Unusual timing of CD127 expression by mouse uterine natural killer cells

Journal of Leukocyte Biology

Volumn 91, Issue 3, 2012, Pages 417-426

  Zhang, Jianhong ^a   Chen, Zhilin ^a   Fritz, Jörg H ^b   Rochman, Yrina ^c   Leonard, Warren J ^c   Gommerman, Jennifer L ^d   Plumb, Adam W ^e   Abraham, Ninan ^e   Anne Croy, B ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Decidua; Interleukin 7; Stromal factor; Thymic stromal lymphopoietin

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; PODOPLANIN; THYMIC STROMAL LYMPHOPOIETIN;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL; CELL EXPANSION; CELL MATURATION; DECIDUA; FEMALE; LYMPHOID CELL; LYMPHOID ORGAN; MATERNAL BLOOD; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UTERUS;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERLEUKIN-7; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; KILLER CELLS, NATURAL; LIGANDS; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; STROMAL CELLS; TIME FACTORS; TRANSCRIPTION, GENETIC; UTERUS;

MUS; RODENTIA;

EID: 84863293786     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1011501     Document Type: Article

References (49)

1. Croy, B. A., van den Heuvel, M. J., Borzychowski, A. M., Tayade, C. (2006) Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol. Rev. 214, 161-185.
2. Moffett-King, A. (2002) Natural killer cells and pregnancy. Nat. Rev. Immunol. 2, 656-663.
3. 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.
4. Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron, S., Prus, D., Cohen-Daniel, L., Arnon, T. I., Manaster, I., Gazit, R., Yutkin, V., Benharroch, D., Porgador, A., Keshet, E., Yagel, S., Mandelboim, O. (2006) Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat. Med. 12, 1065-1074.
5. Germeyer, A., Sharkey, A. M., Prasadajudio, M., Sherwin, R., Moffett, A., Bieback, K., Clausmeyer, S., Masters, L., Popovici, R. M., Hess, A. P., Strowitzki, T., von Wolff, M. (2009) Paracrine effects of uterine leucocytes on gene expression of human uterine stromal fibroblasts. Mol. Hum. Reprod. 15, 39-48.
6. King, A., Burrows, T., Verma, S., Hiby, S., Loke, Y. W. (1998) Human uterine lymphocytes. Hum. Reprod. Update. 4, 480-485.
7. 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.
8. Aharon G., Freud, M. A. C. (2006) Human natural killer cell development. Immunol. Rev. 214, 56-72.
9. Chiossone, L., Chaix, J., Fuseri, N., Roth, C., Vivier, E., Walzer, T. (2009) Maturation of mouse NK cells is a 4-stage developmental program. Blood 113, 5488-5496.
10. Male, V., Hughes, T., McClory, S., Colucci, F., Caligiuri, M. A., Moffett, A. (2010) Immature NK cells, capable of producing IL-22, are present in human uterine mucosa. J. Immunol. 185, 3913-3918.
11. Di Santo, J. P., Vosshenrich, C. A. J. (2006) Bone marrow versus thymic pathways of natural killer cell development. Immunol. Rev. 214, 35-46.
12. Di Santo, J. P. (2006) Natural killler cell developmental pathways: a question of balance. Annu. Rev. Immunol. 24, 257-286.
13. Luther, C., Warner, K., Takei, F. (2011) Unique progenitors in mouse lymph node develop into CD127+ NK cells: thymus-dependent and thymus-independent pathways. Blood 117, 4012-4021.
14. Shi, F-D., Ljunggren, H-G., La Cava, A., Van Kaer, L. (2011) Organ-specific features of natural killer cells. Nat. Rev. Immunol. 11, 658-671.
15. Vosshenrich, C. A. J., Garcia-Ojeda, M. E., Samson-Villeger, S. I., Pasqualetto, V., Enault, L., Goff, O. R-L., Corcuff, E., Guy-Grand, D., Rocha, B., Cumano, A., Rogge, L., Ezine, S., Di Santo, J. P. (2006) A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat. Immunol. 7, 1217-1224.
16. bright natural killer cells. Immunity 22, 295-304.
17. Chantakru, S., Wang, W. C., van den Heuvel, M., Bashar, S., Simpson, A., Chen, Q., Croy, B. A., Evans, S. S. (2003) Coordinate regulation of lymphocyte-endothelial interactions by pregnancy-associated hormones. J. Immunol. 171, 4011-4019.
18. Zhang, J. H., Yamada, A. T., Croy, B. A. (2009) DBA-lectin reactivity defines natural killer cells that have homed to mouse decidua. Placenta 30, 968-973.
19. Croy, B. A., Xie, X. (2006) In vivo models for studying homing and function of murine uterine natural killer cells. Methods Mol. Med. 122, 77-92.
20. Croy, B. A., Zhang, J., Tayade, C., Colucci, F., Yadi, H., Yamada, A. T. (2010) Analysis of uterine natural killer cells in mice. In Natural Killer Cell Protocols of Methods in Molecular Biology, Humana, New York, NY, USA, 465-503.
21. Fletcher, A. L., Seach, N., Reiseger, J. J., Lowen, T. E., Hammett, M. V., Scott, H. S., Boyd, R. L. (2009) Reduced thymic Aire expression and abnormal NF-κB2 signaling in a model of systemic autoimmunity. J. Immunol. 182, 2690-2699.
22. Ueda, Y., Kondo, M., Kelsoe, G. (2005) Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J. Exp. Med. 201, 1771-1780.
