Fertility and Sterility
Volume 90, Issue 4, Supplement , Pages 1487-1495 , October 2008

Modeling the early endometriotic lesion: mesothelium-endometrial cell co-culture increases endometrial invasion and alters mesothelial and endometrial gene transcription

Received 13 August 2007 ,Revised 24 September 2007 ,Accepted 24 September 2007.

References 

  1. Witz CA. Pathogenesis of endometriosis. In:  Olive DL editors. Endometriosis in clinical practice. Andover, Hampshire, United Kingdom: Taylor & Francis; 2005;p. 61–78
  2. Sampson J. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol. 1927;14:422–469
  3. Witz CA, Allsup KT, Montoya-Rodriguez IA, Vaughn SL, Centonze VE, Schenken RS. Culture of menstrual endometrium with peritoneal explants and mesothelial monolayers confirms attachment to intact mesothelial cells. Hum Reprod. 2002;17:2832–2838
  4. Witz CA, Cho S, Centonze VE, Montoya-Rodriguez IA, Schenken RS. Time series analysis of transmesothelial invasion by endometrial stromal and epithelial cells using three-dimensional confocal microscopy. Fertil Steril. 2003;79:770–778
  5. Witz CA, Thomas MR, Montoya-Rodriguez IA, Nair AS, Centonze VE, Schenken RS. Short-term culture of peritoneum explants confirms attachment of endometrium to intact peritoneal mesothelium. Fertil Steril. 2001;75:385–390
  6. Dechaud H, Witz CA, Montoya-Rodriguez IA, Degraffenried L, Schenken RS. Mesothelial cell-associated hyaluronic acid facilitates endometrial stromal and epithelial cell binding to mesothelium. Fertil Steril. 2001;76:1012–1018
  7. Kirk D, Irwin JC. Normal human endometrium in cell culture. Methods Cell Biol. 1980;21B:51–77
  8. Lucidi RS, Witz CA, Chrisco M, Binkley PA, Shain SA, Schenken RS. A novel in vitro model of the early endometriotic lesion demonstrates that attachment of endometrial cells to mesothelial cells is dependent on the source of endometrial cells. Fertil Steril. 2005;84:16–21
  9. Gill K, Kirma N, Gunna VS, Santanam N, Parthasarathy S, Tekmal RR. Regulation of colony stimulating factor-1 (CSF-1) in endometrial cells: glucocorticoids and oxidative stress regulate the expression of CSF-1 and its receptor c-fms in endometrial cells. Fertil Steril. 2001;76:1005–1011
  10. Rong R, Ramachandran S, Santanam N, Murphy AA, Parthasarathy S. Induction of monocyte chemotactic protein-1 in peritoneal mesothelial and endometrial cells by oxidized low-density lipoprotein and peritoneal fluid from women with endometriosis. Fertil Steril. 2002;78:843–848
  11. Wanichkul T, Han S, Huang RP, Sidell N. Cytokine regulation by peroxisome proliferator-activated receptor gamma in human endometrial cells. Fertil Steril. 2003;79:763–769
  12. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402–408
  13. Yuan JS, Reed A, Chen F, Stewart CN. Statistical analysis of real-time PCR data. BMC Bioinformatics. 2006;7:85–96
  14. Witz CA, Montoya-Rodriguez IA, Schenken RS. Whole peritoneal explants—a novel model of the early endometriosis lesion. Fertil Steril. 1999;71:56–60
  15. Redwine DB. Attachment of endometrial cells to peritoneum—facilitated?. Fertil Steril. 2001;76:421–422
  16. Kleinman HK, Mcgarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry. 1982;21:6188–6193
  17. Vukicevic S, Kleinman HK, Luyten FP, Roberts AB, Roche NS, Reddi AH. Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp Cell Res. 1992;202:1–8
  18. Groothuis PG, Koks CA, De Goeij AF, Dunselman GA, Arends JW, Evers JL. Adhesion of human endometrium to the epithelial lining and extracellular matrix of amnion in vitro: an electron microscopic study. Hum Reprod. 1998;13:2275–2281
  19. Groothuis PG, Koks CA, De Goeij AF, Dunselman GA, Arends JW, Evers JL. Adhesion of human endometrial fragments to peritoneum in vitro. Fertil Steril. 1999;71:1119–1124
  20. Koks CA, Groothuis PG, Dunselman GA, De Goeij AF, Evers JL. Adhesion of shed menstrual tissue in an in-vitro model using amnion and peritoneum: a light and electron microscopic study. Hum Reprod. 1999;14:816–822
