Towards an understanding of the molecular mechanism of endometriosis: Unbalancing epithelial-stromal genetic conflict

Gynecological Endocrinology

Volumn 30, Issue 1, 2014, Pages 7-15

  Kobayashi, Hiroshi ^a   Uekuri, Chiharu ^a   Shigetomi, Hiroshi ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Decidualization; Endometriosis; Epigenetics; Genome wide association study; Pathogenesis

Indexed keywords

CYCLIN DEPENDENT KINASE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GELATINASE A; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; PROGESTERONE RECEPTOR; SOMATOMEDIN A; SOMATOMEDIN C; STROMAL CELL DERIVED FACTOR 1; STROMELYSIN; STROMELYSIN 3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR HOXA10; TUMOR NECROSIS FACTOR ALPHA; UROKINASE;

ARTICLE; CELL ADHESION; CELL CYCLE REGULATION; CELL MOTILITY; DECIDUALIZATION; DETOXIFICATION; DOWN REGULATION; ENDOMETRIOSIS; GENETIC ASSOCIATION; HUMAN; IMMUNE RESPONSE; INFLAMMATION; MACROPHAGE; METABOLISM; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW; UPREGULATION;

EMBRYO IMPLANTATION; ENDOMETRIOSIS; ENDOMETRIUM; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; PERITONEAL DISEASES; PREGNANCY; STROMAL CELLS;

EID: 84890455692     PISSN: 09513590     EISSN: 14730766     Source Type: Journal    
DOI: 10.3109/09513590.2013.831832     Document Type: Article

References (91)

