Hypoxia: The force of endometriosis

Wu, Meng‐Hsing; Hsiao, Kuei‐Yang; Tsai, Shaw‐Jenq

doi:10.1111/jog.13900

Cited by 88Endometriosis Research and TreatmentEctopic Pregnancy Diagnosis and ManagementReproductive Biology and Fertility

Hypoxia: The force of endometriosis

Wu, Meng‐Hsing, Hsiao, Kuei‐Yang, Tsai, Shaw‐Jenq·2019·Journal of Obstetrics and Gynaecology Research

DOI 10.1111/jog.13900

Open this paper in CoChat — free account

Abstract

Aim: Summarize recent findings of how hypoxia regulates numerous important processes to facilitate the implantation, proliferation and progression of ectopic endometriotic lesions. Methods: Most up‐to‐date evidences about how hypoxia contributes to the disease pathogenesis of endometriosis and potential therapeutic approaches were collected by conducting a comprehensive search of medical literature electronic databases. Quality of data was analyzed by experienced experts including gynecologist and basic scientists. Results: Uterus is a highly vascularized organ, which makes endometrial cells constantly expose to high concentration of oxygen. When endometrial tissues shed off from the eutopic uterus and retrograde to the peritoneal cavity, they face severe hypoxic stress. Even with successful implantation to ovaries or peritoneum, the hypoxic stress remains as a critical issue because endometrial cells are used to live in the well‐oxygenated environment. Under the hypoxia condition, cells undergo epigenetic modulation and evolve several survival processes including steroidogenesis, angiogenesis, inflammation and metabolic switch. The complex gene regulatory network driven by hypoxia ensures endometriotic cells can survive under the hostile peritoneal microenvironment. Conclusion: Hypoxia plays critical roles in promoting pathological processes to facilitate the development of endometriosis. Targeting hypoxia‐mediated gene network represents an alternative approach for the treatment of endometriosis.

Integrity signals

Registry

Crossref · 10.1111/jog.13900

Cites

102 of 102 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Hypoxia, occurring to menstrual debris devoid of blood supply when regurgitated into peritoneal cavity, can dramatically turn endometrial stromal cells into endometriotic counterpart, causing completely different phenotypes.
“Recent studies have shown that hypoxia, occurred to menstrual debris that is devoid of blood supply when regurgitated into the peritoneal cavity, can dramatically turn endometrial stromal cells into endometriotic counterpart, causing completely different phenotypes39.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [39]
Activated platelets can directly induce a hypoxia state in endometriotic lesions, which subsequently cause further phenotypic changes.
“Third, our study provides evidence that activated platelets can directly induce a hypoxia state in endometriotic lesions, which subsequently cause further phenotypic changes39.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [39]

