Unique phenotype of human uterine NK cells and their regulation by endogenous TGF-β

Journal of Leukocyte Biology

Volumn 76, Issue 3, 2004, Pages 667-675

  Eriksson, Mikael ^a   Meadows, Sarah K ^a   Wira, Charles R ^b   Sentman, Charles L ^a,b  

^a DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Cellular activation; Cytokines; Reproductive immunology

Indexed keywords

CD16 ANTIGEN; CD3 ANTIGEN; CD56 ANTIGEN; CD57 ANTIGEN; CD9 ANTIGEN; CD94 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; KILLER INHIBITORY RECEPTOR; LYMPHOCYTE RECEPTOR; NATURAL KILLER CELL RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; ENDOMETRIUM; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IC 50; IMMUNOLOGY; IMMUNOREGULATION; LEUKOCYTE ACTIVATION; LYMPHOCYTE CLONE; LYMPHOCYTE SUBPOPULATION; NATURAL KILLER CELL; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REPRODUCTION; REPRODUCTIVE IMMUNOLOGY; UTERUS;

ADULT; ANTIGENS, SURFACE; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOMETRIUM; FEEDBACK, BIOCHEMICAL; FEMALE; HUMANS; IMMUNITY, NATURAL; IMMUNOPHENOTYPING; INTERFERON TYPE II; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-15; KILLER CELLS, NATURAL; MIDDLE AGED; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 4344579499     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0204090     Document Type: Article

References (46)

