Phenotypic analysis and proliferative responses of human endometrial granulated lymphocytes during the menstrual cycle

Biology of Reproduction

Volumn 60, Issue 4, 1999, Pages 871-878

  Searle, Roger F ^a   Jones, Rebecca K ^a   Bulmer, Judith N ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL PROLIFERATION; ENDOMETRIUM; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LYMPHOCYTE PROLIFERATION; MENSTRUAL CYCLE; PRIORITY JOURNAL;

EID: 0032984831     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod60.4.871     Document Type: Article

References (46)

1. Morris H, Edwards J, Tiltman A, Emms M. Endometrial lymphoid tissue: an immunohistological study. J Clin Pathol 1985; 38:644-652.
2. Kamat BR, Isaacson PG. The immunocytochemical distribution of leukocytic subpopulations in human endometrium. Am J Pathol 1987; 127:66-73.
3. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod 1991; 6:791-798.
4. Klentzeris LD, Bulmer JN, Warren A, Morrison L, Li TC, Cooke ID. Endometrial lymphoid tissue in the timed endometrial biopsy: morphometric and immunohistochemical aspects. Am J Obstet Gynecol 1992; 167:667-674.
5. Starkey PM, Clover LM, Rees MC. Variation during the menstrual cycle of immune cell populations in human endometrium. Eur J Obstet Gynecol Reprod Biol 1991; 39:203-207.
6. Jones RK, Searle RF, Stewart JA, Turner S, Bulmer JN. Apoptosis, bcl-2 expression and proliferation activity in human endometrial stroma and endometrial granulated lymphocytes. Biol Reprod 1998; 58: 995-1002.
7. Manaseki S, Searle RF. Natural killer (NK) cell activity of first trimester human decidua. Cell Immunol 1989; 121:166-173.
8. Ferry BL, Starkey PM, Sargent IL, Watt GM, Jackson M, Redman CW. Cell populations in the human early pregnancy decidua: natural killer activity and response to interleukin-2 of CD56-positive large granular lymphocytes. Immunology 1990; 70:446-452.
9. King A, Loke YW. Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell Immunol 1990; 129:435-448.
10. Saito S, Morii T, Enomoto M, Sakakura S, Nishikawa K, Narita N, Ichijo M. The effect of interleukin-2 and transforming growth factor-beta 2 (TGF-beta 2) on the proliferation and natural killer activity of decidual CD16-CD56 bright natural killer cells. Cell Immunol 1993; 152:605-613.
11. Ritson A, Bulmer JN. Isolation and functional studies of granulated lymphocytes in first trimester human decidua. Clin Exp Immunol 1989; 77:263-268.
12. Jones RK, Searle RF, Bulmer JN. Cytotoxic activity of endometrial granulated lymphocytes during the menstrual cycle. Biol Reprod 1997; 57:1217-1222.
13. Chumbley G, King A, Robertson K, Holmes N, Loke YW. Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell Immunol 1994; 155:312-322.
14. Soderstrom K, Corliss B, Lanier L, Phillips JH. CD94/NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J Immunol 1997; 159:1072-1075.
15. Verma S, King A, Loke YW. Expression of killer cell inhibitory receptors on human uterine NK cells. Eur J Immunol 1997; 27:979-983.
16. Saito S, Nishikawa K, Morii T, Enomoto M, Narita N, Motoyoshi K, Ichijo M. Cytokine production by CD 16-CD56 bright natural killer cells in the human early pregnancy decidua. Int Immunol 1993; 5: 559-563.
17. Jokhi PR, King A, Sharkey AM, Smith SK, Loke YW. Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction. J Immunol 1994; 153:4427-4435.
18. Jokhi PP, King A, Loke YW. Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface. Cytokine 1997; 9:126-137.
19. Dietl J, Ruck P, Marzusch K, Horny HP, Kaiserling E, Handgretinger R. Uterine granular lymphocytes are activated natural killer cells expressing VLA-1. Immunol Today 1992; 13:236.
20. Marzusch K, Ruck P, Geiselhart A, Handgretinger R, Dietl JA, Kaiserling E, Horny HP, Vince G, Redman CW. Distribution of cell adhesion molecules on CD56++ , CD3-, CD16-large granular lymphocytes and endothelial cells in first-trimester human decidua. Hum Reprod 1993; 8:1203-1208.
21. Burrows TD, King A, Loke YW. Expression of adhesion molecules by human decidual large granular lymphocytes. Cell Immunol 1993; 147:81-94.
22. Starkey PM. Expression on cells of early human pregnancy decidua, of the p75, IL-2 and p145, IL-4 receptor proteins. Immunology 1991; 73:64-70.
23. King A, Wheeler R, Carter NP, Francis DP, Loke YW. The response of human decidual leukocytes to IL-2. Cell Immunol 1992; 141:409-421.
