Endometrial Inflammation and Impaired Spontaneous Decidualization: Insights into the Pathogenesis of Adenomyosis
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Selection of Studies
3.2. Fibrotic Lesion Formation Due to Repeated Injury and Repair of the Myometrium
3.3. An Altered Expression of Angiogenesis-Related Molecules
3.4. Dysfunction of Spontaneous Decidualization via Aberrant Epigenetic Alterations
3.5. Impaired Spontaneous Decidualization Due to Persistent Inflammation
3.6. Defense Processes against Inflammation and External Stimuli in the Endometrium
4. Conclusions
Supplementary Materials
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zhai, J.; Vannuccini, S.; Petraglia, F.; Giudice, L.C. Adenomyosis: Mechanisms and Pathogenesis. Semin. Reprod. Med. 2020, 38, 129–143. [Google Scholar] [CrossRef] [PubMed]
- Guo, S.W. The Pathogenesis of Adenomyosis vis-à-vis Endometriosis. J. Clin. Med. 2020, 9, 485. [Google Scholar] [CrossRef] [Green Version]
- Benagiano, G.; Brosens, I. The endometrium in adenomyosis. Womens Health 2012, 8, 301–312. [Google Scholar] [CrossRef]
- Peng, Y.; Jin, Z.; Liu, H.; Xu, C. Impaired decidualization of human endometrial stromal cells from women with adenomyosis. Biol. Reprod. 2021, 104, 1034–1044. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, H. Molecular Targets for Nonhormonal Treatment Based on a Multistep Process of Adenomyosis Development. Reprod. Sci. 2022. [Google Scholar] [CrossRef]
- Panganamamula, U.R.; Harmanli, O.H.; Isik-Akbay, E.F.; Grotegut, C.A.; Dandolu, V.; Gaughan, J.P. Is prior uterine surgery a risk factor for adenomyosis? Obstet. Gynecol. 2004, 104, 1034–1038. [Google Scholar] [CrossRef]
- Kazemi, E.; Alavi, A.; Aalinezhad, F.; Jahanshahi, K. Evaluation of the relationship between prior uterine surgery and the incidence of adenomyosis in the Shariati Hospital in Bandar-Abbas, Iran, from 2001 to 2011. Electron. Physician 2014, 6, 912–918. [Google Scholar] [CrossRef] [PubMed]
- Leyendecker, G.; Wildt, L.; Laschke, M.W.; Mall, G. Archimetrosis: The evolution of a disease and its extant presentation: Pathogenesis and pathophysiology of archimetrosis (uterine adenomyosis and endometriosis). Arch. Gynecol. Obstet. 2022, 307, 93–112. [Google Scholar] [CrossRef]
- Leyendecker, G.; Wildt, L.; Mall, G. The pathophysiology of endometriosis and adenomyosis: Tissue injury and repair. Arch. Gynecol. Obstet. 2009, 280, 529–538. [Google Scholar] [CrossRef] [Green Version]
- Gellersen, B.; Brosens, J.J. Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr. Rev. 2014, 35, 851–905. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.; Shen, M.; Qi, Q.; Zhang, H.; Guo, S.W. Corroborating evidence for platelet-induced epithelial-mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation in the development of adenomyosis. Hum. Reprod. 2016, 31, 734–749. [Google Scholar] [CrossRef] [Green Version]
- Armstrong, G.M.; Maybin, J.A.; Murray, A.A. Endometrial apoptosis and neutrophil infiltration during menstruation exhibits spatial and temporal dynamics that are recapitulated in a mouse model. Sci. Rep. 2017, 7, 17416. [Google Scholar] [CrossRef] [Green Version]
- Zohni, K.M.; Gat, I.; Librach, C. Recurrent implantation failure: A comprehensive review. Minerva Ginecol. 2016, 68, 653–667. [Google Scholar]
- Ashary, N.; Laheri, S.; Modi, D. Homeobox genes in endometrium: From development to decidualization. Int. J. Dev. Biol. 2020, 64, 227–237. [Google Scholar] [CrossRef] [PubMed]
- Ni, N.; Li, Q. TGFβ superfamily signaling and uterine decidualization. Reprod. Biol. Endocrinol. 2017, 15, 84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Emera, D.; Romero, R.; Wagner, G. The evolution of menstruation: A new model for genetic assimilation: Explaining molecular origins of maternal responses to fetal invasiveness. Bioessays 2012, 34, 26–35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Goldstuck, N.D. Modern menstruation: Is it abnormal and unhealthy? Med. Hypotheses 2020, 144, 109955. [Google Scholar] [CrossRef]
- Evans, J.; Salamonsen, L.A. Inflammation, leukocytes and menstruation. Rev. Endocr. Metab. Disord. 2012, 13, 277–288. [Google Scholar] [CrossRef]
- Dunk, C.; Smith, S.; Hazan, A.; Whittle, W.; Jones, R.L. Promotion of angiogenesis by human endometrial lymphocytes. Immunol. Investig. 2008, 37, 583–610. [Google Scholar] [CrossRef]
