Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2010

Open Access 01-12-2010 | Research

The frequency of CD25+CD4+ and FOXP3+ regulatory T cells in ectopic endometrium and ectopic decidua

Authors: Pawel Basta, Marcin Majka, Wojciech Jozwicki, Ewelina Lukaszewska, Anna Knafel, Marek Grabiec, Elzbieta Stasienko, Lukasz Wicherek

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

Login to get access

Abstract

Background

The presence of regulatory T (Treg) cells in human endometrium is crucial for maintaining immunological homeostasis within the uterus. For this study we decided to evaluate the subpopulations of Treg cells in conditions where a disturbance in the immunological equilibrium in ectopic endometrium and decidua has been observed, such as in cases of ovarian endometriosis (involving local immune cell suppression) and ectopic pregnancy (involving an increase in local immune system activity). We then compared these findings to what we observed in the normal eutopic endometrium of women during the secretory phase of the menstrual cycle (with immune cells under individual control).

Methods

The endometrium tissue samples evaluated in our study were obtained from 47 women during one of two kinds of laparoscopic procedures. 16 of the women underwent laparoscopies due to Fallopian tube pregnancies (EP), and 16 due to ovarian endometrioma, while 15 women made up a control group. The presence of regulatory T cells in these tissue samples was evaluated by FACS.

Results

In our study, the percentages of FOXP3+ cells within the subpopulation of CD4+ T lymphocytes found in the decidua of the patients treated for Fallopian tube pregnancies were statistically significantly lower than both those observed in the ovarian endometriosis tissue samples and those found in the secretory eutopic endometrium samples of the control group.

