Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2006

Open Access 01-12-2006 | Research

Comparison of RCAS1 and metallothionein expression and the presence and activity of immune cells in human ovarian and abdominal wall endometriomas

Authors: Lukasz Wicherek, Magdalena Dutsch-Wicherek, Krystyna Galazka, Tomasz Banas, Tadeusz Popiela, Agata Lazar, Beata Kleinrok-Podsiadlo

Published in: Reproductive Biology and Endocrinology | Issue 1/2006

Login to get access

Abstract

Background

The coexistence of endometrial and immune cells during decidualization is preserved by the ability of endometrial cells to regulate the cytotoxic immune activity and their capability to be resistant to immune-mediated apoptosis. These phenomena enable the survival of endometrial ectopic cells. RCAS1 is responsible for regulation of cytotoxic activity. Metallothionein expression seems to protect endometrial cells against apoptosis. The aim of the present study was to evaluate RCAS1 and metallothionein expression in human ovarian and scar endometriomas in relation to the presence of immune cells and their activity.

Methods

Metallothionein, RCAS1, CD25, CD69, CD56, CD16, CD68 antigen expression was assessed by immunohistochemistry in ovarian and scar endometriomas tissue samples which were obtained from 33 patients. The secretory endometrium was used as a control group (15 patients).

Results

The lowest metallothionein expression was revealed in ovarian endometriomas in comparison to scar endometriomas and to the control group. RCAS1 expression was at the highest level in the secretory endometrium and it was at comparable levels in ovarian and scar endometriomas. Similarly, the number of CD56-positive cells was lower in scar and ovarian endometriomas than in the secretory endometrium. The highest number of macrophages was found in ovarian endometriomas. RCAS1-positive macrophages were observed only in ovarian endometriomas. CD25 and CD69 antigen expression was higher in scar and ovarian endometriomas than in the control group.