- Kanter, J.R.; Mani, S.; Gordon, S.M.; Mainigi, M. Uterine natural killer cell biology and role in early pregnancy establishment and outcomes. F S Rev. 2021, 2, 265–286. [Google Scholar] [CrossRef]
- Agostinis, C.; Mangogna, A.; Bossi, F.; Ricci, G.; Kishore, U.; Bulla, R. Uterine Immunity and Microbiota: A Shifting Paradigm. Front. Immunol. 2019, 10, 2387. [Google Scholar] [CrossRef] [Green Version]
- Haig, D. Genetic conflicts in human pregnancy. Q. Rev. Biol. 1993, 68, 495–532. [Google Scholar] [CrossRef] [Green Version]
- Finn, C.A. Menstruation: A nonadaptive consequence of uterine evolution. Q. Rev. Biol. 1998, 73, 163–173. [Google Scholar] [CrossRef] [PubMed]
- Renfree, M.B. Why menstruate? Bioessays 2012, 34, 1. [Google Scholar] [CrossRef]
- Short, R.V. The evolution of human reproduction. Proc. R. Soc. Lond. B. Biol. Sci. 1976, 195, 3–24. [Google Scholar] [PubMed]
- Kaunitz, A.M. Menstruation: Choosing whether... and when. Contraception 2000, 62, 277–284. [Google Scholar] [CrossRef]
- Yang, Z.; Kong, B.; Mosser, D.M.; Zhang, X. TLRs, macrophages, and NK cells: Our understandings of their functions in uterus and ovary. Int. Immunopharmacol. 2011, 11, 1442–1450. [Google Scholar] [CrossRef] [PubMed]
- Nakashima, A.; Shima, T.; Inada, K.; Ito, M.; Saito, S. The balance of the immune system between T cells and NK cells in miscarriage. Am. J. Reprod. Immunol. 2012, 67, 304–310. [Google Scholar] [CrossRef]
- Critchley, H.O.D.; Maybin, J.A.; Armstrong, G.M.; Williams, A.R.W. Physiology of the Endometrium and Regulation of Menstruation. Physiol. Rev. 2020, 100, 1149–1179. [Google Scholar] [CrossRef]
- Turner, M.L.; Healey, G.D.; Sheldon, I.M. Immunity and inflammation in the uterus. Reprod. Domest. Anim. 2012, 47, 402–409. [Google Scholar] [CrossRef]
- Chen, C.; Song, X.; Wei, W.; Zhong, H.; Dai, J.; Lan, Z.; Li, F.; Yu, X.; Feng, Q.; Wang, Z.; et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat. Commun. 2017, 8, 875. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- An, M.; Li, D.; Yuan, M.; Li, Q.; Zhang, L.; Wang, G. Interaction of macrophages and endometrial cells induces epithelial-mesenchymal transition-like processes in adenomyosis. Biol. Reprod. 2017, 96, 46–57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mosele, S.; Stratopoulou, C.A.; Camboni, A.; Donnez, J.; Dolmans, M.M. Investigation of the role of platelets in the aetiopathogenesis of adenomyosis. Reprod. Biomed. Online 2021, 42, 826–834. [Google Scholar] [CrossRef] [PubMed]
- Bourdon, M.; Santulli, P.; Doridot, L.; Jeljeli, M.; Chêne, C.; Chouzenoux, S.; Nicco, C.; Marcellin, L.; Chapron, C.; Batteux, F. Immune cells and Notch1 signaling appear to drive the epithelial to mesenchymal transition in the development of adenomyosis in mice. Mol. Hum. Reprod. 2021, 27, gaab053. [Google Scholar] [CrossRef]
- Carrarelli, P.; Yen, C.F.; Funghi, L.; Arcuri, F.; Tosti, C.; Bifulco, G.; Luddi, A.; Lee, C.L.; Petraglia, F. Expression of Inflammatory and Neurogenic Mediators in Adenomyosis. Reprod. Sci. 2017, 24, 369–375. [Google Scholar] [CrossRef]
- Chang, H.J.; Lee, J.H.; Hwang, K.J.; Kim, M.R.; Chang, K.H.; Park, D.W.; Min, C.K. Transforming growth factor (TGF)-beta1-induced human endometrial stromal cell decidualization through extracellular signal-regulated kinase and Smad activation in vitro: Peroxisome proliferator-activated receptor gamma acts as a negative regulator of TGF-beta1. Fertil. Steril. 2008, 90, 1357–1365. [Google Scholar] [CrossRef]
- Wynn, T.A.; Vannella, K.M. Macrophages in tissue repair, regeneration, and fibrosis. Immunity 2016, 44, 450–462. [Google Scholar] [CrossRef] [Green Version]
- Shen, M.; Liu, X.; Zhang, H.; Guo, S.W. Transforming growth factor β1 signaling coincides with epithelial-mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation in the development of adenomyosis in mice. Hum. Reprod. 2016, 31, 355–3569. [Google Scholar] [CrossRef] [Green Version]
- Ibrahim, M.G.; Sillem, M.; Plendl, J.; Chiantera, V.; Sehouli, J.; Mechsner, S. Myofibroblasts Are Evidence of Chronic Tissue Microtrauma at the Endometrial-Myometrial Junctional Zone in Uteri with Adenomyosis. Reprod. Sci. 2017, 24, 1410–1418. [Google Scholar] [CrossRef]
- Kishi, Y.; Shimada, K.; Fujii, T.; Uchiyama, T.; Yoshimoto, C.; Konishi, N.; Ohbayashi, C.; Kobayashi, H. Phenotypic characterization of adenomyosis occurring at the inner and outer myometrium. PLoS ONE 2017, 12, e0189522. [Google Scholar] [CrossRef]
