatal Med. 2008 Jul;21(7):429-42
pubmed: 18570123
J Matern Fetal Neonatal Med. 2008 Aug;21(8):529-47
pubmed: 18609361
Virchows Arch. 2008 Oct;453(4):387-400
pubmed: 18791734
Proc Natl Acad Sci U S A. 2008 Oct 14;105(41):15819-24
pubmed: 18824694
Eur J Immunol. 2008 Nov;38(11):3015-27
pubmed: 18991278
Proc Natl Acad Sci U S A. 2008 Nov 25;105(47):18472-7
pubmed: 19011096
Nat Rev Immunol. 2009 May;9(5):338-52
pubmed: 19365409
J Reprod Immunol. 2009 Jun;80(1-2):91-9
pubmed: 19371956
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9731-6
pubmed: 19497882
Reprod Biol Endocrinol. 2009 Jul 14;7:70
pubmed: 19602262
Scand J Immunol. 2009 Sep;70(3):206-15
pubmed: 19703010
Int J Dev Biol. 2010;54(2-3):457-67
pubmed: 19757386
J Reprod Immunol. 2009 Dec;83(1-2):109-16
pubmed: 19875178
Glycobiology. 2010 Mar;20(3):270-9
pubmed: 19939826
Biol Reprod. 2010 May;82(5):809-14
pubmed: 20089887
Trends Endocrinol Metab. 2010 Jul;21(7):428-34
pubmed: 20304670
J Reprod Immunol. 2010 May;85(1):51-7
pubmed: 20347158
Am J Reprod Immunol. 2010 Jun;63(6):506-19
pubmed: 20384620
Placenta. 2010 Jul;31(7):561-7
pubmed: 20427084
Am J Reprod Immunol. 2010 Jun;63(6):601-10
pubmed: 20455873
Placenta. 2011 Feb;32 Suppl:S21-9
pubmed: 20541258
FEBS Lett. 2010 Jul 16;584(14):3193-7
pubmed: 20541553
BJOG. 2010 Oct;117(11):1384-9
pubmed: 20840693
Clin Immunol. 2011 Apr;139(1):48-56
pubmed: 21292557
Ann N Y Acad Sci. 2011 Mar;1221:80-7
pubmed: 21401634
Immunol Rev. 2011 May;241(1):20-38
pubmed: 21488887
Am J Obstet Gynecol. 2011 Jul;205(1):83.e8-16
pubmed: 21514552
Am J Obstet Gynecol. 2011 Aug;205(2):156.e1-14
pubmed: 21596368
PLoS One. 2011;6(7):e21564
pubmed: 21799738
Reprod Sci. 2012 Jan;19(1):16-30
pubmed: 21989657
Clin Immunol. 2012 Feb;142(2):107-16
pubmed: 22019770
Trends Endocrinol Metab. 2012 Jan;23(1):23-31
pubmed: 22036528
Reprod Sci. 2013 Feb;20(2):154-67
pubmed: 22614625
Wien Med Wochenschr. 2012 May;162(9-10):191-5
pubmed: 22717872
Glycobiology. 2012 Oct;22(10):1374-86
pubmed: 22752006
Front Immunol. 2012 Jul 13;3:199
pubmed: 22811679
J Reprod Immunol. 2012 Sep;95(1-2):1-14
pubmed: 22819759
Mol Hum Reprod. 2013 Jan;19(1):43-53
pubmed: 23002109
Front Immunol. 2012 Nov 27;3:362
pubmed: 23205021
Nat Rev Immunol. 2013 Jan;13(1):23-33
pubmed: 23237963
Am J Obstet Gynecol. 2013 Apr;208(4):287.e1-287.e15
pubmed: 23333542
Am J Obstet Gynecol. 2013 Apr;208(4):310.e1-310.e11
pubmed: 23333548
Am J Reprod Immunol. 2013 Mar;69(3):212-30
pubmed: 23347265
Fetal Diagn Ther. 2013;33(4):257-64
pubmed: 23406577
Am J Reprod Immunol. 2013 Apr;69(4):395-407
pubmed: 23432707
J Reprod Immunol. 2013 Mar;97(1):36-42
pubmed: 23432870
J Leukoc Biol. 2013 Aug;94(2):247-57
pubmed: 23633414
Semin Immunopathol. 2013 Jul;35(4):439-53
