Fertility and Sterility
Volume 91, Issue 5, Supplement , Pages 2199-2209 , May 2009

Induction of peritoneal endometriosis in nude mice with use of human immortalized endometriosis epithelial and stromal cells: a potential experimental tool to study molecular pathogenesis of endometriosis in humans

  • Sakhila K. Banu, Ph.D.

      Affiliations

    • Reproductive Endocrinology and Cell Signaling Laboratory, Department of Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas
    • ,
  • Anna Starzinski-Powitz, Ph.D.

      Affiliations

    • Molekulare Zellbiologie und Humangenetik, Institut für Zellbiologie und Neurowissenschaft, Johann Wolfgang Goethe-Universität, Frankfurt am Main, Germany
    • ,
  • V.O. Speights, D.O.

      Affiliations

    • Division of Anatomic Pathology, Department of Pathology, Scott & White Memorial Hospital, Texas A&M University Health Science Center, Temple, Texas
    • ,
  • Robert C. Burghardt, Ph.D.

      Affiliations

    • Department of Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas
    • ,
  • Joe A. Arosh, Ph.D.

      Affiliations

    • Reproductive Endocrinology and Cell Signaling Laboratory, Department of Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas
    • Department of Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas
    • Corresponding Author InformationReprint requests: Joe A. Arosh, Ph.D., Department of Integrative Biosciences, College of Veterinary Medicine & Biomedical Sciences, Mail Stop: TAMU 4458, Texas A&M University, College Station, Texas 77843 (FAX: 979-847-8981).

Received 22 March 2008 ,Revised 25 June 2008 ,Accepted 26 June 2008.