1. Sampson JA. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927;14:422-69.
2. Augoulea A, Alexandrou A, Creatsa M, et al. Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch Gynecol Obstet 2012;286:99-103.
3. 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;22:551-60.
4. Bischoff F, Simpson JL. Genetics of endometriosis: heritability and candidate genes. Best Pract Res Clin Obstet Gynaecol 2004;18: 219-32.
5. Hu WP, Tay SK, Zhao Y. Endometriosis-specific genes identified by real-time reverse transcription-polymerase chain reaction expression profiling of endometriosis versus autologous uterine endometrium. J Clin Endocrinol Metab 2006;91:228-38.
6. 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; 148:3814-26.
7. Zafrakas M, Tarlatzis BC, Streichert T, et al. Genome-wide microarray gene expression, array-CGH analysis, and telomerase activity in advanced ovarian endometriosis: a high degree of differentiation rather than malignant potential. Int J Mol Med 2008; 21:335-44.
8. Honda H, Barrueto FF, Gogusev J, et al. Serial analysis of gene expression reveals differential expression between endometriosis and normal endometrium. Possible roles for AXL and SHC1 in the pathogenesis of endometriosis. Reprod Biol Endocrinol 2008;6:59.
9. Guo SW. Epigenetics of endometriosis. Mol Hum Reprod 2009;15: 587-607.
10. Kobayashi H, Yamada Y, Kanayama S, et al. The role of iron in the pathogenesis of endometriosis. Gynecol Endocrinol 2009;25:39-52.
11. Pelch KE, Schroder AL, Kimball PA, et al. Aberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women. Fertil Steril 2010;93:1615-27.
12. Borghese B, Barbaux S, Mondon F, et al. Research resource: genome-wide profiling of methylated promoters in endometriosis reveals a subtelomeric location of hypermethylation. Mol Endocrinol 2010;24:1872-85.
13. Evian Annual Reproduction (EVAR) Workshop Group 2010, Fauser BC, Diedrich K, et al. Contemporary genetic technologies and female reproduction. Hum Reprod Update 2011;17:829-47.
14. Nasu K, Kawano Y, Tsukamoto Y, et al. Aberrant DNA methylation status of endometriosis: epigenetics as the pathogenesis, biomarker and therapeutic target. J Obstet Gynaecol Res 2011;37:683-95.
15. Borghese B, Santulli P, Héquet D, et al. Genetic polymorphisms of DNMT3L involved in hypermethylation of chromosomal ends are associated with greater risk of developing ovarian endometriosis. Am J Pathol 2012;180:1781-6.
16. Monsivais D, Bray JD, Su E, et al. Activated glucocorticoid and eicosanoid pathways in endometriosis. Fertil Steril 2012;98:117-25.
17. Bulun SE, Monsavais D, Pavone ME, et al. Role of estrogen receptor-b in endometriosis. Semin Reprod Med 2012;30:39-45.
18. Aghajanova L, Horcajadas JA, Weeks JL, et al. The protein kinase A pathway-regulated transcriptome of endometrial stromal fibroblasts reveals compromised differentiation and persistent proliferative potential in endometriosis. Endocrinology 2010;151:1341-55.
19. Pellegrini C, Gori I, Achtari C, et al. The expression of estrogen receptors as well as GREB1, c-MYC, and cyclin D1, estrogenregulated genes implicated in proliferation, is increased in peritoneal endometriosis. Fertil Steril 2012;98:1200-8.
20. Camargo-Kosugi CM, da Silva ID, Sato H, et al. The V109G polymorphism in the p27 gene is associated with endometriosis. Eur J Obstet Gynecol Reprod Biol 2009;145:180-3.
21. Sun WS, Misao R, Iwagaki S, et al. Coexpression of growth arrestspecific gene 6 and receptor tyrosine kinases, Axl and Sky, in human uterine endometrium and ovarian endometriosis. Mol Hum Reprod 2002;8:552-8.
22. Kim JG, Suh CS, Kim SH, et al. Insulin-like growth factors (IGFs), IGF-binding proteins (IGFBPs), and IGFBP-3 protease activity in the peritoneal fluid of patients with and without endometriosis. Fertil Steril 2000;73:996-1000.
23. Kim H, Park JH, Ku SY, et al. Association between endometriosis and polymorphisms in insulin-like growth factors (IGFs) and IGF-I receptor genes in Korean women. Eur J Obstet Gynecol Reprod Biol 2011;156:87-90.