Untitled work
Bartel (2004) · doi:10.1016/s0092-8674(04)00045-5 · Cited by 34,714 · see citing works
Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1
Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., et al. (2009) · Science · doi:10.1126/science.1170116 · Cited by 5,836 · see citing works
Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine
Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C., & Zhang, Y. (2011) · Science · doi:10.1126/science.1210597 · Cited by 3,451 · see citing works
Requirement of Vascular Integrin α <sub>v</sub> β <sub>3</sub> for Angiogenesis
Brooks, P. C., Clark, R. A. F., & Cheresh, D. A. (1994) · Science · doi:10.1126/science.7512751 · Cited by 3,020 · see citing works
Tet-Mediated Formation of 5-Carboxylcytosine and Its Excision by TDG in Mammalian DNA
He, Y., Li, B.-Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., et al. (2011) · Science · doi:10.1126/science.1210944 · Cited by 2,776 · see citing works
RNA Maps Reveal New RNA Classes and a Possible Function for Pervasive Transcription
Kapranov, P., Cheng, J., Dike, S., Nix, D. A., Duttagupta, R., Willingham, A. T., Stadler, P. F., Jana Hertel, A., Jörg Hackermüller, A., Hofacker, I. L., et al. (2007) · Science · doi:10.1126/science.1138341 · Cited by 2,519 · see citing works
Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334 · see citing works
Estrogen Receptor Null Mice: What Have We Learned and Where Will They Lead Us?
Couse, J. F., & Korach, K. S. (1999) · Endocrine Reviews · doi:10.1210/edrv.20.3.0370 · Cited by 2,045 · see citing works
Biological Action of Leptin as an Angiogenic Factor
Sierra-Honigmann, M. R., Nath, A. K., Murakami, C., García‐Cardeña, G., Papapetropoulos, A., Sessa, W. C., Madge, L. A., Schechner, J. S., Schwabb, M. B., Polverini, P. J., et al. (1998) · Science · doi:10.1126/science.281.5383.1683 · Cited by 1,371 · see citing works
Definition of Two Angiogenic Pathways by Distinct α v Integrins
Friedlander, M., Brooks, P. C., Shaffer, R. W., Kincaid, C. M., Varner, J. A., & Cheresh, D. A. (1995) · Science · doi:10.1126/science.270.5241.1500 · Cited by 1,310 · see citing works
Untitled work
(1984) · PubMed · Cited by 997 · see citing works
Hypoxia-Inducible Factor 1 (HIF-1) Pathway
Semenza, G. L. (2007) · Science s STKE · doi:10.1126/stke.4072007cm8 · Cited by 942 · see citing works
TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm
Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y., & DePamphilis, M. L. (2001) · Genes & Development · doi:10.1101/gad.888601 · Cited by 719 · see citing works
Cancer-associated mutations in endometriosis without cancer
Anglesio, M. S., Papadopoulos, N., Ayhan, A., Nazeran, T. M., Noë, M., Horlings, H. M., Lum, A., Jones, S., Senz, J., Seckin, T., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1614814 · Cited by 628 · see citing works
Potential role of leptin in angiogenesis: leptin induces endothelial cell proliferation and expression of matrix metalloproteinases in vivo and in vitro
Park, H., Kwon, H. M., Lim, H. J., Hong, B., Lee, J. Y., Park, B. E., Jang, Y., Cho, S. Y., & Kim, H. S. (2001) · Experimental & Molecular Medicine · doi:10.1038/emm.2001.17 · Cited by 464 · see citing works
Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF
Cao, R., Brakenhielm, E., Wahlestedt, C., Thyberg, J., & Cao, Y. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.101564798 · Cited by 446 · see citing works
Clonal Expansion and Diversification of Cancer-Associated Mutations in Endometriosis and Normal Endometrium
Suda, K., Nakaoka, H., Yoshihara, K., Ishiguro, T., Tamura, R., Mori, Y., Yamawaki, K., Adachi, S., Takahashi, T., Kase, H., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.037 · Cited by 414 · see citing works
Circular RNA – New member of noncoding RNA with novel functions
Hsiao, K., Sun, H. S., & Tsai, S. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370217708978 · Cited by 393 · see citing works
Self-citation
The unfolding stories of GPR30, a new membrane-bound estrogen receptor
Maggiolini, M., & Picard, D. (2010) · Journal of Endocrinology · doi:10.1677/joe-09-0242 · Cited by 360 · see citing works
Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis
McLaren, J. F., Prentice, A., Jones, D. S., & Smith, S. K. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019023 · Cited by 350 · see citing works
Promoter Methylation Regulates Estrogen Receptor 2 in Human Endometrium and Endometriosis1