Conclusion

The disturbance in the immunological equilibrium observed in ectopic endometrium and decidua would seem to be related to the alteration in the Treg cell population that occurs in these ectopic tissues.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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. 10.1016/0028-2243(91)90058-S.CrossRefPubMed 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. 10.1016/0028-2243(91)90058-S.CrossRefPubMed
2.
go back to reference King A, Burrows T, Loke YW: Human uterine natural killer cells. Nat Immun. 1996, 15: 41-52.PubMed King A, Burrows T, Loke YW: Human uterine natural killer cells. Nat Immun. 1996, 15: 41-52.PubMed
3.
go back to reference Gardner L, Moffett A: Dendritic cells in the human decidua. Biol Reprod. 2003, 69: 1438-1446. 10.1095/biolreprod.103.017574.CrossRefPubMed Gardner L, Moffett A: Dendritic cells in the human decidua. Biol Reprod. 2003, 69: 1438-1446. 10.1095/biolreprod.103.017574.CrossRefPubMed
4.
go back to reference Wilczynski JR, Kalinka J, Radwan M: The role of the T-regulatory cells in pregnancy and cancer. Front Biosci. 2008, 13: 2275-2289. 10.2741/2841.CrossRefPubMed Wilczynski JR, Kalinka J, Radwan M: The role of the T-regulatory cells in pregnancy and cancer. Front Biosci. 2008, 13: 2275-2289. 10.2741/2841.CrossRefPubMed
5.
go back to reference Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, Brumlik M, Cheng P, Curiel T, Myers L, Lackner A, Alvarez X, Ochoa A, Chen L, Zou W: B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med. 2006, 203: 871-881. 10.1084/jem.20050930.PubMedCentralCrossRefPubMed Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, Brumlik M, Cheng P, Curiel T, Myers L, Lackner A, Alvarez X, Ochoa A, Chen L, Zou W: B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med. 2006, 203: 871-881. 10.1084/jem.20050930.PubMedCentralCrossRefPubMed
6.
go back to reference Wicherek L, Gałązka K, Lazar A: The analysis of Metallothionein, RCAS1 immunoreactivity regarding immune cells concentration in endometrium and tubal mucosa in ectopic pregnancy during the course of tubal rupture. Gynecol Obstet Invest. 2008, 65: 52-61. 10.1159/000107649.CrossRefPubMed Wicherek L, Gałązka K, Lazar A: The analysis of Metallothionein, RCAS1 immunoreactivity regarding immune cells concentration in endometrium and tubal mucosa in ectopic pregnancy during the course of tubal rupture. Gynecol Obstet Invest. 2008, 65: 52-61. 10.1159/000107649.CrossRefPubMed
7.
go back to reference Wicherek L, Popiela TJ, Galazka K, Dutsch-Wicherek M, Opławski M, Basta A, Klimek M: Metallothionein and RCAS1 expression in comparison to immunological cell activity in endometriosis, endometrial adenocarcinoma, and the endometrium according to menstrual cycle changes. Gynecol Oncol. 2005, 99: 622-630. 10.1016/j.ygyno.2005.07.003.CrossRefPubMed Wicherek L, Popiela TJ, Galazka K, Dutsch-Wicherek M, Opławski M, Basta A, Klimek M: Metallothionein and RCAS1 expression in comparison to immunological cell activity in endometriosis, endometrial adenocarcinoma, and the endometrium according to menstrual cycle changes. Gynecol Oncol. 2005, 99: 622-630. 10.1016/j.ygyno.2005.07.003.CrossRefPubMed
8.
go back to reference Budiu RA, Diaconu I, Chrissluis R, Dricu A, Edwards RP, Vlad AM: A conditional mouse model for human MUC1-positive endometriosis shows the presence of anti-MUC1 antibodies and Foxp3+ regulatory T cells. Dis Model Mech. 2009, 2: 593-603. 10.1242/dmm.002535.CrossRefPubMed Budiu RA, Diaconu I, Chrissluis R, Dricu A, Edwards RP, Vlad AM: A conditional mouse model for human MUC1-positive endometriosis shows the presence of anti-MUC1 antibodies and Foxp3+ regulatory T cells. Dis Model Mech. 2009, 2: 593-603. 10.1242/dmm.002535.CrossRefPubMed
9.
go back to reference Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S: Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod. 2004, 10: 347-353. 10.1093/molehr/gah044.CrossRefPubMed Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S: Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod. 2004, 10: 347-353. 10.1093/molehr/gah044.CrossRefPubMed
10.
