Profiling Lgals9 splice variant expression at the fetal-maternal interface: Implications in normal and pathological human pregnancy

Biology of Reproduction

Volumn 88, Issue 1, 2013, Pages

  Heusschen, Roy ^a   Freitag, Nancy ^b   Tirado González, Irene ^b   Barrientos, Gabriela ^b   Moschansky, Petra ^b   Muñoz Fernández, Raquel ^c   Leno Durán, Ester ^d   Klapp, Burghard F ^b   Thijssen, Victor L J L ^a   Blois, Sandra M ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b HUMBOLDT UNIVERSITY   (Germany)

^c INSTITUTO DE PARASITOLOGÍA Y BIOMEDICINA LÓPEZ NEYRA   (Spain)

^d UNIVERSITY OF GRANADA   (Spain)

Author keywords

IFNG; LGALS9; Normal pregnancy; Splice variants; Spontaneous abortion

Indexed keywords

ECALECTIN; GAMMA INTERFERON; LGALS9 D5 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA SPLICING; SPONTANEOUS ABORTION;

ABORTION, SPONTANEOUS; ANIMALS; BIOLOGICAL MARKERS; FEMALE; GALECTINS; GENE EXPRESSION REGULATION; HUMANS; KILLER CELLS, NATURAL; MALE; MATERNAL-FETAL RELATIONS; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; PREGNANCY; PROTEIN ISOFORMS;

MUS;

EID: 84875051565     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.105460     Document Type: Article

References (38)

