Endometrial NK cells are special immature cells that await pregnancy

Journal of Immunology

Volumn 181, Issue 3, 2008, Pages 1869-1876

  Manaster, Irit ^a   Mizrahi, Saar ^a   Goldman Wohl, Debra ^b   Sela, Hen Y ^b   Stern Ginossar, Noam ^a   Lankry, Dikla ^a   Gruda, Raizy ^a   Hurwitz, Arye ^b   Bdolah, Yuval ^b   Haimov Kochman, Ronit ^b   Yagel, Simcha ^b   Mandelboim, Ofer ^a  

^a HEBREW UNIVERSITY   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CHEMOKINE RECEPTOR; INTERLEUKIN 15; PROTEIN P30; LIGAND;

ADULT; ARTICLE; CELL ACTIVITY; CELL FUNCTION; CELL STIMULATION; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DECIDUA; ENDOMETRIUM CELL; FEMALE; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PHENOTYPE; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CERCOPITHECUS; CYTOLOGY; DRUG EFFECT; ENDOMETRIUM; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; UPREGULATION;

ADULT; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; ENDOMETRIUM; FEMALE; HUMANS; INTERLEUKIN-15; KILLER CELLS, NATURAL; LIGANDS; LYMPHOCYTE ACTIVATION; PREGNANCY; RECEPTORS, CHEMOKINE; UP-REGULATION;

EID: 49649094044     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.3.1869     Document Type: Article

References (47)

