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 ORCID:

Zhijian SU

https://orcid.org/0000-0001-6261-1294

Xiaokun LI

https://orcid.org/0000-0002-6556-6262

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Journal of Zhejiang University SCIENCE B 2025 Vol.26 No.6 P.573-588

http://doi.org/10.1631/jzus.B2300830


Fibroblast growth factors and endometrial decidualization: models, mechanisms, and related pathologies


Author(s):  Xueni ZHANG, Yidi MO, Chunbin LU, Zhijian SU, Xiaokun LI

Affiliation(s):  Department of Developmental Biology and Regenerative Medicine, Jinan University, Guangzhou 510632, China; more

Corresponding email(s):   tjnuszj@jnu.edu.cn, xiaokunli@wmu.edu.cn

Key Words:  Fibroblast growth factor (FGF), Decidualization, Pregnancy, Adverse pregnancy outcome


Xueni ZHANG, Yidi MO, Chunbin LU, Zhijian SU, Xiaokun LI. Fibroblast growth factors and endometrial decidualization: models, mechanisms, and related pathologies[J]. Journal of Zhejiang University Science B, 2025, 26(6): 573-588.

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author="Xueni ZHANG, Yidi MO, Chunbin LU, Zhijian SU, Xiaokun LI",
journal="Journal of Zhejiang University Science B",
volume="26",
number="6",
pages="573-588",
year="2025",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2300830"
}

%0 Journal Article
%T Fibroblast growth factors and endometrial decidualization: models, mechanisms, and related pathologies
%A Xueni ZHANG
%A Yidi MO
%A Chunbin LU
%A Zhijian SU
%A Xiaokun LI
%J Journal of Zhejiang University SCIENCE B
%V 26
%N 6
%P 573-588
%@ 1673-1581
%D 2025
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2300830

TY - JOUR
T1 - Fibroblast growth factors and endometrial decidualization: models, mechanisms, and related pathologies
A1 - Xueni ZHANG
A1 - Yidi MO
A1 - Chunbin LU
A1 - Zhijian SU
A1 - Xiaokun LI
J0 - Journal of Zhejiang University Science B
VL - 26
IS - 6
SP - 573
EP - 588
%@ 1673-1581
Y1 - 2025
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2300830


Abstract: 
The onset of pregnancy is marked by the formation of a zygote, while the culmination of gestation is manifested by the delivery of a fetus. Meanwhile, a successful pregnancy entails a meticulously coordinated sequence of events from embryo implantation to sustained decidualization of the uterus to placental development and childbirth. The decidual reaction, a pivotal process occurring within the endometrium during pregnancy, is finely regulated by sex steroids and cytokines. Notably, fibroblast growth factors (FGFs), particularly FGF2, play a critical role in this physiological cascade. Dysregulated FGF expression may trigger inadequate decidualization, precipitating a spectrum of adverse pregnancy outcomes, including preeclampsia, recurrent implantation failure, and miscarriage. Furthermore, the human decidua, distinct from most mammalian species and similar to great apes, undergoes regular cycles of formation and shedding, independent of the presence of the embryo in the endometrium. This process is also tightly controlled by various FGFs. In this review, we comprehensively compare diverse research decidualization models, delineate the trend of endometrial FGFs during the menstrual cycle, and provide a synopsis of endometrial diseases triggered by FGF dysregulation.

成纤维细胞生长因子与子宫内膜蜕膜化:模型、机制和相关病理学

张雪妮1,莫一迪1,芦春斌1,苏志坚1,2,3,李校堃4
1暨南大学发育与再生生物学系,中国广州市,510632
2暨南大学细胞生物学系,广东省生物医学工程重点实验室,中国广州市,510632
3暨南大学基因工程药物国家工程研究中心,中国广州市,510632
4温州医科大学大分子药物与规模化制备全国重点实验室,中国温州市,325035
摘要:受精卵的形成代表妊娠的开始,胎儿的分娩则代表妊娠的结束。成功怀孕需要一系列精心策划的阶段:胚胎植入、子宫持续蜕膜化、胎盘形成和分娩。蜕膜化是妊娠期间子宫内膜发生的重要事件,需要性激素和细胞因子精确调节。其中,成纤维细胞生长因子(FGFs),尤其是FGF2,在这一生理过程中发挥着至关重要的作用。FGF的表达失调可导致蜕膜化不足,进而引发包括先兆子痫、反复着床失败和流产等多种不良妊娠结局。此外,与大多数哺乳动物物种不同,人类子宫内膜的蜕膜化具有规律性的形成和脱落周期,与胚胎是否存在无关。在这篇综述中,我们全面比较各种研究蜕膜化的模型,同时总结子宫内膜FGFs在月经周期中的变化趋势以及由FGF失调引发的子宫内膜疾病。