pubmed: 23649713
Nat Med. 2013 May;19(5):548-56
pubmed: 23652115
Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11451-6
pubmed: 23798433
PLoS One. 2013 Jun 17;8(6):e67029
pubmed: 23799140
Virchows Arch. 2013 Sep;463(3):445-58
pubmed: 23807541
J Reprod Immunol. 2014 Mar;101-102:127-134
pubmed: 23953090
J Perinat Med. 2014 Sep;42(5):591-601
pubmed: 24607918
PLoS One. 2014 Mar 20;9(3):e92371
pubmed: 24651720
Front Immunol. 2014 Mar 28;5:125
pubmed: 24734032
Front Immunol. 2014 May 08;5:196
pubmed: 24847324
Front Immunol. 2014 May 26;5:244
pubmed: 24904591
Cell Mol Immunol. 2014 Nov;11(6):571-81
pubmed: 24954221
Am J Reprod Immunol. 2014 Aug;72(2):107-16
pubmed: 24995526
Cell Mol Immunol. 2014 Nov;11(6):522-37
pubmed: 25066422
Front Oncol. 2014 Jul 02;4:131
pubmed: 25072019
Science. 2014 Aug 15;345(6198):760-5
pubmed: 25124429
J Immunol. 2014 Sep 15;193(6):3070-9
pubmed: 25135830
Front Immunol. 2014 Aug 20;5:348
pubmed: 25191322
Methods Mol Biol. 2015;1207:1-35
pubmed: 25253130
Placenta. 2014 Nov;35(11):855-65
pubmed: 25266889
Am J Reprod Immunol. 2015 Jun;73(6):487-500
pubmed: 25269386
Eur J Obstet Gynecol Reprod Biol. 2014 Nov;182:194-201
pubmed: 25305662
Placenta. 2014 Dec;35(12):1027-34
pubmed: 25449030
Front Immunol. 2014 Dec 23;5:652
pubmed: 25566263
Pathol Oncol Res. 2015 Jul;21(3):659-68
pubmed: 25583406
J Reprod Immunol. 2015 Apr;108:33-41
pubmed: 25622880
Am J Reprod Immunol. 2015 Sep;74(3):201-8
pubmed: 25640631
J Reprod Immunol. 2015 Apr;108:83-9
pubmed: 25771398
J Reprod Infertil. 2015 Apr-Jun;16(2):59-60
pubmed: 25927021
Obstet Gynecol. 2015 May;125(5):1258-67
pubmed: 25932865
J Biol Chem. 2015 Jul 3;290(27):16797-811
pubmed: 25947381
J Pathol Transl Med. 2015 May;49(3):181-208
pubmed: 26018511
Front Immunol. 2015 Jun 01;6:189
pubmed: 26082773
Adv Exp Med Biol. 2015;868:211-25
pubmed: 26178852
Am J Obstet Gynecol. 2015 Dec;213(6):836.e1-836.e18
pubmed: 26232508
Fetal Diagn Ther. 2016;39(1):56-63
pubmed: 26314825
Cold Spring Harb Perspect Med. 2015 Sep 18;5(12):null
pubmed: 26385089
Am J Obstet Gynecol. 2015 Oct;213(4 Suppl):S131-7
pubmed: 26428492
Chimerism. 2015 Apr 3;6(1-2):8-20
pubmed: 26517600
Cell Tissue Res. 2016 Jan;363(1):249-265
pubmed: 26572540
PLoS One. 2016 Jan 20;11(1):e0147186
pubmed: 26789128
Immunology. 2016 May;148(1):13-21
pubmed: 26855005
Cell Adh Migr. 2016 Mar 3;10(1-2):208-25
pubmed: 26933824
J Leukoc Biol. 2016 Jun;99(6):825-38
pubmed: 27004978
Int J Mol Sci. 2016 Apr 28;17(5):
pubmed: 27136536
Arch Pathol Lab Med. 2016 Jul;140(7):698-713
pubmed: 27223167
J Reprod Immunol. 2016 Nov;118:92-99
pubmed: 27792886
Hypertens Res. 2017 Apr;40(4):305-310
pubmed: 27829661
Front Immunol. 2016 Dec 05;7:565
pubmed: 27994595
