Effect of TIM-3 blockade on the immunophenotype and cytokine profile of murine uterine NK cells

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Tripathi, Sudipta ^a   Chabtini, Lola ^a   Dakle, Pranal J ^a   Smith, Brian ^a   Akiba, Hisaya ^b   Yagita, Hideo ^b   Guleria, Indira ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b JUNTENDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; T CELL IMMUNOGLOBULIN MUCIN 3; UNCLASSIFIED DRUG; CD11B ANTIGEN; CHEMOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HAVCR2 PROTEIN, MOUSE; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; INTERLEUKIN 15; LY ANTIGEN; LY6 PROTEIN, MOUSE; VIRUS RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FETOPLACENTAL UNIT; IMMUNOLOGICAL TOLERANCE; IMMUNOPHENOTYPING; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; CBA MOUSE; CELL CULTURE; CYTOLOGY; HISTOCOMPATIBILITY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PLACENTA; PREGNANCY; UTERUS;

MURINAE; MUS;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, LY; CELLS, CULTURED; CHEMOKINES; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEPATITIS A VIRUS CELLULAR RECEPTOR 2; HISTOCOMPATIBILITY, MATERNAL-FETAL; IMMUNE TOLERANCE; IMMUNOPHENOTYPING; INTERLEUKIN-15; KILLER CELLS, NATURAL; MALE; MICE, INBRED C57BL; MICE, INBRED CBA; PLACENTA; PREGNANCY; RECEPTORS, VIRUS; UTERUS;

EID: 84928243507     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123439     Document Type: Article

References (41)