Conclusion

The expression of RCAS1 and metallothionein by endometrial cells may favor the persistence of these cells in ectopic localization both in scar following cesarean section and in ovarian endometriosis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Douglas C, Rotimi O: Extragenital endometriosis – a clinicopathological review of a Glasgow hospital experience with case illustrations. J Obstet Gynaecol. 2004, 24: 804-808. 10.1080/01443610400009568.CrossRefPubMed Douglas C, Rotimi O: Extragenital endometriosis – a clinicopathological review of a Glasgow hospital experience with case illustrations. J Obstet Gynaecol. 2004, 24: 804-808. 10.1080/01443610400009568.CrossRefPubMed
2.
go back to reference Scott RB, Telinde RW: Clinical external endometriosis: probable viability of menstrually shed fragments of endometrium. Obstet Gynecol. 1954, 4: 502-510.PubMed Scott RB, Telinde RW: Clinical external endometriosis: probable viability of menstrually shed fragments of endometrium. Obstet Gynecol. 1954, 4: 502-510.PubMed
3.
go back to reference Sampson JA: Endometrial carcinoma of the ovary, arising in endometrial tissue of that organ. Arch Surg. 1925, 10: 1-72.CrossRef Sampson JA: Endometrial carcinoma of the ovary, arising in endometrial tissue of that organ. Arch Surg. 1925, 10: 1-72.CrossRef
4.
go back to reference Fazleabas AT: A baboon model for inducing endometriosis. Methods Mol Med. 2006, 121: 95-99.PubMed Fazleabas AT: A baboon model for inducing endometriosis. Methods Mol Med. 2006, 121: 95-99.PubMed
5.
go back to reference Nishida M, Nasu K, Fukuda J, Kawano Y, Narahara H, Miyakawa I: Down-regulation of Interleukin-1 receptor type 1 expression causes the dysregulated expression of CXC chemokines in endometriotic stromal cells: a possible mechanism for altered immunological functions in endometriosis. J Clin Endocrinol Metab. 2004, 89: 5094-5100. 10.1210/jc.2004-0354.CrossRefPubMed Nishida M, Nasu K, Fukuda J, Kawano Y, Narahara H, Miyakawa I: Down-regulation of Interleukin-1 receptor type 1 expression causes the dysregulated expression of CXC chemokines in endometriotic stromal cells: a possible mechanism for altered immunological functions in endometriosis. J Clin Endocrinol Metab. 2004, 89: 5094-5100. 10.1210/jc.2004-0354.CrossRefPubMed
6.
go back to reference Beliard A, Noel A, Foidart JM: Reduction of apoptosis and proliferation in endometriosis. Fertil Steril. 2004, 82: 80-85. 10.1016/j.fertnstert.2003.11.048.CrossRefPubMed Beliard A, Noel A, Foidart JM: Reduction of apoptosis and proliferation in endometriosis. Fertil Steril. 2004, 82: 80-85. 10.1016/j.fertnstert.2003.11.048.CrossRefPubMed
7.
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
8.
go back to reference Sonoda K, Miyamoto S, Hirakawa T, Yagi H, Yotsumoto F, Nakashima M, Watanabe T: 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: 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
9.
go back to reference Chiou SH, Sheu BC, Chang WC, Huang SC, Hong-Nerng H: Current concepts of tumor-infiltrating lymphocytes in human malignancies. J Reprod Immunol. 2005, 67: 35-50. 10.1016/j.jri.2005.06.002.CrossRefPubMed Chiou SH, Sheu BC, Chang WC, Huang SC, Hong-Nerng H: Current concepts of tumor-infiltrating lymphocytes in human malignancies. J Reprod Immunol. 2005, 67: 35-50. 10.1016/j.jri.2005.06.002.CrossRefPubMed
10.
go back to reference Wicherek L, Popiela TJ, Galazka K, Dutsch-Wicherek M, Oplawski M, Basta A, Klimek M: Metallothionein and RCAS1 expression in comparison to immunological cells activity in endometriosis, endometrial adenocarcinoma and 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, Oplawski M, Basta A, Klimek M: Metallothionein and RCAS1 expression in comparison to immunological cells activity in endometriosis, endometrial adenocarcinoma and endometrium according to menstrual cycle changes. Gynecol Oncol. 2005, 99: 622-630. 10.1016/j.ygyno.2005.07.003.CrossRefPubMed