Xue, Q., Lin, Z., Cheng, Y.-H., Huang, C.-C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.061804 · Cited by 346 · see citing works
Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis
Kishimoto, K., Liu, S.-M., Tsuji, T., Olson, K., & Hu, G. (2005) · Oncogene · doi:10.1038/sj.onc.1208223 · Cited by 325 · see citing works
Promoter Hypermethylation of Progesterone Receptor Isoform B (PR-B) in Endometriosis
Wu, Y., Strawn, E., Basir, Z., Halverson, G., & Guo, S. (2006) · Epigenetics · doi:10.4161/epi.1.2.2766 · Cited by 323 · see citing works
Pathophysiological implications of hypoxia in human diseases
Chen, P.-S., Chiu, W.-T., Hsu, P.-L., Lin, S.-C., Peng, I.-C., Wang, C.-Y., & Tsai, S.-J. (2020) · Journal of Biomedical Science · doi:10.1186/s12929-020-00658-7 · Cited by 318 · see citing works
Self-citation
Osteopontin induces angiogenesis through activation of PI3K/AKT and ERK1/2 in endothelial cells
Dai, J., Peng, L., Fan, K., Wang, H., Wei, R.-L., Ji, G., Cai, J., Lu, B., Li, B., Zhang, D., et al. (2009) · Oncogene · doi:10.1038/onc.2009.189 · Cited by 317 · see citing works
The role of microRNAs in endometriosis and associated reproductive conditions
Ohlsson Teague, E. M. C., Print, C. G., & Hull, M. L. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmp034 · Cited by 309 · see citing works
Prostaglandin E2 Stimulates Aromatase Expression in Endometriosis-Derived Stromal Cells
Noble, L. S. (1997) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.2.600 · Cited by 301 · see citing works
Aberrant methylation at HOXA10 may be responsible for its aberrant expression in the endometrium of patients with endometriosis
Wu, Y., Halverson, G., Basir, Z., Strawn, E., Yan, P., & Guo, S.-W. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.01.034 · Cited by 283 · see citing works
Untitled work
(1987) · PubMed · Cited by 275 · see citing works
Endometriosis in association with uterine anomaly
Sanfilippo, J. S., Wakim, N. G., Schikler, K. N., & Yussman, M. A. (1986) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(86)90389-3 · Cited by 270 · see citing works
Osteopontin Promotes Vascular Endothelial Growth Factor–Dependent Breast Tumor Growth and Angiogenesis via Autocrine and Paracrine Mechanisms
Chakraborty, G., Jain, S., & Kundu, G. C. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-2126 · Cited by 267 · see citing works
Aromatase and other steroidogenic genes in endometriosis: translational aspects.
Attar, E., & Bulun, S. E. (2006) · Human Reproduction Update · doi:10.1093/humupd/dmi034 · Cited by 255 · see citing works
Vascular Endothelial Growth Factor Expression in Human Endometrium Is Regulated by Hypoxia
Sharkey, A., Day, K., McPherson, A., Malik, S., Licence, D., Smith, S. K., & Jones, D. S. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.1.6229 · Cited by 228 · see citing works
Transcriptional activation of steroidogenic factor-1 by hypomethylation of the 5′ CpG island in endometriosis
Xue, Q., Lin, Z., Yin, P., Milad, M. P., Cheng, Y.-H., Confino, E., Reierstad, S., & Bulun, S. E. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0494 · Cited by 219 · see citing works
Stimulation of Aromatase P450 Promoter (II) Activity in Endometriosis and Its Inhibition in Endometrium Are Regulated by Competitive Binding of Steroidogenic Factor-1 and Chicken Ovalbumin Upstream Promoter Transcription Factor to the Same cis-Acting Element
Zeitoun, K., Takayama, K., Michael, M. D., & Bulun, S. E. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.2.0229 · Cited by 216 · see citing works
Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis
Dyson, M. T., Roqueiro, D., Monsivais, D., Ercan, C. M., Pavone, M. E., Brooks, D. C., Kakinuma, T., Ono, M., Jafari, N., Dai, Y., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004158 · Cited by 211 · see citing works
Prostaglandin E2 Via Steroidogenic Factor-1 Coordinately Regulates Transcription of Steroidogenic Genes Necessary for Estrogen Synthesis in Endometriosis
Attar, E., Tokunaga, H., Imir, G., Yilmaz, M. B., Redwine, D., Putman, M., Gurates, B., Attar, R., Yaegashi, N., Hales, D. B., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1180 · Cited by 207 · see citing works
Site-directed mutagenesis of histidine-13 and histidine-114 of human angiogenin. Alanine derivatives inhibit angiogenin-induced angiogenesis
Shapiro, R., & Vallée, B. L. (1989) · Biochemistry · doi:10.1021/bi00444a038 · Cited by 193 · see citing works
Transforming Growth Factor-β Induced Warburg-Like Metabolic Reprogramming May Underpin the Development of Peritoneal Endometriosis
