Cytotoxic potential of decidual NK cells and CD8+ T cells awakened by infections

Journal of Reproductive Immunology

Volumn 119, Issue , 2017, Pages 85-90

  Crespo, Ângela C ^a,b   van der Zwan, Anita ^a,c   Ramalho Santos, João ^b   Strominger, Jack L ^a   Tilburgs, Tamara ^a  

^a Harvard University   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

EVT; HCMV; Human; Perforin; Pregnancy

Indexed keywords

ANTIGEN SPECIFICITY; BACTERIAL IMMUNITY; CD8+ T LYMPHOCYTE; CELL MIGRATION; CYTOLYSIS; CYTOTOXICITY; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; INFECTION; NATURAL KILLER CELL; PLACENTA DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; TROPHOBLAST; VIRUS INFECTION; ADAPTIVE IMMUNITY; DECIDUA; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PASSIVE IMMUNIZATION; PLACENTA CIRCULATION;

HLA C ANTIGEN;

ADAPTIVE IMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; DECIDUA; FEMALE; HLA-C ANTIGENS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, INNATE; IMMUNITY, MATERNALLY-ACQUIRED; INFECTION; KILLER CELLS, NATURAL; PLACENTAL CIRCULATION; PREGNANCY; TROPHOBLASTS;

EID: 85027947707     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2016.08.001     Document Type: Short Survey

References (63)