go back to reference Kingsley CL, Karim M, Bushell AR, Wood KJ: CD25+CD4+ regulatory T cells prevent graft rejection: CTLA4- and IL-10-dependent immunoregulation of alloresponses. J Immunol. 2002, 168: 1080-1086.CrossRefPubMed Kingsley CL, Karim M, Bushell AR, Wood KJ: CD25+CD4+ regulatory T cells prevent graft rejection: CTLA4- and IL-10-dependent immunoregulation of alloresponses. J Immunol. 2002, 168: 1080-1086.CrossRefPubMed
11.
go back to reference Hori S, Sakaguchi S: Foxp3: a critical regulator of the development and function of regulatory T cells. Microbes Infect. 2004, 6: 745-751. 10.1016/j.micinf.2004.02.020.CrossRefPubMed Hori S, Sakaguchi S: Foxp3: a critical regulator of the development and function of regulatory T cells. Microbes Infect. 2004, 6: 745-751. 10.1016/j.micinf.2004.02.020.CrossRefPubMed
12.
go back to reference Saito S, Sasaki Y, Sakai M: CD4(+)CD25high regulatory T cells in human pregnancy. J Reprod Immunol. 2005, 65: 111-120. 10.1016/j.jri.2005.01.004.CrossRefPubMed Saito S, Sasaki Y, Sakai M: CD4(+)CD25high regulatory T cells in human pregnancy. J Reprod Immunol. 2005, 65: 111-120. 10.1016/j.jri.2005.01.004.CrossRefPubMed
13.
go back to reference Saito S, Shiozaki A, Sasaki Y, Nakashima A, Shima T, Ito M: Regulatory T cells and regulatory NK cells play an important roles in feto-maternal tolerance. Semin Immunopathol. 2007, 29: 115-122. 10.1007/s00281-007-0067-2.CrossRefPubMed Saito S, Shiozaki A, Sasaki Y, Nakashima A, Shima T, Ito M: Regulatory T cells and regulatory NK cells play an important roles in feto-maternal tolerance. Semin Immunopathol. 2007, 29: 115-122. 10.1007/s00281-007-0067-2.CrossRefPubMed
14.
go back to reference Tilburgs T, Roelen DL, van der Mast BJ, de Groot-Swings GM, Kleijburg C, Scherjon SA, Claas FH: Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J Immunol. 2008, 180: 5737-5745.CrossRefPubMed Tilburgs T, Roelen DL, van der Mast BJ, de Groot-Swings GM, Kleijburg C, Scherjon SA, Claas FH: Evidence for a selective migration of fetus-specific CD4+CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J Immunol. 2008, 180: 5737-5745.CrossRefPubMed
15.
go back to reference Arruvito L, Sanz M, Banham AH, Fainboim L: Expansion of CD4+CD25+and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol. 2007, 178: 2572-2578.CrossRefPubMed Arruvito L, Sanz M, Banham AH, Fainboim L: Expansion of CD4+CD25+and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol. 2007, 178: 2572-2578.CrossRefPubMed
16.
go back to reference Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, Dolaptchieva M, Alexander T, Taran A, Malfertheiner SF, Costa SD, Zimmermann G, Nitschke C, Volk HD, Alexander H, Gunzer M, Zenclussen AC: Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol. 2009, 182: 5488-5497. 10.4049/jimmunol.0803177.CrossRefPubMed Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, Dolaptchieva M, Alexander T, Taran A, Malfertheiner SF, Costa SD, Zimmermann G, Nitschke C, Volk HD, Alexander H, Gunzer M, Zenclussen AC: Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol. 2009, 182: 5488-5497. 10.4049/jimmunol.0803177.CrossRefPubMed
17.
go back to reference Saito S, Nakashima A, Shima T, Ito M: Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol. 2010, 63: 601-610. 10.1111/j.1600-0897.2010.00852.x.CrossRefPubMed Saito S, Nakashima A, Shima T, Ito M: Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol. 2010, 63: 601-610. 10.1111/j.1600-0897.2010.00852.x.CrossRefPubMed
18.
go back to reference Raghupathy R, Al-Mutawa E, Al-Azemi M, Makhseed M, Azizieh F, Szekeres-Bartho J: Progesterone-induced blocking factor (PIBF) modulates cytokine production by lymphocytes from women with recurrent miscarriage or preterm delivery. J Reprod Immunol. 2009, 80: 91-99. 10.1016/j.jri.2009.01.004.CrossRefPubMed Raghupathy R, Al-Mutawa E, Al-Azemi M, Makhseed M, Azizieh F, Szekeres-Bartho J: Progesterone-induced blocking factor (PIBF) modulates cytokine production by lymphocytes from women with recurrent miscarriage or preterm delivery. J Reprod Immunol. 2009, 80: 91-99. 10.1016/j.jri.2009.01.004.CrossRefPubMed
19.
20.
