Differential transcription of Eomes and T-bet during maturation of mouse uterine natural killer cells

Journal of Leukocyte Biology

Volumn 78, Issue 6, 2005, Pages 1347-1355

  Tayade, Chandrakant ^a,e   Fang, Yuan ^a   Black, Gordon P ^a   Paffaro Jr , V A ^b   Erlebacher, Adrian ^c   Croy, B Anne ^d  

^a UNIVERSITY OF GUELPH   (Canada)

^b Biological Sciences   (Brazil)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d QUEEN S UNIVERSITY   (Canada)

^e UNIVERSITY OF GUELPH   (Canada)

Author keywords

Cell differentiation; Granzyme; Interferon ; Perform; Reproductive immunology; Transcription factors

Indexed keywords

BETA ACTIN; CD8 ANTIGEN; GAMMA INTERFERON; GRANZYME A; LECTIN; PERFORIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EOMES; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DECIDUALIZATION; FEMALE; GESTATIONAL AGE; LASER CAPTURE MICRODISSECTION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; MESODERM; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA ISOLATION; SENESCENCE; T LYMPHOCYTE;

ANIMALS; CELL DIFFERENTIATION; ESTROUS CYCLE; FEMALE; GRANZYMES; INTERFERON TYPE II; KILLER CELLS, NATURAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PORE FORMING CYTOTOXIC PROTEINS; PREGNANCY; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SERINE ENDOPEPTIDASES; T-BOX DOMAIN PROTEINS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; UTERUS;

ANIMALIA; RODENTIA;

EID: 28844499194     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0305142     Document Type: Article

References (38)

