Decidua-associated suppressor cells in abortion-prone DBA/2-mated CBA/J mice that release bioactive transforming growth factor β2-related immunosuppressive molecules express a bone marrow-derived natural suppressor cell marker and γδ T-cell receptor

Biology of Reproduction

Volumn 56, Issue 5, 1997, Pages 1351-1360

  Clark, David A ^a   Merali, Fatima S ^a   Hoskin, David W ^b   Steel Norwood, Darlene ^a   Arck, Petra C ^a   Croitoru, Kenneth ^a   Murgita, Robert A ^c   Hirte, Holger ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTICLE; CELLULAR DISTRIBUTION; DECIDUA; FEMALE; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SUPPRESSOR CELL; TISSUE DISTRIBUTION; TROPHOBLAST;

ANIMALIA; MURINAE;

EID: 0030892181     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod56.5.1351     Document Type: Article

References (51)

1. Clark DA, Chaput A, Walker C, Rosenthal KL. Active suppression of host vs graft reaction in pregnant mice. VI. Soluble suppressor activity obtained from decidua of allopregnant mice blocks the response to IL-2. J Immunol 1985; 134:1659-1664.
2. Slapsys RM, Richards CD, Clark DA. Active suppression of host-versus-graft reaction in pregnant mice. VIII. The uterine decidua-associated suppressor cell is distinct from decidual NK cells. Cell Immunol 1985; 99:140-149.
3. Clark DA, Flanders KC, Banwatt D, Millar-Book W, Stedronska-Clark J. Murine pregnancy decidua produces a unique immunosuppressive molecule related to transforming growth factor beta-2. J Immunol 1990; 144:3008-3014.
4. Clark DA, Lea RG, Flanders KC, Banwatt D, Chaouat G. Role of a unique species of TGF-β in preventing rejection of the conceptus during pregnancy. In: Gergely J, Benczur M. Erdei A, Falus A, Faust Gy, Medgyesi G, Petranyi Gy, Rajnavolgyi E (eds.), Progress in Immunology VIII. Budapest: Springer-Verlag; 1992: 841-847.
5. Slapsys RM, Younglai E, Clark DA. A novel suppressor cell develops in uterine decidua in response to fetal trophoblast-type cells. Reg Immunol 1988; 1:182-189.
6. Clark DA, Flanders KC, Hirte H, Dasch JR, Coker R, McAnulty RJ, Laurent GJ. Characterization of murine pregnancy decidua TGFβ. I. TGFβ2-like molecules of unusual molecular size released in bioactive form. Biol Reprod 1995; 52:1380-1388.
7. Hoskin DW, Gronvik K-O, Hooper DC, Reilly BD, Murgita RA. Altered immune response patterns in syngeneic pregnancy: presence of natural null suppressor cells in maternal spleen identifiable by monoclonal antibodies. Cell Immunol 1989; 120:42-60.
8. Hoskin DW, Brooks-Kaiser JC, Kaiser M, Murgita RA. Reactivity of monoclonal antibody 1E5/B5 with a novel phenotypic marker expressed on murine natural suppressor cells. Hybridoma 1992; 11:203-215.
9. Brooks-Kaiser JC, Hoskin DW. Inhibition of DNA synthesis and IL-2 bioactivity in MLR by pregnancy-associated natural suppressor cells involves the production of a TGF-β1-like molecule and a second distinct inhibitory factor. J Reprod Immunol 1993; 25:31-49.
10. Krcek J, Clark DA. Localization of a small sized bone marrow sub-population at the implantation site of the murine fetus. Am J Reprod Immunol 1985; 7:95-98.
11. Heyborne K, Fu Y-X, Nelson A, Farr A, O'Brien R, Born W. Recognition of trophoblasts by γδ T cells. J Immunol 1994; 153:2918-2926.
12. Suzuki T, Hiromatsu K, Ando Y, Okamoto T, Tomoda Y, Yosjikai Y. Regulatory role of γδ T cells in uterine intraepithelial lymphocytes in maternal antifetal immune response. J Immunol 1995; 154:4476-4484.
13. Clark DA. Controversies in reproductive immunology. Crit Rev Immunol 1991; 11:215-247.