1. Ameres, S., et al. Presentation of an immunodominant immediate-early CD8+ T cell epitope resists human cytomegalovirus immunoevasion. PLoS Pathog., 9, 2013, e1003383.
2. Barman, H., et al. Cholesterol in negatively charged lipid bilayers modulates the effect of the antimicrobial protein granulysin. J. Membr. Biol. 212 (2006), 29–39.
3. Bonagura, V.R., et al. Recurrent respiratory papillomatosis: a complex defect in immune responsiveness to human papillomavirus-6 and -11. APMIS 118 (2010), 455–470.
4. Bouma, G.J., et al. Pregnancy can induce priming of cytotoxic T lymphocytes specific for paternal HLA antigens that is associated with antibody formation. Transplantation 62 (1996), 672–678.
5. Bulmer, J.N., Morrison, L., Longfellow, M., Ritson, A., Pace, D., Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum. Reprod. 6 (1991), 791–798.
6. Chaturvedi, V., et al. CXCR3 blockade protects against Listeria monocytogenes infection-induced fetal wastage. J. Clin. Invest. 125 (2015), 1713–1725.
7. Chong, A.S., Alegre, M.L., Transplantation tolerance and its outcome during infections and inflammation. Immunol. Rev. 258 (2014), 80–101.
8. Clark, D.R., et al. Perinatal Listeria monocytogenes susceptibility despite preconceptual priming and maintenance of pathogen-specific CD8(+) T cells during pregnancy. Cell. Mol. Immunol. 11 (2014), 595–605.
9. Constantin, C.M., et al. Normal establishment of virus-specific memory CD8T cell pool following primary infection during pregnancy. J. Immunol. 179 (2007), 4383–4389.
10. Cook, M., et al. Donor KIR genotype has a major influence on the rate of cytomegalovirus reactivation following T-cell replete stem cell transplantation. Blood 107 (2006), 1230–1232.
11. Erlebacher, A., Vencato, D., Price, K.A., Zhang, D., Glimcher, L.H., Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J. Clin. Invest. 117 (2007), 1399–1411.
12. Falk, K., et al. Allele-specific peptide ligand motifs of HLA-C molecules. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 12005–12009.
13. Hanna, J., et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12 (2006), 1065–1074.
14. Hiby, S.E., et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200 (2004), 957–965.
15. Hiby, S.E., et al. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120 (2010), 4102–4110.
16. Holland, O.J., et al. Minor histocompatibility antigens are expressed in syncytiotrophoblast and trophoblast debris: implications for maternal alloreactivity to the fetus. Am. J. Pathol. 180 (2012), 256–266.
17. Kieckbusch, J., Gaynor, L.M., Moffett, A., Colucci, F., MHC-dependent inhibition of uterine NK cells impedes fetal growth and decidual vascular remodeling. Nat. Commun., 5, 2014, 3359.
18. King, A., Wellings, V., Gardner, L., Loke, Y.W., Immunocytochemical characterization of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle. Hum. Immunol. 24 (1989), 195–205.
19. King, A., Kalra, P., Loke, Y.W., Human trophoblast cell resistance to decidual NK lysis is due to lack of NK target structure. Cell. Immunol. 127 (1990), 230–237.
20. King, A., Wooding, P., Gardner, L., Loke, Y.W., Expression of perforin, granzyme A and TIA-1 by human uterine CD56+ NK cells implies they are activated and capable of effector functions. Hum. Reprod. 8 (1993), 2061–2067.
21. Koopman, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198 (2003), 1201–1212.
22. Kopcow, H.D., et al. Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 15563–15568.
23. Lissauer, D., Choudhary, M., Pachnio, A., Goodyear, O., Moss, P.A., Kilby, M.D., Cytomegalovirus sero positivity dramatically alters the maternal CD8+ T cell repertoire and leads to the accumulation of highly differentiated memory cells during human pregnancy. Hum. Reprod. 12 (2011), 3355–3365.
24. Lissauer, D., Piper, K., Goodyear, O., Kilby, M.D., Moss, P.A., Fetal-specific CD8+ cytotoxic T cell responses develop during normal human pregnancy and exhibit broad functional capacity. J. Immunol. 189 (2012), 1072–1080.
25. Long, E.O., Regulation of immune responses through inhibitory receptors. Annu. Rev. Immunol. 17 (1999), 875–904.
26. Makadzange, A.T., et al. Characterization of an HLA-C-restricted CTL response in chronic HIV infection. Eur. J. Immunol. 40 (2010), 1036–1041.
27. Martin, M.P., et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat. Genet. 39 (2007), 733–740.
28. Nakashima, A., et al. Granulysin produced by uterine natural killer cells induces apoptosis of extravillous trophoblasts in spontaneous abortion. Am. J. Pathol. 173 (2008), 653–664.
29. Nakimuli, A., et al. A KIR B centromeric region present in Africans but not Europeans protects pregnant women from pre-eclampsia. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 845–850.
30. Nancy, P., Tagliani, E., Tay, C.S., Asp, P., Levy, D.E., Erlebacher, A., Chemokine gene silencing in decidual stromal cells limits T cell access to the maternal-fetal interface. Science 336 (2012), 1317–1321.
31. Pereira, L., Maidji, E., Cytomegalovirus infection in the human placenta: maternal immunity and developmentally regulated receptors on trophoblasts converge. Curr. Top. Microbiol. Immunol. 325 (2008), 383–395.
32. Pereira, L., et al. Intrauterine growth restriction caused by underlying congenital cytomegalovirus infection. J. Infect. Dis. 209 (2014), 1573–1584.
33. Racicot, K., et al. Viral infection of the pregnant cervix predisposes to ascending bacterial infection. J. Immunol. 191 (2013), 934–941.