1. Wang C, Tanaka T, Nakamura H, Umesaki N, Hirai K, Ishiko O, et al. (2003) Granulated metrial gland cells in the murine uterus: localization, kinetics, and the functional role in angiogenesis during pregnancy. Microsc Res Tech 60: 420-429. PMID: 12567399
2. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C (2006) Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 214: 161-185. PMID: 17100884
3. Zhang J, Croy BA, Tian Z (2005) Uterine natural killer cells: their choices, their missions. Cell Mol Immunol 2: 123-129. PMID: 16191418
4. Karimi K, Solano ME, Ashkar AA, Ho H, Steidle EM, McVey Neufeld KA, et al. (2012) Regulation of pregnancy maintenance and fetal survival in mice by CD27(low) mature NK cells. J Mol Med (Berl) 90: 1047-1057. doi: 10.1007/s00109-012-0872-5 PMID: 22358070
5. Fu B, Li X, Sun R, Tong X, Ling B, Tian Z, et al. (2013) Natural killer cells promote immune tolerance by regulating inflammatory TH17 cells at the human maternal-fetal interface. Proc Natl Acad Sci U S A 110: E231-240. doi: 10.1073/pnas.1206322110 PMID: 23271808
6. Freeman GJ, Casasnovas JM, Umetsu DT, DeKruyff RH (2010) TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol Rev 235: 172-189. doi: 10.1111/j.0105-2896.2010.00903.x PMID: 20536563
7. Yeung MY, McGrath M, Najafian N (2011) The emerging role of the TIM molecules in transplantation. Am J Transplant 11: 2012-2019. doi: 10.1111/j.1600-6143.2011.03727.x PMID: 21906254
8. Wu W, Shi Y, Li S, Zhang Y, Liu Y, Wu Y, et al. (2012) Blockade of Tim-3 signaling restores the virus-specific CD8(+) T-cell response in patients with chronic hepatitis B. Eur J Immunol 42: 1180-1191. doi: 10.1002/eji.201141852 PMID: 22539292
9. Ju Y, Hou N, Meng J, Wang X, Zhang X, Zhao D, et al. (2010) T cell immunoglobulin- and mucin-domain-containing molecule-3 (Tim-3) mediates natural killer cell suppression in chronic hepatitis B. J Hepatol 52: 322-329. doi: 10.1016/j.jhep.2009.12.005 PMID: 20133006
10. Anderson AC (2012) Tim-3, a negative regulator of anti-tumor immunity. Curr Opin Immunol 24: 213-216. doi: 10.1016/j.coi.2011.12.005 PMID: 22226204
11. Patel J, Bozeman EN, Selvaraj P (2012) Taming dendritic cells with TIM-3: another immunosuppressive strategy used by tumors. Immunotherapy 4: 1795-1798. doi: 10.2217/imt.12.126 PMID: 23240746
12. Chabtini L, Mfarrej B, Mounayar M, Zhu B, Batal I, Dakle PJ, et al. (2013) TIM-3 regulates innate immune cells to induce fetomaternal tolerance. J Immunol 190: 88-96. doi: 10.4049/jimmunol.1202176 PMID: 23180822
13. Zhao J, Lei Z, Liu Y, Li B, Zhang L, Fang H, et al. (2009) Human pregnancy up-regulates Tim-3 in innate immune cells for systemic immunity. J Immunol 182: 6618-6624. doi: 10.4049/jimmunol.0803876 PMID: 19414817
14. Ndhlovu LC, Lopez-Verges S, Barbour JD, Jones RB, Jha AR, Long BR, et al. (2012) Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity. Blood 119: 3734-3743. doi: 10.1182/blood-2011-11-392951 PMID: 22383801
15. Gleason MK, Lenvik TR, McCullar V, Felices M, O'Brien MS, Cooley SA, et al. (2012) Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood 119: 3064-3072. doi: 10.1182/blood-2011-06-360321 PMID: 22323453
16. Dardalhon V, Anderson AC, Karman J, Apetoh L, Chandwaskar R, Lee DH, et al. (2010) Tim-3/galectin-9 pathway: regulation of Th1 immunity through promotion of CD11b+Ly-6G+ myeloid cells. J Immunol 185: 1383-1392. doi: 10.4049/jimmunol.0903275 PMID: 20574007
17. Tang ZH, Liang S, Potter J, Jiang X, Mao HQ, et al. (2013) Tim-3/galectin-9 regulate the homeostasis of hepatic NKT cells in a murine model of nonalcoholic fatty liver disease. J Immunol 190: 1788-1796. doi: 10.4049/jimmunol.1202814 PMID: 23296703
18. Carlyle JR, Mesci A, Ljutic B, Belanger S, Tai LH, Li Z. (2006) Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J Immunol 176: 7511-7524. PMID: 16751398
19. Damjanov A, Damjanov I (1992) Isolation of serine protease from granulated metrial gland cells of mice and rats with lectin from Dolichos biflorus. J Reprod Fertil 95: 679-684. PMID: 1404084
20. Paffaro VA Jr., Bizinotto MC, Joazeiro PP, Yamada AT (2003) Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta 24: 479-488. PMID: 12744924