go back to reference Dmowski WP, Ding J, Shen J, Rana N, Fernandez BB, Braun DP: Apoptosis in endometrial glandular cells in women with and without endometriosis. Hum Reprod. 2001, 16: 1802-1808. 10.1093/humrep/16.9.1802.CrossRefPubMed Dmowski WP, Ding J, Shen J, Rana N, Fernandez BB, Braun DP: Apoptosis in endometrial glandular cells in women with and without endometriosis. Hum Reprod. 2001, 16: 1802-1808. 10.1093/humrep/16.9.1802.CrossRefPubMed
21.
go back to reference Berbic M, Hey-Cunningham AJ, Ng C, Tokushige N, Ganewatta S, Markham R, Russell P, Fraser IS: The role of Foxp3+ regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum Reprod. 2010, 25: 900-907. 10.1093/humrep/deq020.CrossRefPubMed Berbic M, Hey-Cunningham AJ, Ng C, Tokushige N, Ganewatta S, Markham R, Russell P, Fraser IS: The role of Foxp3+ regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum Reprod. 2010, 25: 900-907. 10.1093/humrep/deq020.CrossRefPubMed
22.
go back to reference Polanczyk MJ, Hopke C, Vandenbark AA, Offner H: Treg suppressive activity involves estrogen-dependent expression of programmed death-1 (PD-1). Int Immunol. 2007, 19: 337-343. 10.1093/intimm/dxl151.CrossRefPubMed Polanczyk MJ, Hopke C, Vandenbark AA, Offner H: Treg suppressive activity involves estrogen-dependent expression of programmed death-1 (PD-1). Int Immunol. 2007, 19: 337-343. 10.1093/intimm/dxl151.CrossRefPubMed
23.
go back to reference Lebovic DI, Mueller MD, Taylor RN: Immunobiology of endometriosis. Fertil Steril. 2001, 75: 1-10. 10.1016/S0015-0282(00)01630-7.CrossRefPubMed Lebovic DI, Mueller MD, Taylor RN: Immunobiology of endometriosis. Fertil Steril. 2001, 75: 1-10. 10.1016/S0015-0282(00)01630-7.CrossRefPubMed
24.
go back to reference Wicherek L: Alterations in RCAS1 serum concentration levels during menstrual cycle in patients with uterine leiomyoma and lack of analogical changes in adenomyosis. Gynecol Obstet Invest. 2009, 67: 195-201. 10.1159/000188045.CrossRefPubMed Wicherek L: Alterations in RCAS1 serum concentration levels during menstrual cycle in patients with uterine leiomyoma and lack of analogical changes in adenomyosis. Gynecol Obstet Invest. 2009, 67: 195-201. 10.1159/000188045.CrossRefPubMed
25.
go back to reference Wicherek L: Alterations in RCAS1 Serum Concentration Levels during the Normal Menstrual Cycle and the Lack of Analogical Changes in Ovarian Endometriosis. Am J Reprod Immunol. 2008, 59: 535-544. 10.1111/j.1600-0897.2008.00584.x.CrossRefPubMed Wicherek L: Alterations in RCAS1 Serum Concentration Levels during the Normal Menstrual Cycle and the Lack of Analogical Changes in Ovarian Endometriosis. Am J Reprod Immunol. 2008, 59: 535-544. 10.1111/j.1600-0897.2008.00584.x.CrossRefPubMed
26.
go back to reference Basta P, Mach P, Pitynski K, Bednarek W, Klimek M, Ziƙtek J, Zając K, Wicherek L: Differences in the blood serum levels of soluble HLA-G concentrations between the menstrual cycle phases and menopause in patients with ovarian endometriosis and uterine leiomyoma. Neuro Endocrinol Lett. 2009, 30: 91-98.PubMed Basta P, Mach P, Pitynski K, Bednarek W, Klimek M, Ziƙtek J, Zając K, Wicherek L: Differences in the blood serum levels of soluble HLA-G concentrations between the menstrual cycle phases and menopause in patients with ovarian endometriosis and uterine leiomyoma. Neuro Endocrinol Lett. 2009, 30: 91-98.PubMed
27.
go back to reference Menier C, Prevot S, Carosella ED, Rouas-Freiss N: Human leukocyte antigen-G is expressed in advanced-stage ovarian carcinoma of high-grade histology. Hum Immunol. 2009, 70: 1006-1009. 10.1016/j.humimm.2009.07.021.CrossRefPubMed Menier C, Prevot S, Carosella ED, Rouas-Freiss N: Human leukocyte antigen-G is expressed in advanced-stage ovarian carcinoma of high-grade histology. Hum Immunol. 2009, 70: 1006-1009. 10.1016/j.humimm.2009.07.021.CrossRefPubMed
28.
go back to reference Nakashima M, Sonoda K, Watanabe T: Inhibition of cell growth and induction of apoptotic cell death by the human tumor-associated antigen RCAS1. Nat Med. 1999, 5: 938-942. 10.1038/11383.CrossRefPubMed Nakashima M, Sonoda K, Watanabe T: Inhibition of cell growth and induction of apoptotic cell death by the human tumor-associated antigen RCAS1. Nat Med. 1999, 5: 938-942. 10.1038/11383.CrossRefPubMed
29.