11.
go back to reference Matsushima T, Nakashima M, Oshima K, Abe Y, Nishimura J, Nawata H, Watanabe T, Muta K: Receptor binding cancer antigen expressed on SiSo cells, a novel regulator of apoptosis of erythroid progenitor cells. Blood. 2001, 98: 313-321. 10.1182/blood.V98.2.313.CrossRefPubMed Matsushima T, Nakashima M, Oshima K, Abe Y, Nishimura J, Nawata H, Watanabe T, Muta K: Receptor binding cancer antigen expressed on SiSo cells, a novel regulator of apoptosis of erythroid progenitor cells. Blood. 2001, 98: 313-321. 10.1182/blood.V98.2.313.CrossRefPubMed
12.
go back to reference Dutsch-Wicherek M, Tomaszewska R, Popiela TJ, Wicherek L, Szywala M, Wierzchowski W, Modrzejewski M, Klimek M, Czekierdowska S, Skladzien J: RCAS1 expression in lymphoid tissue of Waldeyer's ring. Pol J Environ Stud. 2005, 14 (Suppl 2): 73-76. Dutsch-Wicherek M, Tomaszewska R, Popiela TJ, Wicherek L, Szywala M, Wierzchowski W, Modrzejewski M, Klimek M, Czekierdowska S, Skladzien J: RCAS1 expression in lymphoid tissue of Waldeyer's ring. Pol J Environ Stud. 2005, 14 (Suppl 2): 73-76.
13.
go back to reference Wicherek L, Dutsch-Wicherek M, Mak P, Klimek M: The role of RCAS1 and oxytocinase in immune tolerance during pregnancy. Fetal Diagn Ther. 2005, 20: 420-425. 10.1159/000086824.CrossRefPubMed Wicherek L, Dutsch-Wicherek M, Mak P, Klimek M: The role of RCAS1 and oxytocinase in immune tolerance during pregnancy. Fetal Diagn Ther. 2005, 20: 420-425. 10.1159/000086824.CrossRefPubMed
14.
go back to reference Theocharis SE, Margeli AP, Klijanienko JT, Kouraklis GP: Metallothionein expression in human neoplasia. Histopathology. 2004, 45: 103-118. 10.1111/j.1365-2559.2004.01922.x.CrossRefPubMed Theocharis SE, Margeli AP, Klijanienko JT, Kouraklis GP: Metallothionein expression in human neoplasia. Histopathology. 2004, 45: 103-118. 10.1111/j.1365-2559.2004.01922.x.CrossRefPubMed
15.
go back to reference Cherian MG, Jayasurya A, Bay BH: Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat Res. 2003, 533: 201-209.CrossRefPubMed Cherian MG, Jayasurya A, Bay BH: Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat Res. 2003, 533: 201-209.CrossRefPubMed
16.
go back to reference Ioachin E: Immunohistochemical tumor markers in endometrial carcinoma. Eur J Gynaecol Oncol. 2005, 26: 363-371.PubMed Ioachin E: Immunohistochemical tumor markers in endometrial carcinoma. Eur J Gynaecol Oncol. 2005, 26: 363-371.PubMed
17.
go back to reference Klimek M, Wicherek L, Galazka K, Tetlak T, Popiela TJ, Kulczycka M, Rudnicka-Sosin L, Dutsch-Wicherek M: Cycle dependent expression of endometrial metallothionein. Neuro Endocrinol Lett. 2005, 26: 663-666.PubMed Klimek M, Wicherek L, Galazka K, Tetlak T, Popiela TJ, Kulczycka M, Rudnicka-Sosin L, Dutsch-Wicherek M: Cycle dependent expression of endometrial metallothionein. Neuro Endocrinol Lett. 2005, 26: 663-666.PubMed
18.
19.
go back to reference Gaunt A, Heard G, McKain ES, Stephenson BM: Casarean scar endometrioma. Lancet. 2004, 364: 368-10.1016/S0140-6736(04)16726-3.CrossRefPubMed Gaunt A, Heard G, McKain ES, Stephenson BM: Casarean scar endometrioma. Lancet. 2004, 364: 368-10.1016/S0140-6736(04)16726-3.CrossRefPubMed
20.
go back to reference Sammour RN, Leibovitz Z, Shapiro I, Degani S, Levitan Z, Aharoni A, Tal J, Lurie M, Ohel G: Decidualization of ovarian endometriosis during pregnancy mimicking malignancy. J Ultrasound Med. 2005, 24: 1289-1294.PubMed Sammour RN, Leibovitz Z, Shapiro I, Degani S, Levitan Z, Aharoni A, Tal J, Lurie M, Ohel G: Decidualization of ovarian endometriosis during pregnancy mimicking malignancy. J Ultrasound Med. 2005, 24: 1289-1294.PubMed
21.