关键词:成纤维细胞生长因子(FGF);蜕膜化;妊娠;不良妊娠结局

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]AfrinS, el SabahM, ManzoorA, et al., 2023. Adipocyte coculture induces a pro-inflammatory, fibrotic, angiogenic, and proliferative microenvironment in uterine leiomyoma cells. Biochim Biophys Acta (BBA)-Mol Basis Dis, 1869(1):166564.

[2]AfsharY, MieleL, FazleabasAT, 2012. Notch1 is regulated by chorionic gonadotropin and progesterone in endometrial stromal cells and modulates decidualization in primates. Endocrinology, 153(6):2884-2896.

[3]BaerwaldAR, AdamsGP, PiersonRA, 2012. Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum Reprod Update, 18(1):73-91.

[4]BhurkeAS, BagchiIC, BagchiMK, 2016. Progesterone-regulated endometrial factors controlling implantation. Am J Reprod Immunol, 75(3):237-245.

[5]Bodner-AdlerB, MayerhoferK, CzerwenkaK, et al., 2016. The role of fibroblast growth factor 2 in patients with uterine smooth muscle tumors: an immunohistochemical study. Eur J Obstet Gynecol Reprod Biol, 207:62-67.

[6]BorahayMA, Al-HendyA, KilicGS, et al., 2015. Signaling pathways in leiomyoma: understanding pathobiology and implications for therapy. Mol Med, 21(1):242-256.

[7]Buell-AcostaJD, GarcesMF, Parada-BañosAJ, et al., 2022. Maternal fibroblast growth factor 21 levels decrease during early pregnancy in normotensive pregnant women but are higher in preeclamptic women—a longitudinal study. Cells, 11(14):2251.

[8]ChavanAR, GriffithOW, WagnerGP, 2017. The inflammation paradox in the evolution of mammalian pregnancy: turning a foe into a friend. Curr Opin Genet Dev, 47:24-32.

[9]ChengJH, LiangJ, LiYZ, et al., 2022. Shp2 in uterine stromal cells critically regulates on time embryo implantation and stromal decidualization by multiple pathways during early pregnancy. PLoS Genet, 18(1):e1010018.

[10]ChengJH, ShaZZ, LiJY, et al., 2023. Progress on the role of estrogen and progesterone signaling in mouse embryo implantation and decidualization. Reprod Sci, 30(6):1746-1757.

[11]ChoJH, YoonMS, KooJB, et al., 2011. The progesterone receptor as a transcription factor regulates phospholipase D1 expression through independent activation of protein kinase A and Ras during 8-Br-cAMP-induced decidualization in human endometrial stromal cells. Biochem J, 436(1):181-191.

[12]ChungD, GaoF, JeggaAG, et al., 2015. Estrogen mediated epithelial proliferation in the uterus is directed by stromal Fgf10 and Bmp8a. Mol Cell Endocrinol, 400:48-60.

[13]ConradKP, RabaglinoMB, Post UiterweerED, 2017. Emerging role for dysregulated decidualization in the genesis of preeclampsia. Placenta, 60:119-129.

[14]DambaevaS, BilalM, SchneidermanS, et al., 2021. Decidualization score identifies an endometrial dysregulation in samples from women with recurrent pregnancy losses and unexplained infertility. F S Rep, 2(1):95-103.

[15]de ClercqK, HennesA, VriensJ, 2017. Isolation of mouse endometrial epithelial and stromal cells for in vitro decidualization. J Vis Exp, (121):55168.

[16]DeySK, LimH, DasSK, et al., 2004. Molecular cues to implantation. Endocr Rev, 25(3):341-373.

[17]DingJH, TanXJ, SongKK, et al., 2018. Bushen Huoxue recipe alleviates implantation loss in mice by enhancing estrogen-progesterone signals and promoting decidual angiogenesis through FGF2 during early pregnancy. Front Pharmacol, 9:437.

[18]DingJL, YinTL, YanNN, et al., 2019. FasL on decidual macrophages mediates trophoblast apoptosis: a potential cause of recurrent miscarriage. Int J Mol Med, 43(6):2376-2386.

