Endometrial-peritoneal interactions during endometriotic lesion establishment

American Journal of Pathology

Volumn 173, Issue 3, 2008, Pages 700-715

  Hull, M Louise ^a,b,i   Escareno, Claudia Rangel ^c,d   Godsland, Jane M ^a   Doig, John R ^e   Johnson, Claire M ^f   Phillips, Stephen C ^f   Smith, Stephen K ^a,g   Tavaré, Simon ^a,c   Print, Cristin G ^a,h   Charnock Jones, D Stephen ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d INSTITUTO NACIONAL DE MEDICINA GENÓMICA   (Mexico)

^e Oxford Clinic   (New Zealand)

^f PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United Kingdom)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h UNIVERSITY OF AUCKLAND   (New Zealand)

ⁱ UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEASOME; UBIQUITIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE MODEL; ENDOMETRIOSIS; ENDOMETRIUM CELL; FEMALE; HEALING; HUMAN; HUMAN TISSUE; MESOTHELIUM; MORPHOMETRICS; MOUSE; NECROSIS; NONHUMAN; NUDE MOUSE; ONCOGENE RAS; OVARY INFLAMMATION; PATHOPHYSIOLOGY; PERITONEUM CELL; PRIORITY JOURNAL; RNA TRANSCRIPTION; TISSUE MICROARRAY; TISSUE REPAIR; XENOGRAFT;

EID: 51349131016     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.071128     Document Type: Article

References (80)