  21. Van Der Linden PJ, De Goeij AF, Dunselman GA, Erkens HW, Evers JL. Endometrial cell adhesion in an in vitro model using intact amniotic membranes. Fertil Steril. 1996;65:76–80
  22. Borland G, Ross JA, Guy K. Forms and functions of CD44. Immunology. 1998;93:139–148
  23. Ponta H, Wainwright D, Herrlich P. The CD44 protein family. Int J Biochem Cell Biol. 1998;30:299–305
  24. Meisenberg G, Simmons WH. Principles of medical biochemistry. St. Louis, MO: Mosby; 1998;
  25. Fujita N, Yaegashi N, Ide Y, Sato S, Nakamura M, Ishiwata I, et al. Expression of CD44 in normal human versus tumor endometrial tissues: possible implication of reduced expression of CD44 in lymph-vascular space involvement of cancer cells. Cancer Res. 1994;54:3922–3928
  26. Naot D, Sionov RV, Ish-Shalom D. CD44: structure, function, and association with the malignant process. Adv Cancer Res. 1997;71:241–319
  27. Nishimura S, Chung YS, Yashiro M, Inoue T, Sowa M. CD44H plays an important role in peritoneal dissemination of scirrhous gastric cancer cells. Jpn J Cancer Res. 1996;87:1235–1244
  28. Jothy S. CD44 and its partners in metastasis. Clin Exp Metastasis. 2003;20:195–201
  29. Herrlich P, Morrison H, Sleeman J, Orian-Rousseau V, Konig H, Weg-Remers S, et al. CD44 acts both as a growth- and invasiveness-promoting molecule and as a tumor-suppressing cofactor. Ann NY Acad Sci. 2000;910:106–118[discussion: 18–20]
  30. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001;22:153–183
  31. Gollob JA, Wilhelm S, Carter C, Kelley SL. Role of Raf kinase in cancer: therapeutic potential of targeting the Raf/MEK/ERK signal transduction pathway. Semin Oncol. 2006;33:392–406
  32. Adjei AA. The role of mitogen-activated ERK-kinase inhibitors in lung cancer therapy. Clin Lung Cancer. 2005;7:221–223
  33. Nicosia SV, Bai W, Cheng JQ, Coppola D, Kruk PA. Oncogenic pathways implicated in ovarian epithelial cancer. Hematol Oncol Clin North Am. 2003;17:927–943
  34. Smalley KS. A pivotal role for ERK in the oncogenic behaviour of malignant melanoma?. Int J Cancer. 2003;104:527–532
  35. Yoshino O, Osuga Y, Hirota Y, Koga K, Hirata T, Harada M, et al. Possible pathophysiological roles of mitogen-activated protein kinases (MAPKs) in endometriosis. Am J Reprod Immunol. 2004;52:306–311
  36. Chambers SK, Wang Y, Gertz RE, Kacinski BM. Macrophage colony-stimulating factor mediates invasion of ovarian cancer cells through urokinase. Cancer Res. 1995;55:1578–1585
  37. Kacinski BM. CSF-1 and its receptor in breast carcinomas and neoplasms of the female reproductive tract. Mol Reprod Dev. 1997;46:71–74
  38. Sapi E. The role of CSF-1 in normal physiology of mammary gland and breast cancer: an update. Exp Biol Med. 2004;229:1–11
  39. Kacinski BM, Carter D, Mittal K, Yee LD, Scata KA, Donofrio L, et al. Ovarian adenocarcinomas express fms-complementary transcripts and fms antigen, often with coexpression of CSF-1. Am J Pathol. 1990;137:135–147
  40. Baiocchi G, Kavanagh JJ, Talpaz M, Wharton JT, Gutterman JU, Kurzrock R. Expression of the macrophage colony-stimulating factor and its receptor in gynecologic malignancies. Cancer. 1991;67:990–996
  41. Demetri GD, Zenzie BW, Rheinwald JG, Griffin JD. Expression of colony-stimulating factor genes by normal human mesothelial cells and human malignant mesothelioma cells lines in vitro. Blood. 1989;74:940–946
  42. Lidor YJ, Xu FJ, Martinez-Maza O, Olt GJ, Marks JR, Berchuck A, et al. Constitutive production of macrophage colony-stimulating factor and interleukin-6 by human ovarian surface epithelial cells. Exp Cell Res. 1993;207:332–339
  43. Ziltener HJ, Maines-Bandiera S, Schrader JW, Auersperg N. Secretion of bioactive interleukin-1, interleukin-6, and colony-stimulating factors by human ovarian surface epithelium. Biol Reprod. 1993;49:635–641
  44. Fukaya T, Sugawara J, Yoshida H, Yajima A. The role of macrophage colony stimulating factor in the peritoneal fluid in infertile patients with endometriosis. Tohoku J Exp Med. 1994;172:221–226
  45. Mettler L, Schmutzler AG, Koch K, Schollmeyer T, Salmassi A. Identification of the M-CSF receptor in endometriosis by immunohistochemistry and RT-PCR. Am J Reprod Immunol. 2004;52:298–305