1. Trinchieri, G. (1989) Biology of natural killer cells. Adv. Immunol. 47, 187-376.
2. Robertson, M. J., Ritz, J. (1990) Biology and clinical relevance of human natural killer cells. Blood 76, 2421-2438.
3. Sedlmayr, P., Schallhammer, L., Hammer, A., Wilders-Truschnig, M., Wintersteiger, R., Dohr, G. (1996) Differential phenotypic properties of human peripheral blood CD56dim+ and CD56bright+ natural killer cell subpopulations. Int. Arch. Allergy Immunol. 110, 308-313.
4. King, A., Jokhi, P. P., Burrows, T. D., Gardner, L., Sharkey, A. M., Loke, Y. W. (1996) Functions of human decidual NK cells. Am. J. Reprod. Immunol. 35, 258-260.
5. Tabibzadeh, S. (1990) Proliferative activity of lymphoid cells in human endometrium throughout the menstrual cycle. J. Clin. Endocrinol. Metab. 70, 437-443.
6. Wira, C. R., Fahey, J. V., White, H. D., Yeaman, G. R., Givan, A. L., Howell, A. L. (2002) The mucosal immune system in the human female reproductive tract: influence of stage of the menstrual cycle and menopause on mucosal immunity in the uterus. In Endometrium (S. Glasser, J. Aplin, L. Giudice, S. Tabibzadeh, eds.), Harwood Academic Publishers, UK, 371-404.
7. Spomitz, U. M. (1992) The functional morphology of the human endometrium and decidua. Adv. Anat. Embryol. Cell Biol. 124, 1-99.
8. Yeaman, G. R., Guyre, P. M., Fanger, M. W., Collins, J. E., White, H. D., Rathbun, W., Orndorff, K. A., Gonzalez, J., Stem, J. E., White, C. R. (1997) Unique CD8+ T cell-rich lymphoid aggregates in human uterine endometrium. J. Leukoc. Biol. 61, 427-435.
9. Givan, A. L., White, H. D., Stern, J. E., Colby, E., Gosselin, E. J., Guyre, P. M., Wira, C. R. (1997) Flow cytometric analysis of leukocytes in the human female reproductive tract: comparison of fallopian tube, uterus, cervix, and vagina. Am. J. Reprod. Immunol. 38, 350-359.
10. Hunt, J. S. (1994) Immunologically relevant cells in the uterus. Biol. Reprod. 50, 461-466.
11. King, A., Wellings, V., Gardner, L., Loke, Y. W. (1989) Immunocytochemical characterization of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle. Hum. Immunol. 24, 195-205.
12. Cooper, M. A., Fehniger, T. A., Turner, S. C., Chen, K. S., Ghaheri, B. A., Ghayur, T., Carson, W. E., Caligiuri, M. A. (2001) Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97, 3146-3151.
13. Lanier, L. L., Le, A. M., Civin, C. I., Loken, M. R., Phillips, J. H. (1986) The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J. Immunol. 136, 4480-4486.
14. Nagler, A., Lanier, L. L., Cwirla, S., Phillips, J. H. (1989) Comparative studies of human FcRIII-positive and negative natural killer cells. J. Immunol. 143, 3183-3191.
15. Kehrl, J. H., Wakefield, L. M., Roberts, A. B., Jakowlew, S., Alvarez-Mon, M., Derynck, R., Sporn, M. B., Fauci, A. S. (1986). Production of transforming growth factor β by human T lymphocytes and its potential role in the regulation of T cell growth. J. Exp. Med. 163, 1037-1050.
16. Ruegemer, J. J., Ho, S. N., Augustine, J. A., Schlager, J. W., Bell, M. P., McKean, D. J., Abraham, R. T. (1990) Regulatory effects of transforming growth factor-β on IL-2- and IL-4-dependent T cell-cycle progression. J. Immunol. 144, 1767-1776.
17. Wira, C. R., Roche, M. A., Rossoll, R. M. (2002) Antigen presentation by vaginal cells: role of TGFβ as a mediator of estradiol inhibition of antigen presentation. Endocrinology 143, 2872-2879.
18. Nelson, B. J., Ralph, P., Green, S. J., Nacy, C. A. (1991) Differential susceptibility of activated macrophage cytotoxic effector reactions to the suppressive effects of transforming growth factor-β 1. J. Immunol. 146, 1849-1857.
19. Khalil, N. (2001) Post translational activation of latent transforming growth factor β (L-TGF-β): clinical implications. Histol. Histopathol. 16, 541-551.
20. Ruscetti, F. W., Palladino, M. A. (1991) Transforming growth factor-β and the immune system. Prog. Growth Factor Res. 3, 159-175.
21. Bellone, G., Aste-Amezaga, M., Trinchieri, G., Rodeck, U. (1995) Regulation of NK cell functions by TGF-β 1. J. Immunol. 155, 1066-1073.
22. Lee, H. M., Rich, S. (1991) Co-stimulation of T cell proliferation by transforming growth factor-β 1. J. Immunol. 147, 1127-1133.
23. Weinberg, A. D., Whitham, R., Swain, S. L., Morrison, W. J., Wyrick, G., Hoy, C., Vandenbark, A. A., Offner, H. (1992) Transforming growth factor-β enhances the in vivo effector function and memory phenotype of antigen-specific T helper cells in experimental autoimmune, encephalomyelitis. J. Immunol. 148, 2109-2117.
