Rat postnatal prostate development is impaired by in vitro high-glucose environment

in Reproduction

Correspondence should be addressed to D L Ribeiro; Email: daniele.ribeiro@icbim.ufu.br
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The prostate development has an important postnatal period where cell proliferation begins at the first days after birth and is related to gland growth and ramification. Any metabolic and/or hormonal changes occurring during the postnatal period can interfere with prostate branching. Hyperglycemia is a common condition in low-weight preterm babies at neonatal period and also a disorder found in the offspring of obese mothers. Thus, this study aimed to investigate the in vitro effects of a glucose-rich environment during prostate postnatal development. Wistar rats prostate were removed at birth and cultured for 1, 2 and 3 days in DMEM under normal (5.5 mM) or elevated (7 and 25 mM) glucose concentrations. Samples were processed for morphological analysis, PCNA and smooth muscle α-actin immunohistochemistry, evaluation of active caspase-3, ERK1/2 and Wnt5a gene expression. High glucose concentrations reduced the number of prostatic buds and proliferating cells. The natural increase in smooth muscle cells and collagen deposition observed in control prostates during the first 3 days of development was reduced by elevated glucose concentrations. The amount of active caspase-3 was higher in prostates incubated at 7 mM and TGF-β levels also increased sharply after both glucose concentrations. Additionally, high glucose environment decreased ERK 1/2 activation and increased Wnt5a expression. These data show that high levels of glucose during the first postnatal days affected prostate development by inhibiting cell proliferation which impairs bud branching and this was associated with anti-proliferative signals such as decreased ERK1/2 activation and increased Wnt5a expression.

 

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  • AllgeierSHLinTMVezinaCMMooreRWFritzWAChiuSYZhangCPetersonRE 2008 Wnt5a selectively inhibits mouse ventral prostate development. Developmental Biology 324 1017. (https://doi.org/10.1016/j.ydbio.2008.08.018)

    • Search Google Scholar
    • Export Citation
  • ArcolinoFORibeiroDLGobboMGTabogaSRGóesRM 2010 Proliferation and apoptotic rates and increased frequency of p63-positive cells in the prostate acinar epithelium of alloxan-induced diabetic rats. International Journal of Experimental Pathology 91 144154. (https://doi.org/10.1111/j.1365-2613.2009.00696.x)

    • Search Google Scholar
    • Export Citation
  • AumüllerGSeitzJ 1990 Protein secretion and secretory processes in male accessory sex glands. Internacional Review of Cytology 1 127231. (https://doi.org/10.1016/S0074-7696(08)60660-9)

    • Search Google Scholar
    • Export Citation
  • BaarsmaHKönigshoffM 2013 WNT5A antagonizes canonical WNT/β-catenin signaling in lung epithelial cells. European Respiratory Journal 42 P4893.

    • Search Google Scholar
    • Export Citation
  • BradfordMM 1976 Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248254.

    • Search Google Scholar
    • Export Citation
  • BrownleeM 2001 Biochemistry and molecular cell biology of diabetic complications. Nature 414 813820. (https://doi.org/10.1038/414813a)

    • Search Google Scholar
    • Export Citation
  • Bruni-CardosoACarvalhoHF 2007 Dynamics of the epithelium during canalization of the rat ventral prostate. Anatomical Record 290 12231232. (https://doi.org/10.1002/ar.20591)

    • Search Google Scholar
    • Export Citation
  • Bruni-CardosoAVilamaiorPSTabogaSRCarvalhoHF 2008 Localized matrix metalloproteinase (MMP)-2 and MMP-9 activity in the rat ventral prostate during the first week of postnatal development. Histochemistry and Cell Biology 129 805815. (https://doi.org/10.1007/s00418-008-0407-x)

    • Search Google Scholar
    • Export Citation
  • BurénJLiuHXLauritzJErikssonJW 2003 High glucose and insulin in combination cause insulin receptor substrate-1 and -2 depletion and protein kinase B desensitisation in primary cultured rat adipocytes: possible implications for insulin resistance in type 2 diabetes. European Journal of Endocrinology 148 157167. (https://doi.org/10.1530/eje.0.1480157)

