Tim-3 Is Upregulated in NK Cells during Early Pregnancy and Inhibits NK Cytotoxicity toward Trophoblast in Galectin-9 Dependent Pathway

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Sun, Jintang ^a   Yang, Meixiang ^a   Ban, Yanli ^a   Gao, Wenjuan ^a   Song, Bingfeng ^a   Wang, Yang ^a   Zhang, Yun ^a   Shao, Qianqian ^a   Kong, Beihua ^a   Qu, Xun ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; CD94 ANTIGEN; ECALECTIN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; KIDNEY INJURY MOLECULE 1; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; GALECTIN; HAVCR2 PROTEIN, HUMAN; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; LGALS9 PROTEIN, HUMAN; MEMBRANE PROTEIN; MESSENGER RNA;

ADULT; ARTICLE; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTOXICITY ASSAY; DEGRANULATION; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SPONTANEOUS ABORTION; TROPHOBLAST; UPREGULATION; CELL CULTURE; CYTOTOXICITY; DECIDUA; ENZYME IMMUNOASSAY; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; YOUNG ADULT;

ADULT; BLOTTING, WESTERN; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; DECIDUA; FEMALE; GALECTINS; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; HUMANS; IMMUNOENZYME TECHNIQUES; KILLER CELLS, NATURAL; MEMBRANE PROTEINS; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA1; TROPHOBLASTS; UP-REGULATION; YOUNG ADULT;

EID: 84958191346     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147186     Document Type: Article

References (31)

