Conversion of peripheral blood NK cells to a decidual NK-like phenotype by a cocktail of defined factors

Journal of Immunology

Volumn 190, Issue 8, 2013, Pages 3939-3948

  Cerdeira, Ana Sofia ^a,b,c   Rajakumar, Augustine ^a,d   Royle, Caroline M ^a   Lo, Agnes ^a   Husain, Zaheed ^e   Thadhani, Ravi I ^a   Sukhatme, Vikas P ^a   Karumanchi, S Ananth ^a,d   Kopcow, Hernan D ^a,f  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Gulbenkian Program for Advanced Medical Education   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 INTEGRIN; CD9 ANTIGEN; CHEMOKINE RECEPTOR; DEMETHYLATING AGENT; IMMUNOGLOBULIN RECEPTOR; REAGENT; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; CELL INVASION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DECIDUA; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; KILLER CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TROPHOBLAST;

ANGIOGENIC PROTEINS; ANTIGENS, CD56; AZACITIDINE; CELL LINE, TRANSFORMED; CELL MOVEMENT; CYTOPLASMIC GRANULES; DECIDUA; FEMALE; GPI-LINKED PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOPHENOTYPING; KILLER CELLS, NATURAL; RECEPTORS, IGG; RECEPTORS, KIR;

EID: 84875986821     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202582     Document Type: Article

References (55)