    • Search Google Scholar
    • Export Citation
  • CunhaGRDonjacourAACookePSMeeSBigsbyRMHigginsSJSugimuraY 1987 The endocrinology and developmental biology of the prostate. Endocrine Reviews 8 338362. (https://doi.org/10.1210/edrv-8-3-338)

    • Search Google Scholar
    • Export Citation
  • CunhaGRHaywardSWDahiyaRFosterBA 1996 Smooth muscle-epithelial interactions in normal and neoplastic prostatic development. Acta Anatomica 155 6372. (https://doi.org/10.1159/000147791)

    • Search Google Scholar
    • Export Citation
  • CunhaGRCookePSKuritaT 2004 Role of stromal-epithelial interactions in hormonal responses. Archives of Histology and Cytology 67 417434. (https://doi.org/10.1679/aohc.67.417)

    • Search Google Scholar
    • Export Citation
  • CunhaGR 2008 Mesenchymal-epithelial interactions: past, present, and future. Differentiation 76 578586. (https://doi.org/10.1111/j.1432-0436.2008.00290.x)

    • Search Google Scholar
    • Export Citation
  • CunhaGRVezinaCMIsaacsonDRickeWATimmsBGCaoMFrancoOBaskinLS 2018 Development of the human prostate. Differentiation 103 2445. (https://doi.org/10.1016/j.diff.2018.08.005)

    • Search Google Scholar
    • Export Citation
  • D’arcyMS 2019 Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biology International 43 582592. (https://doi.org/10.1002/cbin.11137)

    • Search Google Scholar
    • Export Citation
  • DamascenoAACarvalhoCPSantosEMBotelhoFVAraújoFADeconteSRTomiossoTCBalbiAPZanonRGTabogaSR 2014 Effects of maternal diabetes on male offspring: high cell proliferation and increased activity of MMP-2 in the ventral prostate. Cell and Tissue Research 358 257269. (https://doi.org/10.1007/s00441-014-1941-6)

    • Search Google Scholar
    • Export Citation
  • De NigrisVPujadasGLa SalaLTestaRGenoveseSCerielloA 2015 Short-term high glucose exposure impairs insulin signaling in endothelial cells. Cardiovascular Diabetology 14 114. (https://doi.org/10.1186/s12933-015-0278-0)

    • Search Google Scholar
    • Export Citation
  • DonmezYBKizilayGTopcu-TarladacalisirY 2014 MAPK immunoreactivity in streptozotocin-induced diabetic rat testis. Acta Cirurgica Brasileira 29 644650. (https://doi.org/10.1590/S0102-8650201400160004)

    • Search Google Scholar
    • Export Citation
  • FangTTCaoRPYeHWMaSFGaoQ 2019 Effects of high glucose induced primary cardiomyocytes injury on necroptosis and the related mechanism. Chinese Journal of Applied Physiology 2 160164. (https://doi.org/10.12047/j.cjap.5710.2019.035)

    • Search Google Scholar
    • Export Citation
  • Flores-LópezLADíaz-FloresMGarcía-MacedoRÁvalos-RodríguezAVergara-OnofreMCruzMContreras-RamosAKonigsbergMOrtega-CamarilloC 2013 High glucose induces mitochondrial p53 phosphorylation by p38 MAPK in pancreatic RINm5F cells. Molecular Biology Reports 40 49474958. (https://doi.org/10.1007/s11033-013-2595-2)

    • Search Google Scholar
    • Export Citation
  • GibsonTBLawrenceMCGibsonCJVanderbiltCAMcGlynnKArnetteDChenWCollinsJNaziruddinBLevyMF 2006 Inhibition of glucose-stimulated activation of extracellular signal regulated protein kinases 1 and 2 by epinephrine in pancreatic beta-cells. Diabetes 55 10661073. (https://doi.org/10.2337/diabetes.55.04.06.db05-1266)