go back to reference Sonoda K, Miyamoto S, Hirakawa T, Yagi H, Yotsumoto F, Nakashima M, Watanabe T, Nakano H: Association between RCAS1 expression and microenvironmental immune cell death in uterine cervical cancer. Gynecol Oncol. 2005, 97: 772-779. 10.1016/j.ygyno.2005.02.025.CrossRefPubMed Sonoda K, Miyamoto S, Hirakawa T, Yagi H, Yotsumoto F, Nakashima M, Watanabe T, Nakano H: Association between RCAS1 expression and microenvironmental immune cell death in uterine cervical cancer. Gynecol Oncol. 2005, 97: 772-779. 10.1016/j.ygyno.2005.02.025.CrossRefPubMed
30.
go back to reference Sonoda K, Miyamoto S, Nakashima M, Wake N: The biological role of the unique molecule RCAS1: a bioactive marker that induces connective tissue remodeling and lymphocyte apoptosis. Front Biosci. 2008, 13: 1106-1116. 10.2741/2748.CrossRefPubMed Sonoda K, Miyamoto S, Nakashima M, Wake N: The biological role of the unique molecule RCAS1: a bioactive marker that induces connective tissue remodeling and lymphocyte apoptosis. Front Biosci. 2008, 13: 1106-1116. 10.2741/2748.CrossRefPubMed
31.
go back to reference Jasper MJ, Tremellen KP, Robertson SA: Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod. 2006, 12: 301-308. 10.1093/molehr/gal032.CrossRefPubMed Jasper MJ, Tremellen KP, Robertson SA: Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod. 2006, 12: 301-308. 10.1093/molehr/gal032.CrossRefPubMed
32.
go back to reference Arruvito L, Sotelo AI, Billordo A, Fainboim L: A physiological role for inducible FOXP3(+) TREG cells Lessons from women with reproductive failure. Clin Immunol. 2010, 136: 432-441. 10.1016/j.clim.2010.05.002.CrossRefPubMed Arruvito L, Sotelo AI, Billordo A, Fainboim L: A physiological role for inducible FOXP3(+) TREG cells Lessons from women with reproductive failure. Clin Immunol. 2010, 136: 432-441. 10.1016/j.clim.2010.05.002.CrossRefPubMed
33.
go back to reference Tilburgs T, Claas FH, Scherjon SA: Elsevier Trophoblast Research Award Lecture: Unique properties of decidual T cells and their role in immune regulation during human pregnancy. Placenta. 2010, 31: 82-86. 10.1016/j.placenta.2010.01.007.CrossRef Tilburgs T, Claas FH, Scherjon SA: Elsevier Trophoblast Research Award Lecture: Unique properties of decidual T cells and their role in immune regulation during human pregnancy. Placenta. 2010, 31: 82-86. 10.1016/j.placenta.2010.01.007.CrossRef
34.
go back to reference Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, Kanhai HH, Roelen DL, Claas FH: Comparison of decidual leukocytes following spontaneous vaginal delivery and elective cesarean section in uncomplicated human term pregnancy. J Reprod Immunol. 2004, 62: 125-137. 10.1016/j.jri.2003.11.007.CrossRefPubMed Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, Kanhai HH, Roelen DL, Claas FH: Comparison of decidual leukocytes following spontaneous vaginal delivery and elective cesarean section in uncomplicated human term pregnancy. J Reprod Immunol. 2004, 62: 125-137. 10.1016/j.jri.2003.11.007.CrossRefPubMed
35.
go back to reference Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, van Schip JJ, Kanhai HH, Roelen DL, Claas FH: Differential distribution of NK cells in decidua basalis compared with decidua parietalis after uncomplicated human term pregnancy. Hum Immunol. 2003, 64: 921-929. 10.1016/S0198-8859(03)00170-8.CrossRefPubMed Sindram-Trujillo AP, Scherjon SA, van Hulst-van Miert PP, van Schip JJ, Kanhai HH, Roelen DL, Claas FH: Differential distribution of NK cells in decidua basalis compared with decidua parietalis after uncomplicated human term pregnancy. Hum Immunol. 2003, 64: 921-929. 10.1016/S0198-8859(03)00170-8.CrossRefPubMed
36.
go back to reference Sindram-Trujillo A, Scherjon S, Kanhai H, Roelen D, Claas F: Increased T-cell activation in decidua parietalis compared to decidua basalis in uncomplicated human term pregnancy. Am J Reprod Immunol. 2003, 49: 261-268. 10.1034/j.1600-0897.2003.00041.x.CrossRefPubMed Sindram-Trujillo A, Scherjon S, Kanhai H, Roelen D, Claas F: Increased T-cell activation in decidua parietalis compared to decidua basalis in uncomplicated human term pregnancy. Am J Reprod Immunol. 2003, 49: 261-268. 10.1034/j.1600-0897.2003.00041.x.CrossRefPubMed