1. Hanna, J., and O. Mandelboim. 2007. When killers become helpers. Trends Immunol. 28: 201-206.
2. Vosshenrich, C. A., M. E. Garcia-Ojeda, S. I. Samson-Villeger, V. Pasqualetto, L. Enault, O. Richard-Le Goff, E. Corcuff, D. Guy-Grand, B. Rocha, A. Cumano, et al. 2006. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat. Immunol. 7: 1217-1224.
3. Croy, B. A., M. J. van den Heuvel, A. M. Borzychowski, and C. Tayade. 2006. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 214: 161-185.
4. Manaster, I., and O. Mandelboim. 2008. The unique properties of human NK cells in the uterine mucosa. Placenta 29S: 60-66.
5. Hanna, J., P. Bechtel, Y. Zhai, F. Youssef, K. McLachlan, and O. Mandelboim. 2004. Novel insights on human NK cells' immunological modalities revealed by gene expression profiling. J. Immunol. 173: 6547-6563.
6. 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.
7. Arnon, T. I., G. Markel, and O. Mandelboim. 2006. Tumor and viral recognition by natural killer cells receptors. Semin. Cancer Biol. 16: 348-358.
8. Hanna, J., O. Wald, D. Goldman-Wohl, D. Prus, G. Markel, R. Gazit, G. Katz, R. Haimov-Kochman, N. Fujii, S. Yagel, et al. 2003. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16-human natural killer cells. Blood 102: 1569-1577.
9. King, A., C. Birkby, and Y. W. Loke. 1989. Early human decidual cells exhibit NK activity against the K562 cell line but not against first trimester trophoblast. Cell. Immunol. 118: 337-344.
10. 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.
11. Pace, D., L. Morrison, and J. N. Bulmer. 1989. Proliferative activity in endometrial stromal granulocytes throughout menstrual cycle and early pregnancy. J. Clin. Pathol. 42: 35-39.
12. Eriksson, M., S. K. Meadows, C. R. Wira, and C. L. Sentman. 2004. Unique phenotype of human uterine NK cells and their regulation by endogenous TGF-β. J. Leukocyte Biol. 76: 667-675.
13. Searle, R. F., R. K. Jones, and J. N. Bulmer. 1999. Phenotypic analysis and proliferative responses of human endometrial granulated lymphocytes during the menstrual cycle. Biol. Reprod. 60: 871-878.
14. Barash, A., N. Dekel, S. Fieldust, I. Segal, E. Schechtman, and I. Granot. 2003. Local injury to the endometrium doubles the incidence of successful pregnancies in patients undergoing in vitro fertilization. Fertil. Steril. 79: 1317-1322.
15. Porgador, A., O. Mandelboim, N. P. Restifo, and J. L. Strominger. 1997. Natural killer cell lines kill autologous β2-microglobulin-deficient melanoma cells: implications for cancer immunotherapy. Proc. Natl. Acad. Sci. USA 94: 13140-13145.
16. Mandelboim, O., P. Malik, D. M. Davis, C. H. Jo, J. E. Boyson, and J. L. Strominger. 1999. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc. Natl. Acad. Sci. USA 96: 5640-5644.
17. Pende, D., S. Parolini, A. Pessino, S. Sivori, R. Augugliaro, L. Morelli, E. Marcenaro, L. Accame, A. Malaspina, R. Biassoni, et al. 1999. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J. Exp. Med. 190: 1505-1516.
18. Ferlazzo, G., D. Thomas, S. L. Lin, K. Goodman, B. Morandi, W. A. Muller, A. Moretta, and C. Munz. 2004. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J. Immunol. 172: 1455-1462.
19. Hoxie, J. A., M. Ahuja, E. Belmonte, S. Pizarro, R. Parton, and L. F. Brass. 1993. Internalization and recycling of activated thrombin receptors. J. Biol. Chem. 268: 13756-13763.
20. Becknell, B., and M. A. Caligiuri. 2005. Interleukin-2, interleukin-15, and their roles in human natural killer cells. Adv. Immunol. 86: 209-239.
21. Caligiuri, M. A., A. Zmuidzinas, T. J. Manley, H. Levine, K. A. Smith, and J. Ritz. 1990. Functional consequences of interleukin 2 receptor expression on resting human lymphocytes. Identification of a novel natural killer cell subset with high affinity receptors. J. Exp. Med. 171: 1509-1526.
22. Verma, S., S. E. Hiby, Y. W. Loke, and A. King. 2000. Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol. Reprod. 62: 959-968.
23. 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.
24. Hanna, J., T. Gonen-Gross, J. Fitchett, T. Rowe, M. Daniels, T. I. Arnon, R. Gazit, A. Joseph, K. W. Schjetne, A. Steinle, et al. 2004. Novel APC-like properties of human NK cells directly regulate T cell activation. J. Clin. Invest. 114: 1612-1623.
25. Nagler, A., L. L. Lanier, S. Cwirla, and J. H. Phillips. 1989. Comparative studies of human FcRIII-positive and negative natural killer cells. J. Immunol. 143: 3183-3191.
26. Saito, S., K. Nishikawa, T. Morii, M. Enomoto, N. Narita, K. Motoyoshi, and M. Ichijo. 1993. Cytokine production by CD16-CD56bright natural killer cells in the human early pregnancy decidua. Int. Immunol. 5: 559-563.
27. Platt, J. S., and J. S. Hunt. 1998. Interferon-γ gene expression in cycling and pregnant mouse uterus: temporal aspects and cellular localization. J. Leukocyte Biol. 64: 393-400.
28. Cosman, D., J. Mullberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14: 123-133.
29. Steinle, A., P. Li, D. L. Morris, V. Groh, L. L. Lanier, R. K. Strong, and T. Spies. 2001. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 53: 279-287.
30. Mandelboim, O., N. Lieberman, M. Lev, L. Paul, T. I. Arnon, Y. Bushkin, D. M. Davis, J. L. Strominger, J. W. Yewdell, and A. Porgador. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409: 1055-1060.
31. Arnon, T. I., M. Lev, G. Katz, Y. Chernobrov, A. Porgador, and O. Mandelboim. 2001. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur. J. Immunol. 31: 2680-2689.
32. Arnon, T. I., H. Achdout, N. Lieberman, R. Gazit, T. Gonen-Gross, G. Katz, A. Bar-Ilan, N. Bloushtain, M. Lev, A. Joseph, et al. 2004. The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood. 103: 664-672.
33. 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.
34. Starkey, P. M., L. M. Clover, and M. C. Rees. 1991. Variation during the menstrual cycle of immune cell populations in human endometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 39: 203-207.
35. Ho, H. N., K. H. Chao, C. K. Chen, Y. S. Yang, and S. C. Huang. 1996. Activation status of T and NK cells in the endometrium throughout menstrual cycle and normal and abnormal early pregnancy. Hum. Immunol. 49: 130-136.
36. Lachapelle, M. H., P. Miron, R. Hemmings, and D. C. Roy. 1996. Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion: altered profile and pregnancy outcome. J. Immunol. 156: 4027-4034.
37. Sentman, C. L., S. K. Meadows, C. R. Wira, and M. Eriksson. 2004. Recruitment of uterine NK cells: induction of CXC chemokine ligands 10 and 11 in human endometrium by estradiol and progesterone. J. Immunol. 173: 6760-6766.
38. Kitaya, K., T. Nakayama, N. Daikoku, S. Fushiki, and H. Honjo. 2004. Spatial and temporal expression of ligands for CXCR3 and CXCR4 in human endometrium. J. Clin. Endocrinol. Metab. 89: 2470-2476.
39. Tabiasco, J., M. Rabot, M. Aguerre-Girr, H. El Costa, A. Berrebi, O. Parant, G. Laskarin, K. Juretic, A. Bensussan, D. Rukavina, and P. Le Bouteiller. 2006. Human decidual NK cells: unique phenotype and functional properties: a review. Placenta 27 (Suppl. A): S34-S39.
40. Matsuura-Sawada, R., T. Murakami, Y. Ozawa, H. Nabeshima, J. Akahira, Y. Sato, Y. Koyanagi, M. Ito, Y. Terada, and K. Okamura. 2005. Reproduction of menstrual changes in transplanted human endometrial tissue in immunodeficient mice. Human reproduction (Oxford, England). 20: 1477-1484.
41. Lynch, L., L. Golden-Mason, M. Eogan, C. O'Herlihy, and C. O'Farrelly. 2007. Cells with haematopoietic stem cell phenotype in adult human endometrium: relevance to infertility? Hum. Reprod. 22: 919-926.
42. + natural killer cells. Biol. Reprod. 47: 227-232.
43. Chantakru, S., C. Miller, L. E. Roach, W. A. Kuziel, N. Maeda, W. C. Wang, S. S. Evans, and B. A. Croy. 2002. Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy. J. Immunol. 168: 22-28.
44. Oppenheim, D. E., S. J. Roberts, S. L. Clarke, R. Filler, J. M. Lewis, R. E. Tigelaar, M. Girardi, and A. C. Hayday. 2005. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat. Immunol. 6: 928-937.
45. - natural killer cells into human endometrium. J. Clin. Endocrinol. Metab. 90: 2932-2940.
46. 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.
47. Kitaya, K., J. Yasuda, I. Yagi, Y. Tada, S. Fushiki, and H. Honjo. 2000. IL-15 expression at human endometrium and decidua. Biol. Reprod. 63: 683-687.