Activated Platelets Induce Hypoxia-Inducible Factor-1α Expression Likely through Transforming Growth Factor-β1 in Human Endometrial Stromal Cells
Open accessAbstract
Objective: Endometriosis is a common gynecological disease with an enigmatic pathogenesis. Recent studies suggest that the behavior of normal endometrial stromal cells can dramatically change under hypoxic conditions, which effectively turns them into endometriotic stromal cells. Because menstrual debris is not only hypoxic but may also contain platelet aggregates, at present, we aimed to approve that activated platelets could induce hypoxia-inducible factor-1α (HIF-1α) expression in endometrial stromal cells, signaling the presence of hypoxia. Methods: We evaluated the gene and protein expression levels of HIF-1α and its target gene erythropoietin (EPO) in both human endometriotic stromal cells (HESCs) and a human endometrial stromal cell line (ESCL) cocultured with or without activated platelets for 48 h. Results: We found that the gene and protein expression levels of HIF-1α and EPO in both HESC and ESCL were significantly increased after coculture with activated platelets. We also found that neutralization of transforming growth factor-β1 completely abolishes this induction. Conclusions: Platelets can induce a hypoxic state in endometrial and endometriotic stromal cells, resulting in increased angiogenesis, as well as enhanced survival and proliferation. In conjunction with other roles that platelets play in the development of endometriosis, our findings further highlight the important roles of platelets in the development and initiation of endometriosis, shedding new light into the etiology of endometriosis.
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Activated platelets can activate HIF-1α in endometrial and endometriotic stromal cells, generating a state of hypoxia.
“More remarkably, activated platelets can activate HIF-1α in endometrial and endometriotic stromal cells, effectively generating a state of hypoxia [97].”
From The Pathogenesis of Adenomyosis vis-à-vis Endometriosis (2020) · cites this paper as [97]
Activated platelets induced significantly higher expression of HIF-1α, COX-2, and VEGF at both transcriptional and protein levels in endometriotic stromal cells (all p≤0.012).
“In addition, activated platelets induced significantly higher expression of HIF-1α, COX-2 and VEGF (which is downstream of HIF-1α) at both transcriptional and protein expression levels in endometriotic stromal cells (all p-values ≤ 0.012, Fig. 2C–E), consistent with our previous report40.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [40]
Platelets can induce HIF-1α expression, effectively inducing a hypoxic state in both endometriotic and endometrial stromal cells.
“we recent found that platelets can induce hypoxia-inducible factor 1α (HIF-1α) expression, effectively inducing a hypoxic sate in both endometriotic and endometrial stromal cells40.”
From Platelets induce increased estrogen production through NF-κB and TGF-β1 signaling pathways in endometriotic stromal cells (2020) · cites this paper as [40]
Cites
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“[54] While it may seem logical that the TGF-β1/ Smad3 pathway is a therapeutic target for endometriosis, it is worth noting that this pathway also plays many important physiological functions in the endometrium.[55] In other words, targeting this pathway directly may cause unintended collateral damage to normal tissue…”
BackgroundRetractedAnalysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · cited 1× · see citing works
“Expression values were normalized to the geometric mean of GAPDH measurements, and the quantification of mRNA abundance was made using the method described previously.[26]”
MethodActivation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1
Forsythe, J. A., Jiang, B.-H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D., & Semenza, G. L. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.9.4604 · Cited by 3,981 · cited 2× · see citing works
“[31,32] VEGF, a major driver of angiogenesis in cancer and in endometriosis, is also transcriptionally regulated by HIF-1α under hypoxic conditions.[33] HIF-1α binds to the HRE regions of the VEGF promoter and is positively correlated with VEGF expression in endometriosis.”
BackgroundCyclooxygenase regulates angiogenesis induced by colon cancer cells
Tsujii, M., Kawano, S., Tsuji, S., Sawaoka, H., Hori, M., & DuBois, R. N. (1998) · Cell · doi:10.1016/s0092-8674(00)81433-6 · Cited by 2,272 · see citing works
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“[30] HIF-1α-induced COX-2 expression leads to elevated prostaglandin E2 (PGE2) levels, which can induce PGE2-mediated vascularization.[31,32] VEGF, a major driver of angiogenesis in cancer and in endometriosis, is also transcriptionally regulated by HIF-1α under hypoxic conditions.”