37.
go back to reference Galazka K, Wicherek L, Pitynski K, Kijowski J, Zajac K, Bednarek W, Dutsch-Wicherek M, Rytlewski K, Kalinka J, Basta A, Majka M: Changes in the subpopulation of CD25+ CD4+ and FOXP3+ regulatory T cells in decidua with respect to the progression of labor at term and the lack of analogical changes in the subpopulation of suppressive B7-H4 macrophages--a preliminary report. Am J Reprod Immunol. 2009, 61: 136-146. 10.1111/j.1600-0897.2008.00674.x.CrossRefPubMed Galazka K, Wicherek L, Pitynski K, Kijowski J, Zajac K, Bednarek W, Dutsch-Wicherek M, Rytlewski K, Kalinka J, Basta A, Majka M: Changes in the subpopulation of CD25+ CD4+ and FOXP3+ regulatory T cells in decidua with respect to the progression of labor at term and the lack of analogical changes in the subpopulation of suppressive B7-H4 macrophages--a preliminary report. Am J Reprod Immunol. 2009, 61: 136-146. 10.1111/j.1600-0897.2008.00674.x.CrossRefPubMed
38.
go back to reference Wicherek L, Basta P, Sikora J, Galazka K, Rytlewski K, Grabiec M, Lazar A, Kalinka J: RCAS1 decidual immunoreactivity in severe pre-eclampsia: immune cell presence and activity. Am J Reprod Immunol. 2007, 58: 358-366. 10.1111/j.1600-0897.2007.00521.x.CrossRefPubMed Wicherek L, Basta P, Sikora J, Galazka K, Rytlewski K, Grabiec M, Lazar A, Kalinka J: RCAS1 decidual immunoreactivity in severe pre-eclampsia: immune cell presence and activity. Am J Reprod Immunol. 2007, 58: 358-366. 10.1111/j.1600-0897.2007.00521.x.CrossRefPubMed
39.
go back to reference Wicherek L, Galazka K, Lazar A: RCAS1 Decidual Immunoreactivity during Placental Abruption: Immune Cell Presence and Activity. Am J Reprod Immunol. 2007, 58: 46-55. 10.1111/j.1600-0897.2007.00490.x.CrossRefPubMed Wicherek L, Galazka K, Lazar A: RCAS1 Decidual Immunoreactivity during Placental Abruption: Immune Cell Presence and Activity. Am J Reprod Immunol. 2007, 58: 46-55. 10.1111/j.1600-0897.2007.00490.x.CrossRefPubMed
40.
go back to reference Wicherek L: The role of the endometrium in the regulation of immune cell activity. Front Biosci. 2008, 13: 1018-1035. 10.2741/2740.CrossRefPubMed Wicherek L: The role of the endometrium in the regulation of immune cell activity. Front Biosci. 2008, 13: 1018-1035. 10.2741/2740.CrossRefPubMed
41.
go back to reference Wicherek L, Galazka K, Popiela TJ, Dutsch-Wicherek M, Czekierdowski A, Pabian W, Banas T, Migdal M, Klimek M: Metallothionein expression and infiltration of cytotoxic lymphocytes in uterine and tubal implantation sites. J Reprod Immunol. 2006, 70: 119-131. 10.1016/j.jri.2005.12.003.CrossRefPubMed Wicherek L, Galazka K, Popiela TJ, Dutsch-Wicherek M, Czekierdowski A, Pabian W, Banas T, Migdal M, Klimek M: Metallothionein expression and infiltration of cytotoxic lymphocytes in uterine and tubal implantation sites. J Reprod Immunol. 2006, 70: 119-131. 10.1016/j.jri.2005.12.003.CrossRefPubMed
42.
go back to reference Wicherek L, Basta P, Pitynski K, Marianowski P, Kijowski J, Wiatr J, Majka M: The characterization of the subpopulation of suppressive B7H4(+) macrophages and the subpopulation of CD25(+) CD4(+) and FOXP3(+) regulatory T-cells in decidua during the secretory cycle phase, Arias Stella reaction, and spontaneous abortion-a preliminary report. Am J Reprod Immunol. 2009, 61: 303-312. 10.1111/j.1600-0897.2009.00696.x.CrossRefPubMed Wicherek L, Basta P, Pitynski K, Marianowski P, Kijowski J, Wiatr J, Majka M: The characterization of the subpopulation of suppressive B7H4(+) macrophages and the subpopulation of CD25(+) CD4(+) and FOXP3(+) regulatory T-cells in decidua during the secretory cycle phase, Arias Stella reaction, and spontaneous abortion-a preliminary report. Am J Reprod Immunol. 2009, 61: 303-312. 10.1111/j.1600-0897.2009.00696.x.CrossRefPubMed
Metadata
Title
The frequency of CD25+CD4+ and FOXP3+ regulatory T cells in ectopic endometrium and ectopic decidua
Authors
Pawel Basta
Marcin Majka
Wojciech Jozwicki
Ewelina Lukaszewska
Anna Knafel
Marek Grabiec
Elzbieta Stasienko
Lukasz Wicherek
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-8-116

Other articles of this Issue 1/2010

Reproductive Biology and Endocrinology 1/2010 Go to the issue