- Kay, N.; Huang, C.Y.; Shiu, L.Y.; Yu, Y.C.; Chang, Y.; Schatz, F.; Suen, J.L.; Tsai, E.M.; Huang, S.J. TGF-β1 Neutralization Improves Pregnancy Outcomes by Restoring Endometrial Receptivity in Mice with Adenomyosis. Reprod. Sci. 2021, 28, 877–887. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Yu, P.; Sun, F.; Li, T.C.; Cheng, J.M.; Duan, H. Expression of oxytocin receptors in the uterine junctional zone in women with adenomyosis. Acta. Obstet. Gynecol. Scand. 2015, 94, 412–418. [Google Scholar] [CrossRef] [PubMed]
- Khan, N.; Smith, M.T. Neurotrophins and Neuropathic Pain: Role in Pathobiology. Molecules 2015, 20, 10657–10688. [Google Scholar] [CrossRef] [PubMed]
- Kawamura, K.; Kawamura, N.; Sato, W.; Fukuda, J.; Kumagai, J.; Tanaka, T. Brain-derived neurotrophic factor promotes implantation and subsequent placental development by stimulating trophoblast cell growth and survival. Endocrinology 2009, 150, 3774–3782. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haider, S.; Pollheimer, J.; Knöfler, M. Notch signalling in placental development and gestational diseases. Placenta 2017, 56, 65–72. [Google Scholar] [CrossRef]
- Tremellen, K.P.; Russell, P. The distribution of immune cells and macrophages in the endometrium of women with recurrent reproductive failure. II: Adenomyosis and macrophages. J. Reprod. Immunol. 2012, 93, 58–63. [Google Scholar] [CrossRef]
- Orazov, M.R.; Radzinsky, V.E.; Nosenko, E.N.; Khamoshina, M.B.; Dukhin, A.O.; Lebedeva, M.G. Immune-inflammatory predictors of the pelvic pain syndrome associated with adenomyosis. Gynecol. Endocrinol. 2017, 33 (Suppl. S1), 44–46. [Google Scholar] [CrossRef] [Green Version]
- Zhu, B.; Chen, Y.; Shen, X.; Liu, X.; Guo, S.W. Anti-platelet therapy holds promises in treating adenomyosis: Experimental evidence. Reprod. Biol. Endocrinol. 2016, 14, 66. [Google Scholar] [CrossRef] [Green Version]
- Guo, S.W. Cracking the Enigma of Adenomyosis: An Update on Its Pathogenesis and Pathophysiology. Reproduction 2022, 164, R101–R121. [Google Scholar] [CrossRef]
- Harmsen, M.J.; Wong, C.F.C.; Mijatovic, V.; Griffioen, A.W.; Groenman, F.; Hehenkamp, W.J.K.; Huirne, J.A.F. Role of angiogenesis in adenomyosis-associated abnormal uterine bleeding and subfertility: A systematic review. Hum. Reprod. Update 2019, 25, 647–671. [Google Scholar] [CrossRef]
- Guo, S.; Zhang, D.; Lu, X.; Zhang, Q.; Gu, R.; Sun, B.; Sun, Y. Hypoxia and its possible relationship with endometrial receptivity in adenomyosis: A preliminary study. Reprod. Biol. Endocrinol. 2021, 19, 7. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Liu, J.; Gao, S.; Qiu, Y.; Wang, Y.; Zhang, Y.; Gao, L.; Qi, G.; Wu, Y.; Lash, G.E.; et al. Role of Slit2 upregulation in recurrent miscarriage through regulation of stromal decidualization. Placenta 2021, 103, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Goteri, G.; Lucarini, G.; Montik, N.; Zizzi, A.; Stramazzotti, D.; Fabris, G.; Tranquilli, A.L.; Ciavattini, A. Expression of vascular endothelial growth factor (VEGF), hypoxia inducible factor-1alpha (HIF-1alpha), and microvessel density in endometrial tissue in women with adenomyosis. Int. J. Gynecol. Pathol. 2009, 28, 157–163. [Google Scholar] [CrossRef] [PubMed]
- Yalaza, C.; Canacankatan, N.; Gürses, İ.; Aytan, H.; Taşdelen, B. Altered VEGF, Bcl-2 and IDH1 expression in patients with adenomyosis. Arch. Gynecol. Obstet. 2020, 302, 1221–1227. [Google Scholar] [CrossRef]
- Harmsen, M.J.; Arduç, A.; Bleeker, M.C.G.; Juffermans, L.J.M.; Griffioen, A.W.; Jordanova, E.S.; Huirne, J.A.F. Increased Angiogenesis and Lymphangiogenesis in Adenomyosis Visualized by Multiplex Immunohistochemistry. Int. J. Mol. Sci. 2022, 23, 8434. [Google Scholar] [CrossRef]
- Li, T.; Li, Y.G.; Pu, D.M. Matrix metalloproteinase-2 and -9 expression correlated with angiogenesis in human adenomyosis. Gynecol. Obstet. Investig. 2006, 62, 229–235. [Google Scholar] [CrossRef]
- Stratopoulou, C.A.; Camboni, A.; Donnez, J.; Dolmans, M.M. Identifying Common Pathogenic Features in Deep Endometriotic Nodules and Uterine Adenomyosis. J. Clin. Med. 2021, 10, 4585. [Google Scholar] [CrossRef]