go back to reference Chao KH, Wu MY, Yang JH, Chen SU, Yang YS, Ho HN: Expression of the interleukin-2 receptor alfa (CD25) is selectively decreased on decidual CD4+ and CD8+ T lymphocytes in normal pregnancies. Mol Hum Reprod. 2002, 8: 667-673. 10.1093/molehr/8.7.667.CrossRefPubMed Chao KH, Wu MY, Yang JH, Chen SU, Yang YS, Ho HN: Expression of the interleukin-2 receptor alfa (CD25) is selectively decreased on decidual CD4+ and CD8+ T lymphocytes in normal pregnancies. Mol Hum Reprod. 2002, 8: 667-673. 10.1093/molehr/8.7.667.CrossRefPubMed
22.
go back to reference Maeda N, Izumiya C, Kusum T, Masumoto T, Yamashita C, Yamamoto Y, Oguri H, Fukaya T: Killer inhibitory receptor CD158a overexpression among NK cells in women with endometriosis is undiminished by laparoscopic surgery and gonadotropin releasing hormone agonist treatment. Am J Reprod Immunol. 2004, 51: 364-372. 10.1111/j.1600-0897.2004.00170.x.CrossRefPubMed Maeda N, Izumiya C, Kusum T, Masumoto T, Yamashita C, Yamamoto Y, Oguri H, Fukaya T: Killer inhibitory receptor CD158a overexpression among NK cells in women with endometriosis is undiminished by laparoscopic surgery and gonadotropin releasing hormone agonist treatment. Am J Reprod Immunol. 2004, 51: 364-372. 10.1111/j.1600-0897.2004.00170.x.CrossRefPubMed
23.
go back to reference Wu MH, Shoji Y, Wu MC, Chuang PC, Lin CC, Huang MF, Tsai SJ: Suppression of matrix metalloproteinase-9 by prostaglandin E(2) in peritoneal macrophage is associated with severity of endometriosis. Am J Pathol. 2005, 167: 1061-1069.PubMedCentralCrossRefPubMed Wu MH, Shoji Y, Wu MC, Chuang PC, Lin CC, Huang MF, Tsai SJ: Suppression of matrix metalloproteinase-9 by prostaglandin E(2) in peritoneal macrophage is associated with severity of endometriosis. Am J Pathol. 2005, 167: 1061-1069.PubMedCentralCrossRefPubMed
24.
go back to reference Vernet-Tomas Mdel M, Perez-Ares CT, Verdu N, Molinero JL, Fernandez-Figueras MT, Carreras R: The endometria of patients with endometriosis show higher expression of class I human leukocyte antigen than the endometria of healthy women. Fertil Steril. 2006, 85: 78-83. 10.1016/j.fertnstert.2005.06.057.CrossRefPubMed Vernet-Tomas Mdel M, Perez-Ares CT, Verdu N, Molinero JL, Fernandez-Figueras MT, Carreras R: The endometria of patients with endometriosis show higher expression of class I human leukocyte antigen than the endometria of healthy women. Fertil Steril. 2006, 85: 78-83. 10.1016/j.fertnstert.2005.06.057.CrossRefPubMed
25.
go back to reference Yang JH, Chen MJ, Chen HF, Lee TH, Ho HN, Yang YS: Decreased expression of killer cell inhibitory receptors on natural killer cells in eutopic endometrium in women with adenomyosis. Hum Reprod. 2004, 19: 1974-1978. 10.1093/humrep/deh372.CrossRefPubMed Yang JH, Chen MJ, Chen HF, Lee TH, Ho HN, Yang YS: Decreased expression of killer cell inhibitory receptors on natural killer cells in eutopic endometrium in women with adenomyosis. Hum Reprod. 2004, 19: 1974-1978. 10.1093/humrep/deh372.CrossRefPubMed
26.
go back to reference Zhang C, Maeda N, Izumiya C, Yamamoto Y, Kusume T, Oguri H, Yamashita C, Nishimori Y, Hayashi K, Luo J, Fukaya T: Killer immunoglobulin-like receptor and human leukocyte antigen expression as immunodiagnostic parameters for pelvic endometriosis. Am J Reprod Immunol. 2006, 55: 106-114. 10.1111/j.1600-0897.2005.00332.x.CrossRefPubMed Zhang C, Maeda N, Izumiya C, Yamamoto Y, Kusume T, Oguri H, Yamashita C, Nishimori Y, Hayashi K, Luo J, Fukaya T: Killer immunoglobulin-like receptor and human leukocyte antigen expression as immunodiagnostic parameters for pelvic endometriosis. Am J Reprod Immunol. 2006, 55: 106-114. 10.1111/j.1600-0897.2005.00332.x.CrossRefPubMed
27.
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
28.
go back to reference Akoum A, Lemay A, Maheux R: Estradiol and interleukin-1beta exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells. J Clin Endocrinol Metab. 2002, 87: 5785-5792. 10.1210/jc.2002-020106.CrossRefPubMed Akoum A, Lemay A, Maheux R: Estradiol and interleukin-1beta exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells. J Clin Endocrinol Metab. 2002, 87: 5785-5792. 10.1210/jc.2002-020106.CrossRefPubMed
