Transcriptional characterizations of differences between eutopic and ectopic endometrium
Abstract
Endometriosis, defined as the presence of endometrial glandular and stromal cells outside the uterine cavity, is a common gynecological disease with poorly understood pathogenesis. Using laser capture microdissection and a cDNA microarray with 9600 genes/expressed sequence tags (ESTs), we have conducted a comprehensive profiling of gene expression differences between the ectopic and eutopic endometrium taken from 12 women with endometriosis adjusted for menstrual phase and the location of the lesions. With dye-swapping and replicated arrays, we found 904 genes/ESTs that are differentially expressed. We validated the gene expression using real-time RT-PCR. We found that the expression patterns of these genes/ESTs correctly classified the 12 patients into ovarian and nonovarian endometriosis. We identified gene clusters that are location-specific. In addition, we identified several biological themes using Expression Analysis Systematic Explorer. Finally, we identified 79 pathways with over 100 genes with known functions, which include oxidative stress, focal adhesion, Wnt signaling, and MAPK signaling. The identification of these genes and their associated pathways provides new insight. Our findings will stimulate future investigations on molecular genetic mechanisms underlying the pathogenesis of endometriosis.
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Over 1000 genes are differentially expressed between adenomyotic lesions and eutopic endometrium, and close to 1000 genes are differentially expressed between ectopic and eutopic endometrium.
“In fact, over 1000 genes are documented to be differentially expressed between adenomyotic lesions and eutopic endometrium [65] and close to 1000 genes are differentially expressed between ectopic and eutopic endometrium [66].”
From The Pathogenesis of Adenomyosis vis-à-vis Endometriosis (2020) · cites this paper as [66]
Normal endometrial stromal cells are very different in behavior from endometriotic or adenomyotic stromal cells.
“Yet normal endometrial stromal cells are very different in behavior from endometriotic or even adenomyotic stromal cells.”
From The Pathogenesis of Adenomyosis vis-à-vis Endometriosis (2020) · cites this paper as [66]
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Genomic alterations in the endometrium may be a proximate cause for endometriosis
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Atherosclerosis, Oxidation and Endometriosis
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Flagged first, then by citations
1 of the 120 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772 · see citing works
Bulun, S. E., Yilmaz, B. D., Sison, C., Miyazaki, K., Bernardi, L., Liu, S., Kohlmeier, A., Yin, P., Milad, M., & Wei, J. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00242 · Cited by 844 · see citing works
Recurrence of endometriosis and its control
Guo, S.-W. (2009) · Human Reproduction Update · doi:10.1093/humupd/dmp007 · Cited by 719 · see citing works
Boretto, M., Maenhoudt, N., Luo, X., Hennes, A., Boeckx, B., Bui, B. N., Heremans, R., Perneel, L., Kobayashi, H., Zundert, I. V., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0360-z · Cited by 507 · see citing works
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“…inside of the cyst involves very numerous studies and their description is beyond the scope of this review (Cox et al., 2001; Arimoto et al., 2003; Wu et al., 2006; Eyster et al., 2007; Hever et al., 2007; Mettler et al., 2007; Borghese et al., 2008; Zafrakas et al., 2008; Di Carlo et al., 2009;…”
BackgroundAgarwal, A. K., Gupta, S., Sekhon, L. H., & Shah, R. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1964 · Cited by 360 · see citing works
“Cell proliferation and angiogenesis are cellular responses to OS that also may be determined by differential gene expression (246).”
MicroRNA-regulated pathways associated with endometriosis
Ohlsson Teague, E. M. C., Van der Hoek, K. H., Van der Hoek, M. B., Perry, N., Wagaarachchi, P., Robertson, S. A., Print, C. G., & Hull, L. M. (2009) · Molecular Endocrinology · doi:10.1210/me.2008-0387 · Cited by 357 · see citing works
Contemporary genetic technologies and female reproduction
The Evian Annual Reproduction (EVAR) Workshop Group 2010, Fauser, B. C. J. M., Diedrich, K., Bouchard, P., Domı́nguez, F., Matzuk, M. M., Franks, S., Hamamah, S., Simón, C., Devroey, P., et al. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr033 · Cited by 341 · see citing works
“Gene expression microarray studies have identified a number of candidate gene families that may be differentially regulated in endometriosis (Kao et al., 2003; Wu et al., 2006; Burney et al., 2007; Hull et al., 2008; Ohlsson Teague et al., 2009).”