[19]DingNZ, QiQR, GuXW, et al., 2018. De novo synthesis of sphingolipids is essential for decidualization in mice. Theriogenology, 106:227-236.

[20]DuncanWC, 2021. The inadequate corpus luteum. Reprod Fertil, 2(1):C1-C7.

[21]EmeraD, RomeroR, WagnerG, 2012. The evolution of menstruation: a new model for genetic assimilation: explaining molecular origins of maternal responses to fetal invasiveness. BioEssays, 34(1):26-35.

[22]EstellaC, HerrerI, Moreno-MoyaJM, et al., 2012. miRNA signature and Dicer requirement during human endometrial stromal decidualization in vitro. PLoS ONE, 7(7):e41080.

[23]EvansJ, SalamonsenLA, WinshipA, et al., 2016. Fertile ground: human endometrial programming and lessons in health and disease. Nat Rev Endocrinol, 12(11):654-667.

[24]FabiF, GrenierK, ParentS, et al., 2017. Regulation of the PI3K/Akt pathway during decidualization of endometrial stromal cells. PLoS ONE, 12(5):e0177387.

[25]FangZS, TianY, SuiC, et al., 2022. Single-cell transcriptomics of proliferative phase endometrium: systems analysis of cell‒cell communication network using CellChat. Front Cell Dev Biol, 10:919731.

[26]FerrianiRA, Charnock-JonesDS, PrenticeA, et al., 1993. Immunohistochemical localization of acidic and basic fibroblast growth factors in normal human endometrium and endometriosis and the detection of their mRNA by polymerase chain reaction. Hum Reprod, 8(1):11-16.

[27]FigueroaV, RodríguezMS, LanariC, et al., 2019. Nuclear action of FGF members in endocrine-related tissues and cancer: interplay with steroid receptor pathways. Steroids, 152:108492.

[28]FlanneryCA, FlemingAG, ChoeGH, et al., 2016. Endometrial cancer-associated FGF18 expression is reduced by bazedoxifene in human endometrial stromal cells in vitro and in murine endometrium. Endocrinology, 157(10):3699-3708.

[29]FuT, ZhengHT, ZhangHY, et al., 2019. Oncostatin M expression in the mouse uterus during early pregnancy promotes embryo implantation and decidualization. FEBS Lett, 593(15):2040-2050.

[30]FujimotoJ, HoriM, IchigoS, et al., 1996a. Ability of ovarian steroids to regulate the expression of the fibroblast growth factor family in fibroblasts derived from uterine endometrium. J Biomed Sci, 3(4):280-285.

[31]FujimotoJ, HoriM, IchigoS, et al., 1996b. Expression of basic fibroblast growth factor and its mRNA in uterine endometrium during the menstrual cycle. Gynecol Endocrinol, 10(3):193-197.

[32]Garrido-GomezT, QuiñoneroA, DominguezF, et al., 2020. Preeclampsia: a defect in decidualization is associated with deficiency of Annexin A2. Am J Obstet Gynecol, 222(4):376.e1-376.e17.

[33]Garrido-GómezT, Castillo-MarcoN, CorderoT, et al., 2022. Decidualization resistance in the origin of preeclampsia. Am J Obstet Gynecol, 226(2S):S886-S894.

[34]GellersenB, ReimannK, SamalecosA, et al., 2010. Invasiveness of human endometrial stromal cells is promoted by decidualization and by trophoblast-derived signals. Hum Reprod, 25(4):862-873.

[35]GibsonDA, SimitsidellisI, CousinsFL, et al., 2016. Intracrine androgens enhance decidualization and modulate expression of human endometrial receptivity genes. Sci Rep, 6:19970.

[36]GongH, WuWQ, XuJJ, et al., 2019. Flutamide ameliorates uterine decidualization and angiogenesis in the mouse hyperandrogenemia model during mid-pregnancy. PLoS ONE, 14(5):e0217095.

[37]GuoB, TianXC, LiDD, et al., 2014. Expression, regulation and function of Egr1 during implantation and decidualization in mice. Cell Cycle, 13(16):2626-2640.

[38]HagueS, ManekS, OehlerMK, et al., 2002. Tamoxifen induction of angiogenic factor expression in endometrium. Br J Cancer, 86(5):761-767.

[39]HalariCD, NandiP, JeyarajahMJ, et al., 2020. Decorin production by the human decidua: role in decidual cell maturation. Mol Hum Reprod, 26(10):784-796.