29.
go back to reference Braun DP, Ding J, Shen J, Rana N, Fernandez BB, Dmowski WP: Relationship between apoptosis and the number of macrophages in eutopic endometrium from women with and without endometriosis. Fertil Steril. 2002, 78: 830-835. 10.1016/S0015-0282(02)03334-4.CrossRefPubMed Braun DP, Ding J, Shen J, Rana N, Fernandez BB, Dmowski WP: Relationship between apoptosis and the number of macrophages in eutopic endometrium from women with and without endometriosis. Fertil Steril. 2002, 78: 830-835. 10.1016/S0015-0282(02)03334-4.CrossRefPubMed
30.
go back to reference Wicherek L, Galazka K, Dutsch-Wicherek M, Migdal M, Tetlak T, Klimek M: The presence of RCAS1 positive macrophages in ovarian endometriosis. Eur J Obstet Gynecol Reprod Biol. 2005, 123 (Suppl 1): S46- Wicherek L, Galazka K, Dutsch-Wicherek M, Migdal M, Tetlak T, Klimek M: The presence of RCAS1 positive macrophages in ovarian endometriosis. Eur J Obstet Gynecol Reprod Biol. 2005, 123 (Suppl 1): S46-
31.
go back to reference Dutsch-Wicherek M, Tomaszewska R, Strek P, Wicherek L, Skladzien J: The analysis of RCAS1 and DFF-45 expression in nasal polyps with respect to immune cells infiltration. BMC Immunol. 2006, 7: 4-10.1186/1471-2172-7-4.PubMedCentralCrossRefPubMed Dutsch-Wicherek M, Tomaszewska R, Strek P, Wicherek L, Skladzien J: The analysis of RCAS1 and DFF-45 expression in nasal polyps with respect to immune cells infiltration. BMC Immunol. 2006, 7: 4-10.1186/1471-2172-7-4.PubMedCentralCrossRefPubMed
32.
go back to reference Enjoji M, Kotoh K, Nakashima M, Yoshimoto T, Miyagi Y, Kohjima M, Nakamuta M: RCAS1-expressing macrophages in inflammatory liver diseases. Liver Int. 2006, 26: 358-367. 10.1111/j.1478-3231.2005.01223.x.CrossRef Enjoji M, Kotoh K, Nakashima M, Yoshimoto T, Miyagi Y, Kohjima M, Nakamuta M: RCAS1-expressing macrophages in inflammatory liver diseases. Liver Int. 2006, 26: 358-367. 10.1111/j.1478-3231.2005.01223.x.CrossRef
33.
go back to reference Kale S, Shuster M, Shangold J: Endometrioma in cesarean scar: case report and review of literature. Am J Obstet Gynecol. 1971, 111: 596-597.PubMed Kale S, Shuster M, Shangold J: Endometrioma in cesarean scar: case report and review of literature. Am J Obstet Gynecol. 1971, 111: 596-597.PubMed
34.
go back to reference Honore GM: Extrapelvic endometriosis. Clin Obstet Gynecol. 1999, 42: 699-711. 10.1097/00003081-199909000-00021.CrossRefPubMed Honore GM: Extrapelvic endometriosis. Clin Obstet Gynecol. 1999, 42: 699-711. 10.1097/00003081-199909000-00021.CrossRefPubMed
35.
go back to reference Patterson GK, Winburn GB: Abdominal wall endometriomas: report of 8 cases. Am Surg. 1999, 65: 36-39.PubMed Patterson GK, Winburn GB: Abdominal wall endometriomas: report of 8 cases. Am Surg. 1999, 65: 36-39.PubMed
36.
go back to reference Rukavina D, Podack ER: Abundant perforin expression at the maternal-fetal interface: guarding the semiallogeneic transplant?. Immunol Today. 2000, 21: 160-163. 10.1016/S0167-5699(00)01603-0.CrossRefPubMed Rukavina D, Podack ER: Abundant perforin expression at the maternal-fetal interface: guarding the semiallogeneic transplant?. Immunol Today. 2000, 21: 160-163. 10.1016/S0167-5699(00)01603-0.CrossRefPubMed
37.
go back to reference Szekeres-Bartho J, Varga B, Pacsa AS: Immunologic factors contributing to the initiation of labor-lymphocytes reactivity in term labor and threatened preterm delivery. Am J Obstet Gynecol. 1986, 155: 108-112.CrossRefPubMed Szekeres-Bartho J, Varga B, Pacsa AS: Immunologic factors contributing to the initiation of labor-lymphocytes reactivity in term labor and threatened preterm delivery. Am J Obstet Gynecol. 1986, 155: 108-112.CrossRefPubMed
38.