34. Racicot, K., Kwon, J.Y., Aldo, P., Abrahams, V., El-Guindy, A., Romero, R., Mor, G., Type I interferon regulates the placental inflammatory response to bacteria and is targeted by virus: mechanism of polymicrobial infection-induced preterm birth. Am. J. Reprod. Immunol. 75 (2016), 451–460.
35. Revello, M.G., et al. Lymphoproliferative response in primary human cytomegalovirus (HCMV) infection is delayed in HCMV transmitter mothers. J. Infect. Dis. 193 (2006), 269–276.
36. Saini, Reena V., et al. Granulysin delivered by cytotoxic cells damages endoplasmic reticulum and activates caspase-7 in target cells. J. Immunol. 186 (2011), 3497–3504.
37. Saito, S., et al. A study of CD45RO, CD45RA and CD29 antigen expression on human decidual T cells in an early stage of pregnancy. Immunol. Lett. 40 (1994), 193–197.
38. Scaife, P.J., Bulmer, J.N., Robson, S.C., Innes, B.A., Searle, R.F., Effector activity of decidual CD8+ T lymphocytes in early human pregnancy. Biol. Reprod. 75 (2006), 562–567.
39. Sharkey, A.M., et al. Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J. Immunol. 181 (2008), 39–46.
40. Siewiera, J., et al. Human cytomegalovirus infection elicits new decidual natural killer cell effector functions. PLoS Pathog., 9, 2013, e1003257.
41. Stern, M., Elsasser, H., Honger, G., Steiger, J., Schaub, S., Hess, C., The number of activating KIR genes inversely correlates with the rate of CMV infection/reactivation in kidney transplant recipients. Am. J. Transplant. 8 (2008), 1312–1317.
42. Stern, M., et al. Telomeric rather than centromeric activating KIR genes protect from cytomegalovirus infection after kidney transplantation. Am. J. Transplant. 11 (2011), 1302–1307.
43. Tafuri, A., Alferink, J., Moller, P., Hammerling, G.J., Arnold, B., T cell awareness of paternal alloantigens during pregnancy. Science 270 (1995), 630–633.
44. Tewary, P., et al. Granulysin activates antigen-presenting cells through TLR4 and acts as an immune alarmin. Blood 116 (2010), 3465–3474.
45. Tilburgs, T., Strominger, J.L., CD8+ effector T cells at the fetal-maternal interface, balancing fetal tolerance and antiviral immunity. Am. J. Reprod. Immunol. 69 (2013), 395–407.
46. Tilburgs, T., et al. Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J. Immunol. 180 (2008), 5737–5745.
47. Tilburgs, T., Scherjon, S.A., Roelen, D.L., Claas, F.H., Decidual CD8+CD28- T cells express CD103 but not perforin. Hum. Immunol. 70 (2009), 96–100.
48. Tilburgs, T., et al. Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J. Reprod. Immunol. 82 (2009), 148–157.
49. Tilburgs, T., et al. Human decidual tissue contains differentiated CD8+ effector-memory T cells with unique properties. J. Immunol. 185 (2010), 4470–4477.
50. Tilburgs, T., et al. Human HLA-G+ extravillous trophoblasts: immune-activating cells that interact with decidual leukocytes. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 7219–7224.
51. Tilburgs, T., Evans, J.E., Crespo, A.C., Strominger, J.L., The HLA-G cycle provides for both NK tolerance and immunity at the maternal-fetal interface. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 13312–13317.
52. Trifari, S., et al. MicroRNA-directed program of cytotoxic CD8+ T-cell differentiation. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 18608–18613.
53. van Egmond, E.A., van der Keur, C., Swings, G.M., Scherjon, S.A., Claas, F.H., The possible role of virus-specific CD8(+) memory T cells in decidual tissue. J. Reprod. Immunol. 113 (2016), 1–8.
54. Verdijk, R.M., et al. Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells: implications for stem cell transplantation and immunotherapy. Blood 103 (2004), 1961–1964.
55. Vujaklija, D.V., et al. First trimester pregnancy decidual natural killer cells contain and spontaneously release high quantities of granulysin. Am. J. Reprod. Immunol. 66 (2011), 363–372.
56. Vujaklija, D.V., et al. Granulysin expression and the interplay of granulysin and perforin at the maternal–fetal interface. J. Reprod. Immunol. 97 (2013), 186–196.
57. Walch, M., et al. Cytotoxic cells kill intracellular bacteria through granulysin-mediated delivery of granzymes. Cell 157 (2014), 1309–1323.
58. Wang, T., et al. Infection with the intracellular bacterium, Listeria monocytogenes, overrides established tolerance in a mouse cardiac allograft model. Am. J. Transplant. 10 (2010), 1524–1533.
59. Warner, J.A., Zwezdaryk, K.J., Day, B., Sullivan, D.E., Pridjian, G., Morris, C.A., Human cytomegalovirus infection inhibits CXCL12-mediated migration and invasion of human extravillous cytotrophoblasts. J. Virol., 9, 2012, 255.
60. Xie, F., et al. An association between cytomegalovirus infection and pre-eclampsia: a case-control study and data synthesis. Acta Obstet. Gynecol. Scand. 89 (2010), 1162–1167.
61. Xiong, S., et al. Maternal uterine NK cell-activating receptor KIR2DS1 enhances placentation. J. Clin. Invest. 123 (2013), 4264–4272.
62. Yao, Y., Song, J., Wang, W., Liu, N., Decidual vascular endothelial cells promote maternal-fetal immune tolerance by inducing regulatory T cells through canonical Notch1 signaling. Immunol. Cell. Biol., 119, 2015 (Epub ahead of print).
63. Zeldovich, V.B., Robbins, J.R., Kapidzic, M., Lauer, P., Bakardjiev, A.I., Invasive extravillous trophoblasts restrict intracellular growth and spread of Listeria monocytogenes. PLoS Pathog., 7, 2011, e1002005.