14. Arck PC, Merali FS, Stanisz AM, Stead RH, Chaouat G, Manuel J, Clark DA. Stress-induced murine abortion associated with substance P-dependent alteration in cytokines in maternal uterine decidua. Biol Reprod 1995; 53:814-819.
15. Lea RG, Flanders KC, Harley CB, Manuel J, Banwatt D, Clark DA. Release of a TGF-β2-related suppressor factor from post-implantation murine decidual tissue can be correlated with the detection of a sub-population of cells containing RNA for TGF-β2. J Immunol 1992; 148:778-787.
16. Leo OM, Foo DH, Sachs D, Samelson L, Bluestone JA. Identification of a monoclonal antibody specific for a murine T3 polypeptide. Proc Natl Acad Sci USA 1987; 84:1374-1378.
17. Goodman T, Lefrancois L. Intraepithelial lymphocytes. Anatomical site, not T cell receptor form, dictates phenotype and function. J Exp Med 1989; 170:1569-1581.
18. 51Cr release cytotoxicity assay for cytotoxic lymphocytes. Cell Immunol 1974; 14: 284-302.
19. Merali F, Manuel J, Arck P, Clark DA. Do murine decidual natural suppressor cells synthesize novel TGF-β2-related suppressor factor? Am J Reprod Immunol 1994; 31:230 (abstract).
20. Ferguson MWJ, Whitby DJ, Shah M, Armstrong J, Siebert JW, Longnaker MT. Scar formation: the spectral nature of fetal and adult wound repair. Plast Reconstr Surg 1996; 97:854-860.
21. Arck PC, Ferrick DA, Steele-Norwood D, Croitoru K, Clark DA. Murine T cell determination of pregnancy outcome. I. Effects of strain, αβ T cell receptor, γδ T cell receptor, and γδ T cell subsets. Am J Reprod Immunol 1997; (in press).
22. Clark DA, Phillips RA, Miller RG. Characterization of the cells that suppress the cytotoxic activity of T lymphocytes. II. Physical properties, specificity, and developmental kinetics of the inhibitory non T cell population. Cell Immunol 1977; 34:25-37.
23. Clark DA, Damji N, Chaput A, Daya S, Rosenthal KL, Brierley J. Decidua-associated suppressor cells and suppressor factors regulating interleukin-2: their role in the survival of the "fetal allograft." In: Cinader B, Miller RG (eds.), Progress in Immunology VI. London: Academic Press; 1986: 1089-1099.
24. + lymphocyte populations with different T cell receptors: a role for the gut epithelium in T cell differentiation. J Exp Med 1991; 173:471-481.
25. Bandera A, Itohara S, Bonneville M, Burlen-Defranox O, Mota-Santos T, Couthino A, Tonegawa S. Extrathymic origin of intestinal intraepithelial lymphocytes bearing T-cell antigen receptor γδ. Proc Natl Acad Sci USA 1991; 88:43-47.
26. Cheng H-L, Schneider SL, Kane CM, Gollnick SO, Grande C, Thompson D, Pietrzak E, Tomasi TB. TGF-β2 gene and protein expression in maternal and fetal tissue at various stages of murine development. J Reprod Immunol 1991; 25:133-148.
27. Das SK, Flanders KC, Andrews GK, Dey SK. Expression of transforming growth factor-β isoforms (β2 and β3) in the mouse uterus: analysis of the preimplantation period and effect of ovarian steroids. Endocrinology 1992; 130:3459-3466.
28. Schneider SL, Gollnick SO, Grande C, Pazik JE, Tomasi TB. Differential regulation of TGF-β2 by hormones in rat uterus and mammary gland. J Reprod Immunol 1996; 31:125-144.
29. Arck PC, Ferrick DA, Steele-Norwood D, Croitoru K, Clark DA. Regulation of abortion by γδ T cells. Am J Reprod Immunol 1997; (in press).
30. Lang F, Peyrat MA, Constant P, Davodeau F, David-Ameline J, Poquet Y, Vie H, Fournie JJ, Bonneville M. Early activation of human V-γ9Vδ2 T cell broad cytotoxicity and TNF production by nonpeptidic mycobacterial ligands. J Immunol 1995; 154:5986-5994.