BackgroundPriorities for Endometriosis Research: Recommendations From an International Consensus Workshop
Rogers, P. A. W., D’Hooghe, T. M., Fazleabas, A., Gargett, C. E., Giudice, L. C., Montgomery, G. W., Rombauts, L., Salamonsen, L. A., & Zondervan, K. T. (2009) · Reproductive Sciences · doi:10.1177/1933719108330568 · Cited by 346 · see citing works
Guo, S.-W. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap064 · Cited by 328 · see citing works
“…that many genes are deregulated in endometriosis (Carson et al., 2002; Arimoto et al., 2003; Kao et al., 2003; Matsuzaki et al., 2005; Wu et al., 2006a; Burney et al., 2007; Chand et al., 2007; Eyster et al., 2007; Flores et al., 2007; Hever et al., 2007; Konno et al., 2007; Mettler…”
BackgroundLessey, B. A., & Kim, J. J. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.05.031 · Cited by 286 · see citing works
Wnt Signalling in Implantation, Decidualisation and Placental Differentiation – Review
Sonderegger, S., Pollheimer, J., & Knöfler, M. (2010) · Placenta · doi:10.1016/j.placenta.2010.07.011 · Cited by 265 · see citing works
“Moreover, elevated expression of Wnt7a, Wnt2 and FZD1 was observed in endometriotic tissues [84,85].”
BackgroundPan, Q., Luo, X., Toloubeydokhti, T., & Chegini, N. (2007) · Molecular Human Reproduction · doi:10.1093/molehr/gam063 · Cited by 261 · see citing works
“Conventional and recent large-scale gene expression studies have provided further evidence reflecting the molecular environments that differentiate normal endometrium from disorders affecting this tissue, including endometrial cancer, adenomyosis and endometriosis (Eyster et al., 2002; Kao et al., 2002; Riesewijk et a…”
InfluentialRetractedRole of oxidative stress in endometriosis
Gupta, S., Agarwal, A., Krajcir, N., & Alvarez, J. G. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62026-3 · Cited by 240 · see citing works
Review on the role of glutathione on oxidative stress and infertility
Oyewopo, A. O., Johnson, O., Adeleke, O. S., & Christiania, O. (2017) · JBRA · doi:10.5935/1518-0557.20180003 · Cited by 226 · see citing works
Wu, Y., Strawn, E., Basir, Z., Halverson, G., & Guo, S.-W. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.05.077 · Cited by 193 · see citing works
Self-citationEyster, K. M., Klinkova, O. V., Kennedy, V., & Hansen, K. A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.01.056 · Cited by 192 · see citing works
Immune-inflammation gene signatures in endometriosis patients
Ahn, S. H., Khalaj, K., Young, S. L., Lessey, B. A., Koti, M., & Tayade, C. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.07.005 · Cited by 187 · see citing works
“(52) profiled gene expression differences between Ahn et al.”
BackgroundMechanisms of endometrial progesterone resistance
Al-Sabbagh, M., Lam, E. W.-F., & Brosens, J. J. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.035 · Cited by 183 · see citing works
“Progesterone resistance is also a hallmark of ectopic implants and probably plays a role in ovarian and tubal dysfunction associated with the endometriosis (Bulun, 2009; Wu et al., 2006a,b).”
Endometriosis and Ovarian Cancer
Wei, J., William, J., & Bulun, S. E. (2011) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0b013e31821f4b85 · Cited by 174 · see citing works
“from the gene profiles can differentiate ectopic from eutopic endometria and classify different subtypes of endometrioses from the peritoneum and ovary (72).”