- Lai, T.H.; Wu, P.H.; Wu, W.B. Involvement of NADPH oxidase and NF-κB activation in CXCL1 induction by vascular endothelial growth factor in human endometrial epithelial cells of patients with adenomyosis. J. Reprod. Immunol. 2016, 118, 61–69. [Google Scholar] [CrossRef]
- Wheeler, K.C.; Jena, M.K.; Pradhan, B.S.; Nayak, N.; Das, S.; Hsu, C.D.; Wheeler, D.S.; Chen, K.; Nayak, N.R. VEGF may contribute to macrophage recruitment and M2 polarization in the decidua. PLoS ONE 2018, 13, e0191040. [Google Scholar] [CrossRef]
- Guo, X.; Yi, H.; Li, T.C.; Wang, Y.; Wang, H.; Chen, X. Role of Vascular Endothelial Growth Factor (VEGF) in Human Embryo Implantation: Clinical Implications. Biomolecules 2021, 11, 253. [Google Scholar] [CrossRef]
- Wu, C.L.; Yin, R.; Wang, S.N.; Ying, R. A Review of CXCL1 in Cardiac Fibrosis. Front. Cardiovasc. Med. 2021, 8, 674498. [Google Scholar] [CrossRef] [PubMed]
- Ma, C.; Liu, G.; Liu, W.; Xu, W.; Li, H.; Piao, S.; Sui, Y.; Feng, W. CXCL1 stimulates decidual angiogenesis via the VEGF-A pathway during the first trimester of pregnancy. Mol. Cell. Biochem. 2021, 476, 2989–2998. [Google Scholar] [CrossRef]
- Garrido-Gomez, T.; Quiñonero, A.; Dominguez, F.; Rubert, L.; Perales, A.; Hajjar, K.A.; Simon, C. Preeclampsia: A defect in decidualization is associated with deficiency of Annexin A2. Am. J. Obstet. Gynecol. 2020, 222, 376.e1–376.e17. [Google Scholar] [CrossRef] [PubMed]
- Dallacasagrande, V.; Hajjar, K.A. Annexin A2 in Inflammation and Host Defense. Cells 2020, 9, 1499. [Google Scholar] [CrossRef] [PubMed]
- Zhou, S.; Yi, T.; Liu, R.; Bian, C.; Qi, X.; He, X.; Wang, K.; Li, J.; Zhao, X.; Huang, C.; et al. Proteomics identification of annexin A2 as a key mediator in the metastasis and proangiogenesis of endometrial cells in human adenomyosis. Mol. Cell. Proteom. 2012, 11, M112-017988. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, F.; Liu, L.; Zheng, J. Expression of annexin A2 in adenomyosis and dysmenorrhea. Arch. Gynecol. Obstet. 2019, 300, 711–716. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Graham, A.; Holbert, J.; Nothnick, W.B. miR-181b-5p Modulates Cell Migratory Proteins, Tissue Inhibitor of Metalloproteinase 3, and Annexin A2 During In Vitro Decidualization in a Human Endometrial Stromal Cell Line. Reprod. Sci. 2017, 24, 1264–1274. [Google Scholar] [CrossRef] [PubMed]
- Schatz, F.; Guzeloglu-Kayisli, O.; Arlier, S.; Kayisli, U.A.; Lockwood, C.J. The role of decidual cells in uterine hemostasis, menstruation, inflammation, adverse pregnancy outcomes and abnormal uterine bleeding. Hum. Reprod. Update 2016, 22, 497–515. [Google Scholar] [CrossRef] [Green Version]
- Krikun, G.; Schatz, F.; Taylor, H.; Lockwood, C.J. Endometriosis and tissue factor. Ann. N. Y. Acad. Sci. 2008, 1127, 101–105. [Google Scholar] [CrossRef] [Green Version]
- Liu, X.; Nie, J.; Guo, S.W. Elevated immunoreactivity to tissue factor and its association with dysmenorrhea severity and the amount of menses in adenomyosis. Hum. Reprod. 2011, 26, 337–345. [Google Scholar] [CrossRef] [Green Version]
- Tokyol, C.; Aktepe, F.; Dilek, F.H.; Sahin, O.; Arioz, D.T. Expression of cyclooxygenase-2 and matrix metalloproteinase-2 in adenomyosis and endometrial polyps and its correlation with angiogenesis. Int. J. Gynecol. Pathol. 2009, 28, 148–156. [Google Scholar] [CrossRef] [PubMed]
- Lockwood, C.J.; Krikun, G.; Hausknecht, V.A.; Papp, C.; Schatz, F. Matrix metalloproteinase and matrix metalloproteinase inhibitor expression in endometrial stromal cells during progestin-initiated decidualization and menstruation-related progestin withdrawal. Endocrinology 1998, 139, 4607–4613. [Google Scholar] [CrossRef] [PubMed]
- Naruse, K.; Lash, G.E.; Innes, B.A.; Otun, H.A.; Searle, R.F.; Robson, S.C.; Bulmer, J.N. Localization of matrix metalloproteinase (MMP)-2, MMP-9 and tissue inhibitors for MMPs (TIMPs) in uterine natural killer cells in early human pregnancy. Hum. Reprod. 2009, 24, 553–561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Huang, C.; Jiang, R.; Du, Y.; Zhou, J.; Jiang, Y.; Yan, Q.; Xing, J.; Hou, X.; Zhou, J.; et al. Decreased Endometrial IL-10 Impairs Endometrial Receptivity by Downregulating HOXA10 Expression in Women with Adenomyosis. BioMed Res. Int. 2018, 2018, 2549789. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, G.; Zhang, X.; Lin, H.; Wang, H.; Li, Q.; Ni, J.; Zhu, C. Effects of E-cadherin on mouse embryo implantation and expression of matrix metalloproteinase-2 and -9. Biochem. Biophys. Res. Commun. 2006, 343, 832–838. [Google Scholar] [CrossRef] [PubMed]