References 

  1. Garai J, Molnar V, Varga T, Koppan M, Torok A, Bodis J. Endometriosis: harmful survival of an ectopic tissue. Front Biosci. 2006;11:595–619
  2. Farquhar C. Endometriosis. BMJ. 2007;334:249–253
  3. Wu MH, Shoji Y, Chuang PC, Tsai SJ. Endometriosis: disease pathophysiology and the role of prostaglandins. Expert Rev Mol Med. 2007;9:1–20
  4. Hastings JM, Fazleabas AT. A baboon model for endometriosis: implications for fertility. Reprod Biol Endocrinol. 2006;4(Suppl 1):S7
  5. Starzinski-Powitz A, Gaetje R, Zeitvogel A, Kotzian S, Handrow-Metzmacher H, Herrmann G, et al. Tracing cellular and molecular mechanisms involved in endometriosis. Hum Reprod Update. 1998;4:724–729
  6. Starzinski-Powitz A, Zeitvogel A, Schreiner A, Baumann R. In search of pathogenic mechanisms in endometriosis: the challenge for molecular cell biology. Curr Mol Med. 2001;1:655–664
  7. Osteen KG, Bruner-Tran KL, Eisenberg E. Endometrial biology and the etiology of endometriosis. Fertil Steril. 2005;84:33–34discussion 8–9
  8. Sampson J. Peritoneal endometritis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol. 1927;14:442–469
  9. Bulun SE, Yang S, Fang Z, Gurates B, Tamura M, Sebastian S. Estrogen production and metabolism in endometriosis. Ann N Y Acad Sci. 2002;955:75–85discussion 6–8, 396–406
  10. Laschke MW, Menger MD. In vitro and in vivo approaches to study angiogenesis in the pathophysiology and therapy of endometriosis. Hum Reprod Update. 2007;13:331–342
  11. Laschke MW, Elitzsch A, Vollmar B, Vajkoczy P, Menger MD. Combined inhibition of vascular endothelial growth factor (VEGF), fibroblast growth factor and platelet-derived growth factor, but not inhibition of VEGF alone, effectively suppresses angiogenesis and vessel maturation in endometriotic lesions. Hum Reprod. 2006;21:262–268
  12. Laschke MW, Elitzsch A, Scheuer C, Vollmar B, Menger MD. Selective cyclo-oxygenase-2 inhibition induces regression of autologous endometrial grafts by down-regulation of vascular endothelial growth factor–mediated angiogenesis and stimulation of caspase-3–dependent apoptosis. Fertil Steril. 2007;87:163–171
  13. 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
  14. Banu SK, Lee J, Speights VO, Starzinski-Powitz A, Arosh JA. Cyclooxygenase-2 regulates survival, migration and invasion of human endometriotic cells through multiple mechanisms. Endocrinology. 2008;149:1180–1189
  15. D'Hooghe TM, Debrock S. Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum Reprod Update. 2002;8:84–88
  16. Fazleabas AT, Brudney A, Chai D, Mwenda J. Endometriosis in the baboon. Gynecol Obstet Invest. 2004;57:46–47
  17. Hastings JM, Fazleabas AT. Future directions in endometriosis research. Semin Reprod Med. 2003;21:255–262
  18. Efstathiou JA, Sampson DA, Levine Z, Rohan RM, Zurakowski D, Folkman J, et al. Nonsteroidal antiinflammatory drugs differentially suppress endometriosis in a murine model. Fertil Steril. 2005;83:171–181
  19. Matsuzaki S, Canis M, Darcha C, Dallel R, Okamura K, Mage G. Cyclooxygenase-2 selective inhibitor prevents implantation of eutopic endometrium to ectopic sites in rats. Fertil Steril. 2004;82:1609–1615
  20. Zamah NM, Dodson MG, Stephens LC, Buttram VC, Besch PK, Kaufman RH. Transplantation of normal and ectopic human endometrial tissue into athymic nude mice. Am J Obstet Gynecol. 1984;149:591–597
  21. Bergqvist A, Jeppsson S, Kullander S, Ljungberg O. Human uterine endometrium and endometriotic tissue transplanted into nude mice. Morphologic effects of various steroid hormones. Am J Pathol. 1985;121:337–341
  22. Bergqvist A, Jeppsson S, Kullander S, Ljungberg O. Human endometrium transplanted into nude mice. Histologic effects of various steroid hormones. Am J Pathol. 1985;119:336–344
  23. Bruner KL, Matrisian LM, Rodgers WH, Gorstein F, Osteen KG. Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice. J Clin Invest. 1997;99:2851–2857