1. Strathy JH, Molgaard CA, Coulam CB, Melton LJ 3rd: Endometriosis and infertility: a laparoscopic study of endometriosis among fertile and infertile women. Fertil Steril 1982, 38:667-672
2. Giudice LC, Kao LC: Endometriosis. Lancet 2004, 364:1789-1799
3. Sampson JA: Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927, 14:442-469
4. Bulun SE, Yang S, Fang Z, Gurates B, Tamura M, Sebastian S: Estrogen production and metabolism in endometriosis. Ann NY Acad Sci 2002, 955:75-85
5. Ho HN, Wu MY, Yang YS: Peritoneal cellular immunity and endometriosis. Am J Reprod Immunol 1997, 38:400-412
6. Simpson JL, Bischoff F: Heritability and candidate genes for endometriosis. Reprod Biomed Online 2003, 7:162-169
7. Rier S, Foster WG: Environmental dioxins and endometriosis. Semin Reprod Med 2003, 21:145-154
8. Hull ML, Charnock-Jones DS, Chan CL, Bruner-Tran KL, Osteen KG, Tom BD, Fan TP, Smith SK: Antiangiogenic agents are effective inhibitors of endometriosis. J Clin Endocrinol Metab 2003, 88:2889-2899
9. Nap AW, Griffioen AW, Dunselman GA, Bouma-Ter Steege JC, Thijssen VL, Evers JL, Groothuis PG: Antiangiogenesis therapy for endometriosis. J Clin Endocrinol Metab 2004, 1089-1095
10. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC: Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003, 144:2870-2881
11. Eyster KM, Boles AL, Brannian JD, Hansen KA: DNA microarray analysis of gene expression markers of endometriosis. Fertil Steril 2002, 77:38-42
12. Arimoto T, Katagiri T, Oda K, Tsunoda T, Yasugi T, Osuga Y, Yoshikawa H, Nishii O, Yano T, Taketani Y, Nakamura Y: Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis. Int J Oncol 2003, 22:551-560
13. Wu Y, Kajdacsy-Balla A, Strawn E, Basir Z, Halverson G, Jailwala P, Wang Y, Wang X, Ghosh S, Guo SW: Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology 2006, 147:232-246
14. Zamah NM, Dodson MG, Stephens LC, Buttram VC, Jr., Besch PK, Kaufman RH: Transplantation of normal and ectopic human endometrial tissue into athymic nude mice. Am J Obstet Gynecol 1984, 149:591-597
15. 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
16. Tabibzadeh S, Miller S, Dodson WC, Satyaswaroop PG: An experimental model for the endometriosis in athymic mice. Front Biosci 1999, 4:C4-9
17. Cunha GR, Vanderslice KD: Identification in histological sections of species origin of cells from mouse, rat and human. Stain Technol 1984, 59:7-12
18. Schwartz DR, Moin K, Yao B, Matrisian LM, Coussens LM, Bugge TH, Fingleton B, Acuff HB, Sinnamon M, Nassar H, Platts AE, Krawetz SA, Linebaugh BE, Sloane BF: Hu/Mu ProtIn oligonucleotide microarray: dual-species array for profiling protease and protease inhibitor gene expression in tumors and their microenvironment. Mol Cancer Res 2007, 5:443-454
19. Acuff HB, Sinnamon M, Fingleton B, Boone B, Levy SE, Chen X, Pozzi A, Carbone DP, Schwartz DR, Moin K, Sloane BF, Matrisian LM: Analysis of host- and tumor-derived proteinases using a custom dual species microarray reveals a protective role for stromal matrix metalloproteinase-12 in non-small cell lung cancer. Cancer Res 2006, 66:7968-7975
20. Noyes RW, Hertig AT, Rock J: Dating the endometrial biopsy. Fertil Steril 1975, 1:3-25
21. Hull ML, Prentice A, Wang DY, Butt RP, Phillips SC, Smith SK, Charnock-Jones DS: Nimesulide, a COX-2 inhibitor, does not reduce lesion size or number in a nude mouse model of endometriosis. Hum Reprod 2005, 20:350-358
22. R Development Core Group (2008). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-90051-07-01
23. Cheng CW, Bielby H, Licence D, Smith SK, Print CG, Charnock-Jones DS: Quantitative cellular and molecular analysis of the effect of progesterone withdrawal in a murine model of decidualization. Biol Reprod 2007, 76:871-883
24. Smyth G.K.: LIMMA: Linear Models for Microarray Data. New York, Springer, 2005, pp 397-420
25. Long AD, Mangalam HJ, Chan BY, Tolleri L, Hatfield GW, Baldi P: Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework: analysis of global gene expression in Escherichia coli K12. J Biol Chem 2001, 276:19937-19944
26. Baldi P, Long AD: A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 2001, 17:509-519
27. Breitling R, Armengaud P, Amtmann A, Herzyk P: Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 2004, 573:83-92
28. Al-Shahrour F, Diaz-Uriarte R, Dopazo J: FatiGO: a web tool for finding significant associations of gene ontology terms with groups of genes. Bioinformatics 2004, 20:578-580
29. Gonzalez-Ramos R, Van Langendonckt A, Defrere S, Lousse JC, Mettlen M, Guillet A, Donnez J: 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