    • Search Google Scholar
    • Export Citation
  • GobboMGTabogaSRRibeiroDLGóesRM 2012 Short-term stromal alterations in the rat ventral prostate following alloxan-induced diabetes and the influence of insulin replacement. Micron 43 326333. (https://doi.org/10.1016/j.micron.2011.09.009)

    • Search Google Scholar
    • Export Citation
  • GrindelAGuggenbergerBEichbergerLPöppelmeyerCGschaiderMTosevskaAMareGBriskeyDBrathHWagnerKH. 2016 Oxidative stress, DNA damage and DNA repair in female patients with diabetes mellitus type 2. PLoS ONE 11 e0162082. (https://doi.org/10.1371/journal.pone.0162082)

    • Search Google Scholar
    • Export Citation
  • HaywardSWCunhaGR 2000 The prostate: development and physiology. Radiologic Clinics of North America 1 114. (https://doi.org/10.1016/S0033-8389(05)70146-9)

    • Search Google Scholar
    • Export Citation
  • HuangLPuYHuWYBirchLLuccio-CameloDYamaguchiTPrinsGS 2009 The role of Wnt5a in prostate gland development. Developmental Biology 328 188199. (https://doi.org/10.1016/j.ydbio.2009.01.003)

    • Search Google Scholar
    • Export Citation
  • JavelaudDMauvielA 2004 Mammalian transforming growth factor-βs: smad signaling and physio-pathological roles. International Journal of Biochemistry and Cell Biology 36 11611165. (https://doi.org/10.1016/S1357-2725(03)00255-3)

    • Search Google Scholar
    • Export Citation
  • KatsoulierisENDrossopoulouGIKotsopoulouESVlahakosDVLianosEATsilibaryEC 2016 High glucose impairs insulin signaling in the glomerulus: an in vitro and ex vivo approach. PLoS ONE 11 e0158873. (https://doi.org/10.1371/journal.pone.0158873)

    • Search Google Scholar
    • Export Citation
  • KarpovaTde OliveiraAANaasHPrivieroFNunesKP 2020 Blockade of Toll-like receptor 4 (TLR4) reduces oxidative stress and restores phospho-ERK1/2 levels in Leydig cells exposed to high glucose. Life Sciences 27 117365. (https://doi.org/10.1016/j.lfs.2020.117365)

    • Search Google Scholar
    • Export Citation
  • KawanoYRyderJWRinconJZierathJRKrookAWallberg-HenrikssonH 2001 Evidence against high glucose as a mediator of ERK1/2 or p38 MAPK phosphorylation in rat skeletal muscle. American Journal of Physiology: Endocrinology and Metabolism 281 E1255E1259. (https://doi.org/10.1152/ajpendo.2001.281.6.e1255)

    • Search Google Scholar
    • Export Citation
  • KorsmoHWEdwardsKDaveBJack-RobertsCYuHSaxenaASalvadorMDembitzerMPhagooraJJiangX 2020 Prenatal choline supplementation during high-fat feeding improves long-term blood glucose control in male mouse offspring. Nutrients 12 E144. (https://doi.org/10.3390/nu12010144)

    • Search Google Scholar
    • Export Citation
  • LiangWChenMZhengDHeJSongMMoLFengJLanJ 2017 A novel damage mechanism: contribution of the interaction between necroptosis and ROS to high glucose-induced injury and inflammation in H9c2 cardiac cells. Internacional Journal of Molecular Medicine 40 201208. (https://doi.org/10.3892/ijmm.2017.3006)

    • Search Google Scholar
    • Export Citation
  • LiuDLiangXZhangH 2016 Effects of high glucose on cell viability and differentiation in primary cultured schwann cells: potential role of ERK signaling pathway. Neurochemical Research 41 12811290. (https://doi.org/10.1007/s11064-015-1824-6)

    • Search Google Scholar
    • Export Citation
  • LivakKJSchmittgenTD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 402408. (https://doi.org/10.1006/meth.2001.1262)

    • Search Google Scholar
    • Export Citation
  • LopesERFosterBADonjacourAACunhaGR 1996 Initiation of secretory activity of rat prostatic epithelium in organ culture. Endocrinology 137 42254234. (https://doi.org/10.1210/endo.137.10.8828481)