go back to reference Levadoux-Martin M, Hesketh JE, Beattie JH, Wallace HM: Influence of metallothionein-1 localization on its function. Biochem J. 2001, 355: 473-479. 10.1042/0264-6021:3550473.PubMedCentralCrossRefPubMed Levadoux-Martin M, Hesketh JE, Beattie JH, Wallace HM: Influence of metallothionein-1 localization on its function. Biochem J. 2001, 355: 473-479. 10.1042/0264-6021:3550473.PubMedCentralCrossRefPubMed
39.
go back to reference Tsangaris GT, Tzortzatou-Stathopoulou F: Metallothionein expression prevents apoptosis: a study with antisense phosphorothioate oligodeoxynucleotides in a human T cell line. Anticancer Res. 1998, 18: 2423-2433.PubMed Tsangaris GT, Tzortzatou-Stathopoulou F: Metallothionein expression prevents apoptosis: a study with antisense phosphorothioate oligodeoxynucleotides in a human T cell line. Anticancer Res. 1998, 18: 2423-2433.PubMed
40.
go back to reference Mocchegiani E, Muzzioli M, Giacconi R, Cipriano C, Gasparini N, Franceschi C, Gaetti R, Cavalieri E, Suzuki H: Metallothioneins/PARP-1/IL-6 interplay on natural killer cell activity in elderly: parallelism with nonagenarians and old infected humans. Effect of zinc supply. Mech Ageing Dev. 2003, 124: 459-468. 10.1016/S0047-6374(03)00023-X.CrossRefPubMed Mocchegiani E, Muzzioli M, Giacconi R, Cipriano C, Gasparini N, Franceschi C, Gaetti R, Cavalieri E, Suzuki H: Metallothioneins/PARP-1/IL-6 interplay on natural killer cell activity in elderly: parallelism with nonagenarians and old infected humans. Effect of zinc supply. Mech Ageing Dev. 2003, 124: 459-468. 10.1016/S0047-6374(03)00023-X.CrossRefPubMed
41.
go back to reference Fan LZ, Cherian MG: Potential role of p53 on metallothionein induction in human epithelial breast cancer cells. Br J Cancer. 2002, 87: 1019-1026. 10.1038/sj.bjc.6600549.PubMedCentralCrossRefPubMed Fan LZ, Cherian MG: Potential role of p53 on metallothionein induction in human epithelial breast cancer cells. Br J Cancer. 2002, 87: 1019-1026. 10.1038/sj.bjc.6600549.PubMedCentralCrossRefPubMed
42.
go back to reference Nishida M, Nasu K, Ueda T, Fukuda J, Takai N, Miyakawa I: Endometriotic cells are resistant to interferon-gamma-induced cell growth inhibition and apoptosis: a possible mechanism involved in the pathogenesis of endometriosis. Mol Hum Reprod. 2005, 11: 29-34. 10.1093/molehr/gah133.CrossRefPubMed Nishida M, Nasu K, Ueda T, Fukuda J, Takai N, Miyakawa I: Endometriotic cells are resistant to interferon-gamma-induced cell growth inhibition and apoptosis: a possible mechanism involved in the pathogenesis of endometriosis. Mol Hum Reprod. 2005, 11: 29-34. 10.1093/molehr/gah133.CrossRefPubMed
43.
go back to reference Goumenou AG, Matalliotakis IM, Tzardi M, Fragouli YG, Mahutte NG, Arici A: Apoptosis and differential expression of apoptosis-related proteins in endometriotic glandular and stromal cells. J Soc Gynecol Investig. 2004, 11: 318-322. 10.1016/j.jsgi.2004.02.005.CrossRefPubMed Goumenou AG, Matalliotakis IM, Tzardi M, Fragouli YG, Mahutte NG, Arici A: Apoptosis and differential expression of apoptosis-related proteins in endometriotic glandular and stromal cells. J Soc Gynecol Investig. 2004, 11: 318-322. 10.1016/j.jsgi.2004.02.005.CrossRefPubMed
44.
go back to reference Dmowski WP, Ding J, Shen J, Rana N, Fernandez BB, Braun DP: Apoptosis in endometrial glandular and stromal 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 and stromal cells in women with and without endometriosis. Hum Reprod. 2001, 16: 1802-1808. 10.1093/humrep/16.9.1802.CrossRefPubMed
Metadata
Title
Comparison of RCAS1 and metallothionein expression and the presence and activity of immune cells in human ovarian and abdominal wall endometriomas
Authors
Lukasz Wicherek
Magdalena Dutsch-Wicherek
Krystyna Galazka
Tomasz Banas
Tadeusz Popiela
Agata Lazar
Beata Kleinrok-Podsiadlo
Publication date
01-12-2006
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2006
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-4-41

Other articles of this Issue 1/2006

Reproductive Biology and Endocrinology 1/2006 Go to the issue