24. Saito S, Umekage H, Nishikawa K, Morii T, Narita N, Enomoto M, Sakakura S, Harada N, Ichijo M, Morikawa H. Interleukin-4 (IL-4) blocks the IL-2-induced increase in natural killer activity and DNA synthesis of decidual CD16-CD56 bright NK cells by inhibiting expression of the IL-2 receptor alpha, beta and gamma. Cell Immunol 1996; 170:71-77.
25. Maruyama T, Makino T, Sugi T, Matsubayashi H, Ozawa N, Nozawa S. Flow-cytometric analysis of immune cell populations in human decidua from various types of first-trimester pregnancy. Hum Immunol 1992; 34:212-218.
26. Nishikawa K, Saito S, Morii T, Hamada K, Ako H, Narita N, Ichijo M, Kurahayashi M, Sugamura K. Accumulation of CD16-CD56+ natural killer cells with high affinity interleukin 2 receptors in human early pregnancy decidua. Int Immunol 1991; 3:743-750.
27. King A, Balendran N, Wooding P, Carter NP, Loke YW. CD3-leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterization of the CD56++ population. Dev Immunol 1991; 1:169-190.
28. Noyes RW, Hertig AT. Dating the endometrial biopsy. Fertil Steril 1950; 1:3-25.
29. O'Brien J, Knight S, Quick NA, Moore EH, Platt AS. A simple technique for harvesting lymphocytes cultured in Terasaki plates. J Immunol Methods 1979; 27:219-223.
30. Hayakawa S, Saito S, Nemoto N, Chishima F, Akiyama K, Shiraishi H, Hayakawa J, Karasaki-Suzuki M, Fujii KT, Ichijo M. Expression of recombinase-activating genes (RAG-1 and 2) in human decidual mononuclear cells. J Immunol 1994; 153:4934-4939.
31. Gudelj L, Deniz G, Rukavina D, Johnson PM, Christmas SE. Expression of functional molecules by human CD3-decidual granular leucocyte clones. Immunology 1996; 87:609-615.
32. King A, Gardner L, Sharkey A, Loke YW. Expression of CD3 epsilon, CD3 zeta and RAG-1/RAG-2 in decidual CD56+ NK cells. Cell Immunol 1998; 183:99-105.
33. Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W. In: Voico R (ed.), Current Protocols in Immunology. New York: John Wiley & Sons. Inc.; 1977.
34. Mincheva-Nilsson L, Kling M, Hammarstrom S, Nagaeva O, Sundqvist KG, Hammarstrom ML, Baranov V. Gamma delta T cells of human early pregnancy decidua. J Immunol 1997; 159:3266-3277.
35. Grabstein KH, Eisenman J, Shaneback K, Rach C, Srinivasen S, Fung V, Beers C, Richardson J, Schoenborn MA, Ahdieh D, Johnson L, Alderson MR, Watson JD, Anderson DM, Giri JG. Cloning of a novel T-cell growth factor which interacts with the beta chain of the interleukin-2 receptor. Science 1994; 264:965-968.
36. Bulmer JN, Morrison L, Longfellow M, Ritson A. Leukocytes in human decidua: investigation of surface markers and function. In: Chaouat G, Mowbray J (eds.), Cellular and Molecular Biology of the Materno-Fetal Relationship, vol. 212. London, England: Colloque INSERM/John Libbey Eurotext Ltd; 1991: 189-196.
37. Clark DA, Vince G, Flanders KC, Hirte H, Starkey P. CD56+ lymphoid cells in human first trimester pregnancy decidua as a source of novel transforming growth factor-beta 2-related immunosuppressive factors. Hum Reprod 1994; 9:2270-2277.
38. Loke YW, King A. Human Implantation, Cell Biology and Immunology. Cambridge: Cambridge University Press; 1995.
39. Tabibzadeh S. Distinct subsets of stromal cells confined to unique microenvironments in human endometrium throughout the menstrual cycle. Am J Reprod Immunol 1991; 26:5-10.
40. Pace D, Longfellow M, Bulmer JN. Characterization of intraepithelial lymphocytes in human endometrium. J Reprod Fertil 1991; 91:165-174.
41. Aplin JD, Charlton AK, Ayad S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res 1988; 253:231-240.
42. Beliard A, Donnez J, Nisolle M, Foidart J-M. Localization of laminin, fibronectin, E-cadherin, and integrins in endometrium and endometriosis. Fertil Steril 1997; 67:226-272.
43. Robertson MJ, Caligiuri MA, Manley TJ, Levine H, Ritz J. Human natural killer cell adhesion molecules. Differential expression after activation and participation in cytolysis. J Immunol 1990; 145:3194-3201.
44. Storkus WJ, Dawson JR. Target structures involved in natural killing NK: characteristics, distribution, and candidate molecules. Crit Rev Immunol 1991; 10:393-416.
45. Vassiliadou N, Bulmer JN. Expression of CD69 activation marker by endometrial granulated lymphocytes throughout the menstrual cycle and in early pregnancy. Immunology 1998; 94:368-375.
46. White HD, Crassi KM, Givan AL, Stern JE, Gonzalez JL, Memoli VA, Green WR, Wira CR. CD3+ CD8+ CTL activity within the human female reproductive tract. J Immunol 1997; 158:3017-3027.