BackgroundEndometrial-Peritoneal Interactions during Endometriotic Lesion Establishment
Hull, M. L., Rangel‐Escareño, C., Godsland, J. M., Doig, J. R., Johnson, C. M., Phillips, S. C., Smith, S. K., Tavaré, S., Print, C. G., & Jones, D. S. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.071128 · Cited by 174 · see citing works
“In addition, laser capture microdissection of glandular epithelial cells from eutopic and ectopic sites identified differentially expressed transcripts associated with several biological processes in epithelial cells.(13) Taken together, these studies have identified large numbers of endometriosisassociated RNA transc…”
BackgroundMolecular and Cellular Pathogenesis of Endometriosis
Klemmt, P. A. B., & Starzinski‐Powitz, A. (2017) · Current Women s Health Reviews · doi:10.2174/1573404813666170306163448 · Cited by 175 · see citing works
Filigheddu, N., Gregnanin, I., Porporato, P. E., Surico, D., Perego, B., Galli, L., Patrignani, C., Graziani, A., & Surico, N. (2010) · Journal of Biomedicine and Biotechnology · doi:10.1155/2010/369549 · Cited by 162 · see citing works
The Pathogenesis of Adenomyosis vis-à-vis Endometriosis
Guo, S.-W. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020485 · Cited by 165 · see citing works
“In fact, over 1000 genes are documented to be differentially expressed between adenomyotic lesions and eutopic endometrium [65] and close to 1000 genes are differentially expressed between ectopic and eutopic endometrium [66].”
BackgroundProgesterone Resistance in Endometriosis: an Acquired Property?
McKinnon, B. D., Mueller, M. D., & Montgomery, G. W. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.05.006 · Cited by 153 · see citing works
Borghese, B., Mondon, F., Noël, J., Fayt, I., Mignot, T.-M., Vaiman, D., & Chapron, C. (2008) · Molecular Endocrinology · doi:10.1210/me.2008-0322 · Cited by 150 · see citing works
Makker, A., Goel, M. M., Das, V., & Ak, A. (2011) · Gynecological Endocrinology · doi:10.3109/09513590.2011.583955 · Cited by 142 · see citing works
“together with microarray data [64] advocate involvement of”
BackgroundGuo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000096047 · Cited by 140 · see citing works
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
Gilabert–Estellés, J., Ramón, L., España, F., Gilabert, J., Vila, V., Regañón, E., Castelló, R., Chirivella, M., & Estellés, A. (2007) · Human Reproduction · doi:10.1093/humrep/dem149 · Cited by 126 · see citing works
“Moreover, in the last few years, several papers based on microarray methods have shown differences in gene expression of MMP components, between normal and eutopic endometrium from women with endo- metriosis (Wu et al., 2006).”
Eutopic endometrium in women with endometriosis: ground zero for the study of implantation defects
Lessey, B., Lebovic, D., & Taylor, R. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333476 · Cited by 113 · see citing works
The mTOR/AKT Inhibitor Temsirolimus Prevents Deep Infiltrating Endometriosis in Mice
Leconte, M., Nicco, C., Ngô, C., Chéreau, C., Chouzenoux, S., Marut, W., Guibourdenche, J., Arkwright, S., Weill, B. J., Chapron, C., et al. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.04.020 · Cited by 115 · see citing works
Liu, X., Zhang, Q., & Guo, S.-W. (2018) · Reproductive Sciences · doi:10.1177/1933719117718275 · Cited by 110 · see citing works
Flores, I., Rivera, E., Ruiz, L. A., Santiago, O. I., Vernon, M. W., & Appleyard, C. B. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.07.1550 · Cited by 107 · see citing works
Takemura, Y., Osuga, Y., Yoshino, O., Hasegawa, A., Hirata, T., Hirota, Y., Nose, E., Morimoto, C., Harada, M., Koga, K., et al. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2486 · Cited by 102 · see citing works
Yotova, I., Quan, P., Leditznig, N., Beer, U., Wenzl, R. J., & Tschugguel, W. (2011) · Human Reproduction · doi:10.1093/humrep/der010 · Cited by 101 · see citing works
Female Infertility and Antioxidants
Sekhon, L. H., Gupta, S., Kim, Y., & Agarwal, A. K. (2010) · Current Women s Health Reviews · doi:10.2174/157340410791321381 · Cited by 101 · see citing works
“Differential gene expression of ectopic and normal endometrial tissue has been identified, including differential gene expression of glutathione-S-transferase, an enzyme in the metabolism of the potent antioxidant glutathione [45].”