1. Wada J, Kanwar YS. Identification and characterization of galectin-9, a novel beta-galactoside-binding mammalian lectin. J Biol Chem 1997; 272:6078-6086.
2. Rabinovich GA, Toscano MA. Turning 'sweet' on immunity: galectinglycan interactions in immune tolerance and inflammation. Nat Rev Immunol 2009; 9:338-352.
3. Wiersma VR, de Bruyn M, Helfrich W, Bremer E. Therapeutic potential of galectin-9 in human disease. Med Res Rev 2013; (in press). Published online ahead of print 26 July 2011; DOI 10.1002/med.20249.
4. Liu FT, Rabinovich GA. Galectins as modulators of tumor progression. Nat Rev Cancer 2005; 5:29-41.
5. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, Zheng XX, Strom TB, Kuchroo VK. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 2005; 6:1245-1252.
6. Kashio Y, Nakamura K, Abedin MJ, Seki M, Nishi N, Yoshida N, Nakamura T, Hirashima M. Galectin-9 induces apoptosis through the calcium-calpain-caspase-1 pathway. J Immunol 2003; 170:3631-3636.
7. Niwa H, Satoh T, Matsushima Y, Hosoya K, Saeki K, Niki T, Hirashima M, Yokozeki H. Stable form of galectin-9, a Tim-3 ligand, inhibits contact hypersensitivity and psoriatic reactions: a potent therapeutic tool for Th1-and/or Th17-mediated skin inflammation. Clin Immunol 2009; 132:184-194.
8. Dai SY, Nakagawa R, Itoh A, Murakami H, Kashio Y, Abe H, Katoh S, Kontani K, Kihara M, Zhang SL, Hata T, Nakamura T, et al. Galectin-. induces maturation of human monocyte-derived dendritic cells. J Immunol 2005; 175:2974-2981.
9. Wang F, He W, Yuan J, Wu K, Zhou H, Zhang W, Chen ZK. Activation of Tim-3-Galectin-9 pathway improves survival of fully allogeneic skin grafts. Transpl Immunol 2008; 19:12-19.
10. Seki M, Oomizu S, Sakata KM, Sakata A, Arikawa T, Watanabe K, Ito K, Takeshita K, Niki T, Saita N, Nishi N, Yamauchi A, et al. Galectin-. suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin Immunol 2008; 127:78-88.
11. Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B, Tirado I, Markert UR, et al. A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 2007; 13:1450-1457.
12. Popovici RM, Krause MS, Germeyer A, Strowitzki T, von Wolff M. Galectin-9: a new endometrial epithelial marker for the mid- and latesecretory and decidual phases in humans. J Clin Endocrinol Metab 2005;90:6170-6176.
13. Shimizu Y, Kabir-Salmani M, Azadbakht M, Sugihara K, Sakai K, Iwashita M. Expression and localization of galectin-9 in the human uterodome. Endocr J 2008; 55:879-887.
14. 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.
15. Froehlich R, Hambruch N, Haeger JD, Dilly M, Kaltner H, Gabius HJ, Pfarrer C. Galectin fingerprinting detects differences in expression profiles between bovine endometrium and placentomes as well as early and late gestational stages. Placenta 2012; 33:195-201.
16. Spitzenberger F, Graessler J, Schroeder HE. Molecular and functional characterization of galectin 9 mRNA isoforms in porcine and human cells and tissues. Biochimie 2001; 83:851-862.
17. Chabot S, Kashio Y, Seki M, Shirato Y, Nakamura K, Nishi N, Nakamura T, Matsumoto R, Hirashima M. Regulation of galectin-9 expression and release in Jurkat T cell line cells. Glycobiology 2002; 12:111-118.
18. Zhang F, Zheng M, Qu Y, Li J, Ji J, Feng B, Lu A, Wang M, Liu B. Different roles of galectin-9 isoforms in modulating E-selectin expression and adhesion function in LoVo colon carcinoma cells. Mol Biol Rep 2009;36:823-830.
19. Clark DA, Banwatt D, Chaouat G. Stress-triggered abortion in mice prevented by alloimmunization. Am J Reprod Immunol 1993; 29:141-147.
20. Clark DA, Arck PC, Chaouat G. Why did your mother reject you. Immunogenetic determinants of the response to environmental selective pressure expressed at the uterine level. Am J Reprod Immunol 1999; 41:5-22.
21. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993; 151:4562-4573.
22. Piccinni MP, Beloni L, Livi C, Maggi E, Scarselli G, Romagnani S. Defective production of both leukemia inhibitory factor and type 2 Thelper cytokines by decidual T cells in unexplained recurrent abortions. Nat Med 1998; 4:1020-1024.
23. Blois SM, Joachim R, Kandil J, Margni R, Tometten M, Klapp BF, Arck PC. 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 2004; 172:5893-5899.
24. Clark DA, Yu G, Arck PC, Levy GA, Gorczynski RM. MD-1 is a critical part of the mechanism causing Th1-cytokine-triggered murine fetal loss syndrome. Am J Reprod Immunol 2003; 49:297-307.
25. Nishi N, Itoh A, Shoji H, Miyanaka H, Nakamura T. Galectin-8 and galectin-9 are novel substrates for thrombin. Glycobiology 2006; 16:15C-20C.
26. Yamamoto H, Kashio Y, Shoji H, Shinonaga R, Yoshimura T, Nishi N, Nabe T, Nakamura T, Kohno S, Hirashima M. Involvement of galectin-. in guinea pig allergic airway inflammation. Int Arch Allergy Immunol 2007; 143(suppl 1):95-105.
27. Li Y, Feng J, Geng S, Wei H, Chen G, Li X, Wang L, Wang R, Peng H, Han G, Shen B. The N- and C-terminal carbohydrate recognition domains of galectin-9 contribute differently to its multiple functions in innate immunity and adaptive immunity. Mol Immunol 2011; 48:670-677.
28. Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H. Molecular cues to implantation. Endocr Rev 2004; 25:341-373.
29. Kadowaki T, Arikawa T, Shinonaga R, Oomizu S, Inagawa H, Soma G, Niki T, Hirashima M. Galectin-9 signaling prolongs survival in murine lung-cancer by inducing macrophages to differentiate into plasmacytoid dendritic cell-like macrophages. Clin Immunol 2012; 142:296-307.
30. Nobumoto A, Nagahara K, Oomizu S, Katoh S, Nishi N, Takeshita K, Niki T, Tominaga A, Yamauchi A, Hirashima M. Galectin-9 suppresses tumor metastasis by blocking adhesion to endothelium and extracellular matrices. Glycobiology 2008; 18:735-744.
31. Kageshita T, Kashio Y, Yamauchi A, Seki M, Abedin MJ, Nishi N, Shoji H, Nakamura T, Ono T, Hirashima M. Possible role of galectin-9 in cell aggregation and apoptosis of human melanoma cell lines and its clinical significance. Int J Cancer 2002; 99:809-816.
32. Yamauchi A, Kontani K, Kihara M, Nishi N, Yokomise H, Hirashima M. Galectin-9, a novel prognostic factor with antimetastatic potential in breast cancer. Breast J 2006; 12:S196-S200.
33. Dziadek M, Darling P, Zhang RZ, Pan TC, Tillet E, Timpl R, Chu ML. Expression of collagen alpha 1(VI), alpha 2(VI), and alpha 3(VI) chains in the pregnant mouse uterus. Biol Reprod 1995; 52:885-894.
34. Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA. Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod 1997; 56:169-179.
35. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 2002; 250:358-373.
36. Zhang J, Chen Z, Smith GN, Croy BA. Natural killer cell-triggered vascular transformation: maternal care before birth? Cell Mol Immunol 2011; 8:1-11.
37. Girardi G, Yarilin D, Thurman JM, Holers VM, Salmon JE. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006; 203:2165-2175.
38. Lipkowitz MS, Leal-Pinto E, Cohen BE, Abramson RG. Galectin 9 is the sugar-regulated urate transporter/channel UAT. Glycoconj J 2004; 19:491-498.