  24. Nisolle M, Casanas-Roux F, Donnez J. Early-stage endometriosis: adhesion and growth of human menstrual endometrium in nude mice. Fertil Steril. 2000;74:306–312
  25. Beliard A, Noel A, Goffin F, Frankenne F, Foidart JM. Role of endocrine status and cell type in adhesion of human endometrial cells to the peritoneum in nude mice. Fertil Steril. 2002;78:973–978
  26. Nap AW, Griffioen AW, Dunselman GA, Bouma-Ter Steege JC, Thijssen VL, Evers JL, et al. Antiangiogenesis therapy for endometriosis. J Clin Endocrinol Metab. 2004;89:1089–1095
  27. Eggermont J, Donnez J, Casanas-Roux F, Scholtes H, Van Langendonckt A. Time course of pelvic endometriotic lesion revascularization in a nude mouse model. Fertil Steril. 2005;84:492–499
  28. Gonzalez-Ramos R, Van Langendonckt A, Defrere S, Lousse JC, Mettlen M, Guillet A, et al. Agents blocking the nuclear factor–kappaB pathway are effective inhibitors of endometriosis in an in vivo experimental model. Gynecol Obstet Invest. 2007;65:174–186
  29. Awwad JT, Sayegh RA, Tao XJ, Hassan T, Awwad ST, Isaacson K. The SCID mouse: an experimental model for endometriosis. Hum Reprod. 1999;14:3107–3111
  30. Aoki D, Katsuki Y, Shimizu A, Kakinuma C, Nozawa S. Successful heterotransplantation of human endometrium in SCID mice. Obstet Gynecol. 1994;83:220–228
  31. Ozawa Y, Murakami T, Tamura M, Terada Y, Yaegashi N, Okamura K. A selective cyclooxygenase-2 inhibitor suppresses the growth of endometriosis xenografts via antiangiogenic activity in severe combined immunodeficiency mice. Fertil Steril. 2006;86(Suppl 4):1146–1151
  32. diZerega GS, Coad J, Donnez J. Clinical evaluation of endometriosis and differential response to surgical therapy with and without application of Oxiplex/AP∗ adhesion barrier gel. Fertil Steril. 2007;87:485–489
  33. Moen MH, Halvorsen TB. Histologic confirmation of endometriosis in different peritoneal lesions. Acta Obstet Gynecol Scand. 1992;71:337–342
  34. Nisolle M, Casanas-Roux F, Donnez J. Immunohistochemical analysis of proliferative activity and steroid receptor expression in peritoneal and ovarian endometriosis. Fertil Steril. 1997;68:912–919
  35. Nisolle M, Donnez J. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. Fertil Steril. 1997;68:585–596
  36. Walter AJ, Hentz JG, Magtibay PM, Cornella JL, Magrina JF. Endometriosis: correlation between histologic and visual findings at laparoscopy. Am J Obstet Gynecol. 2001;184:1407–1411discussion 11–3
  37. Stratton P, Winkel CA, Sinaii N, Merino MJ, Zimmer C, Nieman LK. Location, color, size, depth, and volume may predict endometriosis in lesions resected at surgery. Fertil Steril. 2002;78:743–749
  38. Nisolle M, Casanas-Roux F, Anaf V, Mine JM, Donnez J. Morphometric study of the stromal vascularization in peritoneal endometriosis. Fertil Steril. 1993;59:681–684
  39. American Society for Reproductive Medicine . Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67:817–821
  40. Tulandi T, Redwine D. Endometriosis: advances and controversies. 1st ed.. New York: Marcel Dekker; 2004;
  41. Matsuzaki S, Canis M, Murakami T, Dechelotte P, Bruhat MA, Okamura K. Immunohistochemical analysis of the role of angiogenic status in the vasculature of peritoneal endometriosis. Fertil Steril. 2001;76:712–716
  42. Brosens IA. Is mild endometriosis a progressive disease?. Hum Reprod. 1994;9:2209–2211
  43. Donnez J, Smoes P, Gillerot S, Casanas-Roux F, Nisolle M. Vascular endothelial growth factor (VEGF) in endometriosis. Hum Reprod. 1998;13:1686–1690
  44. Kokorine I, Nisolle M, Donnez J, Eeckhout Y, Courtoy PJ, Marbaix E. Expression of interstitial collagenase (matrix metalloproteinase-1) is related to the activity of human endometriotic lesions. Fertil Steril. 1997;68:246–251
  45. Zeitvogel A, Baumann R, Starzinski-Powitz A. Identification of an invasive, N-cadherin–expressing epithelial cell type in endometriosis using a new cell culture model. Am J Pathol. 2001;159:1839–1852