24. Cerwenka, A., Bevec, D., Majdic, O., Knapp, W., Holter, W. (1994) TGF-β 1 is a potent inducer of human effector T cells. J. Immunol. 153, 4367-4377.
25. White, H. D., Prabhala, R. H., Humphrey, S. L., Crassi, K. M., Richardson, J. M., Wira, C. R. (2000) A method for the dispersal and characterization of leukocytes from the human female reproductive tract. Am. J. Reprod. Immunol. 44, 96-103.
26. Campbell, K. S., Colonna, M. (2000) Natural Killer Cell Protocols: Cellular and Molecular Methods, Humana Press, Totowa, NJ, 1-4.
27. Koopman, L. A., Kopcow, H. D., Rybalov, B., Boyson, J. E., Orange, J. S., Schatz, F., Masch, R., Lockwood, C. J., Schachter, A. D., Park, P. J., Strominger, J. L. (2003) Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med 198, 1201-1212.
28. Mrozek, E., Anderson, P., Caligiuri, M. A. (1996) Role of interleukin-15 in the development of human CD56+ natural killer cells from CD34+ hematopoietic progenitor cells. Blood 87, 2632-2640.
29. Fehniger, T. A., Caligiuri, M. A. (2001) Interleukin 15: biology and relevance to human disease. Blood 97, 14-32.
30. Polli, V., Bulletti, C., Galassi, A., Borini, A., Ciotti, P. M., Seracchioli, R., Alfieri, S., Flamigni, C. (1996) Transforming growth factor-β 1 in the human endometrium. Gynecol. Endocrinol. 10, 297-302.
31. Boucheix, C., Rubinstein, E. (2001) Tetraspanins. Cell. Mol. Life Sci. 58, 1189-1205.
32. Hemler, M. E. (2001) Specific tetraspanin functions. J. Cell Biol. 155, 1103-1107.
33. Yawata, M., Yawata, N., Abi-Rached, L., Parham, P. (2002) Variation within the human killer cell immunoglobulin-like receptor (KIR) gene family. Crit. Rev. Immunol. 22, 463-481
34. Valiante, N. M., Uhrberg, M., Shilling, H. G., Lienert-Weidenbach, K., Arnett, K. L., D'Andrea, A., Phillips, J. H., Lanier, L. L., Parham, P. (1997) Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7, 739-751.
35. Carson, W. E., Giri, J. G., Lindemann, M. J., Linett, M. L., Ahdieh, M., Paxton, R., Anderson, D., Eisenmann, J., Grabstein, K., Caligiuri, M. A. (1994) Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 180, 1395-1403.
36. Fehniger, T. A., Shah, M. H., Turner, M. J., VanDeusen, J. B., Whitman, S. P., Cooper, M. A., Suzuki, K., Wechser, M., Goodsaid, F., Caligiuri, M. A. (1999) Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 162, 4511-4520.
37. Aste-Amezaga, M., D'Andrea, A., Kubin, M., Trinchieri, G. (1994) Cooperation of natural killer cell stimulatory factor/interleukin-12 with other stimuli in the induction of cytokines and cytotoxic cell-associated molecules in human T and NK cells. Cell. Immunol. 156, 480-492.
38. Kitaya, K., Yasuda, J., Yagi, I., Tada, Y., Fushiki, S., Honjo, H. (2000) IL-15 expression at human endometrium and decidua. Biol. Reprod. 63, 683-687.
39. Verma, S., Hiby, S. E., Loke, Y. W., King, A. (2000) Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol. Reprod. 62, 959-968.
40. Yoshino, O., Osuga, Y., Koga, K., Tsutsumi, O., Yano, T., Fujii, T., Kugu, K., Momoeda, M., Fujiwara, T., Tomita, K., Taketani, Y. (2001) Evidence for the expression of interleukin (IL)-18, IL-18 receptor and IL-18 binding protein in the human endometrium. Mol. Hum. Reprod. 7, 649-654.
41. Mazzeo, D., Vigano, P., Di Blasio, A. M., Sinigaglia, F., Vignali, M., Panina-Bordignon, P. (1998) Interleukin-12 and its free p40 subunit regulate immune recognition of endometrial cells: potential role in endometriosis. J. Clin. Endocrinol. Metab. 83, 911-916.
42. Croy, B. A., Chantakru, S., Esadeg, S., Ashkar, A. A., Wei, Q. (2002) Decidual natural killer cells: key regulators of placental development (a review). J. Reprod. Immunol. 57, 151-168.
43. Tangri, S., Raghupathy, R. (1993) Expression of cytokines in placentas of mice undergoing immunologically mediated spontaneous fetal resorptions. Biol. Reprod. 49, 850-856.
44. Yeaman, G. R., Collins, J. E., Currie, J. K., Guyre, P. M., Wira, C. R., Fanger, M. W. (1998) IFN-γ is produced by polymorphonueleay neutiophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils. J. Immunol. 160, 5145-5153.
45. Saito, S., Moirii, T., Enomoto, M., Sakakura, S., Nishikawa, K., Narita, N., Ichijo, M. (1993) The effect of interleukin 2 and transforming growth factor-β P 2 (TGF-β 2) on the proliferation and natural killer activity of decidual CD16-CD56bright natural killer cells. Cell. Immunol. 152, 605-613.
46. Sporn, M. B., Roberts, A. B., Wakefield, L. M., de Crombrugghe, B. (1987) Some recent advances in the chemistry and biology of transforming growth factor-β. J. Cell Biol. 105, 1039-1045.