BackgroundTai, F.-W., Chang, C. Y., Chiang, J., Lin, W.-C., & Wan, L. (2018) · Journal of Clinical Medicine · doi:10.3390/jcm7110379 · Cited by 99 · see citing works
The role of iron in the pathogenesis of endometriosis
Kobayashi, H., Yamada, Y., Kanayama, S., Furukawa, N., 野口, 武., Haruta, S., Yoshida, S., Sakata, M., Sado, T., & Oi, H. (2009) · Gynecological Endocrinology · doi:10.1080/09513590802366204 · Cited by 97 · see citing works
Banu, S. K., Lee, J., Starzinski‐Powitz, A., & Arosh, J. A. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.07.1358 · Cited by 96 · see citing works
New insights into the pathophysiology of endometriosis: from chronic inflammation to danger signal
Kajihara, H., Yamada, Y., Kanayama, S., Furukawa, N., 野口, 武., Haruta, S., Yoshida, S., Sado, T., Oi, H., & Kobayashi, H. (2010) · Gynecological Endocrinology · doi:10.3109/09513590.2010.507292 · Cited by 96 · see citing works
“Recent studies showed that the oxidative stress may be associated with the development of endometriosis: (1) women with endometriosis had increased levels of low-density lipoprotein (LDL) and HSP70b0 as well as decreased levels of paraoxonase-1 (PON-1) compared with controls [23]; (2) the concentrations of receptor fo…”
BackgroundIs it time for a paradigm shift in drug research and development in endometriosis/adenomyosis?
Guo, S., & Groothuis, P. G. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy020 · Cited by 93 · see citing works
Chowdhury, I., Banerjee, S., Driss, A., Xu, W., Mehrabi, S., Nezhat, C., Sidell, N., Taylor, R. N., & Thompson, W. E. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27360 · Cited by 95 · see citing works
“…Al‐Abed, Naccache, & Akoum, 2009; Carvalho, Podgaec, Bellodi‐Privato, Falcone, & Abrão, 2011; Dai, Leng, Lang, Li, & Zhang, 2012; Eyster, Klinkova, Kennedy, & Hansen, 2007; Honda, Barrueto, Gogusev, Im, &Morin, 2008; Hu, Tay, & Zhao, 2006; Hull et al., 2008; Mihalyi et al., 2010; Wu et al., 2006).”
Poli‐Neto, O. B., Meola, J., Silva, J. C. R. E., & Tiezzi, D. G. (2020) · Scientific Reports · doi:10.1038/s41598-019-57207-y · Cited by 97 · see citing works
Cancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Guo, S.-W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz047 · Cited by 96 · see citing works
“Moreover, PR-B has been reported to be hypermethylated in ectopic endometrium (Wu et al., 2006a,b,c) and partially methylated in eutopic endometrium from women with endometriosis (Rocha-Junior et al., 2019), which may account for reduced PR-B expression and subsequent progesterone resistance.”
BackgroundInfluentialTranscriptional profiling of endometriosis tissues identifies genes related to organogenesis defects
Crispi, S., Piccolo, M. T., D’Avino, A., Donizetti, A., Viceconte, R., Spyrou, M., Calogero, R., Baldi, A., & Signorile, P. G. (2013) · Journal of Cellular Physiology · doi:10.1002/jcp.24358 · Cited by 92 · see citing works
“To the best of our knowledge, very few studies compared ectopic and eutopic lesions analyzing only some of the different cell type contained in the lesion (Matsuzaki et al., 2006; Wu et al., 2006).”
BackgroundDienogest inhibits BrdU uptake with G0/G1 arrest in cultured endometriotic stromal cells
Fu, L., Osuga, Y., Morimoto, C., Hirata, T., Hirota, Y., Yano, T., & Taketani, Y. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.03.042 · Cited by 87 · see citing works
Honda, H., Barrueto, F. F., Gogusev, J., Im, D. D., & Morin, P. J. (2008) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-6-59 · Cited by 84 · see citing works
The Expression and Ovarian Steroid Regulation of Endometrial Micro-RNAs
Toloubeydokhti, T., Pan, Q., Luo, X., Bukulmez, O., & Chegini, N. (2008) · Reproductive Sciences · doi:10.1177/1933719108324132 · Cited by 83 · see citing works
“Gene expression profiling has provided considerable evidence in support of altered expression of a number of genes in various endometrial disorders, including EN as compared to normal endometrium.(20-25) Accumulated evidence also suggests that miRNAs play a key regulatory function in gene expression stability through…”
BackgroundRetractedvan der Horst, P. H., Wang, Y., van der Zee, M., Burger, C. W., & Blok, L. J. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.06.010 · Cited by 80 · see citing works
Obstetrical Complications in Women with Endometriosis: A Cohort Study in Japan
Harada, T., Taniguchi, F., Onishi, K., Kurozawa, Y., Hayashi, K., Harada, T., & Japan Environment & Children’s Study Group (2016) · PLoS ONE · doi:10.1371/journal.pone.0168476 · Cited by 76 · see citing works
Li, X., Zhang, Y., Zhao, L., Wang, L., Wu, Z., Mei, Q., Nie, J., Li, X., Li, Y., Fu, X., et al. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu330 · Cited by 74 · see citing works
Li, X., Xiong, W., Long, X., Dai, X., Peng, Y., Xu, Y., Zhang, Z., Zhang, L., & Liu, Y. (2021) · Biology of Reproduction · doi:10.1093/biolre/ioab152 · Cited by 70 · see citing works
New concepts on the etiology of endometriosis
Cousins, F. L., McKinnon, B. D., Mortlock, S., Fitzgerald, H. C., Zhang, C., Montgomery, G. W., & Gargett, C. E. (2023) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15549 · Cited by 82 · see citing works
Khan, M. A., Sengupta, J., Mittal, S., & Ghosh, D. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-84 · Cited by 69 · see citing works
“More over, it is notable that two types of endometriosis, namely ovarian endometriosis and peritoneal endometriosis reportedly show differential characteristics [4,9].”
BackgroundP-selectin as a potential therapeutic target for endometriosis
Guo, S., Ding, D., Geng, J.-G., Wang, L., & Liu, X. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.01.001 · Cited by 68 · see citing works
Wu, M., Lin, S., Hsiao, K., & Tsai, S. (2011) · The Journal of Pathology · doi:10.1002/path.2963 · Cited by 65 · see citing works
“Elevation of activated ERK and MAPK signaling pathway were observed in endometriotic tissues of women with endometriosis [17, 18].”
BackgroundAberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women
Pelch, K. E., Schroder, A. L., Kimball, P. A., Sharpe-Timms, K. L., Davis, J., & Nagel, S. C. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.03.086 · Cited by 64 · see citing works
Sun, P.-R., Jia, S., Lin, H., Leng, J., & Lang, J. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.12.035 · Cited by 63 · see citing works
Harada, T., Taniguchi, F., Amano, H., Kurozawa, Y., Ideno, Y., Hayashi, K., Harada, T., & Japan Environment and Children’s Study Group (2019) · PLoS ONE · doi:10.1371/journal.pone.0220256 · Cited by 61 · see citing works
Cancer driver mutations in endometriosis: Variations on the major theme of fibrogenesis
Guo, S. (2018) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12221 · Cited by 58 · see citing works
Genomic Alterations in Ectopic and Eutopic Endometria of Women with Endometriosis
Wu, Y., Strawn, E., Basir, Z., Wang, Y., Halverson, G., Jailwala, P., & Guo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000093130 · Cited by 58 · see citing works
Sha, G., Wu, D. T., Zhang, L., Chen, X., Lei, M., Sun, H., Lin, S., & Lang, J.-H. (2007) · Human Reproduction · doi:10.1093/humrep/dem266 · Cited by 58 · see citing works
“They have paid attention to epithelial and/or stromal compartments through laser capture microdissection or have used entire endometrial tissue without discriminating between the cellular compartments (Wu et al., 2006).”
BackgroundStructure, Function, and Evaluation of the Female Reproductive Tract
Lessey, B. A., & Young, S. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00009-3 · Cited by 58 · see citing works
Bentamapimod (JNK Inhibitor AS602801) Induces Regression of Endometriotic Lesions in Animal Models
Palmer, S. S., Altan, M., Denis, D., Tos, E. G., Gotteland, J., Osteen, K. G., Bruner‐Tran, K. L., & Nataraja, S. G. (2015) · Reproductive Sciences · doi:10.1177/1933719115600553 · Cited by 54 · see citing works
Mettler, L., Salmassi, A., Schollmeyer, T., Schmutzler, A. G., Püngel, F., & Jonat, W. (2007) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-007-9116-y · Cited by 54 · see citing works
COUP-TFII Regulates Human Endometrial Stromal Genes Involved in Inflammation
Li, X., Large, M. J., Creighton, C. J., Lanz, R. B., Jeong, J., Young, S. L., Lessey, B. A., Palomino, W. A., Tsai, S. Y., & DeMayo, F. J. (2013) · Molecular Endocrinology · doi:10.1210/me.2013-1191 · Cited by 52 · see citing works
A system-wide analysis of differentially expressed genes in ectopic and eutopic endometrium
Wren, J. D., Wu, Y., & Guo, S. (2007) · Human Reproduction · doi:10.1093/humrep/dem129 · Cited by 50 · see citing works
“…2003; Kao et al., 2003; Matsuzaki et al., 2004; Smith, 2004; Fan et al., 2005; Matsuzaki et al., 2005a; Matsuzaki et al., 2005b; Kato et al., 2006; Wu et al., 2006a), differing by focus, study design, microarray platform , quality control measure, data analysis, cell type used for RNA extraction,…”
BackgroundInfluentialMurk, W. K., Atabekoğlu, C. S., Çakmak, H., Heper, A. O., Ensarı, A., Kayisli, U. A., & Arici, A. M. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2051 · Cited by 49 · see citing works
“This is consistent with microarray analyses reporting that genes activating the ERK1/2 MAPK signalingcascadeareup-regulatedinpatientswithendometriosis (21, 22 ).”
ResultZhang, L., Xiong, W., Xiong, Y., Liu, H., Li, N., Du, Y., & Liu, Y. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.115.135574 · Cited by 49 · see citing works
“Several studies have found that the aberrant activation of Wnt/β-catenin signaling may be involved in the pathophysiology of endometriosis [26-28].”
BackgroundTwo unsuccessful clinical trials on endometriosis and a few lessons learned
Guo, S.-W., & Olive, D. L. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000098413 · Cited by 49 · see citing works
Self-citationZhang, H., Li, M., Zheng, X., Sun, Y., Wen, Z., & Zhao, X. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap069 · Cited by 49 · see citing works
Chand, A. L., Murray, A. S., Jones, R. L., Hannan, N. J., Salamonsen, L. A., & Rombauts, L. J. F. (2007) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-5-18 · Cited by 49 · see citing works
Potential mechanisms of postmenopausal endometriosis
Bendon, C. L., & Becker, C. M. (2012) · Maturitas · doi:10.1016/j.maturitas.2012.04.010 · Cited by 48 · see citing works
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Shen, F., Wang, Y., Lu, Y., Yuan, L., Liu, X., & Guo, S. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.04.040 · Cited by 44 · see citing works
Rahmioğlu, N., Drong, A., Lockstone, H. E., Tapmeier, T. T., Hellner, K., Saare, M., Laisk, T., Dew, C., Tough, E., Nicholson, G., et al. (2017) · Epigenetics · doi:10.1080/15592294.2017.1367475 · Cited by 44 · see citing works
Leach, R. E., Jessmon, P., Coutifaris, C., Kruger, M. L., Myers, E. R., Ali‐Fehmi, R., Carson, S. A., Legro, R. S., Schlaff, W. D., Carr, B. R., et al. (2012) · Human Reproduction · doi:10.1093/humrep/der436 · Cited by 43 · see citing works
“, 2005) and in endometriosis (Eyster et al., 2002; Arimoto et al., 2003; Matsuzaki et al., 2004, Matsuzaki et al., 2005; Matsuzaki et al., 2006; Wu et al., 2006) and endometrial cancer (Hever et al.”
BackgroundMatsuzaki, S., Botchorishvili, R., Pouly, J. L., & Canis, M. J. (2014) · Molecular and Cellular Therapies · doi:10.1186/s40591-014-0036-9 · Cited by 43 · see citing works
“Several studies, including those from our laboratory, have suggested that aberrant activation of the Wnt/β-catenin pathway may be involved in the pathophysiology of endometriosis [2-9].”
BackgroundLaser-assisted microdissection for real-time PCR sample preparation
Pinzani, P., Orlando, C., & Pazzagli, M. (2006) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2005.12.006 · Cited by 43 · see citing works
Vestergaard, A. L., Knudsen, U. B., Munk, T., Rosbach, H. K., & Martensen, P. M. (2010) · Molecular Human Reproduction · doi:10.1093/molehr/gaq100 · Cited by 42 · see citing works
“Previous studies of transcriptional levels in Eu versus Ec endometrium have used a single reference gene, such as GAPDH (Matsuzaki et al., 2006; Colette et al., 2009; Watanabe et al., 2009) and 18S (Wu et al., 2006; Lee et al., 2010).”
Vouk, K., Šmuc, T., Guggenberger, C., Ribič-pucelj, M., Šinkovec, J., Husen, B., Thole, H., Houba, P. H. J., Thaete, C., Adamski, J., et al. (2011) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.03.010 · Cited by 40 · see citing works
Jensen, J. R., & Coddington, C. C. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7b84 · Cited by 39 · see citing works
Activated Platelets Induce Estrogen Receptor β Expression in Endometriotic Stromal Cells
Zhang, Q., Ding, D., Liu, X., & Guo, S.-W. (2015) · Gynecologic and Obstetric Investigation · doi:10.1159/000377629 · Cited by 38 · see citing works
Borghese, B., Tost, J., de Surville, M., Busato, F., Letourneur, F., Mondon, F., Vaiman, D., & Chapron, C. (2015) · BioMed Research International · doi:10.1155/2015/461024 · Cited by 38 · see citing works
“SUP, OMA, and DIE have different responsiveness to progesterone [18], differential gene expressions [19, 20], and specific putative variants that may influence one form and not the others [21– 23].”
Johan, M. Z., Ingman, W. V., Robertson, S. A., & Hull, M. L. (2019) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2019.01.002 · Cited by 35 · see citing works
Large-scale gene expression studies of the endometrium: what have we learnt?
Sherwin, R., Catalano, R. D., & Sharkey, A. (2006) · Reproduction · doi:10.1530/rep.1.00355 · Cited by 35 · see citing works
“There is now a wealth of data studying both individual genes and using microarray methods that show differences in gene expression between normal and eutopic endometrium from women with endometriosis (reviewed in Wu et al. 2006).”
BackgroundQuattrone, F., Sanchez, A. M., Pannese, M., Hemmerle, T., Viganò, P., Candiani, M., Petraglia, F., Neri, D., & Panina‐Bordignon, P. (2015) · Reproductive Sciences · doi:10.1177/1933719115578930 · Cited by 35 · see citing works
Heinosalo, T., Gabriel, M., Kallio, L., Adhikari, P. R., Huhtinen, K., Laajala, T. D., Kaikkonen, E., Mehmood, A., Suvitie, P. A., Kujari, H. P., et al. (2018) · Human Reproduction · doi:10.1093/humrep/dey026 · Cited by 35 · see citing works
“…tissues (Anastas and Moon, 2013), and there is evidence that WNT signaling also plays a role in the endometrium and endometrial diseases (Talbi et al., 2006; Wu et al., 2006; Eyster et al., 2007; Aghajanova et al., 2010; Matsuzaki et al., 2010; Matsuzaki and Darcha, 2013; Zhang et al., 2016a).”
BackgroundSchwartz, N. R. M., Afeiche, M. C., Terry, K. L., Farland, L. V., Chavarro, J. E., Missmer, S. A., & Harris, H. R. (2022) · Journal of Nutrition · doi:10.1093/jn/nxac107 · Cited by 37 · see citing works
Miller, D. L., Jones, C. J. P., Aplin, J., & Nardo, L. G. (2009) · Human Reproduction · doi:10.1093/humrep/dep401 · Cited by 34 · see citing works
“Differences in the methylation status of the progesterone receptor B-isoform (PR-B) promoter have been seen between eutopic endometrium and controls (Wu et al., 2006b) but these also did not reach statistical significance.”