  46. Matsuzaki S, Canis M, Vaurs-Barriere C, Boespflug-Tanguy O, Dastugue B, Mage G. DNA microarray analysis of gene expression in eutopic endometrium from patients with deep endometriosis using laser capture microdissection. Fertil Steril. 2005;84(Suppl 2):1180–1190
  47. Bae-Jump V, Segreti EM, Vandermolen D, Kauma S. Hepatocyte growth factor (HGF) induces invasion of endometrial carcinoma cell lines in vitro. Gynecol Oncol. 1999;73:265–272
  48. Park YH, Ryu HS, Choi DS, Chang KH, Park DW, Min CK. Effects of hepatocyte growth factor on the expression of matrix metalloproteinases and their tissue inhibitors during the endometrial cancer invasion in a three-dimensional coculture. Int J Gynecol Cancer. 2003;13:53–60
  49. Wagatsuma S, Konno R, Sato S, Yajima A. Tumor angiogenesis, hepatocyte growth factor, and c-Met expression in endometrial carcinoma. Cancer. 1998;82:520–530
  50. Khan KN, Masuzaki H, Fujishita A, Hamasaki T, Kitajima M, Hasuo A, et al. Association of interleukin-6 and estradiol with hepatocyte growth factor in peritoneal fluid of women with endometriosis. Acta Obstetr Gynecol Scand. 2002;81:764–771
  51. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Hiraki K, Miura S, et al. Peritoneal fluid and serum levels of hepatocyte growth factor may predict the activity of endometriosis. Acta Obstet Gynecol Scand. 2006;85:458–466
  52. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T. Higher activity by opaque endometriotic lesions than nonopaque lesions. Acta Obstet Gynecol Scand. 2004;83:375–382
  53. Osuga Y, Tsutsumi O, Okagaki R, Takai Y, Fujimoto A, Suenaga A, et al. Hepatocyte growth factor concentrations are elevated in peritoneal fluid of women with endometriosis. Hum Reprod. 1999;14:1611–1613
  54. Sugawara J, Fukaya T, Murakami T, Yoshida H, Yajima A. Increased secretion of hepatocyte growth factor by eutopic endometrial stromal cells in women with endometriosis. Fertil Steril. 1997;68:468–472
  55. Ishimaru T, Khan KN, Fujishita A, Kitajima M, Masuzaki H. Hepatocyte growth factor may be involved in cellular changes to the peritoneal mesothelium adjacent to pelvic endometriosis. Fertil Steril. 2004;81(Suppl 1):810–818
  56. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T. Immunoexpression of hepatocyte growth factor and c-Met receptor in the eutopic endometrium predicts the activity of ectopic endometrium. Fertil Steril. 2003;79:173–181
  57. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Ishimaru T. Differential macrophage infiltration in early and advanced endometriosis and adjacent peritoneum. Fertil Steril. 2004;81:652–661
  58. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Hiraki K, Sekine I, et al. Interleukin-6- and tumour necrosis factor alpha-mediated expression of hepatocyte growth factor by stromal cells and its involvement in the growth of endometriosis. Hum Reprod. 2005;20:2715–2723
  59. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Kohno T, Sekine I, et al. Regulation of hepatocyte growth factor by basal and stimulated macrophages in women with endometriosis. Hum Reprod. 2005;20:49–60
  60. Khan KN, Masuzaki H, Fujishita A, Kitajima M, Sekine I, Matsuyama T, et al. Estrogen and progesterone receptor expression in macrophages and regulation of hepatocyte growth factor by ovarian steroids in women with endometriosis. Hum Reprod. 2005;20:2004–2013
  61. Yoshida S, Harada T, Mitsunari M, Iwabe T, Sakamoto Y, Tsukihara S, et al. Hepatocyte growth factor/Met system promotes endometrial and endometriotic stromal cell invasion via autocrine and paracrine pathways. J Clin Endocrinol Metab. 2004;89:823–832

 Presented, in part, at the 62nd Annual Meeting of the American Society of Reproductive Medicine, New Orleans, Louisiana, October 21–25, 2006.

PII: S0015-0282(07)03743-0

doi: 10.1016/j.fertnstert.2007.09.047

Fertility and Sterility
Volume 90, Issue 4, Supplement , Pages 1487-1495 , October 2008

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