1. Townsend, M. J., Weinmann, A. S., Matsuda, J. L., Salomon, R., Farnham, P. J., Biron, C. A., Gapin, L., Glimcher, L. H. (2004) T-bet regulates the terminal maturation and homeostasis of NK and Vα14i NKT cells. Immunity 20, 477-494.
2. Pearce, E. L., Mullen, A. C., Martins, G. A., Krawczyk, C. M., Hutchins, A. S., Zediak, V. P., Banica, M., DiCioccio, C. B., Gross, D. A., Mao, C. A., Shen, H., Cereb, N., Yang, S. Y., Lindsten, T., Rossant, J., Hunter, C. A., Reiner, S. L. (2003) Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302, 1041-1043.
3. Glimcher, L. H., Townsend, M. J., Sullivan, B. M., Lord, G. M. (2004) Recent developments in the transcriptional regulation of cytolytic effector cells. Nat. Rev. Immunol. 4, 900-911.
4. Ashkar, A. A., Di Santo, J. P., Croy, B. A. (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.
5. Moffett-King, A. (2002) Natural killer cells and pregnancy. Nat. Rev. Immunol. 2, 656-663.
6. Delgado, S. R., McBey, B. A., Yamashiro, S., Fujita, J., Kiso, Y., Croy, B. A. (1996) Accounting for the peripartum loss of granulated metrial gland cells, a natural killer cell population, from the pregnant mouse uterus. J. Leukoc. Biol. 59, 262-269.
7. Peel, S. (1989) Granulated metrial gland cells. Adv. Anat. Embryol. Cell Biol. 115, 1-112.
8. Li, X. F., Charnock-Jones, D. S., Zhang, E., Hiby, S., Malik, S., Day, K., Licence, D., Bowen, J. M., Gardner, L., King, A., Loke, Y. W., Smith, S. K. (2001) Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J. Clin. Endocrinol. Metab. 86, 1823-1834.
9. Wang, C., Tanaka, T., Nakamura, H., Umesaki, N., Hirai, K., Ishiko, O., Ogita, S., Kaneda, K. (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.
10. Paffaro Jr., V. A., Bizinotto, M. C., Joazeiro, P. P., Yamada, A. T. (2003) Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta 24, 479-488.
11. Croy, B. A., Ashkar, A. A., Foster, R. A., DiSanto, J. P., Magram, J., Carson, D., Gendler, S. J., Grusby, M. J., Wagner, N., Muller, W., Guimond, M. J. (1997) Histological studies of gene-ablated mice support important functional roles for natural killer cells in the uterus during pregnancy. J. Reprod. Immunol. 35, 111-133.
12. Parr, E. L., Parr, M. B., Young, J. D. (1987) Localization of a pore-forming protein (perform) in granulated metrial gland cells. Biol. Reprod. 37, 1327-1335.
13. Allen, M. P., Nilsen-Hamilton, M. (1998) Granzymes D, E, F, and G are regulated through pregnancy and by IL-2 and IL-15 in granulated metrial gland cells. J. Immunol. 161, 2772-2779.
14. Ashkar, A. A., Black, G. P., Wei, Q., He, H., Liang, L., Head, J. R., Croy, B. A. (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.
15. Muller, H., Liu, B., Croy, B. A., Head, J. R., Hunt, J. S., Dai, G., Soares, M. J. (1999) Uterine natural killer cells are targets for a trophoblast cell-specific cytokine, prolactin-like protein A. Endocrinology 140, 2711-2720.
16. Zhang, J. H., He, H., Borzychowski, A. M., Takeda, K., Akira, S., Croy, B. A. (2003) Analysis of cytokine regulators inducing interferon production by mouse uterine natural killer cells. Biol. Reprod. 69, 404-411.
17. Borzychowski, A. M., Chantakru, S., Minhas, K., Paffaro, V. A., Yamada, A. T., He, H., Korach, K. S., Croy, B. A. (2003) Functional analysis of murine uterine natural killer cells genetically devoid of oestrogen receptors. Placenta 24, 403-411.
18. Chantakru, S., Kuziel, W. A., Maeda, N., Croy, B. A. (2001) A study on the density and distribution of uterine natural killer cells at mid pregnancy in mice genetically ablated for CCR2, CCR5 and the CCR5 receptor ligand, MIP-1 α. J. Reprod. Immunol. 49, 33-47.
19. Moffett-King, A., Entrican, G., Ellis, S., Hutchinson, J., Bainbridge, D. (2002) Natural killer cells and reproduction. Trends Immunol. 23, 332-333.
20. Brosens, J. J., Pijnenborg, R., Brosens, I. A. (2002) The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am. J. Obstet. Gynecol. 187, 1416-1423.
21. Cross, J. C., Baczyk, D., Dobric, N., Hemberger, M., Hughes, M., Simmons, D. G., Yamamoto, H., Kingdom, J. C. (2003) Genes, development and evolution of the placenta. Placenta 24, 123-130.
22. Hiby, S. E., Walker, J. J., O'Shaughnessy, K. M., Redman, C. W., Carrington, M., Trowsdale, J., Moffett, A. (2004) Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J. Exp. Med. 200, 957-965.
23. Parham, P. (2004) NK cells and trophoblasts: partners in pregnancy. J. Exp. Med. 200, 951-955.
24. Lametschwandtner, G., Biedermann, T., Schwarzler, C., Gunther, C., Kund, J., Fassl, S., Hinteregger, S., Carballido-Perrig, N., Szabo, S. J., Glimcher, L. H., Carballido, J. M. (2004) Sustained T-bet expression confers polarized human TH2 cells with TH1-like cytokine production and migratory capacities. J. Allergy Clin. Immunol. 113, 987-994.
25. Ryan, K., Garrett, N., Mitchell, A., Gurdon, J. B. (1996) Eomesodermin, a key early gene in Xenopus mesoderm differentiation. Cell 87, 989-1000.
26. Russ, A. P., Wattler, S., Colledge, W. H., Aparicio, S. A., Carlton, M. B., Pearce, J. J., Barton, S. C., Surani, M. A., Ryan, K., Nehls, M. C., Wilson, V., Evans, M. J. (2000) Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404, 95-99.
27. Ryan, K., Butler, K., Bellefroid, E., Gurdon, J. B. (1998) Xenopus eomesodermin is expressed in neural differentiation. Mech. Dev. 75, 155-158.
28. Ryan, K., Russ, A. P., Levy, R. J., Wehr, D. J., You, J., Easterday, M. C. (2004) Modulation of Eomes activity alters the size of the developing heart: implications for in utero cardiac gene therapy. Hum. Gene Ther. 15, 842-855.
29. Lighvani, A. A., Frucht, D. M., Jankovic, D., Yamane, H., Aliberti, J., Hissong, B. D., Nguyen, B. V., Gadina, M., Sher, A., Paul, W. E., O'Shea, J. J. (2001) T-bet is rapidly induced by interferon-γ in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98, 15137-15142.
30. Kelly, R. W., Illingworth, P., Baldie, G., Leask, R., Brouwer, S., Calder, A. A. (1994) Progesterone control of interleukin-8 production in endometrium and chorio-decidual cells underlines the role of the neutrophil in menstruation and parturition. Hum. Reprod. 9, 253-258.
31. Guimond, M. J., Wang, B., Croy, B. A. (1998) Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg ε 26 mice. J. Exp. Med. 187, 217-223.
32. Ashkar, A. A., Croy, B. A. (1999) Interferon-γ contributes to the normalcy of murine pregnancy. Biol. Reprod. 61, 493-502.
33. Chantakru, S., Miller, C., Roach, L. E., Kuziel, W. A., Maeda, N., Wang, W. C., Evans, S. S., Croy, B. A. (2002) Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy. J. Immunol. 168, 22-28.
34. Hanna, J., Wald, O., Goldman-Wohl, D., Prus, D., Markel, G., Gazit, R., Katz, G., Haimov-Kochman, R., Fujii, N., Yagel, S., Peled, A., Mandelboim, O. (2003) CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood 102, 1569-1577.
35. Kitaya, K., Nakayama, T., Daikoku, N., Fushiki, S., Honjo, H. (2004) Spatial and temporal expression of ligands for CXCR3 and CXCR4 in human endometrium. J. Clin. Endocrinol. Metab. 89, 2470-2476.
36. Red-Horse, K., Drake, P. M., Gunn, M. D., Fisher, S. J. (2001) Chemokine ligand and receptor expression in the pregnant uterus: reciprocal patterns in complementary cell subsets suggest functional roles. Am. J. Pathol. 159, 2199-2213.
37. Colucci, F., Soudais, C., Rosmaraki, E., Vanes, L., Tybulewicz, V. L., Di Santo, J. P. (1999) Dissecting NK cell development using a novel alymphoid mouse model: investigating the role of the c-abl proto-oncogene in murine NK cell differentiation. J. Immunol. 162, 2761-2765.
38. Matsuoka, S., Tsuji, K., Hisakawa, H., Xu, M. J., Ebihara, Y., Ishii, T., Sugiyama, D., Manabe, A., Tanaka, R., Ikeda, Y., Asano, S., Nakahata, T. (2001) Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells. Blood 98, 6-12.