24. Milingos D, Katopodis H, Milingos S, et al. Insulin-like growth factor-1 isoform mRNA expression in women with endometriosis: eutopic endometrium versus endometriotic cyst. Ann N Y Acad Sci 2006;1092:434-9.
25. Khan KN, Masuzaki H, Fujishita A, 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;20:2715-23.
26. Yin X, Pavone ME, Lu Z, et al. Increased activation of the PI3K/ AKT pathway compromises decidualization of stromal cells from endometriosis. J Clin Endocrinol Metab 2012;97:E35-43.
27. Lynch VJ, Brayer K, Gellersen B, Wagner GP. HoxA-11 and FOXO1A cooperate to regulate decidual prolactin expression: towards inferring the core transcriptional regulators of decidual genes. PLoS One 2009;4:e6845.
28. Akbas GE, Taylor HS. HOXC and HOXD gene expression in human endometrium: lack of redundancy with HOXA paralogs. Biol Reprod 2004;70:39-45.
29. Klemmt PA, Carver JG, Kennedy SH, et al. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril 2006; 85:564-72.
30. Aghajanova L, Hamilton A, Kwintkiewicz J, et al. Steroidogenic enzyme and key decidualization marker dysregulation in endometrial stromal cells from women with versus without endometriosis. Biol Reprod 2009;80:105-14.
31. Kane NM, Jones M, Brosens JJ, et al. TGFb1 attenuates expression of prolactin and IGFBP-1 in decidualized endometrial stromal cells by both SMAD-dependent and SMAD-independent pathways. PLoS One 2010;5:e12970.
32. Ramón L, Gilabert-Estellés J, Castelló R, et al. mRNA analysis of several components of the plasminogen activator and matrix metalloproteinase systems in endometriosis using a real-time quantitative RT-PCR assay. Hum Reprod 2005;20:272-8.
33. Wang XQ, Yu J, Luo XZ, et al. The high level of RANTES in the ectopic milieu recruits macrophages and induces their tolerance in progression of endometriosis. J Mol Endocrinol 2010;45:291-9.
34. Kyama CM, Overbergh L, Mihalyi A, et al. Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis. Fertil Steril 2008;89:301-10.
35. Tang L, Wang TT, Wu YT, et al. High expression levels of cyclin B1 and Polo-like kinase 1 in ectopic endometrial cells associated with abnormal cell cycle regulation of endometriosis. Fertil Steril 2009; 91:979-87.
36. Jensen JR, Witz CA, Schenken RS, Tekmal RR. A potential role for colony-stimulating factor 1 in the genesis of the early endometriotic lesion. Fertil Steril 2010;93:251-6.
37. Ahmed A, Dearn S, Shams M, et al. Localization, quantification, and activation of platelet-activating factor receptor in human endometrium during the menstrual cycle: PAF stimulates NO, VEGF, and FAKpp125. FASEB J 1998;12:831-43.
38. Uz YH, Murk W, Bozkurt I, et al. Increased c-Jun N-terminal kinase activation in human endometriotic endothelial cells. Histochem Cell Biol 2011;135:83-91.
39. Zhang L, Patterson AL, Zhang L, et al. Endometrial stromal betacatenin is required for steroid-dependent mesenchymal-epithelial cross talk and decidualization. Reprod Biol Endocrinol 2012;10:75.
40. Sherwin JR, Hastings JM, Jackson KS, et al. The endometrial response to chorionic gonadotropin is blunted in a baboon model of endometriosis. Endocrinology 2010;151:4982-93.
41. Bocklandt S, Lin W, Sehl ME, et al. Epigenetic predictor of age. PLoS One 2011;6:e14821.
42. Ni M, MacFarlane 4th AW, Toft M, et al. B-cell adaptor for PI3K (BCAP) negatively regulates Toll-like receptor signaling through activation of PI3K. Proc Natl Acad Sci USA 2012;109:267-72.
43. Maekawa M, Yamamoto T, Kohno M, et al. Requirement for ERK MAP kinase in mouse preimplantation development. Development 2007;134:2751-9.
44. Shigetomi H, Higashiura Y, Kajihara H, Kobayashi H. A potential link of oxidative stress and cell cycle regulation for development of endometriosis. Gynecol Endocrinol 2012;28:897-902.
45. Yamauchi N, Harada T, Taniguchi F, et al. Tumor necrosis factoralpha induced the release of interleukin-6 from endometriotic stromal cells by the nuclear factor-kappaB and mitogen-activated protein kinase pathways. Fertil Steril 2004;82:1023-8.
46. Guillaumond F, Boyer B, Becquet D, et al. Chromatin remodeling as a mechanism for circadian prolactin transcription: rhythmic NONO and SFPQ recruitment to HLTF. FASEB J 2011;25:2740-56.