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“The EPO gene is under the direct control of hypoxia through HIF-1α, which then binds to a cis-acting DNA site in the HRE of the EPO gene promoter.[36,37] EPO, a widely known growth factor in erythropoiesis, can also stimulate angiogenesis,[38] as well as tumor cell proliferation and survival.”
BackgroundHIF-1 and tumor progression: pathophysiology and therapeutics
Semenza, G. L. (2002) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(02)02317-1 · Cited by 1,060 · cited 1× · see citing works
“One hallmark of hypoxia is the overexpression of the transcription factor hypoxia-inducible factor-1α (HIF-1α), a key mediator of cellular adaptation to low oxygen levels and a potential target for many types of cancer, such as ovarian, prostate, and breast;[6] HIF-1α expression reflects the degree of cell hypoxia; it…”
BackgroundHypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition
Higgins, D. F., Kimura, K., Bernhardt, W. M., Shrimanker, N., Akai, Y., Hohenstein, B., Saito, Y., Johnson, R. S., Kretzler, M., Cohen, C. D., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30487 · Cited by 976 · cited 1× · see citing works
“We note that HIF-1α has also been reported to promote epithelial–mesenchymal transition (EMT) in several types of cancer by modulating one or more EMT-associated genes.[53] Moreover, in this study, we demonstrated that TGF-β1 neutralization completely abolishes platelet-induced HIF-1α expression in endometriotic cells.”
BackgroundHypoxia-Inducible Factor 1 (HIF-1) Pathway
Semenza, G. L. (2007) · Science s STKE · doi:10.1126/stke.4072007cm8 · Cited by 942 · cited 2× · see citing works
“HIF consists of two subunits, α and β, which form a heterodimeric complex.[28] HIF-1β is present under both normoxia and hypoxia, while HIF1α is present only under hypoxic conditions.”
BackgroundKaidi, A., Qualtrough, D., Williams, A. C., & Paraskeva, C. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0425 · Cited by 300 · cited 1× · see citing works
“[29] For example, COX-2 expression is regulated by HIF-1α transcriptional activity.[30] HIF-1α-induced COX-2 expression leads to elevated prostaglandin E2 (PGE2) levels, which can induce PGE2-mediated vascularization.”
BackgroundMasson, N., & Ratcliffe, P. J. (2014) · Cancer & Metabolism · doi:10.1186/2049-3002-2-3 · Cited by 296 · cited 1× · see citing works
“The EPO gene is under the direct control of hypoxia through HIF-1α, which then binds to a cis-acting DNA site in the HRE of the EPO gene promoter.[36,37] EPO, a widely known growth factor in erythropoiesis, can also stimulate angiogenesis,[38] as well as tumor cell proliferation and survival.”
BackgroundA Novel Immortalized Human Endometrial Stromal Cell Line with Normal Progestational Response
Krikun, G., Mor, G., Alvero, A. B., Guller, S. M., Schatz, F., Sapi, E., Rahman, M. M., Caze, R., Qumsiyeh, M. Β., & Lockwood, C. J. (2004) · Endocrinology · doi:10.1210/en.2003-1606 · Cited by 285 · see citing works
Behaviour of Cytokine Levels in Serum and Peritoneal Fluid of Women with Endometriosis
Pizzo, A., Salmeri, F. M., Ardita, F. V., Sofo, V., Tripepi, M., & Marsico, S. (2002) · Gynecologic and Obstetric Investigation · doi:10.1159/000067717 · Cited by 285 · cited 1× · see citing works
“The increased TGF-β1 expression in endometriosis has been well documented.[45-48] In a gene profiling study on a mouse”
BackgroundZhang, W., Shi, X., Peng, Y., Wu, M., Zhang, P., Xie, R., Wu, Y., Yan, Q., Liu, S., & Wang, J. (2015) · PLOS ONE · doi:10.1371/journal.pone.0129603 · Cited by 261 · cited 1× · see citing works
“[28] As a transcription factor, HIF-1α regulates the activities of its downstream genes by binding the HREs in their promoter regions.[29] For example, COX-2 expression is regulated by HIF-1α transcriptional activity.”