[40]HassanE, KojimaR, OzawaF, et al., 2022. Abnormal ciliogenesis in decidual stromal cells in recurrent miscarriage. J Reprod Immunol, 150:103486.

[41]HelmkeBM, MarkowskiDN, MüllerMH, et al., 2011. HMGA proteins regulate the expression of FGF2 in uterine fibroids. Mol Hum Reprod, 17(2):135-142.

[42]JagodzińskaA, Chudecka-GłazA, MichalczykK, et al., 2023. The diagnostic role of FGF 21 in endometrial cancer and other pathologies of the uterine corpus. Diagnostics, 13(3):399.

[43]JiangYL, LiaoYX, HeH, et al., 2015. FoxM1 directs STAT3 expression essential for human endometrial stromal decidualization. Sci Rep, 5:13735.

[44]JinZY, LiuCK, HongYQ, et al., 2022. BHPF exposure impairs mouse and human decidualization. Environ Pollut, 304:119222.

[45]JonesRL, SalamonsenLA, FindlayJK, 2002. Activin A promotes human endometrial stromal cell decidualization in vitro. J Clin Endocrinol Metab, 87(8):4001-4004.

[46]JukicAM, BairdDD, WeinbergCR, et al., 2013. Length of human pregnancy and contributors to its natural variation. Hum Reprod, 28(10):2848-2855.

[47]KajiharaT, BrosensJJ, IshiharaO, 2013. The role of FOXO1 in the decidual transformation of the endometrium and early pregnancy. Med Mol Morphol, 46(2):61-68.

[48]KatoN, IwaseA, IshidaC, et al., 2019. Upregulation of fibroblast growth factors caused by heart and neural crest derivatives expressed 2 suppression in endometriotic cells: a possible therapeutic target in endometriosis. Reprod Sci, 26(7):979-987.

[49]KimuraF, TakakuraK, TakebayashiK, et al., 2001. Messenger ribonucleic acid for the mouse decidual prolactin is present and induced during in vitro decidualization of endometrial stromal cells. Gynecol Endocrinol, 15(6):426-432.

[50]KusamaK, YamauchiN, YoshidaK, et al., 2021. Senolytic treatment modulates decidualization in human endometrial stromal cells. Biochem Biophys Res Commun, 571:174-180.

[51]LarraínD, PradoJ, 2024. New insights into molecular pathogenesis of uterine fibroids: from the lab to a clinician-friendly review. In: Hamid GA (Ed.), Soft Tissue Sarcoma and Leiomyoma—Diagnosis, Management, and New Perspectives. IntechOpen, London, UK, p.91-122.

[52]LashGE, ErnerudhJ, 2015. Decidual cytokines and pregnancy complications: focus on spontaneous miscarriage. J Reprod Immunol, 108:83-89.

[53]LiB, YanYP, LiangC, et al., 2022. Primary cilia restrain PI3K-AKT signaling to orchestrate human decidualization. Int J Mol Sci, 23(24):15573.

[54]LiDD, GaoYJ, TianXC, et al., 2014. Differential expression and regulation of Tdo2 during mouse decidualization. J Endocrinol, 220(1):73-83.

[55]LiMJ, ZhangH, ZhaoXB, et al., 2014. SPRY4-mediated ERK1/2 signaling inhibition abolishes 17β-estradiol-induced cell growth in endometrial adenocarcinoma cell. Gynecol Endocrinol, 30(8):600-604.

[56]LiQX, KannanA, DemayoFJ, et al., 2011. The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science, 331(6019):912-916.

[57]LiXK, WangC, XiaoJ, et al., 2016. Fibroblast growth factors, old kids on the new block. Semin Cell Dev Biol, 53:155-167.

[58]LiXY, ShenC, LiuXQ, et al., 2017. Exposure to benzo[a]pyrene impairs decidualization and decidual angiogenesis in mice during early pregnancy. Environ Pollut, 222:523-531.

[59]LiY, KangZL, QiaoN, et al., 2017. Effects of excess copper ions on decidualization of human endometrial stromal cells. Biol Trace Elem Res, 177(1):10-15.

[60]LiYN, QiangWN, GriffinBB, et al., 2020. HMGA2-mediated tumorigenesis through angiogenesis in leiomyoma. Fertil Steril, 114(5):1085-1096.