Glycobiology. 2017 May 1;27(5):457-468
pubmed: 28104787
J Pathol Transl Med. 2017 May;51(3):264-283
pubmed: 28226203
Trends Immunol. 2017 Apr;38(4):272-286
pubmed: 28279591
Nat Rev Immunol. 2017 Aug;17(8):483-494
pubmed: 28480895
Hypertens Pregnancy. 2017 May;36(2):186-195
pubmed: 28524718
Front Immunol. 2017 Jun 14;8:702
pubmed: 28659928
Fetal Diagn Ther. 2018;43(4):250-265
pubmed: 28728156
Proc Natl Acad Sci U S A. 2017 Aug 8;114(32):E6566-E6575
pubmed: 28747528
Mol Cell Biochem. 2018 Jan;438(1-2):141-152
pubmed: 28770473
F1000Res. 2017 Jul 25;6:1216
pubmed: 28781765
Curr Opin Genet Dev. 2017 Dec;47:24-32
pubmed: 28850905
Sci Immunol. 2017 Sep 1;2(15):null
pubmed: 28864494
Front Immunol. 2017 Sep 15;8:1138
pubmed: 28966619
Int J Mol Sci. 2017 Oct 17;18(10):null
pubmed: 29039764
J Reprod Immunol. 2017 Nov;124:44-53
pubmed: 29055791
Am J Reprod Immunol. 2018 Apr;79(4):e12786
pubmed: 29154462
Front Immunol. 2017 Dec 13;8:1809
pubmed: 29326701
Am J Reprod Immunol. 2018 Jun;79(6):e12820
pubmed: 29457302
Am J Reprod Immunol. 2018 May;79(5):e12851
pubmed: 29577468
J Immunol Res. 2018 Jan 31;2018:9517842
pubmed: 29651447
Immunity. 2018 May 15;48(5):951-962.e5
pubmed: 29768178
Front Immunol. 2018 May 09;9:993
pubmed: 29867970
J Immunol. 2018 Jul 15;201(2):325-334
pubmed: 29987001
Cancer Res. 1986 Apr;46(4 Pt 1):1759-63
pubmed: 3004704
Front Immunol. 2018 Jul 20;9:1659
pubmed: 30079067
Am J Reprod Immunol. 2018 Oct;80(4):e13035
pubmed: 30091267
Nat Commun. 2018 Aug 17;9(1):3287
pubmed: 30120234
Nat Commun. 2018 Aug 17;9(1):3288
pubmed: 30120235
Front Immunol. 2018 Aug 08;9:1661
pubmed: 30135684
Front Immunol. 2018 Aug 14;9:1897
pubmed: 30154799
Front Immunol. 2018 Aug 24;9:1934
pubmed: 30197648
Proc Natl Acad Sci U S A. 1986 Oct;83(20):7603-7
pubmed: 3020551
J Clin Invest. 2018 Oct 1;128(10):4224-4235
pubmed: 30272581
J Obstet Gynaecol Res. 2019 Jan;45(1):39-46
pubmed: 30338894
Front Immunol. 2018 Dec 13;9:2890
pubmed: 30619262
Sci Immunol. 2019 Jan 11;4(31):null
pubmed: 30635356
Placenta. 2019 Jan 15;76:30-39
pubmed: 30803712
Int J Womens Health. 2019 Mar 27;11:213-222
pubmed: 30988643
Front Immunol. 2019 Apr 18;10:846
pubmed: 31057559
Proc Natl Acad Sci U S A. 1981 May;78(5):3039-43
pubmed: 6265934
Oncodev Biol Med. 1983;4(5):343-50
pubmed: 6856484
Nature. 1995 Dec 14;378(6558):736-9
pubmed: 7501023
J Exp Med. 1995 Jan 1;181(1):71-7
pubmed: 7528780
Am J Obstet Gynecol. 1993 Nov;169(5):1299-303
pubmed: 8238198
J Reprod Immunol. 1996 Aug;31(1-2):81-95
pubmed: 8887124
Placenta. 1997 Jul-Aug;18(5-6):433-9
pubmed: 9250706
Dev Dyn. 1997 Aug;209(4):399-405
pubmed: 9264263
Mol Hum Reprod. 1997 Aug;3(8):655-62
pubmed: 9294848
Hum Reprod. 1998 Mar;13(3):730-5
pubmed: 9572443