BackgroundHigh-throughput mRNA sequencing of stromal cells from endometriomas and endometrium
Rekker, K., Saare, M., Eriste, E., Tasa, T., Kukuškina, V., Roost, A. M., Anderson, K. B., Samuel, K., Karro, H., Salumets, A., et al. (2017) · Reproduction · doi:10.1530/rep-17-0092 · Cited by 33 · see citing works
Rai, P., Kota, V., Deendayal, M., & Shivaji, S. (2010) · Journal of Proteome Research · doi:10.1021/pr100657s · Cited by 32 · see citing works
Role of Wnt signalling in early pregnancy
Nayeem, S. B., Arfuso, F., Dharmarajan, A., & Keelan, J. A. (2014) · Reproduction Fertility and Development · doi:10.1071/rd14079 · Cited by 30 · see citing works
The Endometriotic Tissue Lining the Internal Surface of Endometrioma
Sanchez, A., Viganò, P., Somigliana, E., Cioffi, R., Panina-Bordignon, P., & Candiani, M. (2015) · Reproductive Sciences · doi:10.1177/1933719114529374 · Cited by 23 · see citing works
“Based on the statistical analysis that took into account lesion location and menstrual cycle, the genes identified include some ILs and their receptors (ie, IL-8, IL-15, and IL-15R), growth factors (platelet-derived growth factor b), and a member of the transforming growth factor (TGF) family (TGF-b3).(33)”
BackgroundMethodInfluentialQi, X., Zhang, Y., Ji, H., Wu, X., Wang, F., Xie, M., Shu, L., Jiang, S., Mao, Y., Cui, Y., et al. (2014) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2014.09.004 · Cited by 29 · see citing works
“A reasonable explanation may be that eutopic and ectopic stromal cells have different gene expression profiles (Wu et al., 2006).”
BackgroundNiklaus, A. L., Aubuchon, M., Zapantis, G., Li, P., Qian, H., Isaac, B., Kim, M., Adel, G., Pollard, J. W., & Santoro, N. F. (2007) · Human Reproduction · doi:10.1093/humrep/dem032 · Cited by 28 · see citing works
“Previous studies that have utilized LCM for endometrial related research have only used this technology to collectively examine both epithelial cell types (Wu et al., 2003, 2006) or only that of GE (Matsuzaki et al., 2004, 2005, 2006).”
MethodEpithelial Cells of Deep Infiltrating Endometriosis Harbor Mutations in Cancer Driver Genes
Koppolu, A. A., Maksym, R., Paskal, W., Machnicki, M. M., Rak, B., Pępek, M., Garbicz, F., Pełka, K., Kuśmierczyk, Z., Jacko, J., et al. (2021) · Cells · doi:10.3390/cells10040749 · Cited by 27 · see citing works
“They suggested the importance of over seventy pathways with over one hundred genes involved in the disease pathogenesis [32].”
BackgroundA Functional Promoter Polymorphism in NFKB1 Increases Susceptibility to Endometriosis
Zhou, B., Rao, L., Peng, Y., Wang, Y., Qie, M., Zhang, Z., Song, Y., & Zhang, L. (2010) · DNA and Cell Biology · doi:10.1089/dna.2009.0992 · Cited by 27 · see citing works
“Recent large-scale gene expression profiling studies have revealed that many genes are dysregulated in endometriosis (Matsuzaki et al. , 2005; Wu et al. , 2006).”
Zhang, H., Xue, J., Li, M., Ζhao, X., Wei, D., & Li, C. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.06.011 · Cited by 27 · see citing works
“Aberrant Wnt2 expression (Wu et al., 2006) and abnormal activation of Wnt/b-catenin signaling (Matsuzaki et al.”
- Authors
- Wu, Y., Kajdacsy-Balla, A., Strawn, E., Basir, Z., Halverson, G., Jailwala, P., Wang, Y., Wang, X., Ghosh, S., & Guo, S.-W.
- Affiliations
- Medical College of Wisconsin (US)
- Department of Pathology (A.K.-B.), University of Illinois, Chicago, Illinois 60612
- University of California, Santa Barbara (US)
- Corresponding author
- Guo, Sun-Wei
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2006-01-01
- Volume
- 147
- Issue
- 1
- Pages
- 232-246
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2032547793
- Cited by
- 208
- References
- 120
- Citations by year
- 2025: 4 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 12 · 2018: 14 · 2017: 11 · 2016: 8 · 2015: 11 · 2014: 13 · 2013: 11 · 2012: 12
- FWCI
- 13.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical College of Wisconsin
- 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 › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
- Keywords
- endometriosis, ectopic endometrium, eutopic endometrium, gene expression profiling, differentially expressed genes, endometrioma, gene clusters, oxidative stress, focal adhesions, Wnt signaling, MAPK signaling, endometriosis pathogenesis
- MeSH terms
- Base Sequence, Endometrium, Female, Humans, Menstrual Cycle, Ovarian Diseases, Pregnancy, Pregnancy, Ectopic, Reference Values, Transcription, Genetic, DNA Primers, Reverse Transcriptase Polymerase Chain Reaction, Expressed Sequence Tags, Oligonucleotide Array Sequence Analysis
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