[61]LimW, BaeH, BazerFW, et al., 2017. Stimulatory effects of fibroblast growth factor 2 on proliferation and migration of uterine luminal epithelial cells during early pregnancy. Biol Reprod, 96(1):185-198.

[62]LiuH, HuangXB, MorG, et al., 2020. Epigenetic modifications working in the decidualization and endometrial receptivity. Cell Mol Life Sci, 77(11):2091-2101.

[63]LiuMY, DengWB, TangL, et al., 2022. Menin directs regionalized decidual transformation through epigenetically setting PTX3 to balance FGF and BMP signaling. Nat Commun, 13:1006.

[64]LvSJ, WangN, MaJ, et al., 2019. Impaired decidualization caused by downregulation of circadian clock gene BMAL1 contributes to human recurrent miscarriage. Biol Reprod, 101(1):138-147.

[65]MakIYH, BrosensJJ, ChristianM, et al., 2002. Regulated expression of signal transducer and activator of transcription, Stat5, and its enhancement of PRL expression in human endometrial stromal cells in vitro. J Clin Endocrinol Metab, 87(6):2581-2588.

[66]Martinez-FierroML, Garza-VelozI, Castañeda-LopezME, et al., 2022. Evaluation of the effect of the fibroblast growth factor type 2 (FGF-2) administration on placental gene expression in a murine model of preeclampsia induced by L-NAME. Int J Mol Sci, 23(17):10129.

[67]MassimianiM, LacconiV, la CivitaF, et al., 2020. Molecular signaling regulating endometrium-blastocyst crosstalk. Int J Mol Sci, 21(1):23.

[68]McConahaME, EckstrumK, AnJ, et al., 2011. Microarray assessment of the influence of the conceptus on gene expression in the mouse uterus during decidualization. Reproduction, 141(4):511-527.

[69]MengN, YangQ, HeYP, et al., 2019. Decreased NDRG1 expression is associated with pregnancy loss in mice and attenuates the in vitro decidualization of endometrial stromal cells. Mol Reprod Dev, 86(9):1210-1223.

[70]MengXH, ChenCQ, QianJF, et al., 2023. Energy metabolism and maternal-fetal tolerance working in decidualization. Front Immunol, 14:1203719.

[71]Mestre-CitrinovitzAC, KleffV, VallejoG, et al., 2015. A suppressive antagonism evidences progesterone and estrogen receptor pathway interaction with concomitant regulation of Hand2, Bmp2 and ERK during early decidualization. PLoS ONE, 10(4):e0124756.

[72]MöllerB, RasmussenC, LindblomB, et al., 2001. Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometrium during the menstrual cycle. Mol Hum Reprod, 7(1):65-72.

[73]MoriS, HatoriN, KawaguchiN, et al., 2017. The integrin-binding defective FGF2 mutants potently suppress FGF2 signalling and angiogenesis. Biosci Rep, 37(2):BSR20170173.

[74]MurataH, TsuzukiT, KidoT, et al., 2019. Progestin-induced heart and neural crest derivatives-expressed transcript 2 inhibits angiopoietin 2 via fibroblast growth factor 9 in human endometrial stromal cells. Reprod Biol, 19(1):14-21.

[75]MurataH, TanakaS, OkadaH, 2022. The regulators of human endometrial stromal cell decidualization. Biomolecules, 12(9):1275.

[76]MurrayCM, OrrCJ, 2020. Hormonal regulation of the menstrual cycle and ovulation. In: Kovacs CS, Deal CL (Eds.), Maternal-Fetal and Neonatal Endocrinology. Academic Press, London, p.159-167.

[77]MuterJ, BrosensJJ, 2018. Decidua. Academic Press, Oxford, UK, p.424-430.

[78]NagashimaT, MaruyamaT, UchidaH, et al., 2008. Activation of SRC kinase and phosphorylation of signal transducer and activator of transcription-5 are required for decidual transformation of human endometrial stromal cells. Endocrinology, 149(3):1227-1234.

[79]NakamuraM, TakakuraM, FujiiR, et al., 2013. The PRB-dependent FOXO1/IGFBP-1 axis is essential for progestin to inhibit endometrial epithelial growth. Cancer Lett, 336(1):68-75.

[80]NnamaniMC, GangulyS, ErkenbrackEM, et al., 2016. A derived allosteric switch underlies the evolution of conditional cooperativity between HOXA11 and FOXO1. Cell Rep, 15(10):2097-2108.

[81]OkadaH, TsuzukiT, MurataH, 2018. Decidualization of the human endometrium. Reprod Med Biol, 17(3):220-227.