30. Rizki A, Weaver VM, Lee SY, Rozenberg GI, Chin K, Myers CA, Bascom JL, Mott JD, Semeiks JR, Grate LR, Mian IS, Borowsky AD, Jensen RA, Idowu MO, Chen F, Chen DJ, Petersen OW, Gray JW, Bissell MJ: A human breast cell model of preinvasive to invasive transition. Cancer Res 2008, 68:1378-1387
31. Bruner-Tran KL, Eisenberg E, Yeaman GR, Anderson TA, McBean J, Osteen KG: Steroid and cytokine regulation of matrix metalloproteinase expression in endometriosis and the establishment of experimental endometriosis in nude mice. J Clin Endocrinol Metab 2002, 87:4782-4791
32. Becker CMB, Cramer T, Funakoshi T, Rohwer N, Bernhart W, Treston AM, Folkman J, D'Amato RJ: Hypoxia may be an important regulator of disease progression in a mouse model of endometriosis Obstet Gynecol 2005, 123:S19-S20
33. Baldwin AS, Jr.: The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 1996, 14:649-683
34. Overton C, Fernandez-Shaw S, Hicks B, Barlow D, Starkey P: Peritoneal fluid cytokines and the relationship with endometriosis and pain. Hum Reprod 1996, 11:380-386
35. Mori H, Sawairi M, Nakagawa M, Itoh N, Wada K, Tamaya T: Peritoneal fluid interleukin-1 beta and tumor necrosis factor in patients with benign gynecologic disease. Am J Reprod Immunol 1991, 26:62-67
36. Lousse JC, Van Langendonckt A, Gonzalez-Ramos R, Defrere S, Renkin E, Donnez J: Increased activation of nuclear factor-kappa B (NF-kappaB) in isolated peritoneal macrophages of patients with endometriosis. Fertil Steril 2007, 1:217-220
37. Gonzalez-Ramos R, Donnez J, Defrere S, Leclercq I, Squifflet J, Lousse JC, Van Langendonckt A: Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis. Mol Hum Reprod 2007, 13:503-509
38. Lin YJ, Lai MD, Lei HY, Wing LY: Neutrophils and macrophages promote angiogenesis in the early stage of endometriosis in a mouse model. Endocrinology 2006, 147:1278-1286
39. McLaren J, Prentice A, Charnock-Jones DS, Smith SK.: Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis. Hum Reprod 1996, 11:220-223
40. Frangogiannis NG: The role of the chemokines in myocardial ischemia and reperfusion. Curr Vasc Pharmacol 2004, 2:163-174
41. Blobe GC, Schiemann WP, Lodish HF: Role of transforming growth factor beta in human disease. N Engl J Med 2000, 342:1350-1358
42. Oosterlynck DJ, Meuleman C, Lacquet FA, Waer M, Koninckx PR: Flow cytometry analysis of lymphocyte subpopulations in peritoneal fluid of women with endometriosis. Am J Reprod Immunol 1994, 31:25-31
43. Podgaec S, Abrao MS, Dias JA, Jr., Rizzo LV, de Oliveira RM, Baracat EC: Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 2007, 22:1373-1379
44. Akoum A, Lawson C, Herrmann-Lavoie C, Maheux R: Imbalance in the expression of the activating type I and the inhibitory type II interleukin 1 receptors in endometriosis. Hum Reprod 2007, 22:1464-1473
45. Singer AJ, Clark RA: Cutaneous wound healing. N Engl J Med 1999, 341:738-746
46. Small JV, Rottner K, Kaverina I, Anderson KI: Assembling an actin cytoskeleton for cell attachment and movement. Biochim Biophys Acta 1998, 1404:271-281
47. Andoh A, Fujino S, Okuno T, Fujiyama Y, Bamba T: Intestinal subepithelial myofibroblasts in inflammatory bowel diseases. J Gastroenterol 2002, 37(Suppl 14):33-37
48. Dinulescu DM, Ince TA, Quade BJ, Shafer SA, Crowley D, Jacks T: Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat Med 2005, 11:63-70
49. Melin A, Sparen P, Persson I, Bergqvist A: Endometriosis and the risk of cancer with special emphasis on ovarian cancer. Hum Reprod 2006, 21:1237-1242
50. Sharkey AM, Day K, McPherson A, Malik S, Licence D, Smith SK, Charnock-Jones DS: Vascular endothelial growth factor expression in human endometrium is regulated by hypoxia. J Clin Endocrinol Metab 2000, 85:402-409
51. van Kempen LC, de Visser KE, Coussens LM: Inflammation, proteases and cancer. Eur J Cancer 2006, 42:728-734
52. Framson PE, Sage EH: SPARC and tumor growth: where the seed meets the soil? J Cell Biochem 2004, 92:679-690
53. Cheon YP, Li Q, Xu X, DeMayo FJ, Bagchi IC, Bagchi MK: A genomic approach to identify novel progesterone receptor regulated pathways in the uterus during implantation. Mol Endocrinol 2002, 16:2853-2871
54. Flores I, Rivera E, Ruiz LA, Santiago OI, Vernon MW, Appleyard CB: Molecular profiling of experimental endometriosis identified gene expression patterns in common with human disease. Fertil Steril 2007, 87:1180-1199
55. Konno R, Fujiwara H, Netsu S, Odagiri K, Shimane M, Nomura H, Suzuki M: Gene expression profiling of the rat endometriosis model. Am J Reprod Immunol 2007, 58:330-343
56. Wren JD, Wu Y, Guo SW: A system-wide analysis of differentially expressed genes in ectopic and eutopic endometrium. Hum Reprod 2007, 22:2093-2102
57. Pan Q, Luo X, Toloubeydokhti T, Chegini N: The expression profile of micro-RNA: endometrium and endometriosis and the influence of ovarian steroids on their expression. Mol Hum Reprod 2007, 13:797-806
58. Slater M, Quagliotto G, Cooper M, Murphy CR: Endometriotic cells exhibit metaplastic change and oxidative DNA damage as well as decreased function, compared to normal endometrium. J Mol Histol 2005, 36:257-263
59. Nasu K, Nishida M, Ueda T, Yuge A, Takai N, Narahara H: Application of the nuclear factor-kappaB inhibitor BAY 11-7085 for the treatment of endometriosis: an in vitro study. Am J Physiol Endocrinol Metab 2007, 293:E16-E23
60. Ota H, Igarashi S, Sasaki M, Tanaka T: Distribution of cyclooxygenase-2 in eutopic and ectopic endometrium in endometriosis and adenomyosis. Hum Reprod 2001, 16:561-566
61. Semino C, Semino A, Pietra G, Mingari MC, Barocci S, Venturini PL, Ragni N, Melioli G: Role of major histocompatibility complex class I expression and natural killer-like T cells in the genetic control of endometriosis. Fertil Steril 1995, 64:909-916
62. Hornung D, Klingel K, Dohrn K, Kandolf R, Wallwiener D, Taylor RN: Regulated on activation, normal T-cell-expressed and -secreted mRNA expression in normal endometrium and endometriotic implants: assessment of autocrine/paracrine regulation by in situ hybridization. Am J Pathol 2001, 158:1949-1954
63. Jolicoeur C, Boutouil M, Drouin R, Paradis I, Lemay A, Akoum A: Increased expression of monocyte chemotactic protein-1 in the endometrium of women with endometriosis. Am J Pathol 1998, 152:125-133
64. Sharpe-Timms KL, Bruno PL, Penney LL, Bickel JT: Immunohistochemical localization of granulocyte-macrophage colony-stimulating factor in matched endometriosis and endometrial tissues. Am J Obstet Gynecol 1994, 171:740-745
65. McLaren J, Prentice A, Charnock-Jones DS, Millican SA, Muller KH, Sharkey AM, Smith SK: Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J Clin Invest 1996, 98:482-489
66. Halme J, Becker S, Wing R: Accentuated cyclic activation of peritoneal macrophages in patients with endometriosis. Am J Obstet Gynecol 1984, 148:85-90
67. Chegini N, Gold LI, Williams RS: Localization of transforming growth factor beta isoforms TGF-beta 1. TGF-beta 2, and TGF-beta 3 in surgically induced endometriosis in the rat. Obstet Gynecol 1994, 83:455-461
68. Komiyama S, Aoki D, Komiyama M, Nozawa S: Local activation of TGF-beta1 at endometriosis sites. J Reprod Med 2007, 52:306-312
69. Anaf V, Simon P, Fayt I, Noel J: Smooth muscles are frequent components of endometriotic lesions. Hum Reprod 2000, 15:767-771
70. Punnonen J, Teisala K, Ranta H, Bennett B, Punnonen R: Increased levels of interleukin-6 and interleukin-10 in the peritoneal fluid of patients with endometriosis. Am J Obstet Gynecol 1996, 174:1522-1526
71. Garcia-Velasco JA, Arici A: Interleukin-8 stimulates the adhesion of endometrial stromal cells to fibronectin. Fertil Steril 1999, 72:336-340
72. Beliard A, Donnez J, Nisolle M, Foidart JM: Localization of laminin, fibronectin, E-cadherin, and integrins in endometrium and endometriosis. Fertil Steril 1997, 67:266-272
73. Giannelli G, Sgarra C, Di Naro E, Lavopa C, Angelotti U, Tartagni M, Simone O, Trerotoli P, Antonaci S, Loverro G: Endometriosis is characterized by an impaired localization of laminin-5 and alpha3beta1 integrin receptor. Int J Gynecol Cancer 2007, 17:242-247
74. Uzan C, Cortez A, Dufournet C, Fauvet R, Siffroi JP, Darai E: Eutopic endometrium and peritoneal, ovarian and bowel endometriotic tissues express a different profile of matrix metalloproteinases-2, -3 and -11, and of tissue inhibitor metalloproteinases-1 and -2. Virchows Arch 2004, 445:603-609
75. Kauma S, Clark MR, White C, Halme J: Production of fibronectin by peritoneal macrophages and concentration of fibronectin in peritoneal fluid from patients with or without endometriosis. Obstet Gynecol 1988, 72:13-18
76. Harrington DJ, Lessey BA, Rai V, Bergqvist A, Kennedy S, Manek S, Barlow DH, Mardon HJ: Tenascin is differentially expressed in endometrium and endometriosis. J Pathol 1999, 187:242-248
77. Matsuzaki S, Canis M, Darcha C, Dechelotte P, Pouly JL, Bruhat MA: Fibrogenesis in peritoneal endometriosis: a semi-quantitative analysis of type-I collagen. Gynecol Obstet Invest 1999, 47:197-199
78. Toki T, Nakayama K: Proliferative activity and genetic alterations in TP53 in endometriosis. Gynecol Obstet Invest 2000, 50(Suppl 1):33-38
79. Johnson MC, Torres M, Alves A, Bacallao K, Fuentes A, Vega M, Boric MA: Augmented cell survival in eutopic endometrium from women with endometriosis: expression of c-myc. TGF-beta1 and bax genes. Reprod Biol Endocrinol 2005, 3:45
80. Goumenou A, Panayiotides I, Matalliotakis I, Vlachonikolis I, Tzardi M, Koumantakis E: Bcl-2 and Bax expression in human endometriotic and adenomyotic tissues. Eur J Obstet Gynecol Reprod Biol 2001, 99:256-260