23. Laouar, Y., Sutterwala, F. S., Gorelik, L., Flavell, R. A. (2005) Transforming growth factor-β controls T helper type 1 cell development through regulation of natural killer cell interferon-β. Nat. Immunol. 6, 600-607.
24. Demehri, S., Liu, Z., Lee, J., Lin, M. H., Crosby, S. D., Roberts, C. J., Grigsby, P. W., Miner, J. H., Farr, A. G., Kopan, R. (2008) Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS Biol. 6, e123.
25. Rochman, Y., Spolski, R., Leonard, W. J. (2009) New insights into the regulation of T cells by γc family cytokines. Nat. Rev. Immunol. 9, 480-490.
26. Croy, B. A., Guimond, M. J., Luross, J., Hahnel, A., Wang, B., van den Heuvel, M. (1997) Uterine natural killer cells do not require interleukin-interleukin- 2 for their differentiation or maturation. Am. J. Reprod. Immunol. 37, 463-470.
27. 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.
28. Ma, A., Koka, R., Burkett, P. (2006) Diverse functions of IL-2, IL-15 and IL-17 in lymphoid homeostasis. Annu. Rev. Immunol. 24, 657-679.
29. Ye, W., Zheng, L.-M., Young, J., Liu, C. (1996) The involvement of interleukin (IL)-15 in regulating the differentiation of granulated metrial gland cells in mouse pregnant uterus. J. Exp. Med. 184, 2405-2410.
30. Trundley, A., Moffett, A. (2004) Human uterine leukocytes and pregnancy. Tissue Antigens 63, 1-12.
31. Fritz, J. H., Gommerman, J. L. (2011) Cytokine/stromal cell networks and lymphoid tissue environments. J. Interferon Cytokine Res. 31, 277-289.
32. Crellin, N. K., Trifari, S., Kaplan, C. D., Cupedo, T., Spits, H. (2010) Human NKp44+IL-22+ cells and LTi-like cells constitute a stable RORC+ lineage distinct from conventional natural killer cells. J. Exp. Med. 207, 281-290.
33. 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.
34. Anson-Cartwright, L., Dawson, K., Holmyard, D., Fisher, S. J., Lazzarini, R. A., Cross, J. C. (2000) The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25, 311-314.
35. Burke, S. D., Barrette, V. F., Bianco, J., Thorne, J. G., Yamada, A. T., Pang, S. C., Adams, M. A., Croy, B. A. (2010) Spiral arterial remodeling is not essential for normal blood pressure regulation in pregnant mice. Hypertension 55, 729-737.
36. Rochman, Y., Kashyap, M., Robinson, G. W., Sakamoto, K., Gomez-Rodriguez, J., Wagner, K-U., Leonard, W. J. (2010) Thymic stromal lymphopoietin-mediated STAT5 phosphorylation via kinases JAK1 and JAK2 reveals a key difference from IL-7-induced signaling. Proc. Natl. Acad. Sci. USA 107, 19455-19460.
37. Wilson, C. B., Rowell, E., Sekimata, M. (2009) Epigenetic control of Thelper-cell differentiation. Nat. Rev. Immunol. 9, 91-105.
38. Tayade, C., Fang, Y., Black, G. P., V Jr., A. P., Erlebacher, A., Croy, B. A. (2005) Differential transcription of Eomes and T-bet during maturation of mouse uterine natural killer cells. J. Leukoc. Biol. 78, 1347-1355.
39. Yagi, R., Junttila, I. S., Wei, G., Urban Jr., J. F., Zhao, K., Paul, W. E., Zhu, J. (2010) The transcription factor GATA3 actively represses RUNX3 protein-regulated production of Interferon-γ. Immunity 32, 507-517.
40. 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.
41. 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.
42. Ziegler, S. F., Artis, D. (2010) Sensing the outside world: TSLP regulates barrier immunity. Nat. Immunol. 11, 289-293.
43. Ziegler, S. F., Liu, Y-J. (2006) Thymic stromal lymphopoietin in normal and pathogenic T cell development and function. Nat. Immunol.7, 709-714.
44. Taylor, R. T., Patel, S. R., Lin, E., Butler, B. R., Lake, J. G., Newberry, R. D., Williams, I. R. (2007) Lymphotoxin-independent expression of TNF-related activation-induced cytokine by stromal cells in cryptopatches, isolated lymphoid follicles, and Peyer's patches. J. Immunol. 178, 5659-5667.
45. Kruse, A., Merchant, M. J., Hallmann, R., Butcher, E. C. (1999) Evidence of specialized leukocyte-vascular homing interactions at the maternal/ fetal interface. Eur. J. Immunol. 29, 1116-1126.
46. Kruse, A., Martens, N., Fernekorn, U., Hallmann, R., Butcher, E. C. (2002) Alterations in the expression of homing-associated molecules at the maternal/fetal interface during the course of pregnancy. Biol. Reprod. 66, 333-345.
47. Lin, Y., Zhong, Y., Shen, W., Chen, Y., Shi, J., Di, J., Zeng, S., Saito, S. (2008) TSLP-induced placental DC activation and IL-10+ NK cell expansion: comparative study based on BALB/c + C57BL/6 and NOD/ SCID + C57BL/6 pregnant models. Clin. Immunol. 126, 104-117.
48. Kyewski, B., Peterson, P. (2010) Aire, master of many trades. Cell 140, 24-26.
49. Cohen, J. N., Guidi, C. J., Tewalt, E. F., Qiao, H., Rouhani, S. J., Ruddell, A., Farr, A. G., Tung, K. S., Engelhard, V. H. (2010) Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aireindependent direct antigen presentation. J. Exp. Med. 207, 681-688.