21. Yadi H, Burke S, Madeja Z, Hemberger M, Moffett A, Colucci F. (2008) Unique receptor repertoire in mouse uterine NK cells. J Immunol 181: 6140-6147. PMID: 18941204
22. Chazara O, Xiong S, Moffett A (2011) Maternal KIR and fetal HLA-C: a fine balance. J Leukoc Biol 90: 703-716. doi: 10.1189/jlb.0511227 PMID: 21873457
23. Manaster I, Mandelboim O (2010) The unique properties of uterine NK cells. Am J Reprod Immunol 63: 434-444. doi: 10.1111/j.1600-0897.2009.00794.x PMID: 20055791
24. Robertson SA, Care AS, Skinner RJ (2007) Interleukin 10 regulates inflammatory cytokine synthesis to protect against lipopolysaccharide-induced abortion and fetal growth restriction in mice. Biol Reprod 76: 738-748. PMID: 17215490
25. Murphy SP, Fast LD, Hanna NN, Sharma S (2005) Uterine NK cells mediate inflammation-induced fetal demise in IL-10-null mice. J Immunol 175: 4084-4090. PMID: 16148158
26. Murphy SP, Hanna NN, Fast LD, Shaw SK, Berg G, Padbury JF, et al. (2009) Evidence for participation of uterine natural killer cells in the mechanisms responsible for spontaneous preterm labor and delivery. Am J Obstet Gynecol 200: 308 e301-309. doi: 10.1016/j.ajog.2008.10.043 PMID: 19114277
27. Hayakawa Y, Smyth MJ (2006) CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 176: 1517-1524. PMID: 16424180
28. Walzer T, Blery M, Chaix J, Fuseri N, Chasson L, Robbins SH, et al. (2007) Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc Natl Acad Sci U S A 104: 3384-3389. PMID: 17360655
29. Raulet DH, Gasser S, Gowen BG, Deng W, Jung H (2013) Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 31: 413-441. doi: 10.1146/annurev-immunol-032712-095951 PMID: 23298206
30. Sheppard S, Triulzi C, Ardolino M, Serna D, Zhang L, Raulet DH, et al. (2013) Characterization of a novel NKG2D and NKp46 double-mutant mouse reveals subtle variations in the NK cell repertoire. Blood 121: 5025-5033. doi: 10.1182/blood-2012-12-471607 PMID: 23649470
31. Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S, Srikrishna G. (2008) Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol 181: 4666-4675. PMID: 18802069
32. Han G, Chen G, Shen B, Li Y (2013) Tim-3: an activation marker and activation limiter of innate immune cells. Front Immunol 4: 449. doi: 10.3389/fimmu.2013.00449 PMID: 24339828
33. Ashkar AA, Black GP, Wei Q, He H, Liang L, Head JR, et al. (2003) Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J Immunol 171: 2937-2944. PMID: 12960317
34. Ye W, Zheng LM, Young JD, Liu CC (1996) The involvement of interleukin (IL)-15 in regulating the differentiation of granulated metrial gland cells in mouse pregnant uterus. The Journal of experimental medicine 184: 2405-2410. PMID: 8976195
35. Barber EM, Pollard JW (2003) The uterine NK cell population requires IL-15 but these cells are not required for pregnancy nor the resolution of a Listeria monocytogenes infection. Journal of immunology 171: 37-46.
36. Varla-Leftherioti M, Spyropoulou-Vlachou M, Niokou D, Keramitsoglou T, Darlamitsou A, Tsekoura C, et al. (2003) Natural killer (NK) cell receptors' repertoire in couples with recurrent spontaneous abortions. Am J Reprod Immunol 49: 183-191. PMID: 12797525
37. Varla-Leftherioti M, Spyropoulou-Vlachou M, Keramitsoglou T, Papadimitropoulos M, Tsekoura C, Graphou O, et al. (2005) Lack of the appropriate natural killer cell inhibitory receptors in women with spontaneous abortion. Hum Immunol 66: 65-71. PMID: 15620464
38. Rahim MM, Tu MM, Mahmoud AB, Wight A, Abou-Samra E, Lima PD, et al. (2014) Ly49 receptors: innate and adaptive immune paradigms. Front Immunol 5: 145. doi: 10.3389/fimmu.2014.00145 PMID: 24765094
39. Croy BA, Chen Z, Hofmann AP, Lord EM, Sedlacek AL, Gerber SA. (2012) Imaging of vascular development in early mouse decidua and its association with leukocytes and trophoblasts. Biol Reprod 87: 125. doi: 10.1095/biolreprod.112.102830 PMID: 22954796
40. Christiansen OB (2013) Reproductive immunology. Mol Immunol 55: 8-15. doi: 10.1016/j.molimm.2012.08.025 PMID: 23062611
41. Park YJ, Song B, Kim YS, Kim EK, Lee JM, Lee GE, et al. (2013) Tumor microenvironmental conversion of natural killer cells into myeloid-derived suppressor cells. Cancer Res 73: 5669-5681. doi: 10.1158/0008-5472.CAN-13-0545 PMID: 23867469