  46. Banu SK, Lee J, Starzinski-Powitz A, Arosh JA. Gene expression profiles and functional characterization of human immortalized endometriotic epithelial and stromal cells. Fertil Steril. Published online November 26, 2007 [Epub ahead of print].
  47. Grund EM, Kagan D, Tran CA, Zeitvogel A, Starzinski-Powitz A, Nataraja S, et al. Tumor necrosis factor alpha regulates inflammatory and mesenchymal responses via mitogen-activated protein kinase kinase, p38, and nuclear factor kappaB in human endometriotic epithelial cells. Mol Pharmacol. 2008;73:1394–1404
  48. Wu Y, Starzinski-Powitz A, Guo SW. Trichostatin A, a histone deacetylase inhibitor, attenuates invasiveness and reactivates E-cadherin expression in immortalized endometriotic cells. Reprod Sci. 2007;14:374–382
  49. Wu Y, Starzinski-Powitz A, Guo SW. Prolonged stimulation with tumor necrosis factor–alpha induced partial methylation at PR-B promoter in immortalized epithelial-like endometriotic cells. Fertil Steril. 2008;90:234–237
  50. Defrere S, Van Langendonckt A, Gonzalez Ramos R, Jouret M, Mettlen M, Donnez J. Quantification of endometriotic lesions in a murine model by fluorimetric and morphometric analyses. Hum Reprod. 2006;21:810–817
  51. Arosh JA, Banu SK, Chapdelaine P, Emond V, Kim JJ, MacLaren LA, et al. Molecular cloning and characterization of bovine prostaglandin E2 receptors EP2 and EP4: expression and regulation in endometrium and myometrium during the estrous cycle and early pregnancy. Endocrinology. 2003;144:3076–3091
  52. Masuda H, Maruyama T, Hiratsu E, Yamane J, Iwanami A, Nagashima T, et al. Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/gamma c(null) immunodeficient mice. Proc Natl Acad Sci U S A. 2007;104:1925–1930
  53. Chang L, Goldman RD. Intermediate filaments mediate cytoskeletal crosstalk. Nat Rev Mol Cell Biol. 2004;5:601–613
  54. Bohn W, Wiegers W, Beuttenmuller M, Traub P. Species-specific recognition patterns of monoclonal antibodies directed against vimentin. Exp Cell Res. 1992;201:1–7
  55. Krishna TS, Fenyo D, Kong XP, Gary S, Chait BT, Burgers P, et al. Crystallization of proliferating cell nuclear antigen (PCNA) from Saccharomyces cerevisiae. J Mol Biol. 1994;241:265–268
  56. Maga G, Hubscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci. 2003;116:3051–3060
  57. Nagase H, Woessner JF. Matrix metalloproteinases. J Biol Chem. 1999;274:21491–21494
  58. Bruner-Tran KL, Zhang Z, Eisenberg E, Winneker RC, Osteen KG. Down-regulation of endometrial matrix metalloproteinase-3 and -7 expression in vitro and therapeutic regression of experimental endometriosis in vivo by a novel nonsteroidal progesterone receptor agonist, tanaproget. J Clin Endocrinol Metab. 2006;91:1554–1560
  59. Curry TE, Osteen KG. The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr Rev. 2003;24:428–465
  60. Arosh JA, Lee J, Rodriguez R, Starzinski-Powitz A, Banu SK. Prostaglandin E2 signaling in pathophysiology of endometriosis in human. [abstract] In: Presented at: 39th Annual Meeting of Society for the Study of Reproduction. San Antonio, TX: Society for Study of Reproduction; 2007;
  61. Kayisli UA, Berkkanoglu M, Zhang L, Kizilay G, Arici A. The broad-spectrum chemokine inhibitor NR58-3.14.3 suppresses the implantation and survival of human endometrial implants in the nude mice endometriosis model. Reprod Sci. 2007;14:825–835
  62. Braun DP, Ding J, Shaheen F, Willey JC, Rana N, Dmowski WP. Quantitative expression of apoptosis-regulating genes in endometrium from women with and without endometriosis. Fertil Steril. 2007;87:263–268

 S.K.B. has nothing to disclose. A.S.-P. has nothing to disclose. V.O.S. has nothing to disclose. R.C.B. has nothing to disclose. J.A.A. has nothing to disclose.

 Supported by a program development award to J.A.A. from the Department of Integrative Biosciences, Texas A&M University.

PII: S0015-0282(08)01411-8

doi: 10.1016/j.fertnstert.2008.06.050

Fertility and Sterility
Volume 91, Issue 5, Supplement , Pages 2199-2209 , May 2009

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