1. Hunt JS. Stranger in a strange land. Immunological reviews. 2006; 213:36-47. PMID: 16972895.
2. Mold JE, McCune JM. Immunological tolerance during fetal development: from mouse to man. Advances in immunology. 115:73-111. PMID: 22608256. doi: 10.1016/B978-0-12-394299-9.00003-5
3. Erlebacher A. Immunology of the maternal-fetal interface. Annual review of immunology. 31:387-411. PMID: 23298207. doi: 10.1146/annurev-immunol-032712-100003
4. Santoni A, Zingoni A, Cerboni C, Gismondi A. Natural killer (NK) cells from killers to regulators: distinct features between peripheral blood and decidual NK cells. Am J Reprod Immunol. 2007; 58(3):280-8. PMID: 17681044.
5. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. The Journal of experimental medicine. 2003; 198(8):1201-12. PMID: 14568979.
6. Kopcow HD, Allan DS, Chen X, Rybalov B, Andzelm MM, Ge B, et al. Human decidual NK cells form immature activating synapses and are not cytotoxic. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(43):15563-8. PMID: 16230631.
7. Murphy SP, Fast LD, Hanna NN, Sharma S. Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol. 2005; 175(6):4084-90. PMID: 16148158.
8. Murphy SP, Hanna NN, Fast LD, Shaw SK, Berg G, Padbury JF, et al. Evidence for participation of uterine natural killer cells in the mechanisms responsible for spontaneous preterm labor and delivery. American journal of obstetrics and gynecology. 2009; 200(3):308e1-9. PMID: 19114277.
9. Abadia-Molina AC, Ruiz C, Montes MJ, King A, Loke YW, Olivares EG. Immune phenotype and cytotoxic activity of lymphocytes from human term decidua against trophoblast. Journal of reproductive immunology. 1996; 31(1-2):109-23. PMID: 8887126.
10. King A, Loke YW. Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cellular immunology. 1990; 129(2):435-48. PMID: 1696527.
11. Lachapelle MH, Miron P, Hemmings R, Roy DC. Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J Immunol. 1996; 156(10):4027-34. PMID: 8621945.
12. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nature immunology. 2005; 6(12):1245-52. PMID: 16286920.
13. Sabatos CA, Chakravarti S, Cha E, Schubart A, Sanchez-Fueyo A, Zheng XX, et al. Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nature immunology. 2003; 4(11):1102-10. PMID: 14556006.
14. Ndhlovu LC, Lopez-Verges S, Barbour JD, Jones RB, Jha AR, Long BR, et al. Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity. Blood. 119(16):3734-43. PMID: 22383801. doi: 10.1182/blood-2011-11-392951
15. Gleason MK, Lenvik TR, McCullar V, Felices M, O'Brien MS, Cooley SA, et al. Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood. 119(13):3064-72. PMID: 22323453. doi: 10.1182/blood-2011-06-360321
16. da Silva IP, Gallois A, Jimenez-Baranda S, Khan S, Anderson AC, Kuchroo VK, et al. Reversal of NKcell exhaustion in advanced melanoma by Tim-3 blockade. Cancer immunology research. 2(5):410-22. PMID: 24795354. doi: 10.1158/2326-6066.CIR-13-0171
17. Hou H, Liu W, Wu S, Lu Y, Peng J, Zhu Y, et al. Tim-3 negatively mediates natural killer cell function in LPS-induced endotoxic shock. PloS one. 9(10):e110585. PMID: 25337993. doi: 10.1371/journal.pone. 0110585
18. Chabtini L, Mfarrej B, Mounayar M, Zhu B, Batal I, Dakle PJ, et al. TIM-3 regulates innate immune cells to induce fetomaternal tolerance. J Immunol. 190(1):88-96. PMID: 23180822. doi: 10.4049/jimmunol. 1202176
19. Zhao J, Lei Z, Liu Y, Li B, Zhang L, Fang H, et al. Human pregnancy up-regulates Tim-3 in innate immune cells for systemic immunity. J Immunol. 2009; 182(10):6618-24. PMID: 19414817. doi: 10. 4049/jimmunol.0803876
20. Miko E, Meggyes M, Bogar B, Schmitz N, Barakonyi A, Varnagy A, et al. Involvement of Galectin-9/TIM-3 pathway in the systemic inflammatory response in early-onset preeclampsia. PloS one. 8(8): e71811. PMID: 23936526. doi: 10.1371/journal.pone.0071811
21. Li YH, Zhou WH, Tao Y, Wang SC, Jiang YL, Zhang D, et al. The Galectin-9/Tim-3 pathway is involved in the regulation of NK cell function at the maternal-fetal interface in early pregnancy. Cellular & molecular immunology. PMID: 25578313.
22. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, et al. Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res. 1993; 206:204-11. PMID: 7684692
23. Cerdeira AS, Rajakumar A, Royle CM, Lo A, Husain Z, Thadhani RI, et al. Conversion of peripheral blood NK cells to a decidual NK-like phenotype by a cocktail of defined factors. J Immunol. 2013; 190 (8):3939-48. doi: 10.4049/jimmunol.1202582 PMID: 23487420
24. Male V, Hughes T, McClory S, Colucci F, Caligiuri MA, Moffett A. Immature NK cells, capable of producing IL-22, are present in human uterine mucosa. J Immunol. 185(7):3913-8. PMID: 20802153. doi: 10. 4049/jimmunol.1001637
25. Wu X, Wei H, Zhang J, Tian Z. Increased uterine NK-derived IFN-gamma and TNF-Alpha in C57BL/6J mice during early gestation. Cellular & molecular immunology. 2006; 3(2):131-7. PMID: 16696900.
26. Ashkar AA, Di Santo JP, Croy BA. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. The Journal of experimental medicine. 2000; 192(2):259-70. PMID: 10899912.
27. Fu B, Li X, Sun R, Tong X, Ling B, Tian Z, et al. Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proceedings of the National Academy of Sciences of the United States of America. PMID: 23271808.
28. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nature medicine. 2006; 12(9):1065-74. PMID: 16892062.
29. Keskin DB, Allan DS, Rybalov B, Andzelm MM, Stern JN, Kopcow HD, et al. TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16-NK cells with similarities to decidual NK cells. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104(9):3378-83. PMID: 17360654.
30. Eriksson M, Meadows SK, Wira CR, Sentman CL. Unique phenotype of human uterine NK cells and their regulation by endogenous TGF-beta. Journal of leukocyte biology. 2004; 76(3):667-75. PMID: 15178706.
31. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. Journal of immunological methods. 2004; 294(1-2):15-22. PMID: 15604012.