47. Siep M, Sleddens-Linkels E, Mulders S, et al. Basic helix-loop-helix transcription factor Tcfl5 interacts with the Calmegin gene promoter in mouse spermatogenesis. Nucleic Acids Res 2004;32:6425-36.
48. Lee DK, Kurihara I, Jeong JW, et al. Suppression of ERalpha activity by COUP-TFII is essential for successful implantation and decidualization. Mol Endocrinol 2010;24:930-40.
49. Hayashi A, Tanabe A, Kawabe S, et al. Dienogest increases the progesterone receptor isoform B/A ratio in patients with ovarian endometriosis. J Ovarian Res 2012;5:31.
50. Low KG, Nielsen CP, West NB, et al. Proenkephalin gene expression in the primate uterus: regulation by estradiol in the endometrium. Mol Endocrinol 1989;3:852-7.
51. Ramachandran S, Song M, Murphy AA, Parthasarathy S. Expression of scavenger receptor class B1 in endometrium and endometriosis. J Clin Endocrinol Metab 2001;86:3924-8.
52. Chen JI, Hannan NJ, Mak Y, et al. Proteomic characterization of midproliferative and midsecretory human endometrium. J Proteome Res 2009;8:2032-44.
53. Torres PB, Florio P, Ferreira MC, et al. Deranged expression of follistatin and follistatin-like protein in women with ovarian endometriosis. Fertil Steril 2007;88:200-5.
54. Zhou WD, Yang HM, Wang Q, et al. SB203580, a p38 mitogenactivated protein kinase inhibitor, suppresses the development of endometriosis by down-regulating proinflammatory cytokines and proteolytic factors in a mouse model. Hum Reprod 2010;25:3110-6.
55. Konno R, Fujiwara H, Suzuki M. Effectiveness of leukotriene receptor antagonists for dysmenorrhea of endometriosis. Fam Med 2004;36:8-9.
56. Carson DD, Lagow E, Thathiah A, et al. Changes in gene expression during the early to mid-luteal (receptive phase) transition in human endometrium detected by high-density microarray screening. Mol Hum Reprod 2002;8:871-9.
57. Chaen T, Konno T, Egashira M, et al. Estrogen-dependent uterine secretion of osteopontin activates blastocyst adhesion competence. PLoS One 2012;7:e48933.
58. Bellelis P, Barbeiro DF, Rizzo LV, et al. Transcriptional changes in the expression of chemokines related to natural killer and T-regulatory cells in patients with deep infiltrative endometriosis. Fertil Steril 2013;99:1987-93.
59. Podgaec S, Abrao MS, Dias Jr JA, et al. Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 2007;22:1373-9.
60. Alizadeh Z, Shokrzadeh N, Saidijam M, Sanoee MF. Semiquantitative analysis of HOXA11, leukemia inhibitory factor and basic transcriptional element binding protein 1 mRNA expression in the mid-secretory endometrium of patients with endometriosis. Iran Biomed J 2011;15:66-72.
61. Cox KE, Piva M, Sharpe-Timms KL. Differential regulation of matrix metalloproteinase-3 gene expression in endometriotic lesions compared with endometrium. Biol Reprod 2001;65:1297-303.
62. Machado DE, Berardo PT, Palmero CY, Nasciutti LE. Higher expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 (Flk-1) and metalloproteinase-9 (MMP-9) in a rat model of peritoneal endometriosis is similar to cancer diseases. J Exp Clin Cancer Res 2010;29:4.
63. Uzan C, Cortez A, Dufournet C, et al. 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; 445:603-9.
64. Shimoya K, Moriyama A, Ogata I, et al. Increased concentrations of secretory leukocyte protease inhibitor in peritoneal fluid of women with endometriosis. Mol Hum Reprod 2000;6:829-34.
65. Soares SR, Martínez-Varea A, Hidalgo-Mora JJ, Pellicer A. Pharmacologic therapies in endometriosis: a systematic review. Fertil Steril 2012;98:529-55.
66. Penna I, Du H, Ferriani R, Taylor HS. Calpain5 expression is decreased in endometriosis and regulated by HOXA10 in human endometrial cells. Mol Hum Reprod 2008;14:613-8.
67. Vestergaard AL, Knudsen UB, Munk T, et al. Transcriptional expression of type-I interferon response genes and stability of housekeeping genes in the human endometrium and endometriosis. Mol Hum Reprod 2011;17:243-54.
68. Kao LC, Germeyer A, Tulac S, et al. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-81.