- Bedell, V.M.; Yeo, S.Y.; Park, K.W.; Chung, J.; Seth, P.; Shivalingappa, V.; Zhao, J.; Obara, T.; Sukhatme, V.P.; Drummond, I.A.; et al. roundabout4 is essential for angiogenesis in vivo. Proc. Natl. Acad. Sci. USA 2005, 102, 6373–6378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nie, J.; Liu, X.; Zheng, Y.; Geng, J.G.; Guo, S.W. Increased immunoreactivity to SLIT/ROBO1 and its correlation with severity of dysmenorrhea in adenomyosis. Fertil. Steril. 2011, 95, 1164–1167. [Google Scholar] [CrossRef]
- Shen, F.; Liu, X.; Geng, J.G.; Guo, S.W. Increased immunoreactivity to SLIT/ROBO1 in ovarian endometriomas. Am. J. Pathol. 2009, 175, 479–488. [Google Scholar] [CrossRef] [Green Version]
- Kolioulis, I.; Zafrakas, M.; Grimbizis, G.; Miliaras, D.; Timologou, A.; Bontis, J.N.; Tarlatzis, B.C. Immunohistochemical expression pattern of metastasis suppressor KISS-1 protein in adenomyosis lesions and normal endometrium. Eur. J. Obstet. Gynecol. Reprod. Biol. 2017, 210, 64–68. [Google Scholar] [CrossRef]
- Wu, H.M.; Huang, H.Y.; Soong, Y.K.; Leung, P.C.K.; Wang, H.S. Kisspeptin regulation of human decidual stromal cells motility via FAK-Src intracellular tyrosine kinases. Hum. Reprod. 2019, 34, 1291–1301. [Google Scholar] [CrossRef]
- Tamura, I.; Maekawa, R.; Jozaki, K.; Ohkawa, Y.; Takagi, H.; Doi-Tanaka, Y.; Shirafuta, Y.; Mihara, Y.; Taketani, T.; Sato, S.; et al. Transcription factor C/EBPβ induces genome-wide H3K27ac and upregulates gene expression during decidualization of human endometrial stromal cells. Mol. Cell. Endocrinol. 2021, 520, 111085. [Google Scholar] [CrossRef] [PubMed]
- Xiang, Y.; Sun, Y.; Yang, B.; Yang, Y.; Zhang, Y.; Yu, T.; Huang, H.; Zhang, J.; Xu, H. Transcriptome sequencing of adenomyosis eutopic endometrium: A new insight into its pathophysiology. J. Cell. Mol. Med. 2019, 23, 8381–8391. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Taylor, R.N.; Bagchi, I.C.; Bagchi, M.K. Regulation of human endometrial stromal proliferation and differentiation by C/EBPbeta involves cyclin E-cdk2 and STAT3. Mol. Endocrinol. 2012, 26, 2016–2030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, H.S.; Tsai, C.L.; Chang, P.Y.; Chao, A.; Wu, R.C.; Chen, S.H.; Wang, C.J.; Yen, C.F.; Lee, Y.S.; Wang, T.H. Positive associations between upregulated levels of stress-induced phosphoprotein 1 and matrix metalloproteinase-9 in endometriosis/adenomyosis. PLoS ONE 2018, 13, e0190573. [Google Scholar] [CrossRef] [Green Version]
- Kalakonda, S.; Nallar, S.C.; Gong, P.; Lindner, D.J.; Goldblum, S.E.; Reddy, S.P.; Kalvakolanu, D.V. Tumor suppressive protein gene associated with retinoid-interferon-induced mortality (GRIM)-19 inhibits src-induced oncogenic transformation at multiple levels. Am. J. Pathol. 2007, 171, 1352–1368. [Google Scholar] [CrossRef] [Green Version]
- Yang, Y.; Sun, Y.; Cheng, L.; Li, A.; Shen, Y.; Jiang, L.; Deng, X.; Chao, L. GRIM-19, a gene associated with retinoid-interferon-induced mortality, affects endometrial receptivity and embryo implantation. Reprod. Fertil. Dev. 2017, 29, 1447–1455. [Google Scholar] [CrossRef]
- Wang, J.; Deng, X.; Yang, Y.; Yang, X.; Kong, B.; Chao, L. Expression of GRIM-19 in adenomyosis and its possible role in pathogenesis. Fertil. Steril. 2016, 105, 1093–1101. [Google Scholar] [CrossRef] [Green Version]
- Liu, H.; Zhao, Y.; Yang, Y.; Huang, W.; Chao, L. GRIM19 downregulation-induced pyroptosis of macrophages through NLRP3 pathway in adenomyosis. Reprod. Biomed. Online 2022, 44, 211–219. [Google Scholar] [CrossRef]
- Wang, B.; Yang, Y.; Deng, X.; Ban, Y.; Chao, L. Interaction of M2 macrophages and endometrial cells induces downregulation of GRIM-19 in endometria of adenomyosis. Reprod. Biomed. Online 2020, 41, 790–800. [Google Scholar] [CrossRef]
- Zhao, L.; Zhou, S.; Zou, L.; Zhao, X. The expression and functionality of stromal caveolin 1 in human adenomyosis. Hum. Reprod. 2013, 28, 1324–1338. [Google Scholar] [CrossRef] [Green Version]
- Song, Z.; Li, B.; Li, M.; Luo, J.; Hong, Y.; He, Y.; Chen, S.; Yang, Z.; Liang, C.; Yang, Z. Caveolin-1 Regulation and Function in Mouse Uterus during Early Pregnancy and under Human In Vitro Decidualization. Int. J. Mol. Sci. 2022, 23, 3699. [Google Scholar] [CrossRef] [PubMed]