Young, V. J., Brown, J. K., Maybin, J. A., Saunders, P. T. K., Duncan, W. C., & Horne, A. W. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1026 · Cited by 168 · see citing works
2-Methoxyestradiol Inhibits Hypoxia-Inducible Factor-1α and Suppresses Growth of Lesions in a Mouse Model of Endometriosis
Becker, C. M., Rohwer, N., Funakoshi, T., Cramer, T., Bernhardt, W., Birsner, A. E., Folkman, J., & D’Amato, R. J. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.061244 · Cited by 167 · see citing works
Vascular endothelial growth factor and interleukin-6 in peritoneal fluid of women with endometriosis
Mahnke, J. L., Dawood, M. Y., & Huang, J.-C. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00466-5 · Cited by 165 · see citing works
Oestrogen receptor (ER)-alpha and ER- isoforms in normal endometrial and endometriosis-derived stromal cells
Brandenberger, A. W. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.7.651 · Cited by 165 · see citing works
MicroRNA expression profile in endometriosis: its relation to angiogenesis and fibrinolytic factors
Braza-Boïls, A., Marí-Alexandre, J., Gilabert, J., Sánchez-Izquierdo, D., España, F., Estellés, A., & Gilabert-Estellés, J. (2014) · Human Reproduction · doi:10.1093/humrep/deu019 · Cited by 164 · see citing works
Stimulating the GPR30 estrogen receptor with a novel tamoxifen analogue activates SF-1 and promotes endometrial cell proliferation
Lin, B. C., Suzawa, M., Blind, R. D., Tobias, S. C., Bulun, S. E., Scanlan, T. S., & Ingraham, H. A. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-1622 · Cited by 157 · see citing works
Regulation of steroidogenic acute regulatory protein expression and progesterone production in endometriotic stromal cells.
Tsai, S.-J., Wu, M.-H., Lin, C.-C., Sun, H. S., & Chen, H.-M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.12.8082 · Cited by 155 · see citing works
Self-citation
Fgf-9 is required for angiogenesis and osteogenesis in long bone repair
Behr, B., Leucht, P., Longaker, M. T., & Quarto, N. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003317107 · Cited by 144 · see citing works
Role of estrogen receptor signaling required for endometriosis-like lesion establishment in a mouse model.
Burns, K. A., Rodriguez, K., Hewitt, S., Janardhan, K., Young, S., & Korach, K. (2012) · Endocrinology · doi:10.1210/en.2012-1294 · Cited by 143 · see citing works
Clinical relevance of the baboon as a model for the study of endometriosis
D’Hooghe, T. M. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00277-x · Cited by 137 · see citing works
Hypoxia-Induced MicroRNA-20a Expression Increases ERK Phosphorylation and Angiogenic Gene Expression in Endometriotic Stromal Cells
Lin, S., Wang, C.-C., Wu, M., Yang, S., Li, Y.-H., & Tsai, S. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1450 · Cited by 131 · see citing works
Self-citation
Distinct Regulation of Cyclooxygenase-2 by Interleukin-1β in Normal and Endometriotic Stromal Cells
Wu, M., Wang, C.-A., Lin, C.-C., Chen, L.-C., Chang, W., & Tsai, S. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1612 · Cited by 128 · see citing works
Self-citation
Distinct mechanisms regulate cyclooxygenase-1 and -2 in peritoneal macrophages of women with and without endometriosis
Wu, M. (2002) · Molecular Human Reproduction · doi:10.1093/molehr/8.12.1103 · Cited by 127 · see citing works
Self-citation
Expression of oestrogen receptor-alpha and -beta in ovarian endometriomata
Fujimoto, J. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.8.742 · Cited by 123 · see citing works
Aberrant Expression of Leptin in Human Endometriotic Stromal Cells Is Induced by Elevated Levels of Hypoxia Inducible Factor-1α
Wu, M., Chen, K., Lin, S., Lgu, C.-W., & Tsai, S. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.060477 · Cited by 120 · see citing works
Self-citation
RNA biology of angiogenin: Current state and perspectives
Lyons, S. M., Fay, M. M., Akiyama, Y., Anderson, P., & Ivanov, P. (2017) · RNA Biology · doi:10.1080/15476286.2016.1272746 · Cited by 120 · see citing works
Inhibition of CD36-Dependent Phagocytosis by Prostaglandin E2 Contributes to the Development of Endometriosis
Chuang, P., Lin, Y.-J., Wu, M., Wing, L.-Y. C., Shoji, Y., & Tsai, S. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090551 · Cited by 116 · see citing works
Self-citation
The G Protein-coupled Receptor 30 Is Up-regulated by Hypoxia-inducible Factor-1α (HIF-1α) in Breast Cancer Cells and Cardiomyocytes
