Tissue remodeling and nonendometrium-like menstrual cycling are hallmarks of peritoneal endometriosis lesions

Reproductive Sciences

Volumn 20, Issue 1, 2013, Pages 85-102

  Sohler, Florian ^a   Sommer, Anette ^a   Wachter, David L ^b   Agaimy, Abbas ^b   Fischer, Oliver M ^a   Renner, Stefan P ^b   Burghaus, Stefanie ^b   Fasching, Peter A ^b   Beckmann, Matthias W ^b   Fuhrmann, Ulrike ^a   Strick, Reiner ^b   Strissel, Pamela L ^b  

^a BAYER PHARMA AG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

endometriosis; gene expression microarray; menstrual cycle; tissue remodeling

Indexed keywords

ALCOHOL DEHYDROGENASE; ALPHA ACTIN; AQUAPORIN 3; CALDESMON; CELL CYCLE PROTEIN 6; COMPLEMENT; COMPLEMENT COMPONENT C4A; COMPLEMENT COMPONENT C7; COMPLEMENT FACTOR D; CXCL14 CHEMOKINE; DECAY ACCELERATING FACTOR; DESMIN; DICKKOPF 1 PROTEIN; ESTRADIOL; FATTY ACID BINDING PROTEIN 4; FOLLITROPIN; GLUTATHIONE PEROXIDASE 3; HAPTOCORRIN; KYNURENINE 3 MONOOXYGENASE; LUTEINIZING HORMONE; MYOSIN HEAVY CHAIN; NICOTINAMIDE METHYLTRANSFERASE; PROGESTERONE; SECRETED FRIZZLED RELATED PROTEIN 2; SERINE PROTEINASE INHIBITOR; SONIC HEDGEHOG PROTEIN; STEROID RECEPTOR; STROMELYSIN 3; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1; VIMENTIN;

ARTICLE; CARBOHYDRATE SYNTHESIS; CELL ADHESION; CELL DIVISION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENDOMETRIOSIS; ESTRADIOL BLOOD LEVEL; EUTOPIC ENDOMETRIUM LESION; FEMALE; FOLLITROPIN BLOOD LEVEL; GENE CLUSTER; GENE EXPRESSION; GENETIC ANALYSIS; GYNECOLOGIC DISEASE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERPLASIA; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOHISTOCHEMISTRY; LUTEINIZING HORMONE BLOOD LEVEL; MARKER GENE; MENSTRUAL CYCLE; METAPLASIA; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; PERITONEAL ENDOMETRIOSIS LESION; PERITONEUM; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE CONTRACTION; TIGHT JUNCTION; TISSUE SECTION;

ADULT; COHORT STUDIES; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMANS; MENSTRUAL CYCLE; MIDDLE AGED; PERITONEUM; PRINCIPAL COMPONENT ANALYSIS; YOUNG ADULT;

EID: 84870556018     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719112451147     Document Type: Article

References (68)