- Chiossone, L.; Vacca, P.; Orecchia, P.; Croxatto, D.; Damonte, P.; Astigiano, S.; Barbieri, O.; Bottino, C.; Moretta, L.; Mingari, M.C. In vivo generation of decidual natural killer cells from resident hematopoietic progenitors. Haematologica 2014, 99, 448–457. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Propst, A.M.; Quade, B.J.; Nowak, R.A.; Stewart, E.A. Granulocyte macrophage colony-stimulating factor in adenomyosis and autologous endometrium. J. Soc. Gynecol. Investig. 2002, 9, 93–97. [Google Scholar] [CrossRef] [PubMed]
- Kulp, J.L.; Mamillapalli, R.; Taylor, H.S. Aberrant HOXA10 Methylation in Patients with Common Gynecologic Disorders: Implications for Reproductive Outcomes. Reprod. Sci. 2016, 23, 455–463. [Google Scholar] [CrossRef] [Green Version]
- Nie, J.; Liu, X.; Guo, S.W. Promoter hypermethylation of progesterone receptor isoform B (PR-B) in adenomyosis and its rectification by a histone deacetylase inhibitor and a demethylation agent. Reprod. Sci. 2010, 17, 995–1005. [Google Scholar] [CrossRef]
- Benagiano, G.; Brosens, I.; Habiba, M. Structural and molecular features of the endomyometrium in endometriosis and adenomyosis. Hum. Reprod. Update 2014, 20, 386–402. [Google Scholar] [CrossRef]
- Maybin, J.A.; Critchley, H.O. Menstrual physiology: Implications for endometrial pathology and beyond. Hum. Reprod. Update 2015, 21, 748–761. [Google Scholar] [CrossRef] [Green Version]
- Gan, L.; Li, Y.; Chen, Y.; Huang, M.; Cao, J.; Cao, M.; Wang, Z.; Wan, G.; Gui, T. Transcriptome analysis of eutopic endometrial stromal cells in women with adenomyosis by RNA-sequencing. Bioengineered 2022, 13, 12637–12649. [Google Scholar] [CrossRef]
- Streuli, I.; Santulli, P.; Chouzenoux, S.; Chapron, C.; Batteux, F. Activation of the MAPK/ERK cell-signaling pathway in uterine smooth muscle cells of women with adenomyosis. Reprod. Sci. 2015, 22, 1549–1560. [Google Scholar] [CrossRef]
- Li, Y.; Li, H.; Xie, N.; Chen, R.; Lee, A.R.; Slater, D.; Lye, S.; Dong, X. HoxA10 and HoxA11 Regulate the Expression of Contraction-Associated Proteins and Contribute to Regionalized Myometrium Phenotypes in Women. Reprod. Sci. 2018, 25, 44–50. [Google Scholar] [CrossRef] [Green Version]
- Godbole, G.; Suman, P.; Malik, A.; Galvankar, M.; Joshi, N.; Fazleabas, A.; Gupta, S.K.; Modi, D. Decrease in Expression of HOXA10 in the Decidua After Embryo Implantation Promotes Trophoblast Invasion. Endocrinology 2017, 158, 2618–2633. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, J.H.; Wu, M.Y.; Chang, D.Y.; Chang, C.H.; Yang, Y.S.; Ho, H.N. Increased interleukin-6 messenger RNA expression in macrophage-cocultured endometrial stromal cells in adenomyosis. Am. J. Reprod. Immunol. 2006, 55, 181–187. [Google Scholar] [CrossRef] [PubMed]
- Özçelik, K.; Çapar, M.; Gazi Uçar, M.; Çakιr, T.; Özçelik, F.; Tuyan Ilhan, T. Are cytokine levels in serum, endometrial tissue, and peritoneal fluid a promising predictor to diagnosis of endometriosis-adenomyosis? Clin. Exp. Obstet. Gynecol. 2016, 43, 569–572. [Google Scholar] [CrossRef] [PubMed]
- Barkett, M.; Gilmore, T.D. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 1999, 18, 6910–6924. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nakamura, H.; Kimura, T.; Ogita, K.; Koyama, S.; Tsujie, T.; Tsutsui, T.; Shimoya, K.; Koyama, M.; Kaneda, Y.; Murata, Y. Alteration of the timing of implantation by in vivo gene transfer: Delay of implantation by suppression of nuclear factor kappaB activity and partial rescue by leukemia inhibitory factor. Biochem. Biophys. Res. Commun. 2004, 321, 886–892. [Google Scholar] [CrossRef]
- Nie, J.; Lu, Y.; Liu, X.; Guo, S.W. Immunoreactivity of progesterone receptor isoform B, nuclear factor kappaB, and IkappaBalpha in adenomyosis. Fertil. Steril. 2009, 92, 886–889. [Google Scholar] [CrossRef]
- Shang, W.Q.; Yu, J.J.; Zhu, L.; Zhou, W.J.; Chang, K.K.; Wang, Q.; Li, M.Q. Blocking IL-22, a potential treatment strategy for adenomyosis by inhibiting crosstalk between vascular endothelial and endometrial stromal cells. Am. J. Transl. Res. 2015, 7, 1782–1797. [Google Scholar]
- Wang, Q.; Wang, L.; Shao, J.; Wang, Y.; Jin, L.P.; Li, D.J.; Li, M.Q. L-22 enhances the invasiveness of endometrial stromal cells of adenomyosis in an autocrine manner. Int. J. Clin. Exp. Pathol. 2014, 7, 5762–5771. [Google Scholar]