Recchia, A. G., Francesco, E. M. D., Vivacqua, A., Sisci, D., Panno, M. L., Andò, S., & Maggiolini, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.172247 · Cited by 116 · see citing works
Transactivation of steroidogenic acute regulatory protein in human endometriotic stromal cells is mediated by the prostaglandin EP2 receptor.
Sun, H. S., Hsiao, K.-Y., Hsu, C.-C., Wu, M.-H., & Tsai, S.-J. (2003) · Endocrinology · doi:10.1210/en.2003-0289 · Cited by 114 · see citing works
Self-citation
Hypoxia-Inducible Factor-1α Expression in Human Endometrium and Its Regulation by Prostaglandin E-Series Prostanoid Receptor 2 (EP2)
Critchley, H., Osei, J., Henderson, T. A., Boswell, L., Sales, K. J., Jabbour, H. N., & Hirani, N. (2005) · Endocrinology · doi:10.1210/en.2005-1153 · Cited by 113 · see citing works
Aberrant Endometrial DNA Methylome and Associated Gene Expression in Women with Endometriosis
Houshdaran, S., Nezhat, C. R., Vo, K. C., Zelenko, Z., Irwin, J. C., & Giudice, L. C. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.140434 · Cited by 113 · see citing works
Fibroblast Growth Factor-9 Is an Endometrial Stromal Growth Factor
Tsai, S., Wu, M., Chen, H., Chuang, P.-C., & Wing, L. C. (2002) · Endocrinology · doi:10.1210/endo.143.7.8900 · Cited by 109 · see citing works
Self-citation
Suppression of Matrix Metalloproteinase-9 by Prostaglandin E2 in Peritoneal Macrophage Is Associated with Severity of Endometriosis
Wu, M., Shoji, Y., Wu, M., Chuang, P., Lin, C.-C., Huang, M., & Tsai, S. (2005) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61195-9 · Cited by 108 · see citing works
Self-citation
G Protein-Coupled Estrogen Receptor (GPER) Expression in Normal and Abnormal Endometrium
Plante, B. J., Lessey, B. A., Taylor, R. N., Wang, W., Bagchi, M. K., Yuan, L., Scotchie, J. G., Fritz, M. A., & Young, S. L. (2012) · Reproductive Sciences · doi:10.1177/1933719111431000 · Cited by 107 · see citing works
MiR-199a attenuates endometrial stromal cell invasiveness through suppression of the IKK /NF- B pathway and reduced interleukin-8 expression
Dai, L., Gu, L., & Di, W. J. (2011) · Molecular Human Reproduction · doi:10.1093/molehr/gar066 · Cited by 99 · see citing works
Cyr61, a deregulated gene in endometriosis
Absenger, Y. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah053 · Cited by 95 · see citing works
Enhancer of Zeste homolog 2 (EZH2) induces epithelial-mesenchymal transition in endometriosis
Zhang, Q., Dong, P., Liu, X., Sakuragi, N., & Guo, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-06920-7 · Cited by 89 · see citing works
miR-503, a microRNA epigenetically repressed in endometriosis, induces apoptosis and cell-cycle arrest and inhibits cell proliferation, angiogenesis, and contractility of human ovarian endometriotic stromal cells
Hirakawa, T., Nasu, K., Abe, W., Aoyagi, Y., Okamoto, M., Kai, K., Takebayashi, K., & Narahara, H. (2016) · Human Reproduction · doi:10.1093/humrep/dew217 · Cited by 87 · see citing works
Down-Regulation of the Histone Methyltransferase EZH2 Contributes to the Epigenetic Programming of Decidualizing Human Endometrial Stromal Cells
Grimaldi, G., Christian, M., Steel, J. H., Henriet, P., POUTANEN, M. H., & Brosens, J. J. (2011) · Molecular Endocrinology · doi:10.1210/me.2011-1139 · Cited by 84 · see citing works
Induced Endometriosis in the Baboon (Papio anubis) Increases the Expression of the Proangiogenic Factor CYR61 (CCN1) in Eutopic and Ectopic Endometria1
Gashaw, I., Hastings, J. M., Jackson, K. S., Winterhager, E., & Fazleabas, A. T. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.105.049320 · Cited by 81 · see citing works
Epigenetic regulation of the pathological process in endometriosis
Hsiao, K., Wu, M., & Tsai, S. (2017) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12047 · Cited by 79 · see citing works
Self-citation
Increased leptin expression in endometriosis cells is associated with endometrial stromal cell proliferation and leptin gene up-regulation
Wu, M.-H. (2002) · Molecular Human Reproduction · doi:10.1093/molehr/8.5.456 · Cited by 77 · see citing works
Self-citation
Demethylation of a nonpromoter cytosine-phosphate-guanine island in the aromatase gene may cause the aberrant up-regulation in endometriotic tissues
Izawa, M., Taniguchi, F., Uegaki, T., Takai, E., Iwabe, T., Terakawa, N., & Harada, T. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.06.024 · Cited by 73 · see citing works