[82]OrazovMR, RadzinskiyVE, KostinIN, et al., 2021. Endometrial asynchrony in pathogenesis of implantation impairment in women with infertility associated with endometriosis. Gynecol Endocrinol, 37(S1):1-3.

[83]PaivaP, HannanNJ, HincksC, et al., 2011. Human chorionic gonadotrophin regulates FGF2 and other cytokines produced by human endometrial epithelial cells, providing a mechanism for enhancing endometrial receptivity. Hum Reprod, 26(5):1153-1162.

[84]Pan-CastilloB, GazzeSA, ThomasS, et al., 2018. Morphophysical dynamics of human endometrial cells during decidualization. Nanomedicine, 14(7):2235-2245.

[85]PariaBC, MaWG, TanJ, et al., 2001. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci USA, 98(3):1047-1052.

[86]PaulEN, BurnsGW, CarpenterTJ, et al., 2021. Transcriptome analyses of myometrium from fibroid patients reveals phenotypic differences compared to non-diseased myometrium. Int J Mol Sci, 22(7):3618.

[87]PeterseD, de ClercqK, GoossensC, et al., 2018. Optimization of endometrial decidualization in the menstruating mouse model for preclinical endometriosis research. Reprod Sci, 25(11):1577-1588.

[88]PopoviciRM, KaoLC, GiudiceLC, 2000. Discovery of new inducible genes in in vitro decidualized human endometrial stromal cells using microarray technology. Endocrinology, 141(9):3510-3515.

[89]QiQR, ZhaoXY, ZuoRJ, et al., 2015. Involvement of atypical transcription factor E2F8 in the polyploidization during mouse and human decidualization. Cell Cycle, 14(12):1842-1858.

[90]RanLM, SongHB, 2011. The promotion effect of cAMP on decidualization process in vitro of stromal cells in eutopic endometrium of patients with endometriosis. Matern Child Health Care China, 26(7):1092-1094 (in Chinese).

[91]RaukPN, SurtiU, RobertsJM, et al., 1995. Mitogenic effect of basic fibroblast growth factor and estradiol on cultured human myometrial and leiomyoma cells. Am J Obstet Gynecol, 173(2):571-577.

[92]RedmanCW, SargentIL, StaffAC, 2014. IFPA Senior Award Lecture: making sense of pre-eclampsia—two placental causes of preeclampsia? Placenta, 35(Suppl):S20-S25.

[93]RiderV, CarloneDL, FosterRT, 1997. Oestrogen and progesterone control basic fibroblast growth factor mRNA in the rat uterus. J Endocrinol, 154(1):75-84.

[94]RytkönenKT, ErkenbrackEM, PoutanenM, et al., 2019. Decidualization of human endometrial stromal fibroblasts is a multiphasic process involving distinct transcriptional programs. Reprod Sci, 26(3):323-336.

[95]Sahin ErsoyG, ZhouYP, InanH, et al., 2017. Cigarette smoking affects uterine receptivity markers. Reprod Sci, 24(7):989-995.

[96]SahuMB, DeepakV, GonzalesSK, et al., 2019. Decidual cells from women with preeclampsia exhibit inadequate decidualization and reduced sFlt1 suppression. Pregnancy Hypertens, 15:64-71.

[97]SakME, GulT, EvsenMS, et al., 2013. Fibroblast growth factor-1 expression in the endometrium of patients with repeated implantation failure after in vitro fertilization. Eur Rev Med Pharmacol Sci, 17(3):398-402.

[98]SalamonsenLA, JonesRL, 2003. Endometrial remodeling. In: Henry HL, Norman AW (Eds.), Encyclopedia of Hormones. Academic Press, Amsterdam, p.504-512.

[99]SamathanamCA, AdesanyaOO, ZhouJ, et al., 1998. Fibroblast growth factors 1 and 2 in the primate uterus. Biol Reprod, 59(3):491-496.

[100]SanghaRK, LiXF, ShamsM, et al., 1997. Fibroblast growth factor receptor-1 is a critical component for endometrial remodeling: localization and expression of basic fibroblast growth factor and FGF-R1 in human endometrium during the menstrual cycle and decreased FGF-R1 expression in menorrhagia. Lab Invest, 77(4):389-402.

[101]SevostyanovaO, LisovskayaT, ChistyakovaG, et al., 2020. Proinflammatory mediators and reproductive failure in women with uterine fibroids. Gynecol Endocrinol, 36(S1):33-35.

[102]ShuyaLL, MenkhorstEM, YapJ, et al., 2011. Leukemia inhibitory factor enhances endometrial stromal cell decidualization in humans and mice. PLoS ONE, 6(9):e25288.

[103]SongZ, LiB, LiMY, et al., 2022. Caveolin-1 regulation and function in mouse uterus during early pregnancy and under human in vitro decidualization. Int J Mol Sci, 23(7):3699.

[104]SouflaG, SifakisS, SpandidosDA, 2008. FGF2 transcript levels are positively correlated with EGF and IGF-1 in the malignant endometrium. Cancer Lett, 259(2):146-155.

[105]StepanH, KleyK, HindricksJ, et al., 2013. Serum levels of the adipokine fibroblast growth factor-21 are increased in preeclampsia. Cytokine, 62(2):322-326.

[106]StrassmannBI, 1996. The evolution of endometrial cycles and menstruation. Quart Rev Biol, 71(2):181-220.

[107]ŠućurovićS, NikolićT, BrosensJJ, et al., 2017. Spatial and temporal analyses of FGF9 expression during early pregnancy. Cell Physiol Biochem, 42(6):2318-2329.

[108]SuttonEF, MorrisonCD, StephensJM, et al., 2018. Fibroblast growth factor 21, adiposity, and macronutrient balance in a healthy, pregnant population with overweight and obesity. Endocr Res, 43(4):275-283.

[109]TanakaK, MinouraH, IsobeT, et al., 2003. Ghrelin is involved in the decidualization of human endometrial stromal cells. J Clin Endocrinol Metab, 88(5):2335-2340.

[110]TangZJ, GuanHY, WangL, et al., 2021. Research progress on human endometrium decidualization in vitro cell models. Reprod Dev Med, 5(2):119-127.

[111]TangZJ, WangL, HuangZS, et al., 2022. CD55 is upregulated by cAMP/PKA/AKT and modulates human decidualization via Src and ERK pathway and decidualization-related genes. Mol Reprod Dev, 89(5-6):256-268.

[112]TaniguchiF, HaradaT, SakamotoY, et al., 2003. Activation of mitogen-activated protein kinase pathway by keratinocyte growth factor or fibroblast growth factor-10 promotes cell proliferation in human endometrial carcinoma cells. J Clin Endocrinol Metab, 88(2):773-780.

[113]TengCB, DiaoHL, MaXH, et al., 2004. Differential expression and activation of Stat3 during mouse embryo implantation and decidualization. Mol Reprod Dev, 69(1):1-10.

[114]TongJ, LvSJ, YangJQ, et al., 2022. Decidualization and related pregnancy complications. Matern-Fetal Med, 4(1):24-35.

[115]TsaiJH, SchulteM, O'NeillK, et al., 2013. Glucosamine inhibits decidualization of human endometrial stromal cells and decreases litter sizes in mice. Biol Reprod, 89(1):16, 1-10.

[116]VasquezYM, MazurEC, LiXL, et al., 2015. FOXO1 is required for binding of PR on IRF4, novel transcriptional regulator of endometrial stromal decidualization. Mol Endocrinol, 29(3):421-433.

[117]WangC, ZhaoM, ZhangWQ, et al., 2020. Comparative analysis of mouse decidualization models at the molecular level. Genes, 11(8):935.

[118]WangHD, ZhangM, GeL, 2022. Cholesterol: enhancing FGF2 translocation in unconventional secretion. J Cell Biol, 221(11):e202210007.

[119]WuD, KimuraF, ZhengLY, et al., 2017. Chronic endometritis modifies decidualization in human endometrial stromal cells. Reprod Biol Endocrinol, 15(1):16.

[120]WuSP, LiR, DeMayoFJ, 2018. Progesterone receptor regulation of uterine adaptation for pregnancy. Trends Endocrinol Metab, 29(7):481-491.

[121]WuXX, BlanckA, OlovssonM, et al., 2001. Expression of basic fibroblast growth factor (bFGF), FGF receptor 1 and FGF receptor 2 in uterine leiomyomas and myometrium during the menstrual cycle, after menopause and GnRHa treatment. Acta Obstet Gynecol Scand, 80(6):497-504.

[122]XuXX, WangJZ, GuoXY, et al., 2023. GPR30-mediated non-classic estrogen pathway in mast cells participates in endometriosis pain via the production of FGF2. Front Immunol, 14:1106771.

[123]YagelS, Goldman-WohlDS, 2019. Placental implantation and development. In: Yagel S, Silverman NH, Gembruch U (Eds.), Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis, and Perinatal Management of Cardiac Diseases, 3rd Ed. CRC Press, Boca Raton, p.54-66.

[124]YanXY, RongMM, ZhouQH, et al., 2022. DCAF13 is essential for the pathogenesis of preeclampsia through its involvement in endometrial decidualization. Mol Cell Endocrinol, 556:111741.

[125]YangSC, ParkM, HongKH, et al., 2023. CFP1 governs uterine epigenetic landscapes to intervene in progesterone responses for uterine physiology and suppression of endometriosis. Nat Commun, 14:3220.

[126]YerlikayaG, BalendranS, PröstlingK, et al., 2016. Comprehensive study of angiogenic factors in women with endometriosis compared to women without endometriosis. Eur J Obstet Gynecol Reprod Biol, 204:88-98.

[127]YinXQ, PavoneME, LuZX, et al., 2012. Increased activation of the PI3K/AKT pathway compromises decidualization of stromal cells from endometriosis. J Clin Endocrinol Metab, 97(1):E35-E43.

[128]YinY, HallerME, ChadchanSB, et al., 2021. Signaling through retinoic acid receptors is essential for mammalian uterine receptivity and decidualization. JCI Insight, 6(17):e150254.

[129]YoshieM, KusamaK, TamuraK, 2015. Molecular mechanisms of human endometrial decidualization activated by cyclic adenosine monophosphate signaling pathways. J Mamm Ova Res, 32(3):95-102.

[130]YuHF, DuanCC, YangZQ, et al., 2020. Malic enzyme 1 is important for uterine decidualization in response to progesterone/cAMP/PKA/HB-EGF pathway. FASEB J, 34(3):3820-3837.

[131]YuSL, LeeSI, ParkHW, et al., 2022. SIRT1 suppresses in vitro decidualization of human endometrial stromal cells through the downregulation of forkhead box O1 expression. Reprod Biol, 22(3):100672.

[132]YuXY, WangYP, TanXW, et al., 2021. Upregulation of fibroblast growth factor 2 contributes to endometriosis through SPRYs/DUSP6/ERK signaling pathway. Acta Histochem, 123(5):151749.

[133]ZhangXQ, IbrahimiOA, OlsenSK, et al., 2006. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem, 281(23):15694-15700.

[134]ZhangY, ZhangZ, KangNN, et al., 2022. Generation of a mouse artificial decidualization model with ovariectomy for endometrial decidualization research. J Vis Exp, (185):e64278.

[135]ZhaoLJ, YangHL, XuanY, et al., 2015. Increased expression of fibroblast growth factor receptor 1 in endometriosis and its correlation with endometriosis-related dysmenorrhea and recurrence. Eur J Obstet Gynecol Reprod Biol, 184:117-124.

[136]ZhaoM, ZhangWQ, LiuJL, 2017. A study on regional differences in decidualization of the mouse uterus. Reproduction, 153(5):645-653.

[137]ZhaoWJ, XuCF, PengLJ, et al., 2023. cAMP/PKA signaling promotes AKT deactivation by reducing CIP2A expression, thereby facilitating decidualization. Mol Cell Endocrinol, 571:111946.

[138]ZhengWL, ZhaoSF, HeH, et al., 2023. E2F2 is upregulated by the ERK pathway and regulates decidualization via MCM4. Gene, 871:147400.

[139]ZhouPY, OuyangLQ, JiangT, et al., 2024. Progesterone and cAMP synergistically induce SHP2 expression via PGR and CREB1 during uterine stromal decidualization. FEBS J, 291(1):142-157.

[140]ZhouWJ, HouXX, WangXQ, et al., 2017. Fibroblast growth factor 7 regulates proliferation and decidualization of human endometrial stromal cells via ERK and JNK pathway in an autocrine manner. Reprod Sci, 24(12):1607-1619.

[141]ZhuDL, TuoXM, RongY, et al., 2020. Fibroblast growth factor receptor signaling as therapeutic targets in female reproductive system cancers. J Cancer, 11(24):7264-7275.

[142]ZhuJ, LiZY, YinFL, et al., 2023. Fibroblast growth factor 1 ameliorates thin endometrium in rats through activation of the autophagic pathway. Front Pharmacol, 14:1143096.

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