31. Choudhary A, Davodeau F, Moreau A, Peyrat M-A, Bonneville M, Jotereau F. Selective lysis of autologous tumor cells by recurrent γδ tumor-infiltrating lymphocytes from renal carcinoma. J Immunol 1995; 154:3932-3940.
32. Ferrick DA, Schrenzel MD, Mulvania T, Hsieh B, Ferlin WG, Lepper H. Differential production of interferon-γ and interleukin-4 in response to Th1- and Th2-stimulating pathogens by γδ T cells in vivo. Nature 1995; 373:255-257.
33. Lynch F, Shevach EM. Gamma delta T cells promote CD4 and CD8 expression by SCID thymocytes. Int Immunol 1993; 5:991-995.
34. Sandor M, Sperling AI, Cook GA, Weinstock JV, Lynch RG, Bluestone JA. Two waves of γδ T cells expressing different Vδ genes are recruited into schistosome-induced liver granulomas. J Immunol 1995; 155:275-284.
35. Chensue SW, Warmington KS, Ruth JH, Lincoln P, Kunkel SL. Cytokine function during mycobacterial and schistosomal antigen-induced pulmonary granuloma formation. Local and regional participation of IFN-γ, IL1, and TNF. J Immunol 1995; 154:5969-5976.
36. Fu Y-X, Roark CE, Kely K, Drevets D, Campbell P, O'Brien R, Born W. Immune protection and control of inflammatory tissue necrosis by γδ T cells. J Immunol 1994; 153:3101-3115.
37. Peterman GM, Spencer C, Sperling AI, Bluestone JA. Role of γδ T cells in murine collagen-induced arthritis. J Immunol 1993; 151:6546-6558.
38. Carding SR, Allen W, Kyes S, Hayday A, Bottomly K, Doherty PC. Late dominance of the inflammatory process in murine influenza by γ/δ T cells. J Exp Med 1990; 172:1225-1231.
39. + T cells. J Immunol 1996; 156: 232-237.
40. Gronvik K-O, Hoskin DW, Murgita RA. Monoclonal antibodies against murine neonatal and pregnancy-associated natural suppressor cells induce resorption of the fetus. Scand J Immunol 1987; 25:533-540.
41. - cells that make TH2 cytokines and help B cells. Science 1993; 37:247-258.
42. Heyborne KD, Cranfill RL, Carding SR, Born WK, O'Brien RL. Characterization of γδ T lymphocytes at the maternal-fetal interface. J Immunol 1992; 149:2872-2878.
43. Lea RG, Stewart F, Allen WR, Ohno I, Clark DA. Accumulation of chromotrope 2R positive cells in equine endometrium during early pregnancy and expression of transforming growth factor-β2 (TGF-β2). J Reprod Fertil 1995; 103:339-347.
44. Meeusen E, Fox A, Brandon M, Lee C-S. Activation of uterine intraepithelial γδ T cell receptor-positive lymphocytes during pregnancy. Eur J Immunol 1993; 23:1112-1117.
45. + cells and show selective down-regulation of alloreactivity. J Immunol 1992; 149:2203-2211.
46. Daya S, Johnson PM, Clark DA. Trophoblast induction of suppressor-type cell activity in human endometrial tissue. Am J Reprod Immunol 1989; 19:65-72.
47. + lymphoid cells in human first trimester pregnancy decidua as a source of novel TGF-β2-related imrnunosuppressive factors. Hum Reprod 1994; 9:2270-2277.
48. Morii T, Nishikawa K, Saito S, Enomoto M, Ito A, Kurai N, Shimoyama T, Ichijo M, Narita N. T-cell receptors are expressed but down-regulated in intradecidual T lymphocytes. Am J Reprod Immunol 1993; 29:1-4.
49. + lymphocytes from first trimestr decidua using two-colour flow cytometry. Am J Reprod Immunol 1993; 29:5-16.
50. Hayakawa S, Shiraishi H, Saitoh S, Satoh K. Decidua as a site of Vγ1 T-cell differentiation. Am J Reprod Immunol 1996; 35:233-238.
51. Satoh M, Seki S, Hashimoto W, Ogasawara K, Kobayashi T, Kumagai K, Matsuno S, Takeda K. Cytotoxic γδ or αβ T cells with a natural killer cell marker, CD56, induced from human peripheral blood lymphocytes by a combination of IL-12 and IL-2. J Immunol 1996; 157: 3886-3892.