Expression and Mitogenic Effect of Fibroblast Growth Factor-9 in Human Endometriotic Implant Is Regulated by Aberrant Production of Estrogen
Wing, L. C., Chuang, P.-C., Wu, M., Chen, H., & Tsai, S. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030597 · Cited by 65 · see citing works
Self-citation
Ablation of Leptin Signaling Disrupts the Establishment, Development, and Maintenance of Endometriosis-Like Lesions in a Murine Model
Styer, A. K., Sullivan, B. T., Puder, M., Arsenault, D. A., Petrozza, J. C., Serikawa, T., Chang, S., Hasan, T. G., González, R. R., & Rueda, B. R. (2007) · Endocrinology · doi:10.1210/en.2007-1225 · Cited by 65 · see citing works
Demonstration of Angiogenin in Human Endometrium and Its Enhanced Expression in Endometrial Tissues in the Secretory Phase and the Decidua
Koga, K., Osuga, Y., Tsutsumi, O., Yano, T., Yoshino, O., Takai, Y., Matsumi, H., Hiroi, H., Kugu, K., Momoeda, M., et al. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.11.8038 · Cited by 65 · see citing works
Hypoxia‐inhibited dual‐specificity phosphatase‐2 expression in endometriotic cells regulates cyclooxygenase‐2 expression
Wu, M., Lin, S., Hsiao, K., & Tsai, S. (2011) · The Journal of Pathology · doi:10.1002/path.2963 · Cited by 65 · see citing works
Self-citation
Deoxyribonucleic acid methyltransferases and methyl-CpG-binding domain proteins in human endometrium and endometriosis
van Kaam, K. J. A. F., Delvoux, B., Romano, A., D’Hooghe, T., Dunselman, G. A. J., & Groothuis, P. G. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.01.031 · Cited by 64 · see citing works
Coordination of AUF1 and miR-148a destabilizes DNA methyltransferase 1 mRNA under hypoxia in endometriosis
Hsiao, K.-Y., Wu, M.-H., Chang, N., Yang, S.-H., Wu, C.-W., Sun, H. S., & Tsai, S.-J. (2015) · Molecular Human Reproduction · doi:10.1093/molehr/gav054 · Cited by 64 · see citing works
Self-citation
Pathological functions of hypoxia in endometriosis
Hsiao, K.-Y. (2015) · Frontiers in Bioscience · doi:10.2741/e736 · Cited by 61 · see citing works
Prostaglandin E2 Induces Fibroblast Growth Factor 9 via EP3-Dependent Protein Kinase Cδ and Elk-1 Signaling
Chuang, P., Sun, H. S., Chen, T.-M., & Tsai, S. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00941-06 · Cited by 56 · see citing works
Self-citation
Inhibition of dual specificity phosphatase-2 by hypoxia promotes interleukin-8-mediated angiogenesis in endometriosis
Hsiao, K., Chang, N., Lin, S., Li, Y.-H., & Wu, M. (2014) · Human Reproduction · doi:10.1093/humrep/deu255 · Cited by 55 · see citing works
Self-citation
Suppression of COUP-TFII by proinflammatory cytokines contributes to the pathogenesis of endometriosis
Lin, S.-C., Li, Y.-H., Wu, M.-H., Chang, Y.-F., Lee, D.-K., Tsai, S. Y., Tsai, M.-J., & Tsai, S.-J. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-3717 · Cited by 52 · see citing works
Self-citation
Expression of hypoxia-inducible factors in human endometrium and suppression of matrix metalloproteinases under hypoxic conditions do not support a major role for hypoxia in regulating tissue breakdown at menstruation
Zhang, J. (2002) · Human Reproduction · doi:10.1093/humrep/17.2.265 · Cited by 52 · see citing works
ORIGINAL ARTICLE: Endometrial Osteopontin mRNA Expression and Plasma Osteopontin Levels are Increased in Patients with Endometriosis
Cho, S., Ahn, Y. S., Choi, Y. S., Seo, S. K., Nam, A., Kim, H. Y., Kim, J., Park, K. H., Cho, D. J., & Lee, B. S. (2009) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2009.00692.x · Cited by 51 · see citing works
Selective inhibition of prostaglandin E2 receptors EP2 and EP4 modulates DNA methylation and histone modification machinery proteins in human endometriotic cells
Arosh, J. A., Lee, J., Starzinski‐Powitz, A., & Banu, S. K. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.03.023 · Cited by 49 · see citing works
Hypoxia responsive miR-210 promotes cell survival and autophagy of endometriotic cells in hypoxia.
Tx, X., Sz, Z., Dong, M., & Xr, Y. (2016) · PubMed · Cited by 49 · see citing works
Hypoxia and estrogen are functionally equivalent in breast cancer-endothelial cell interdependence
George, A. L., Rajoria, S., Suriano, R., Mittleman, A., & Tiwari, R. K. (2012) · Molecular Cancer · doi:10.1186/1476-4598-11-80 · Cited by 47 · see citing works
Suppression of annexin A2 by prostaglandin E2 impairs phagocytic ability of peritoneal macrophages in women with endometriosis
Wu, M., Chuang, P., Lin, Y.-J., & Tsai, S. (2013) · Human Reproduction · doi:10.1093/humrep/det003 · Cited by 45 · see citing works