1. Caligiuri, M. A. 2008. Human natural killer cells. Blood 112: 461-469.
2. Orange, J. S., M. S. Fassett, L. A. Koopman, J. E. Boyson, and J. L. Strominger. 2002. Viral evasion of natural killer cells. Nat. Immunol. 3: 1006-1012.
3. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510.
4. Bulmer, J. N., L. Morrison, M. Longfellow, A. Ritson, and D. Pace. 1991. Granulated lymphocytes in human endometrium: histochemical and immuno-histochemical studies. Hum. Reprod. 6: 791-798.
5. Bulmer, J. N., P. J. Williams, and G. E. Lash. 2010. Immune cells in the placental bed. Int. J. Dev. Biol. 54: 281-294.
6. ++ population. Dev. Immunol. 1: 169-190.
7. Loke, Y. W., and A. King. 1995. Human Implantation: Cell Biology and Immunology. Cambridge University Press, Cambridge.
8. Hanna, J., D. Goldman-Wohl, Y. Hamani, I. Avraham, C. Greenfield, S. Natanson-Yaron, D. Prus, L. Cohen-Daniel, T. I. Arnon, I. Manaster, et al. 2006. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12: 1065-1074.
9. Koopman, L. A., H. D. Kopcow, B. Rybalov, J. E. Boyson, J. S. Orange, F. Schatz, R. Masch, C. J. Lockwood, A. D. Schachter, P. J. Park, and J. L. Strominger. 2003. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198: 1201-1212.
10. Moffett-King, A. 2002. Natural killer cells and pregnancy. Nat. Rev. Immunol. 2: 656-663.
11. + NK cells as rapid producers of abundant IFN-γ on activation. Proc. Natl. Acad. Sci. USA 108: 728-732.
12. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22: 633-640.
13. bright subset. Blood 97: 3146-3151.
14. Fauriat, C., E. O. Long, H. G. Ljunggren, and Y. T. Bryceson. 2010. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 115: 2167-2176.
15. Vivier, E. 2006. What is natural in natural killer cells? Immunol. Lett. 107: 1-7.
16. Cooper, M. A., and M. A. Caligiuri. 2004. Isolation and characterization of human natural killer cell subsets. Curr. Protoc. Immunol. Chapter 7: Unit 7.34.
17. Sharkey, A. M., L. Gardner, S. Hiby, L. Farrell, R. Apps, L. Masters, J. Goodridge, L. Lathbury, C. A. Stewart, S. Verma, and A. Moffett. 2008. Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age. J. Immunol. 181: 39-46.
18. Verma, S., A. King, and Y. W. Loke. 1997. Expression of killer cell inhibitory receptors on human uterine natural killer cells. Eur. J. Immunol. 27: 979-983.
19. Kopcow, H. D., D. S. Allan, X. Chen, B. Rybalov, M. M. Andzelm, B. Ge, and J. L. Strominger. 2005. Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc. Natl. Acad. Sci. USA 102: 15563-15568.
20. Geiselhart, A., J. Dietl, K. Marzusch, P. Ruck, M. Ruck, H. P. Horny, E. Kaiserling, and R. Handgretinger. 1995. Comparative analysis of the immunophenotypes of decidual and peripheral blood large granular lymphocytes and T cells during early human pregnancy. Am. J. Reprod. Immunol. 33: 315-322.
21. Kalkunte, S. S., T. F. Mselle, W. E. Norris, C. R. Wira, C. L. Sentman, and S. Sharma. 2009. Vascular endothelial growth factor C facilitates immune tolerance and endovascular activity of human uterine NK cells at the maternal-fetal interface. J. Immunol. 182: 4085-4092.
22. Lash, G. E., S. C. Robson, and J. N. Bulmer. 2010. Review: Functional role of uterine natural killer (uNK) cells in human early pregnancy decidua. Placenta 31 (Suppl): S87-S92.
23. Lash, G. E., B. Schiessl, M. Kirkley, B. A. Innes, A. Cooper, R. F. Searle, S. C. Robson, and J. N. Bulmer. 2006. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J. Leukoc. Biol. 80: 572-580.
24. Vacca, P., C. Cantoni, C. Prato, E. Fulcheri, A. Moretta, L. Moretta, and M. C. Mingari. 2008. Regulatory role of NKp44, NKp46, DNAM-1 and NKG2D receptors in the interaction between NK cells and trophoblast cells: evidence for divergent functional profiles of decidual versus peripheral NK cells. Int. Immunol. 20: 1395-1405.
25. Fraser, R., G. S. Whitley, A. P. Johnstone, A. J. Host, N. J. Sebire, B. Thilaganathan, and J. E. Cartwright. 2012. Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J. Pathol. 228: 322-332.
26. Ashkar, A. A., J. P. Di Santo, and B. A. Croy. 2000. Interferon γ contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 192: 259-270.
27. Guimond, M. J., B. Wang, and B. A. Croy. 1998. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tgε26 mice. J. Exp. Med. 187: 217-223.
28. Ashkar, A. A., G. P. Black, Q. Wei, H. He, L. Liang, J. R. Head, and B. A. Croy. 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.
29. Chakraborty, D., M. A. Rumi, T. Konno, and M. J. Soares. 2011. Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc. Natl. Acad. Sci. USA 108: 16295-16300.
30. Hiby, S. E., J. J. Walker, K. M. O'shaughnessy, C. W. Redman, M. Carrington, J. Trowsdale, and A. Moffett. 2004. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200: 957-965.
31. Hiby, S. E., R. Apps, A. M. Sharkey, L. E. Farrell, L. Gardner, A. Mulder, F. H. Claas, J. J. Walker, C. W. Redman, L. Morgan, et al. 2010. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120: 4102-4110.
32. Orange, J. S., N. Ramesh, E. Remold-O'Donnell, Y. Sasahara, L. Koopman, M. Byrne, F. A. Bonilla, F. S. Rosen, R. S. Geha, and J. L. Strominger. 2002. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc. Natl. Acad. Sci. USA 99: 11351-11356.
33. Rajakumar, A., A. Jeyabalan, N. Markovic, R. Ness, C. Gilmour, and K. P. Conrad. 2007. Placental HIF-1a, HIF-2a, membrane and soluble VEGF receptor-1 proteins are not increased in normotensive pregnancies complicated by late-onset intrauterine growth restriction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293: R766-R774.
34. Voss, S. D., J. Daley, J. Ritz, and M. J. Robertson. 1998. Participation of the CD94 receptor complex in costimulation of human natural killer cells. J. Immunol. 160: 1618-1626.
35. Carmeliet, P., Y. Dor, J. M. Herbert, D. Fukumura, K. Brusselmans, M. Dewerchin, M. Neeman, F. Bono, R. Abramovitch, P. Maxwell, et al. 1998. Role of HIF-1a in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490.
36. Shweiki, D., A. Itin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359: 843-845.
37. reg balance by hypoxia-inducible factor 1. Cell 146: 772-784.
38. Eltzschig, H. K., and P. Carmeliet. 2011. Hypoxia and inflammation. N. Engl. J. Med. 364: 656-665.
39. Forsythe, J. A., B. H. Jiang, N. V. Iyer, F. Agani, S. W. Leung, R. D. Koos, and G. L. Semenza. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16: 4604-4613.
40. - NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. USA 104: 3378-3383.
41. Graham, C. H., J. J. Lysiak, K. R. McCrae, and P. K. Lala. 1992. Localization of transforming growth factor-b at the human fetal-maternal interface: role in trophoblast growth and differentiation. Biol. Reprod. 46: 561-572.
42. Allan, D. S., B. Rybalov, G. Awong, J. C. Zúñiga- Pflücker, H. D. Kopcow, J. R. Carlyle, and J. L. Strominger. 2010. TGF-β affects development and differentiation of human natural killer cell subsets. Eur. J. Immunol. 40: 2289-2295.
43. Chan, H. W., Z. B. Kurago, C. A. Stewart, M. J. Wilson, M. P. Martin, B. E. Mace, M. Carrington, J. Trowsdale, and C. T. Lutz. 2003. DNA methyl-ation maintains allele-specific KIR gene expression in human natural killer cells. J. Exp. Med. 197: 245-255.
44. Santourlidis, S., H. I. Trompeter, S. Weinhold, B. Eisermann, K. L. Meyer, P. Wernet, and M. Uhrberg. 2002. Crucial role of DNA methylation in determination of clonally distributed killer cell Ig-like receptor expression patterns in NK cells. J. Immunol. 169: 4253-4261.
45. Tilburgs, T., B. J. van der Mast, N. M. Nagtzaam, D. L. Roelen, S. A. Scherjon, and F. H. Claas. 2009. Expression of NK cell receptors on decidual T cells in human pregnancy. J. Reprod. Immunol. 80: 22-32.
46. Xu, J., A. N. Vallejo, Y. Jiang, C. M. Weyand, and J. J. Goronzy. 2005. Distinct transcriptional control mechanisms of killer immunoglobulin-like receptors in natural killer (NK) and in T cells. J. Biol. Chem. 280: 24277-24285.
47. Li, G., M. Yu, C. M. Weyand, and J. J. Goronzy. 2009. Epigenetic regulation of killer immunoglobulin-like receptor expression in T cells. Blood 114: 3422-3430.
48. Red-Horse, K., Y. Zhou, O. Genbacev, A. Prakobphol, R. Foulk, M. McMaster, and S. J. Fisher. 2004. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J. Clin. Invest. 114: 744-754.
49. Lash, G. E., H. A. Otun, B. A. Innes, K. Percival, R. F. Searle, S. C. Robson, and J. N. Bulmer. 2010. Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Hum. Reprod. 25: 1137-1145.
50. Robson, A., L. K. Harris, B. A. Innes, G. E. Lash, M. M. Aljunaidy, J. D. Aplin, P. N. Baker, S. C. Robson, and J. N. Bulmer. 2012. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J. 26: 4876-4885.
51. Kolundžić, N., Z. Bojić-Trbojević, T. Kovačević, I. Stefanoska, T. Kadoya, and L. Vićovac. 2011. Galectin-1 is part of human trophoblast invasion machinery: a functional study in vitro. PLoS ONE 6: e28514.
52. + hematopoietic precursors are present in human decidua and differentiate into natural killer cells upon interaction with stromal cells. Proc. Natl. Acad. Sci. USA 108: 2402-2407.
53. Carlino, C., H. Stabile, S. Morrone, R. Bulla, A. Soriani, C. Agostinis, F. Bossi, C. Mocci, F. Sarazani, F. Tedesco, et al. 2008. Recruitment of circulating NK cells through decidual tissues: a possible mechanism controlling NK cell accumulation in the uterus during early pregnancy. Blood 111: 3108-3115.
54. Chen, Z., J. Zhang, K. Hatta, P. D. Lima, H. Yadi, F. Colucci, A. T. Yamada, and B. A. Croy. 2012. DBA-lectin reactivity defines mouse uterine natural killer cell subsets with biased gene expression. Biol. Reprod. 87: 81.
55. Zhang, X., and S. M. Ho. 2011. Epigenetics meets endocrinology. J. Mol. Endocrinol. 46: R11-R32.