- Wang, Y.; Xu, B.; Li, M.Q.; Li, D.J.; Jin, L.P. IL-22 secreted by decidual stromal cells and NK cells promotes the survival of human trophoblasts. Int. J. Clin. Exp. Pathol. 2013, 6, 1781–1790. [Google Scholar]
- Li, C.; Chen, R.; Jiang, C.; Chen, L.; Cheng, Z. Correlation of LOX-5 and COX-2 expression with inflammatory pathology and clinical features of adenomyosis. Mol. Med. Rep. 2019, 19, 727–733. [Google Scholar] [CrossRef] [Green Version]
- Shukla, V.; Kaushal, J.B.; Sankhwar, P.; Manohar, M.; Dwivedi, A. Inhibition of TPPP3 attenuates β-catenin/NF-κB/COX-2 signaling in endometrial stromal cells and impairs decidualization. J. Endocrinol. 2019, 240, 417–429. [Google Scholar] [CrossRef] [PubMed]
- Fujiwara, H.; Matsumoto, H.; Sato, Y.; Horie, A.; Ono, M.; Nakamura, M.; Mizumoto, Y.; Kagami, K.; Fujiwara, T.; Hattori, A.; et al. Factors Regulating Human Extravillous Trophoblast Invasion: Chemokine-peptidase and CD9-integrin Systems. Curr. Pharm. Biotechnol. 2018, 19, 764–770. [Google Scholar] [CrossRef]
- Kunaseth, J.; Waiyaput, W.; Chanchaem, P.; Sawaswong, V.; Permpech, R.; Payungporn, S.; Sophonsritsuk, A. Vaginal microbiome of women with adenomyosis: A case-control study. PLoS ONE 2022, 17, e0263283. [Google Scholar] [CrossRef] [PubMed]
- Jiang, C.; Liu, C.; Guo, J.; Chen, L.; Luo, N.; Qu, X.; Yang, W.; Ren, Q.; Cheng, Z. The Expression of Toll-like receptors in eutopic and ectopic endometrium and its implication in the inflammatory pathogenesis of adenomyosis. Sci. Rep. 2017, 7, 7365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khan, K.N.; Fujishita, A.; Ogawa, K.; Koshiba, A.; Mori, T.; Itoh, K.; Nakashima, M.; Kitawaki, J. Occurrence of chronic endometritis in different types of human adenomyosis. Reprod. Med. Biol. 2021, 21, e12421. [Google Scholar] [CrossRef] [PubMed]
- Critchley, H.O.D.; Babayev, E.; Bulun, S.E.; Clark, S.; Garcia-Grau, I.; Gregersen, P.K.; Kilcoyne, A.; Kim, J.J.; Lavender, M.; Marsh, E.E.; et al. Menstruation: Science and society. Am. J. Obstet. Gynecol. 2020, 223, 624–664. [Google Scholar] [CrossRef]
- Pei, Z.; Lu, W.; Feng, Y.; Xu, C.; Hsueh, A.J.W. Out of step societal and Darwinian adaptation during evolution is the cause of multiple women’s health issues. Hum. Reprod. 2022, 37, 1959–1969. [Google Scholar] [CrossRef]
- Lee, S.K.; Kim, C.J.; Kim, D.J.; Kang, J.H. Immune cells in the female reproductive tract. Immune Netw. 2015, 15, 16–26. [Google Scholar] [CrossRef] [Green Version]
- Maekawa, R.; Tamura, I.; Shinagawa, M.; Mihara, Y.; Sato, S.; Okada, M.; Taketani, T.; Tamura, H.; Sugino, N. Genome-wide DNA methylation analysis revealed stable DNA methylation status during decidualization in human endometrial stromal cells. BMC Genom. 2019, 20, 324. [Google Scholar] [CrossRef] [Green Version]
- Karowicz-Bilinska, A.; Plodzidym, M.; Krol, J.; Lewinska, A.; Bartosz, G. Changes of markers of oxidative stress during menstrual cycle. Redox Rep. 2008, 13, 237–240. [Google Scholar] [CrossRef]
- Liu, H.; Huang, X.; Mor, G.; Liao, A. Epigenetic modifications working in the decidualization and endometrial receptivity. Cell Mol. Life Sci. 2020, 77, 2091–2101. [Google Scholar] [CrossRef]
- MacLean, J.A., 2nd; Hayashi, K. Progesterone Actions and Resistance in Gynecological Disorders. Cells 2022, 11, 647. [Google Scholar] [CrossRef] [PubMed]
- Bourdon, M.; Santulli, P.; Jeljeli, M.; Vannuccini, S.; Marcellin, L.; Doridot, L.; Petraglia, F.; Batteux, F.; Chapron, C. Immunological changes associated with adenomyosis: A systematic review. Hum. Reprod. Update 2021, 27, 108–129. [Google Scholar] [CrossRef] [PubMed]
- Hardbower, D.M.; de Sablet, T.; Chaturvedi, R.; Wilson, K.T. Chronic inflammation and oxidative stress: The smoking gun for Helicobacter pylori-induced gastric cancer? Gut Microbes 2013, 4, 475–481. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Amro, B.; Ramirez Aristondo, M.E.; Alsuwaidi, S.; Almaamari, B.; Hakim, Z.; Tahlak, M.; Wattiez, A.; Koninckx, P.R. New Understanding of Diagnosis, Treatment and Prevention of Endometriosis. Int. J. Environ. Res. Public Health 2022, 19, 6725. [Google Scholar] [CrossRef] [PubMed]
Search Mode | The Keyword and Search Term Combinations |
---|---|
Search term 1 | Adenomyosis |
Search term 2 | Inflammation OR Microbiota |
Search term 3 | Innate immunity OR Adaptive immunity OR Aquired immunity |
Search term 4 | Menstruation OR Menses |
Search term 5 | Decidualization OR Decidua OR Implantation |