Self-citation
Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells
Qi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
The Mammalian Target of Rapamycin-p70 Ribosomal S6 Kinase but Not Phosphatidylinositol 3-Kinase-Akt Signaling Is Responsible for Fibroblast Growth Factor-9-induced Cell Proliferation
Wing, L.-Y. C., Chen, H.-M., Chuang, P., Wu, M.-H., & Tsai, S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m411865200 · Cited by 43 · see citing works
Self-citation
MiR-199a inhibits the angiogenic potential of endometrial stromal cells under hypoxia by targeting HIF-1α/VEGF pathway.
Dai, L., Lou, W., Zhu, J., Zhou, X., & Di, W. J. (2015) · PubMed Central · Cited by 42 · see citing works
Targeting hypoxia‐mediated YAP1 nuclear translocation ameliorates pathogenesis of endometriosis without compromising maternal fertility
Lin, S., Lee, H.-C., Hou, P., Fu, J.-L., Wu, M., & Tsai, S. (2017) · The Journal of Pathology · doi:10.1002/path.4922 · Cited by 40 · see citing works
Self-citation
Induction of Pyruvate Dehydrogenase Kinase 1 by Hypoxia Alters Cellular Metabolism and Inhibits Apoptosis in Endometriotic Stromal Cells
Lee, H.-C., Lin, S., Wu, M., & Tsai, S. (2018) · Reproductive Sciences · doi:10.1177/1933719118789513 · Cited by 39 · see citing works
Self-citation
Targeting Anthrax Toxin Receptor 2 Ameliorates Endometriosis Progression
Lin, S., Lee, H.-C., Hsu, C.-T., Huang, Y.-H., Li, W.-N., Hsu, P., Wu, M., & Tsai, S. (2019) · Theranostics · doi:10.7150/thno.30655 · Cited by 38 · see citing works
Self-citation
Aberrant histone modification in endometriosis
Nasu, K. (2014) · Frontiers in bioscience · doi:10.2741/4276 · Cited by 34 · see citing works
Estrogen receptor expression affected by hypoxia inducible factor-1α in stromal cells from patients with endometriosis
Wu, M.-H., Lu, C.-W., Chang, F.-M., & Tsai, S.-J. (2012) · Taiwanese Journal of Obstetrics and Gynecology · doi:10.1016/j.tjog.2012.01.010 · Cited by 33 · see citing works
Self-citation
Effects of histone methyltransferase inhibition in endometriosis†
Colón-Caraballo, M., Torres-Reverón, A., Soto-Vargas, J. L., Young, S. L., Lessey, B. A., Mendoza, A., Urrutia, R. A., & Flores, I. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy030 · Cited by 32 · see citing works
Loss of dual‐specificity phosphatase‐2 promotes angiogenesis and metastasis via up‐regulation of interleukin‐8 in colon cancer
Lin, S., Hsiao, K., Chang, N., Hou, P., & Tsai, S. (2016) · The Journal of Pathology · doi:10.1002/path.4868 · Cited by 31 · see citing works
Self-citation
Congenital Atresia of the Uterine Cervix With Pelvic Endometriosis
Nunley, W. C. (1980) · Archives of Surgery · doi:10.1001/archsurg.1980.01380060055015 · Cited by 29 · see citing works
Suppression of COUP-TFII upregulates angiogenin and promotes angiogenesis in endometriosis
Fu, J.-L., Hsiao, K., Lee, H.-C., Li, W.-N., Chang, N., Wu, M., & Tsai, S. (2018) · Human Reproduction · doi:10.1093/humrep/dey220 · Cited by 26 · see citing works
Self-citation
ORIGINAL ARTICLE: Leptin on Peritoneal Macrophages of Patients with Endometriosis
Wu, M., Huang, M., Chang, F., & Tsai, S. (2009) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2009.00779.x · Cited by 25 · see citing works
Self-citation
The Expression Status of G Protein-Coupled Receptor GPR30 Is Associated with the Clinical Characteristics of Endometriosis
Yuguchi, H., Tanabe, A., Hayashi, A., Tanaka, Y., Okuda, K., Yamashita, Y., Terai, Y., & Ohmichi, M. (2013) · Endocrine Research · doi:10.3109/07435800.2013.774011 · Cited by 20 · see citing works
Endocrine targets of hypoxia-inducible factors
Lee, H.-C., & Tsai, S. (2017) · Journal of Endocrinology · doi:10.1530/joe-16-0653 · Cited by 20 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells
Qi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
Long noncoding RNAs in endometriosis: Biological functions, expressions, and mechanisms
Wang, X., Zhang, J., Liu, X., Wei, B., & Zhan, L. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.29847 · Cited by 24 · see citing works
Activated Platelets Induce Hypoxia-Inducible Factor-1α Expression Likely through Transforming Growth Factor-β1 in Human Endometrial Stromal Cells
Qi, Q.-M., Guo, S.-W., & Liu, X.-S. (2019) · Reproductive and Developmental Medicine · doi:10.4103/2096-2924.262390 · Cited by 15 · see citing works
“of HIF-1α.[9,12] This may explain why endometrial debris invades and establish endometriotic foci in ectopic sites.”
BackgroundResultInfluential