1. Witz CA, Burns WN. Endometriosis and infertility: is there a cause and effect relationship?. Gynecol Obstet Invest. 2002 ; 53 (suppl 1). 2-11
2. Vigano P, Parazzini F, Somigliana E, Vercellini P. Endometriosis: epidemiology and aetiological factors. Best Pract Res Clin Obstet Gynaecol. 2004 ; 18 (2). 177-200
3. Giudice LC, Kao LC. Endometriosis. Lancet. 2004 ; 364 (9447). 1789-1799
4. Adamson GD. Endometriosis classification: an update. Curr Opin Obstet Gynecol. 2011 ; 23 (4). 213-220
5. Valle RF, Sciarra JJ. Endometriosis: treatment strategies. Ann N Y Acad Sci. 2003 ; 997: 229-239
6. Simoens S, Hummelshoj L, D'Hooghe T. Endometriosis: cost estimates and methodological perspective. Hum Reprod Update. 2007 ; 13 (4). 395-404
7. Brandes I, Kleine-Budde K, Mittendorf T. Cost of illness of endometriosis. Geburtshilfe und Frauenheilkunde. 2009 ; 69 (10). 925-930
8. Matarese G, De Placido G, Nikas Y, Alviggi C. Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease?. Trends Mol Med. 2003 ; 9 (5). 223-228
9. Painter JN, Anderson CA, Nyholt DR, et al. Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis. Nat Genet. 2011 ; 43 (1). 51-54
10. Falconer H, D'Hooghe T, Fried G. Endometriosis and genetic polymorphisms. Obstet Gynecol Surv. 2007 ; 62 (9). 616-628
11. Barcena de Arellano ML, Gericke J, Reichelt U, et al. Immunohistochemical characterization of endometriosis-Associated smooth muscle cells in human peritoneal endometriotic lesions. Hum Reprod. 2011 ; 26 (10). 2721-2730
12. Burney RO, Talbi S, Hamilton AE, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007 ; 148 (8). 3814-3826
13. Filigheddu N, Gregnanin I, Porporato PE, et al. Differential expression of microRNAs between eutopic and ectopic endometrium in ovarian endometriosis. J Biomed Biotechnol. 2010 ;: 369549
14. Oppelt P, Renner SP, Strick R, et al. Correlation of high-risk human papilloma viruses but not of herpes viruses or Chlamydia trachomatis with endometriosis lesions. Fertil Steril. 2010 ; 93 (6). 1778-1786
15. Zeitoun K, Takayama K, Sasano H. Deficient 17beta-hydroxysteroid dehydrogenase type 2 expression in endometriosis: failure to metabolize 17beta-estradiol. J Clin Endocrinol Metab. 1998 ; 83 (12). 4474-4480
16. Luo X, Ding L, Chegini N. Gonadotropin-releasing hormone and TGF-beta activate MAP kinase and differentially regulate fibronectin expression in endometrial epithelial and stromal cells. Am J Physiol Endocrinol Metab. 2004 ; 287 (5). E991 - E1001
17. Agic A, von Wussow U, Starzinski-Powitz A, Diedrich K, Altevogt P, Hornung D. Inhibition of cell proliferation, adhesion, and invasion with an anti-L1-cell adhesion molecule monoclonal antibody in an in vitro endometriosis model. Fertil Steril. 2010 ; 94 (3). 1102-1104
18. Tirado-González I, Barrientos G, Tariverdian N, et al. Endometriosis research: animal models for the study of a complex disease. J Reprod Immunol. 2010 ; 86 (2). 141-147
19. Kyama CM, Mihalyi A, Simsa P, et al. Role of cytokines in the endometrial-peritoneal cross-talk and development of endometriosis. Front Biosci (Elite Ed). 2009 ; 1: 444-454
20. Sternberg SS. Histology for Pathologists. 2 nd ed. Philadelphia, NY:Lippincott-Raven;1997:897-908. Philadelphia, NY: Lippincott-Raven ; 1997: 897-908.
21. Herrick SE, Mutsaers SE. Mesothelial progenitor cells and their potential in tissue engineering. Int J Biochem Cell Biol. 2004 ; 36 (4). 621-642
22. Fredericks S, Russell P, Cooper M, Varol N. Smooth muscle in the female pelvic peritoneum: a clinicopathological analysis of 31 women. Pathology. 2005 ; 37 (1). 14-21
23. Yantiss RK, Clement PB, Young RH. Endometriosis of the intestinal tract: a study of 44 cases of a disease that may cause diverse challenges in clinical and pathologic evaluation. Am J Surg Pathol. 2001 ; 25 (4). 445-454
24. Pitt MA, Haboubi NY. Serosal reaction in chronic gastric ulcers: an immunohistochemical and ultrastructural study. J Clin Pathol. 1995 ; 48 (3). 226-228
25. Odagiri K, Konno R, Fujiwara H, Netsu S, Yang C, Suzuki M. Smooth muscle metaplasia and innervation in interstitium of endometriotic lesions related to pain. Fertil Steril. 2009 ; 92 (5). 1525-1531
26. Itoga T, Matsumoto T, Takeuchi H, et al. Fibrosis and smooth muscle metaplasia in rectovaginal endometriosis. Pathol Int. 2003 ; 53 (6). 371-375
27. Tran LV, Tokushige N, Berbic M, Markham R, Fraser IS. Macrophages and nerve fibres in peritoneal endometriosis. Hum Reprod. 2009 ; 24 (4). 835-841
28. Anaf V, Simon P, Fayt I, Noel J. Smooth muscles are frequent components of endometriotic lesions. Hum Reprod. 2000 ; 15 (4). 767-771
29. van Kaam KJ, Schouten JP, Nap AW, Dunselman GA, Groothuis PG. Fibromuscular differentiation in deeply infiltrating endometriosis is a reaction of resident fibroblasts to the presence of ectopic endometrium. Hum Reprod. 2008 ; 23 (12). 2692-2700
30. Jeffery PK. Remodeling in asthma and chronic obstructive lung disease. Am J Respr Crit Care Med. 2001 ; 164 (10). S28 - S38
31. Eyster KM, Boles AL, Brannian JD, Hansen KA. DNA microarray analysis of gene expression markers of endometriosis. Fertil Steril. 2002 ; 77 (1). 38-42
32. Lebovic DI, Baldocchi RA, Mueller MD, Taylor RN.. Altered expression of a cell-cycle suppressor gene, Tob-1, in endometriotic cells by cDNA array analyses. Fertil Steril. 2002 ; 78 (4). 849-854
33. Arimoto T, Katagiri T, Oda K, et al. Genome-wide cDNA microarray analysis of gene-expression profiles involved in ovarian endometriosis. Int J Oncol. 2003 ; 22 (3). 551-560
34. Konno R, Yamada-Okabe H, Fujiwara H, et al. Role of immunoreactions and mast cells in pathogenesis of human endometriosis-morphologic study and gene expression analysis. Hum Cell. 2003 ; 16 (3). 141-149
35. Matsuzaki S, Canis M, Vaurs-Barrière C, et al. DNA microarray analysis of gene expression profiles in deep endometriosis using laser capture microdissection. Mol Hum Reprod. 2004 ; 10 (10). 719-728
36. Wu Y, Kajdacsy-Balla A, Strawn E. Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology. 2006 ; 147 (1). 232-246
37. Mettler L, Salmassi A, Schollmeyer T, Schmutzler AG, Pungel F, Jonat W. Comparison of c-DNA microarray analysis of gene expression between eutopic endometrium and ectopic endometrium (endometriosis). J Assist Reprod Genet. 2007 ; 24 (6). 249-258
38. Borghese B, Mondon F, Noël JC, et al. Gene expression profile for ectopic versus eutopic endometrium provides new insights into endometriosis oncogenic potential. Mol Endocrinol. 2008 ; 22 (11). 2557-2562
39. Eyster KM, Klinkova O, Kennedy V, Hansen KA. Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium. Fertil Steril. 2007 ; 88 (6). 1505-1533
40. Talbi S, Hamilton AE, Vo KC, et al. Molecular phenotyping of human endometrium distinguishes menstrual-cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology. 2006 ; 147 (3). 1097-1121
41. Nogawa Fonzar-Marana RR, Ferriani RA, Soares SG, Cavalcante-Neto FF, Teixeira JE, Barbosa JE. Expression of complement system regulatory molecules in the endometrium of normal ovulatory and hyperstimulated women correlate with menstrual-cycle phase. Fertil Steril. 2006 ; 86 (3). 758-761
42. Ponnampalam AP, Weston GC, Susil B, Rogers PA. Molecular profiling of human endometrium during the menstrual-cycle. Aust N Z J Obstet Gynaecol. 2006 ; 46 (2). 154-158
43. Strissel PL, Ellmann S, Loprich E, et al. Early aberrant insulin-like growth factor signaling in the progression to endometrial carcinoma is augmented by tamoxifen. Int J Cancer. 2008 ; 123 (12). 2871-2879
44. Jiménez-Heffernan JA, Aguilera A, Aroeira LS, et al. Immunohistochemical characterization of fibroblast subpopulations in normal peritoneal tissue and in peritoneal dialysis-induced fibrosis. Virchows Arch. 2004 ; 444 (3). 247-256
45. Watanabe K, Tajino T, Sekiguchi M, Suzuki T.. h-Caldesmon as a specific marker for smooth muscle tumors. Comparison with other smooth muscle markers in bone tumors. Am J Clin Pathol. 2000 ; 113 (5). 663-668
46. Oliver C, Montes MJ, Galindo JA, Ruiz C, Olivares EG. Human decidual stromal cells express alpha-smooth muscle actin and show ultrastructural similarities with myofibroblasts. Hum Reprod. 1999 ; 14 (6). 1599-1605
47. Czernobilsky B, Gabbiani G, Prus D, Lifschitz-Mercer B. Alpha-smooth muscle actin-positive myofibroblasts in endometrial stroma are not a reliable criterion for the diagnosis of well differentiated endometrioid adenocarcinoma in small tissue samples. Int J Gynecol Pathol. 2001 ; 20 (3). 232-238
48. Fujishita A, Nakane PK, Koji T, et al. Expression of estrogen and progesterone receptors in endometrium and peritoneal endometriosis: an immunohistochemical and in situ hybridization study. Fertil Steril. 1997 ; 67 (5). 856-864
49. Schweppe KW, Wynn RM. Ultrastructural changes in endometriotic implants during the menstrual-cycle. Obstet Gynecol. 1981 ; 58 (4). 465-473
50. Metzger DA, Olive DL, Haney AF. Limited hormonal responsiveness of ectopic endometrium: histologic correlation with intrauterine endometrium. Hum Pathol. 1988 ; 19 (12). 1417-1424
51. Lessey BA, Metzger DA, Haney AF, McCarty KS. Immunohistochemical analysis of estrogen and progesterone receptors in endometriosis: comparison with normal endometrium during the menstrual-cycle and the effect of medical therapy. Fertil Steril. 1989 ; 51 (3). 409-415
52. Calcagno A, Grassi T, Mariuzzi L, et al. Expression patterns of Aurora A and B kinases, Ki-67 and the estrogen and progesterone receptors determined using an endometriosis tissue microarray model. Hum Reprod. 2011 ; 26 (10). 2731-2741
53. Noël JC, Chapron C, Bucella D, et al. Estrogen and progesterone receptors in smooth muscle component of deep infiltrating endometriosis. Fertil Steril. 2010 ; 93 (6). 1774-1777
54. Attia GR, Zeitoun K, Edwards D, Johns A, Carr BR, Bulun SE. Progesterone receptor isoform A but not B is expressed in endometriosis. J Clin Endocrinol Metab. 2000 ; 85 (8). 2897-2902
55. Bulun SE, Cheng YH, Pavone ME, et al. 17Beta-hydroxysteroid dehydrogenase-2 deficiency and progesterone resistance in endometriosis. Semin Reprod Med. 2010 ; 28 (1). 44-50
56. Ellmann S, Sticht H, Thiel F, Beckmann MW, Strick R, Strissel PL. Estrogen and progesterone receptors: from molecular structures to clinical targets. Cell Mol Life Sci. 2009 ; 66 (15). 2405-2426
57. Jones CJ, Denton J, Fazleabas AT. Morphological and glycosylation changes associated with the endometrium and ectopic lesions in a baboon model of endometriosis. Hum Reprod. 2006 ; 21 (12). 3068-3080
58. Scotti S, Regidor PA, Schindler AE, Winterhager E. Reduced proliferation and cell adhesion in endometriosis. Mol Hum Reprod. 2000 ; 6 (7). 610-617
59. Gaetje R, Kotzian S, Herrmann G, Baumann R, Starzinski-Powitz A. Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin. Am J Pathol. 1997 ; 150 (2). 461-467
60. Gaetje R, Kotzian S, Herrmann G, Baumann R, Starzinski-Powitz A. Invasiveness of endometriotic cells in vitro. Lancet. 1995 ; 346 (8988). 1463-1464
61. Singh AB, Sharma A, Dhawan P.. Claudin family of proteins and cancer: an overview. J Oncol. 2010 ;: 541957
62. Gaetje R, Holtrich U, Engels K, et al. Differential expression of claudins in human endometrium and endometriosis. Gynecol Endocrinol. 2008 ; 24 (8). 442-449
63. Prat A, Perou CM. Mammary development meets cancer genomics. Nat Med. 2009 ; 15: 842-844
64. Paulin D, Li Z. Desmin: a major intermediate filament protein essential for the structural integrity and function of muscle. Exp Cell Res. 2004 ; 301 (1). 1-7
65. Nunes KP, Rigsby CS, Webb RC. RhoA/Rho-kinase and vascular diseases: what is the link?. Cell Mol Life Sci. 2010 ; 67 (22). 3823-3836
66. Busard MP, van der Houwen LE, Bleeker MC, et al. Deep infiltrating endometriosis of the bowel: MR imaging as a method to predict muscular invasion. [Epub ahead of print Aug 6 2011]. Abdom Imaging. :
67. Donnez J, Spada F, Squifflet J, Nisolle M. Bladder endometriosis must be considered as bladder adenomyosis. Fertil Steril. 2000 ; 74 (6). 1175-1181
68. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927 ; 3 (2). 93-110