Search term 6 | Angiogenesis OR Vasculogenesis |
Search term 7 | Fibrosis OR Fibrogenesis |
Search | Search term 1 AND Search term 2 |
Search term 1 AND Search term 3 | |
Search term 1 AND Search term 4 | |
Search term 1 AND Search term 5 | |
Search term 1 AND Search term 6 | |
Search term 1 AND Search term 7 |
Official Symbol | Official Full Name | Summary | Refs. |
---|---|---|---|
TGFB | transforming growth factor-beta | Smad↑EMT↑FMT↑SMM↑fibrosis↑LIF↑↓; induce or inhibit decidualization | [11,15,33,36,37,38,39,40,41] |
OXTR | oxytocin receptor | COX-2↓PGF2α↓; suppression of decidualization process | [42] |
NTRK2 | neurotrophic receptor tyrosine kinase 2, also known as TrkB | Blastocyst outgrowth↑ | [43,44] |
NOTCH1 | notch receptor 1 | Decidualization and implantation↑ | [45] |
Official Symbol | Official Full Name | Summary | Refs. |
---|---|---|---|
HIF1A | hypoxia inducible factor 1 subunit alpha | Microvessel density↑fibrogenesis↑VEGF↑HOXA10↓HOXA11↓; suppression of decidualization process | [51,53,54] |
VEGFA | vascular endothelial growth factor A | CXCL1↑NF-κB↑M2 polarization↑; promotion of decidualization process | [53,54,55,56,57,58,59,60] |
CXCL1 | C-X-C motif chemokine ligand 1 | Tissue remodeling↑VEGF↑; promotion of decidualization process | [4,61,62] |
ANXA2 | annexin A2 | HIF-1α↑VEGF-A↑β-catenin↑; promotion of decidualization process | [63,64,65,66,67] |
F3 | coagulation factor III, also known as tissue factor | Thrombin↑PRB↓; stabilization of decidualization due to promotion of hemostasis | [50,68,69,70] |
MMP-2, MMP-9 | matrix metallopeptidase 2, matrix metallopeptidase 9 | Endometrial menstrual breakdown↑ | [18,50,56,71,72,73] |
IL10 | interleukin 10 | Anti-angiogenic marker. IL-10↓ during the window of implantation. NF-κB↑HOXA10↓ | [50,74] |
CDH1 | cadherin 1, also known as E-cadherin | Anti-angiogenic marker. MMP2↓MMP9↓; stimulation of the implantation process | [50,75] |
SLIT2 | slit guidance ligand 2 | SLIT-ROBO signaling; suppression of decidualization process | [52,76,77,78,79] |
KISS1 | KiSS-1 metastasis suppressor | Cell motility in human decidual stromal cells↓; progression of decidualization process | [79,80] |
CEBPB | CCAAT enhancer binding protein beta, also known as C/EBPβ | IGFBP-1↑PRL↑; stimulation of decidualization process | [81,82,83] |
STIP1 | stress-induced phosphoprotein 1 | MMP9↑endometrial menstrual breakdown↑ | [84] |
NDUFA13 | NADH:ubiquinone oxidoreductase subunit A13 (NDUFA13), also known as retinoid-interferon (IFN)-induced mortality 19 (GRIM-19) | GRIM19↓(macrophages) IL-1β↑VEGF↑; suppression of decidualization process | [85,86,87,88,89] |
CAV1 | caveolin 1 | CAV1↓IGFBP1↑; stimulation of decidualization process | [90,91] |
CSF2 | colony stimulating factor 2, also known as GMCSF | Macrophage recruitment | [92,93] |
Official Symbol | Official Full Name | Summary | Refs. |
---|---|---|---|
IL6, IL8 | interleukin 6, interleukin 8 | HoxA10↓HoxA11↓MMP↑TIMP↓; suppression of decidualization process | [82,98,99,100,101,102,103] |
NFKB1 | nuclear factor kappa B subunit 1 | LIF↓PRB↓; suppression of decidualization process | [3,64,104,105,106] |
IL22 | interleukin 22 | IL-6↑IL-8↑RANTES↑VEGF↑; suppression of decidualization process | [107,108,109] |
PTGS2 | prostaglandin-endoperoxide synthase 2, also known as COX-2 | IL-6↑IL-8↑; suppression of decidualization process | [110,111] |
CCL5 | C-C motif chemokine ligand 5, also known as RANTES (regulated upon activation, normal T-cell expressed and secreted) | Trophoblast invasion during early human placentation | [90,112] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kobayashi, H. Endometrial Inflammation and Impaired Spontaneous Decidualization: Insights into the Pathogenesis of Adenomyosis. Int. J. Environ. Res. Public Health 2023, 20, 3762. https://doi.org/10.3390/ijerph20043762
Kobayashi H. Endometrial Inflammation and Impaired Spontaneous Decidualization: Insights into the Pathogenesis of Adenomyosis. International Journal of Environmental Research and Public Health. 2023; 20(4):3762. https://doi.org/10.3390/ijerph20043762
Chicago/Turabian StyleKobayashi, Hiroshi. 2023. "Endometrial Inflammation and Impaired Spontaneous Decidualization: Insights into the Pathogenesis of Adenomyosis" International Journal of Environmental Research and Public Health 20, no. 4: 3762. https://doi.org/10.3390/ijerph20043762