Familial risk among Japanese patients with endometriosis
Kashima, K., Ishimaru, T., Okamura, H., Suginami, H., Ikuma, K., Murakami, T., Iwashita, M., & Tanaka, K. (2004) · International Journal of Gynecology & Obstetrics · doi:10.1016/s0020-7292(03)00340-0 · Cited by 48 · see citing works
Biases in the endometriosis literature
Koninckx, P. R. (1998) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(98)00200-0 · Cited by 42 · see citing works
Primate Model Research for Endometriosis
Yamanaka, A., Kimura, F., Takebayashi, A., Kita, N., Takahashi, K., & Murakami, T. (2012) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.226.95 · Cited by 33 · see citing works
The Endometriosis - treatment and new methods
Chrzanowski, J., Ostaszewska, S., Augustynowicz, K., Szymańska, E., & Świąder, K. (2023) · Journal of Education Health and Sport · doi:10.12775/jehs.2023.13.04.008
Symptoms based endometriosis prediction using machine learning
Visalaxi, S., & Sudalaimuthu, T. (2021) · Bulletin of Electrical Engineering and Informatics · doi:10.11591/eei.v10i6.3254 · Cited by 15 · see citing works

Authors: Wu, M., Hsiao, K., & Tsai, S.
Affiliations: National Cheng Kung University (TW)
National Chung Hsing University (TW)
Corresponding author: Tsai, Shaw‐Jenq
ORCID: Wu, Meng‐Hsing
Hsiao, Kuei‐Yang
Tsai, Shaw‐Jenq
Venue: Journal of Obstetrics and Gynaecology Research
Publisher: Wiley
Published: 2019-01-07
Volume: 45
Issue: 3
Pages: 532-541
ISSN: 1341-8076 (ISSN-L)
1447-0756
DOI: 10.1111/jog.13900
OpenAlex: W2909794175
Semantic Scholar: 32a95a5b855616a4ca477c00049b3873f2640784
Cited by: 88
References: 102
Citations by year: 2026: 12 · 2025: 9 · 2024: 14 · 2023: 7 · 2022: 8 · 2021: 21 · 2020: 17
FWCI: 1.62
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of obstetrics and gynaecology research (publishedVersion)
PubMed (publishedVersion)
NCHU Institutional Repository CRIS (submittedVersion)
Funders: Ministry of Science and Technology, Taiwan (MOST 106‐2320‐B‐006‐072‐MY3)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Keywords: endometriosis, hypoxia, endometriosis pathogenesis, peritoneal microenvironment, epigenetic regulation, angiogenesis, inflammation, metabolic switch, steroidogenesis, endometriosis treatment
MeSH terms: Hypoxia, Endometriosis, Endometrium, Female, Humans, Neovascularization, Pathologic

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Hypoxia: The force of endometriosis

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks