Citation: | Tingting Yang, Zhen Qiu, Jiaming Shen, Yutian He, Longxiang Yin, Li Chen, Jiayu Yuan, Junjie Liu, Tao Wang, Zhenzhou Jiang, Changjiang Ying, Sitong Qian, Jinfang Song, Xiaoxing Yin, Qian Lu. 17β-estradiol, through activating G protein-coupled estrogen receptor, exacerbated the complication of benign prostate hyperplasia in type 2 diabetes mellitus by inducing prostatic proliferation[J]. Journal of Pharmaceutical Analysis. doi: 10.1016/j.jpha.2024.03.003 |
[1] |
A.A.A. Saad, F. Zhang, M. Refat, et al., Tamsulosin alters the pharmacokinetics of metformin via inhibition of renal multidrug and toxin extrusion protein 1 and organic cation transporter 2 in rats, Journal of pharmaceutical and biomedical analysis 212(2022) 114666 https://doi.org/10.1016/j.jpba.2022.114666.
|
[2] |
J. Gandhi, S.J. Weissbart, A.N. Kim, et al., Clinical Considerations for Intravesical Prostatic Protrusion in the Evaluation and Management of Bladder Outlet Obstruction Secondary to Benign Prostatic Hyperplasia, Current urology 12(2018) 6-12 https://doi.org/10.1159/000447224.
|
[3] |
B.R. Jin, H.J. An, Baicalin alleviates benign prostate hyperplasia through androgen-dependent apoptosis, Aging 12(2020) 2142-2155 https://doi.org/10.18632/aging.102731.
|
[4] |
J. Hammarsten, B. Högstedt, Hyperinsulinaemia as a risk factor for developing benign prostatic hyperplasia, European urology 39(2001) 151-158 https://doi.org/10.1159/000052430.
|
[5] |
H. Nandeesha, B.C. Koner, L.N. Dorairajan, et al., Hyperinsulinemia and dyslipidemia in non-diabetic benign prostatic hyperplasia, Clinica chimica acta; international journal of clinical chemistry 370(2006) 89-93 https://doi.org/10.1016/j.cca.2006.01.019.
|
[6] |
B.R. Erdogan, G. Liu, E. Arioglu-Inan, et al., Established and emerging treatments for diabetes-associated lower urinary tract dysfunction, Naunyn-Schmiedeberg's archives of pharmacology 395(2022) 887-906 https://doi.org/10.1007/s00210-022-02249-9.
|
[7] |
W.J. Bang, J.Y. Lee, K.C. Koo, et al., Is type-2 diabetes mellitus associated with overactive bladder symptoms in men with lower urinary tract symptoms?, Urology 84(2014) 670-674 https://doi.org/10.1016/j.urology.2014.05.017.
|
[8] |
A.E. Calogero, G. Burgio, R.A. Condorelli, et al., Epidemiology and risk factors of lower urinary tract symptoms/benign prostatic hyperplasia and erectile dysfunction, The aging male : the official journal of the International Society for the Study of the Aging Male 22(2019) 12-19 https://doi.org/10.1080/13685538.2018.1434772.
|
[9] |
H. Nandeesha, Benign prostatic hyperplasia: dietary and metabolic risk factors, International urology and nephrology 40(2008) 649-656 https://doi.org/10.1007/s11255-008-9333-z.
|
[10] |
J.A. Santos-Marcos, M. Mora-Ortiz, M. Tena-Sempere, et al., Interaction between gut microbiota and sex hormones and their relation to sexual dimorphism in metabolic diseases, Biology of sex differences 14(2023) 4 https://doi.org/10.1186/s13293-023-00490-2.
|
[11] |
A. Kautzky-Willer, J. Harreiter, G. Pacini, Sex and Gender Differences in Risk, Pathophysiology and Complications of Type 2 Diabetes Mellitus, Endocrine reviews 37(2016) 278-316 https://doi.org/10.1210/er.2015-1137.
|
[12] |
A. Gambineri, C. Pelusi, Sex hormones, obesity and type 2 diabetes: is there a link?, Endocrine connections 8(2019) R1-r9 https://doi.org/10.1530/ec-18-0450.
|
[13] |
R.E. van Genugten, K.M. Utzschneider, J. Tong, et al., Effects of sex and hormone replacement therapy use on the prevalence of isolated impaired fasting glucose and isolated impaired glucose tolerance in subjects with a family history of type 2 diabetes, Diabetes 55(2006) 3529-3535 https://doi.org/10.2337/db06-0577.
|
[14] |
G. Blohmé, L. Nyström, H.J. Arnqvist, et al., Male predominance of type 1(insulin-dependent) diabetes mellitus in young adults: results from a 5-year prospective nationwide study of the 15-34-year age group in Sweden, Diabetologia 35(1992) 56-62 https://doi.org/10.1007/bf00400852.
|
[15] |
J. Li, H. Lai, S. Chen, et al., Interaction of sex steroid hormones and obesity on insulin resistance and type 2 diabetes in men: the Third National Health and Nutrition Examination Survey, Journal of diabetes and its complications 31(2017) 318-327 https://doi.org/10.1016/j.jdiacomp.2016.10.022.
|
[16] |
J. Hu, A. Zhang, S. Yang, et al., Combined effects of sex hormone-binding globulin and sex hormones on risk of incident type 2 diabetes, Journal of diabetes 8(2016) 508-515 https://doi.org/10.1111/1753-0407.12322.
|
[17] |
T. Muka, J. Nano, L. Jaspers, et al., Associations of Steroid Sex Hormones and Sex Hormone-Binding Globulin With the Risk of Type 2 Diabetes in Women: A Population-Based Cohort Study and Meta-analysis, Diabetes 66(2017) 577-586 https://doi.org/10.2337/db16-0473.
|
[18] |
Y.S. Piao, P. Wiesenfeld, R. Sprando, et al., TGFβ1 alters androgenic metabolites and hydroxysteroid dehydrogenase enzyme expression in human prostate reactive stromal primary cells: Is steroid metabolism altered by prostate reactive stromal microenvironment?, The Journal of steroid biochemistry and molecular biology 138(2013) 206-213 https://doi.org/10.1016/j.jsbmb.2013.05.016.
|
[19] |
Y. Kim, D. Lee, H. Jo, et al., GV1001 interacts with androgen receptor to inhibit prostate cell proliferation in benign prostatic hyperplasia by regulating expression of molecules related to epithelial-mesenchymal transition, Aging 13(2021) 3202-3217 https://doi.org/10.18632/aging.202242.
|
[20] |
C.K. Ho, F.K. Habib, Estrogen and androgen signaling in the pathogenesis of BPH, Nature reviews. Urology 8(2011) 29-41 https://doi.org/10.1038/nrurol.2010.207.
|
[21] |
G. Rastrelli, L. Vignozzi, G. Corona, et al., Testosterone and Benign Prostatic Hyperplasia, Sexual medicine reviews 7(2019) 259-271 https://doi.org/10.1016/j.sxmr.2018.10.006.
|
[22] |
E. Csikós, A. Horváth, K. Ács, et al., Treatment of Benign Prostatic Hyperplasia by Natural Drugs, Molecules (Basel, Switzerland) 26(2021) https://doi.org/10.3390/molecules26237141.
|
[23] |
L. Pan, S. Su, Y. Li, et al., The effect of acupuncture on oestrogen receptors in rats with benign prostatic hyperplasia, The Journal of steroid biochemistry and molecular biology 234(2023) 106402 https://doi.org/10.1016/j.jsbmb.2023.106402.
|
[24] |
T. Yang, Y. Huang, Y. Zhou, et al., Simultaneous quantification of oestrogens and androgens in the serum of patients with benign prostatic hyperplasia by liquid chromatography-Tandem mass spectrometry, Andrologia 52(2020) e13611 https://doi.org/10.1111/and.13611.
|
[25] |
T. Yang, Y. Zhou, H. Wang, et al., Insulin exacerbated high glucose-induced epithelial-mesenchymal transition in prostatic epithelial cells BPH-1 and prostate cancer cells PC-3 via MEK/ERK signaling pathway, Experimental cell research 394(2020) 112145 https://doi.org/10.1016/j.yexcr.2020.112145.
|
[26] |
S.W. Fanning, L. Hodges-Gallagher, D.C. Myles, et al., Specific stereochemistry of OP-1074 disrupts estrogen receptor alpha helix 12 and confers pure antiestrogenic activity, Nature communications 9(2018) 2368 https://doi.org/10.1038/s41467-018-04413-3.
|
[27] |
T. Yang, J. Yuan, Y. Peng, et al., Metformin: A promising clinical therapeutical approach for BPH treatment via inhibiting dysregulated steroid hormones-induced prostatic epithelial cells proliferation, Journal of Pharmaceutical Analysis (2023) https://doi.org/10.1016/j.jpha.2023.08.012.
|
[28] |
Y.Y. Liu, L. Li, B. Ji, et al., Jujuboside A ameliorates tubulointerstitial fibrosis in diabetic mice through down-regulating the YY1/TGF-β1 signaling pathway, Chinese journal of natural medicines 20(2022) 656-668 https://doi.org/10.1016/s1875-5364(22)60200-0.
|
[29] |
X. Qian, L. He, M. Hao, et al., YAP mediates the interaction between the Hippo and PI3K/Akt pathways in mesangial cell proliferation in diabetic nephropathy, Acta diabetologica 58(2021) 47-62 https://doi.org/10.1007/s00592-020-01582-w.
|
[30] |
Y. Liu, Z.Z. Tang, Y.M. Zhang, et al., Thrombin/PAR-1 activation induces endothelial damages via NLRP1 inflammasome in gestational diabetes, Biochemical pharmacology 175(2020) 113849 https://doi.org/10.1016/j.bcp.2020.113849.
|
[31] |
R. Wang, Z. Qiu, G. Wang, et al., Quercetin attenuates diabetic neuropathic pain by inhibiting mTOR/p70S6K pathway-mediated changes of synaptic morphology and synaptic protein levels in spinal dorsal horn of db/db mice, European journal of pharmacology 882(2020) 173266 https://doi.org/10.1016/j.ejphar.2020.173266.
|
[32] |
T. Yang, C. Heng, Y. Zhou, et al., Targeting mammalian serine/threonine-protein kinase 4 through Yes-associated protein/TEA domain transcription factor-mediated epithelial-mesenchymal transition ameliorates diabetic nephropathy orchestrated renal fibrosis, Metabolism: clinical and experimental 108(2020) 154258 https://doi.org/10.1016/j.metabol.2020.154258.
|
[33] |
E.R. Prossnitz, M. Barton, The G-protein-coupled estrogen receptor GPER in health and disease, Nature reviews. Endocrinology 7(2011) 715-726 https://doi.org/10.1038/nrendo.2011.122.
|
[34] |
X. Zhou, S. Wang, Z. Wang, et al., Estrogen regulates Hippo signaling via GPER in breast cancer, The Journal of clinical investigation 125(2015) 2123-2135 https://doi.org/10.1172/jci79573.
|
[35] |
Q. Deng, G. Jiang, Y. Wu, et al., GPER/Hippo-YAP signal is involved in Bisphenol S induced migration of triple negative breast cancer (TNBC) cells, Journal of hazardous materials 355(2018) 1-9 https://doi.org/10.1016/j.jhazmat.2018.05.013.
|
[36] |
E. Donohue, A. Thomas, N. Maurer, et al., The autophagy inhibitor verteporfin moderately enhances the antitumor activity of gemcitabine in a pancreatic ductal adenocarcinoma model, Journal of Cancer 4(2013) 585-596 https://doi.org/10.7150/jca.7030.
|
[37] |
H.Z. Sun, T.W. Yang, W.J. Zang, et al., Dehydroepiandrosterone-induced proliferation of prostatic epithelial cell is mediated by NFKB via PI3K/AKT signaling pathway, The Journal of endocrinology 204(2010) 311-318 https://doi.org/10.1677/joe-09-0270.
|
[38] |
K. Griffiths, C.L. Eaton, M.E. Harper, et al., Steroid hormones and the pathogenesis of benign prostatic hyperplasia, European urology 20 Suppl 1(1991) 68-77 https://doi.org/10.1159/000471750.
|
[39] |
J.B. Arterburn, E.R. Prossnitz, G Protein-Coupled Estrogen Receptor GPER: Molecular Pharmacology and Therapeutic Applications, Annual review of pharmacology and toxicology 63(2023) 295-320 https://doi.org/10.1146/annurev-pharmtox-031122-121944.
|
[40] |
L. Aryan, D. Younessi, M. Zargari, et al., The Role of Estrogen Receptors in Cardiovascular Disease, International journal of molecular sciences 21(2020) https://doi.org/10.3390/ijms21124314.
|
[41] |
S.K. Kim, J.H. Chung, H.C. Park, et al., Association between polymorphisms of estrogen receptor 2 and benign prostatic hyperplasia, Experimental and therapeutic medicine 10(2015) 1990-1994 https://doi.org/10.3892/etm.2015.2755.
|
[42] |
R. Chen, Y. Yu, X. Dong, Progesterone receptor in the prostate: A potential suppressor for benign prostatic hyperplasia and prostate cancer, The Journal of steroid biochemistry and molecular biology 166(2017) 91-96 https://doi.org/10.1016/j.jsbmb.2016.04.008.
|
[43] |
Y. Yang, J. Sheng, S. Hu, et al., Estrogen and G protein-coupled estrogen receptor accelerate the progression of benign prostatic hyperplasia by inducing prostatic fibrosis, Cell death & disease 13(2022) 533 https://doi.org/10.1038/s41419-022-04979-3.
|
[44] |
D.L. Yang, J.W. Xu, J.G. Zhu, et al., Role of GPR30 in estrogen-induced prostate epithelial apoptosis and benign prostatic hyperplasia, Biochemical and biophysical research communications 487(2017) 517-524 https://doi.org/10.1016/j.bbrc.2017.04.047.
|
[45] |
W. Dong, J. Zheng, Y. Huang, et al., Sodium butyrate treatment and fecal microbiota transplantation provide relief from ulcerative colitis-induced prostate enlargement, Frontiers in cellular and infection microbiology 12(2022) 1037279 https://doi.org/10.3389/fcimb.2022.1037279.
|
[46] |
Y. Wang, H. Yu, J. He, Involvement of the Hippo Pathway in the Development of Diabetes, Discovery medicine 31(2021) 37-44.
|
[47] |
X. Li, S. Zhuo, Y.S. Cho, et al., YAP antagonizes TEAD-mediated AR signaling and prostate cancer growth, The EMBO journal 42(2023) e112184 https://doi.org/10.15252/embj.2022112184.
|
[48] |
D. Lei, L. Chengcheng, Q. Xuan, et al., Quercetin inhibited mesangial cell proliferation of early diabetic nephropathy through the Hippo pathway, Pharmacological research 146(2019) 104320 https://doi.org/10.1016/j.phrs.2019.104320.
|
[49] |
J.C. Cheng, L. Fang, Y. Li, et al., G protein-coupled estrogen receptor stimulates human trophoblast cell invasion via YAP-mediated ANGPTL4 expression, Communications biology 4(2021) 1285 https://doi.org/10.1038/s42003-021-02816-5.
|
[50] |
F.X. Yu, B. Zhao, N. Panupinthu, et al., Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling, Cell 150(2012) 780-791 https://doi.org/10.1016/j.cell.2012.06.037.
|
[51] |
Y. Zhao, H. Liu, M. Fan, et al., G protein-coupled receptor 30 mediates cell proliferation of goat mammary epithelial cells via MEK/ERK&PI3K/AKT signaling pathway, Cell cycle (Georgetown, Tex.) 21(2022) 2027-2037 https://doi.org/10.1080/15384101.2022.2083708.
|
[52] |
X. Sheng, W.B. Li, D.L. Wang, et al., YAP is closely correlated with castration-resistant prostate cancer, and downregulation of YAP reduces proliferation and induces apoptosis of PC-3 cells, Molecular medicine reports 12(2015) 4867-4876 https://doi.org/10.3892/mmr.2015.4005.
|
[53] |
E. Desideri, S. Castelli, C. Dorard, et al., Impaired degradation of YAP1 and IL6ST by chaperone-mediated autophagy promotes proliferation and migration of normal and hepatocellular carcinoma cells, Autophagy 19(2023) 152-162 https://doi.org/10.1080/15548627.2022.2063004.
|
[54] |
T. Han, T. Chen, L. Chen, et al., HLF promotes ovarian cancer progression and chemoresistance via regulating Hippo signaling pathway, Cell death & disease 14(2023) 606 https://doi.org/10.1038/s41419-023-06076-5.
|
[55] |
H. Chen, W. Yang, Y. Li, et al., PLAGL2 promotes bladder cancer progression via RACGAP1/RhoA GTPase/YAP1 signaling, Cell death & disease 14(2023) 433 https://doi.org/10.1038/s41419-023-05970-2.
|
[56] |
R.D. Read, Repurposing the drug verteporfin as anti-neoplastic therapy for glioblastoma, Neuro-oncology 24(2022) 708-710 https://doi.org/10.1093/neuonc/noac019.
|
[57] |
X. Li, L. Fan, M. Zhu, et al., Combined intervention of 17β-estradiol and treadmill training ameliorates energy metabolism in skeletal muscle of female ovariectomized mice, Climacteric : the journal of the International Menopause Society 23(2020) 192-200 https://doi.org/10.1080/13697137.2019.1660639.
|
[58] |
A. Inada, N.L. Fujii, O. Inada, et al., Effects of 17β-Estradiol and Androgen on Glucose Metabolism in Skeletal Muscle, Endocrinology 157(2016) 4691-4705 https://doi.org/10.1210/en.2016-1261.
|
[59] |
Z. Bao, Z.Q. Liu, P.Y. He, et al., 17β-estradiol regulates adenosine triphosphate-binding cassette transporters A1 expression via estrogen receptor A to increase macrophage cholesterol efflux, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society 74(2023) https://doi.org/10.26402/jpp.2023.5.05.
|
[60] |
M. Wang, F. Gorelick, A. Bhargava, Sex Differences in the Exocrine Pancreas and Associated Diseases, Cellular and molecular gastroenterology and hepatology 12(2021) 427-441 https://doi.org/10.1016/j.jcmgh.2021.04.005.
|
[61] |
S. Nikanfar, H. Oghbaei, Y. Rastgar Rezaei, et al., Role of adipokines in the ovarian function: Oogenesis and steroidogenesis, The Journal of steroid biochemistry and molecular biology 209(2021) 105852 https://doi.org/10.1016/j.jsbmb.2021.105852.
|
[62] |
M. Pektaş, A.H. Kurt, İ. Ün, et al., Effects of 17β-estradiol and progesterone on the production of adipokines in differentiating 3T3-L1 adipocytes: Role of Rho-kinase, Cytokine 72(2015) 130-134 https://doi.org/10.1016/j.cyto.2014.12.020.
|
[63] |
K. Rabe, M. Lehrke, K.G. Parhofer, et al., Adipokines and insulin resistance, Molecular medicine (Cambridge, Mass.) 14(2008) 741-751 https://doi.org/10.2119/2008-00058.Rabe.
|
[64] |
B. Carrillo, P. Collado, F. Díaz, et al., Blocking of Estradiol Receptors ERα, ERβ and GPER During Development, Differentially Alters Energy Metabolism in Male and Female Rats, Neuroscience 426(2020) 59-68 https://doi.org/10.1016/j.neuroscience.2019.11.008.
|
[65] |
F. Mahboobifard, M.H. Pourgholami, M. Jorjani, et al., Estrogen as a key regulator of energy homeostasis and metabolic health, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie 156(2022) 113808 https://doi.org/10.1016/j.biopha.2022.113808.
|
[66] |
M. Shen, H. Shi, Sex Hormones and Their Receptors Regulate Liver Energy Homeostasis, International journal of endocrinology 2015(2015) 294278 https://doi.org/10.1155/2015/294278.
|