BackgroundErythropoietin Biology in Cancer
Hardee, M. E., Arcasoy, M. O., Blackwell, K., Kirkpatrick, J. P., & Dewhirst, M. W. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1771 · Cited by 223 · cited 1× · see citing works
“[36,37] EPO, a widely known growth factor in erythropoiesis, can also stimulate angiogenesis,[38] as well as tumor cell proliferation and survival.”
BackgroundZhang, Q., Duan, J., Liu, X., & Guo, S.-W. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.03.015 · Cited by 211 · cited 4× · see citing works
“However, because endometriotic stromal cells and platelets used in this study were all derived from humans, and both platelet aggregation and hypoxia are now well documented in endometriosis,[15,17,42,56-59] we believe that platelets must play a role in hypoxia in endometriosis.”
BackgroundInfluentialSelf-citationTranscriptional characterizations of differences between eutopic and ectopic endometrium
Wu, Y., Kajdacsy-Balla, A., Strawn, E., Basir, Z., Halverson, G., Jailwala, P., Wang, Y., Wang, X., Ghosh, S., & Guo, S.-W. (2006) · Endocrinology · doi:10.1210/en.2005-0426 · Cited by 208 · cited 1× · see citing works
“However, the ectopic and eutopic endometria are known to be transcriptionally different,[4] and the difference is presumably attributed to their different microenvironments, the key factor that determines the difference is still unclear.”
BackgroundSelf-citationEndometrial-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 · cited 1× · see citing works
“model, TGF-β1 has been identified to play important roles in the gene network involved in the pathogenesis of endometriosis.[49]”
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 · cited 2× · see citing works
“[51] On the other hand, exposure to TGF-β1 could increase HIF-1α gene and protein expression in many cell types.[48,50,52] In this study, we found that neutralization of TGF-β1 completely abolished the HIF-1α induction by activated platelets in both HESC and ESCL, highlighting the important role of platelets in the in…”
BackgroundZhang, Q., Duan, J., Olson, M., Fazleabas, A., & Guo, S.-W. (2016) · Reproductive Sciences · doi:10.1177/1933719116641763 · Cited by 149 · cited 1× · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citationDing, D., Liu, X., Duan, J., & Guo, S.-W. (2015) · Human Reproduction · doi:10.1093/humrep/dev025 · Cited by 139 · cited 13× · see citing works
“[30] HIF-1α-induced COX-2 expression leads to elevated prostaglandin E2 (PGE2) levels, which can induce PGE2-mediated vascularization.”
BackgroundInfluentialSelf-citationMatsuzaki, S., & Darcha, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076808 · Cited by 138 · cited 2× · see citing works
“[9] This is consistent with the report that both endometriotic and endometrial stromal cells have elevated expression of myofibroblast markers after stimulation with TGF-β1.[54] While it may seem logical that the TGF-β1/ Smad3 pathway is a therapeutic target for endometriosis, it is worth noting that this pathway also…”
ResultHypoxia-Induced Secretion of TGF-β1 in Mesenchymal Stem Cell Promotes Breast Cancer Cell Progression
Hung, S.-P., Yang, M.-H., Tseng, K.-F., & Lee, O. K. (2013) · Cell Transplantation · doi:10.3727/096368912x657954 · Cited by 137 · cited 1× · see citing works
“It has been reported that TGF-β1 promoter activity is regulated by hypoxia, and that HIF-1α could directly regulate TGF-β1 expression through the HRE, which is located in the TGF-β1 proximal promoter.[51] On the other hand, exposure to TGF-β1 could increase HIF-1α gene and protein expression in many cell types.”
BackgroundLin, 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 · cited 1× · see citing works
“Hypoxia is an important factor that regulates numerous physiological and pathological processes.[41] It has been reported”
BackgroundThe M2a macrophage subset may be critically involved in the fibrogenesis of endometriosis in mice
Duan, J., Liu, X., Wang, H., & Guo, S.-W. (2018) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2018.05.017 · Cited by 121 · cited 1× · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citationWu, M., Chen, K., Lin, S., Lgu, C.-W., & Tsai, S. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.060477 · Cited by 120 · cited 2× · see citing works
“However, because endometriotic stromal cells and platelets used in this study were all derived from humans, and both platelet aggregation and hypoxia are now well documented in endometriosis,[15,17,42,56-59] we believe that platelets must play a role in hypoxia in endometriosis.”
BackgroundFemale Infertility and Free Radicals: Potential Role in Adhesions and Endometriosis
Alpay, Z., Saed, G. M., & Diamond, M. P. (2006) · Journal of the Society for Gynecologic Investigation · doi:10.1016/j.jsgi.2006.05.002 · Cited by 119 · cited 1× · see citing works
“However, because endometriotic stromal cells and platelets used in this study were all derived from humans, and both platelet aggregation and hypoxia are now well documented in endometriosis,[15,17,42,56-59] we believe that platelets must play a role in hypoxia in endometriosis.”
BackgroundHypoxia inducible factor-1α: Its role in colorectal carcinogenesis and metastasis
Nagaraju, G. P., Bramhachari, P. V., Raghu, G., & El‐Rayes, B. F. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.06.005 · Cited by 114 · cited 1× · see citing works
“the transcriptional activation of hypoxia-regulated genes, including erythropoietin (EPO), vascular endothelial growth factor (VEGF), and cyclooxygenase-2 (COX-2),[10,11] which are”
BackgroundThe Peritoneum Is Both a Source and Target of TGF-β in Women with Endometriosis
Young, V. J., Brown, J. K., Saunders, P. T. K., Duncan, W. C., & Horne, A. W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106773 · Cited by 105 · cited 2× · see citing works
“[51] On the other hand, exposure to TGF-β1 could increase HIF-1α gene and protein expression in many cell types.[48,50,52] In this study, we found that neutralization of TGF-β1 completely abolished the HIF-1α induction by activated platelets in both HESC and ESCL, highlighting the important role of platelets in the in…”
BackgroundHypoxia: The force of endometriosis
Wu, M., Hsiao, K., & Tsai, S. (2019) · Journal of Obstetrics and Gynaecology Research · doi:10.1111/jog.13900 · Cited by 88 · cited 4× · see citing works
“of HIF-1α.[9,12] This may explain why endometrial debris invades and establish endometriotic foci in ectopic sites.”
BackgroundResultInfluentialGuo, S.-W., Ding, D., Shen, M., & Liu, X. (2015) · Reproductive Sciences · doi:10.1177/1933719115570907 · Cited by 86 · cited 1× · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citationYan, D., Liu, X., & Guo, S.-W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39170-w · Cited by 82 · cited 1× · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citationDu, Y., Liu, X., & Guo, S. (2017) · Human Reproduction · doi:10.1093/humrep/dex014 · Cited by 72 · cited 1× · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citationP-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 · cited 1× · see citing works
“Preparation of platelets Platelets were isolated by centrifugation at room temperature of whole blood samples donated by healthy male volunteers who provided informed consent and did not take any medications for at least 2 weeks prior to donation as reported previously.[25] The blood was first centrifuged at 150 ×g fo…”
MethodSelf-citationWu, M., Lin, S., Hsiao, K., & Tsai, S. (2011) · The Journal of Pathology · doi:10.1002/path.2963 · Cited by 65 · cited 1× · see citing works
“However, because endometriotic stromal cells and platelets used in this study were all derived from humans, and both platelet aggregation and hypoxia are now well documented in endometriosis,[15,17,42,56-59] we believe that platelets must play a role in hypoxia in endometriosis.”
BackgroundPathological functions of hypoxia in endometriosis
Hsiao, K.-Y. (2015) · Frontiers in Bioscience · doi:10.2741/e736 · Cited by 61 · cited 1× · see citing works
“Recently, it has been shown that hypoxia plays a critical role in the survival and angiogenesis of ectopic endometrial cells regurgitated from the uterus.[5] Remarkably, hypoxic conditions alone dramatically change the behavior of endometrial cells that are otherwise “normal.”
BackgroundEvidence for a Hypercoagulable State in Women With Ovarian Endometriomas
Wu, Q., Ding, D., Liu, X., & Guo, S. (2015) · Reproductive Sciences · doi:10.1177/1933719115572478 · Cited by 60 · cited 1× · see citing works
“However, because endometriotic stromal cells and platelets used in this study were all derived from humans, and both platelet aggregation and hypoxia are now well documented in endometriosis,[15,17,42,56-59] we believe that platelets must play a role in hypoxia in endometriosis.”
BackgroundSelf-citationGuo, S., Du, Y., & Liu, X. (2016) · Reproductive Sciences · doi:10.1177/1933719116630428 · Cited by 55 · cited 3× · see citing works
“Reproductive and Developmental Medicine ¦ June 25, 2019 ¦ Volume 3 ¦ Issue 2 71 buffered saline (PBS) three times to remove the platelets as reported previously.[19]”
BackgroundMethodSelf-citationAn overview of the current status of clinical trials on endometriosis: issues and concerns
Guo, S. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.08.050 · Cited by 54 · cited 1× · see citing works
“[1] Despite extensive research, its pathogenesis remains elusive.[2] One widely accepted theory is the retrograde menstruation theory proposed by Sampson,[3] which stipulates that, when viable endometrial cells are regurgitated into the pelvic cavity through the fallopian tubes, they somehow invade the peritoneum and…”
BackgroundSelf-citationExpression of MMIF, HIF-1α and VEGF in Serum and Endometrial Tissues of Patients with Endometriosis
Zhang, F., Liu, X., Wang, W., Dong, H., Xia, Y.-F., Ruan, L.-P., & Liu, L. (2018) · Current Medical Science · doi:10.1007/s11596-018-1906-1 · Cited by 51 · cited 1× · see citing works
“resulting in increased cellular proliferation in an autocrine fashion.[42-44] Our data demonstrate that activated platelets could”
BackgroundSelf-citationSensory nerve-derived neuropeptides accelerate the development and fibrogenesis of endometriosis
Liu, X., Yan, D., & Guo, S.-W. (2019) · Human Reproduction · doi:10.1093/humrep/dey392 · Cited by 51 · cited 1× · see citing works
“endometriotic lesions are essentially wounds undergoing repeated tissue injury and repair,[13-16] and many nonendometriotic cells in the lesional microenvironment, such as platelets,[15,17] macrophages,[13,18] natural killer cells,[19,20] and nerve fibers,[21,22] are involved in facilitating the development of endomet…”
BackgroundSelf-citationHypoxia-inducible factor-1alpha: A promising therapeutic target in endometriosis
Zhan, L., Wang, W., Zhang, Y., Song, E., Fan, Y., & Wei, B. (2016) · Biochimie · doi:10.1016/j.biochi.2016.01.006 · Cited by 48 · cited 1× · see citing works
“in endometriosis, reflecting the increasing need for nutrients and oxygen as endometriotic lesions grow.[8] Conceivably, the menstrual debris, once regurgitated from the uterus to the peritoneal cavity as depicted in Sampson’s hypothesis,[3] would experience hypoxia due to a loss of blood supply.”
BackgroundFerns, G. A., & Heikal, L. (2016) · Angiology · doi:10.1177/0003319716662423 · Cited by 44 · cited 1× · see citing works
“[33] Tissue hypoxia is the main stimulus of EPO production.[34] HIF-1α upregulates the expression of EPO, which mediates its effects by binding to the EPO receptor (EPOR).”
BackgroundFurther Evidence for Hypercoagulability in Women With Ovarian Endometriomas
Ding, D., Liu, X., & Guo, S. (2018) · Reproductive Sciences · doi:10.1177/1933719118799195 · Cited by 44 · cited 1× · see citing works
“However, because endometriotic stromal cells and platelets used in this study were all derived from humans, and both platelet aggregation and hypoxia are now well documented in endometriosis,[15,17,42,56-59] we believe that platelets must play a role in hypoxia in endometriosis.”
BackgroundSelf-citationUnderstanding the Presence and Function of Erythropoietin Receptors on Cancer Cells
Lai, S. Y., & Grandis, J. R. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2006.08.1190 · Cited by 41 · cited 3× · see citing works
“[34] HIF-1α upregulates the expression of EPO, which mediates its effects by binding to the EPO receptor (EPOR).[35] Hypoxia results in the increased production of EPO via the induction of the HIF-1 pathway.”
BackgroundLin, 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 · cited 2× · see citing works
“of HIF-1α.[9,12] This may explain why endometrial debris invades and establish endometriotic foci in ectopic sites.”
BackgroundActivated 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 · cited 2× · see citing works
“To see whether transforming growth factor-β (TGF-β) neutralization can abolish the overexpression of HIF-1α induced by activated platelets in HESC and ESCL, the cells were pretreated for 2 h with 1 μmol/L of A83-01 compound (Santa Cruz, CA, USA), which is a TGF-β receptor inhibitor, and then incubated with activated p…”
MethodSelf-citationYoung, V. J., Ahmad, S. F., Brown, J. K., Duncan, W. C., & Horne, A. W. (2016) · Molecular Human Reproduction · doi:10.1093/molehr/gaw045 · Cited by 33 · cited 1× · see citing works
“[51] On the other hand, exposure to TGF-β1 could increase HIF-1α gene and protein expression in many cell types.[48,50,52] In this study, we found that neutralization of TGF-β1 completely abolished the HIF-1α induction by activated platelets in both HESC and ESCL, highlighting the important role of platelets in the in…”
BackgroundBenderro, G. F., & LaManna, J. (2014) · Brain Research · doi:10.1016/j.brainres.2014.04.035 · Cited by 27 · cited 1×
“Hypoxia is a critical mediator of endothelial growth factors and signaling proteins during periods of metabolic stress and vascular remodeling like angiogenesis or regression,[27] most of which are mediated via transcriptional regulation by HIF.”
BackgroundBadowska-Kozakiewicz, A. M., Sobol, M., & Patera, J. (2016) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/63143 · Cited by 22 · cited 1× · see citing works
“the transcriptional activation of hypoxia-regulated genes, including erythropoietin (EPO), vascular endothelial growth factor (VEGF), and cyclooxygenase-2 (COX-2),[10,11] which are”
BackgroundExpression of erythropoietin and erythropoietin receptor in peritoneal endometriosis
Matsuzaki, S., Canis, M. J., Yokomizo, R., Yaegashi, N., Bruhat, M. A., & Okamura, K. (2003) · Human Reproduction · doi:10.1093/humrep/deg007 · Cited by 17 · cited 5× · see citing works
“[36,37] EPO, a widely known growth factor in erythropoiesis, can also stimulate angiogenesis,[38] as well as tumor cell proliferation and survival.”
BackgroundInfluentialBadowska-Kozakiewicz, A. M., Budzik, M. P., & Przybylski, J. (2016) · Polish Journal of Pathology · doi:10.5114/pjp.2015.57245 · Cited by 14 · cited 1× · see citing works
“Reproductive and Developmental Medicine ¦ June 25, 2019 ¦ Volume 3 ¦ Issue 2 70 is responsible for increased angiogenesis in cancers.[7] Similar to that in cancer, HIF-1α has also been shown to be overexpressed”
BackgroundTGF-β1 mediates estrogen receptor-induced epithelial-to-mesenchymal transition in some tumor lines
Fan, D., Qi, P., Gao, S., Chen, Y., & Cheng, X. (2014) · Tumor Biology · doi:10.1007/s13277-014-2166-8 · Cited by 3 · cited 1× · see citing works
“[35] The expression levels of EPO,[39] VEGF, and COX-2[17] have all been reported to be elevated in endometriosis, resulting in angiogenesis, proliferation, and enhanced survival in lesional development.[35,40] We have previously shown that activated platelets can activate VEGF and COX-2 expression in HESCs;[17] in th…”
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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
“More remarkably, activated platelets can activate HIF-1α in endometrial and endometriotic stromal cells, effectively generating a state of hypoxia [97].”
BackgroundSelf-citationPathogenesis of Human Adenomyosis: Current Understanding and Its Association with Infertility
Khan, K. N., Fujishita, A., & Mori, T. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11144057 · Cited by 74 · see citing works
Xiao, F., Liu, X., & Guo, S. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.610963 · Cited by 62 · see citing works
“Activated platelets can induce estrogen production in endometriotic stromal cells (97, 98), which, in turn,may induceTSLP secretion (30).”
BackgroundSelf-citationQi, Q., Liu, X., Zhang, Q., & Guo, S.-W. (2020) · Scientific Reports · doi:10.1038/s41598-020-57997-6 · Cited by 44 · see citing works
Self-citationYan, D., Liu, X., Xu, H., & Guo, S. (2020) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgaa550 · Cited by 44 · see citing works
Self-citationPlatelets induce endothelial–mesenchymal transition and subsequent fibrogenesis in endometriosis
Yan, D., Liu, X., Xu, H., & Guo, S. (2020) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.03.020 · Cited by 39 · see citing works
Self-citationHao, M., Liu, X., & Guo, S. (2020) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.07.023 · Cited by 40 · see citing works
Self-citationLiu, S., Xin, W., Tang, X., Qiu, J., Zhang, Y., & Hua, K. (2020) · Reproductive Sciences · doi:10.1007/s43032-019-00129-x · Cited by 31 · see citing works
Habiba, M. A., Benagiano, G., & Guo, S. (2023) · Biomolecules · doi:10.3390/biom13060975 · Cited by 31 · see citing works
“Of course, injury involving the vasculature may lead to estrogen production due to platelet activation [60,61], but whether hyperperistalsis can lead to such injury is unclear.”
BackgroundSelf-citationVarious types of adenomyosis and endometriosis: in search of optimal management
Guo, S. (2023) · Fertility and Sterility · doi:10.1016/j.fertnstert.2023.03.021 · Cited by 24 · see citing works
Self-citationUnveiling the Pathogenesis of Adenomyosis through Animal Models
Wang, X., Benagiano, G., Liu, X., & Guo, S. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11061744 · Cited by 19 · see citing works
Self-citationThe Role of Platelets in the Pathogenesis and Pathophysiology of Adenomyosis
Guo, S. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12030842 · Cited by 17 · see citing works
“Yet activated platelets alone can activate HIF-1α—the master regulator of hypoxia, effectively inducing a hypoxic sate in both endometriotic and endometrial stromal cells [77].”
Self-citationAge‐dependent phenotypes of ovarian endometriomas
Benagiano, G., & Guo, S. (2022) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12438 · Cited by 13 · see citing works
Self-citationYang, J., Li, X., Yu, P. E. N. G., Sun, Z., Zhang, L., Duan, J., & Zhong, N. A. (2026) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.71129 · Cited by 4 · see citing works
The Role of Platelets in the Pathogenesis of Endometriosis and New Therapeutic Ideas
许, 万. (2022) · Advances in Clinical Medicine · doi:10.12677/acm.2022.124367
“我们已经知道,在月经来临前的子宫内膜处于缺血缺氧的状态,而缺氧诱导因子 1α (HIF-α)可以在缺 氧的状态下迅速积累,并且在氧气恢复后迅速下降[21]。在易患子宫内膜异位症的女性中,子宫内膜碎片 很可能就处于缺血缺氧的状态,为了建立新的血管来供应氧气和营养,HIF 调节的基因调控血管生成、 增殖、迁移、细胞凋亡和新陈代谢等多种生物过程。在这些过程中,间皮细胞和活化的巨噬细胞表达生 长因子和信号因子等多种信号物质[22]。因此,缺氧可能在血液供应之前的逆行子宫内膜存活和早期植入 的子宫内膜病变中的血管生成当中发挥重要作用[23] [24]。在一项将人类子宫内膜异位症基质细胞 (HESCs)和人类子宫内膜基质细胞(ESCL)与血小…”
- Authors
- Qi, Q.-M., Guo, S.-W., & Liu, X.-S.
- Affiliations
- Fudan University (CN)
- ORCID
- Guo, Sun-Wei
- Venue
- Reproductive and Developmental Medicine
- Published
- 2019-04
- Volume
- 3
- Issue
- 2
- Pages
- 69-76
- ISSN
- 2096-2924 (ISSN-L)
- 2589-8728
- OpenAlex
- W2956467779
- Cited by
- 15
- References
- 58
- Citations by year
- 2026: 1 · 2023: 3 · 2022: 4 · 2020: 7
- FWCI
- 2.64
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- Reproductive and Developmental Medicine (publishedVersion, cc-by-nc-sa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- endometriosis, platelets, activated platelets, hypoxia-inducible factor-1α, TGF-β1, endometrial stromal cells, erythropoietin, hypoxia, angiogenesis, endometriotic stromal cells
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