69. Fukuda MN, Sugihara K. Trophinin in cell adhesion and signal transduction. Front Biosci (Elite Ed) 2012;4:342-50.
70. van den Berg LL, Crane LM, van Oosten M, et al. Analysis of biomarker expression in severe endometriosis and determination of possibilities for targeted intraoperative imaging. Int J Gynaecol Obstet 2013;121:35-40.
71. Vouk K, Smuc T, Guggenberger C, et al. Novel estrogen-related genes and potential biomarkers of ovarian endometriosis identified by differential expression analysis. J Steroid Biochem Mol Biol 2011;125:231-42.
72. Albertsen HM, Chettier R, Farrington P, Ward K. Genome-wide association study link novel loci to endometriosis. PLoS One 2013; 8:e58257.
73. Van Langendonckt A, Casanas-Roux F, Dolmans MM, Donnez J. Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis. Fertil Steril 2002;77:561-70.
74. Ota H, Igarashi S, Kato N, Tanaka T. Aberrant expression of glutathione peroxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis. Fertil Steril 2000;74:313-8.
75. Popiela TJ, Klimek M, Wicherek L, et al. The characterization of the exposure to immune mediated apoptosis and the regulation of immune cytotoxic activity in the environment of a neoplasm and in decidua. Neuro Endocrinol Lett 2006;27:779-85.
76. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 1991;266:11632-9.
77. De Oliveira LG, Lash GE, Murray-Dunning C, et al. Role of interleukin 8 in uterine natural killer cell regulation of extravillous trophoblast cell invasion. Placenta 2010;31:595-601.
78. Singh MN, Stringfellow HF, Taylor SE, et al. Elevated expression of CYP1A1 and gamma-SYNUCLEIN in human ectopic (ovarian) endometriosis compared with eutopic endometrium. Mol Hum Reprod 2008;14:655-63.
79. Painter JN, Nyholt DR, Morris A, et al. High-density fine-mapping of a chromosome 10q26 linkage peak suggests association between endometriosis and variants close to CYP2C19. Fertil Steril 2011;95: 2236-40.
80. Izawa M, Taniguchi F, Terakawa N, Harada T. Epigenetic aberration of gene expression in endometriosis. Front Biosci (Elite Ed) 2013; E5:900-10.
81. Wang H, Xie H, Sun X, et al. Stage-specific integration of maternal and embryonic peroxisome proliferator-activated receptor delta signaling is critical to pregnancy success. J Biol Chem 2007;282: 37770-82.
82. Kavoussi SK, Witz CA, Binkley PA, et al. Peroxisome-proliferator activator receptor-gamma activation decreases attachment of endometrial cells to peritoneal mesothelial cells in an in vitro model of the early endometriotic lesion. Mol Hum Reprod 2009;15: 687-92.
83. Rižner TL. Enzymes of the AKR1B and AKR1C subfamilies and uterine diseases. Front Pharmacol 2012;3:34.
84. Agostino A, Invernizzi F, Tiveron C, et al. Constitutive knockout of Surf1 is associated with high embryonic lethality, mitochondrial disease and cytochrome c oxidase deficiency in mice. Hum Mol Genet 2003;12:399-413.
85. Liu AX, He WH, Yin LJ, et al. Sustained endoplasmic reticulum stress as a cofactor of oxidative stress in decidual cells from patients with early pregnancy loss. J Clin Endocrinol Metab 2011;96: E493-7.
86. Shelton JM, Lee MH, Richardson JA, Patel SB. Microsomal triglyceride transfer protein expression during mouse development. J Lipid Res 2000;41:532-7.
87. Gao F, Ma X, Rusie A, et al. Epigenetic changes through DNA methylation contribute to uterine stromal cell decidualization. Endocrinology 2012;153:6078-90.
88. Novella-Maestre E, Carda C, Noguera I, et al. Dopamine agonist administration causes a reduction in endometrial implants through modulation of angiogenesis in experimentally induced endometriosis. Hum Reprod 2009;24:1025-35.
89. Riesewijk A, Martín J, van Os R, et al. Gene expression profiling of human endometrial receptivity on days LH+2 versus LH+7 by microarray technology. Mol Hum Reprod 2003;9:253-64.
90. Fazleabas AT. Progesterone resistance in a baboon model of endometriosis. Semin Reprod Med 2010;28:75-80.
91. May KE, Villar J, Kirtley S, et al. Endometrial alterations in endometriosis: a systematic review of putative biomarkers. Hum Reprod Update 2011;17:637-53.