    • Search Google Scholar
    • Export Citation
  • PakSParkSKimYParkJHParkCHLeeKJKimCSAhnH 2019 The small molecule WNT/β-catenin inhibitor CWP232291 blocks the growth of castration-resistant prostate cancer by activating the endoplasmic reticulum stress pathway. Journal of Experimental and Clinical Cancer Research 38 342. (https://doi.org/10.1186/s13046-019-1342-5)

    • Search Google Scholar
    • Export Citation
  • PatelRBrzezinskaEARepiscakPAhmadIMuiEGaoMBlommeAHarleVTanEHMalviyaG 2019 Activation of β-catenin cooperates with loss of pten to drive AR-independent castration-resistant prostate cancer. Cancer Research 80 576590. (https://doi.org/10.1158/0008-5472.CAN-19-1684)

    • Search Google Scholar
    • Export Citation
  • PeinettiNScalerandiMVCuello RubioMMLeimgruberCNicolaJPTorresAIQuintarAAMaldonadoCA 2018 The response of prostate smooth muscle cells to testosterone is determined by the subcellular distribution of the androgen receptor. Endocrinology 159 945956. (https://doi.org/10.1210/en.2017-00718)

    • Search Google Scholar
    • Export Citation
  • PeiróCLafuenteNMatesanzNCercasELlergoJLVallejoSRodríguez-MañasLSánchez-FerrerCF 2001 High glucose induces cell death of cultured human aortic smooth muscle cells through the formation of hydrogen peroxide. British Journal of Pharmacology 133 967974. (https://dx.doi.org/10.1038%2Fsj.bjp.0704184)

    • Search Google Scholar
    • Export Citation
  • PengSZhangJChenJWangH 2011 Effects of Wnt5a on proliferation and apoptosis in JAR choriocarcinoma cells. Molecular Medicine Report 4 99104. (https://doi.org/10.3892/mmr.2010.383)

    • Search Google Scholar
    • Export Citation
  • Pinto-FochiMEPytlowancivEZReameVRafachoARibeiroDLTabogaSRGóesRM 2016 A high-fat diet fed during different periods of life impairs steroidogenesis of rat Leydig cells. Reproduction 152 795808. (https://doi.org/10.1530/REP-16-0072)

    • Search Google Scholar
    • Export Citation
  • PortoEMDos SantosSARibeiroLMLacorteLMRinaldiJCJustulinLAJrFelisbinoSL 2011 Lobe variation effects of experimental diabetes and insulin replacement on rat prostate. Microscopy Research and Technique 74 10401048. (https://doi.org/10.1002/jemt.20991)

    • Search Google Scholar
    • Export Citation
  • PostonLCaleyachettyRCnattingiusSCorvalánCUauyRHerringSGillmanMW 2016 Preconceptional and maternal obesity: epidemiology and health consequences. Lancet Diabetes Endocrinology 4 10251036. (https://doi.org/10.1016/S2213-8587(16)30217-0)

    • Search Google Scholar
    • Export Citation
  • PytlowancivEZPinto-FochiMEReameVGobboMGRibeiroDLTabogaSRGóesRM 2016 Differential ontogenetic exposure to obesogenic environment induces hyperproliferative status and nuclear receptors imbalance in the rat prostate at adulthood. Prostate 76 662678. (https://doi.org/10.1002/pros.23158)

    • Search Google Scholar
    • Export Citation
  • RibeiroDLTabogaSRGóesRM 2009 Diabetes induces stromal remodelling and increase in chondroitin sulphate proteoglycans of the rat ventral prostate. International Journal of Experimental Pathology 90 400411. (https://doi.org/10.1111/j.1365-2613.2009.00657.x)

    • Search Google Scholar
    • Export Citation
  • RibeiroDLPintoMERafachoABosqueiroJRMaedaSYAnselmo-FranciJATabogaSRGóesRM 2012 High-fat diet obesity associated with insulin resistance increases cell proliferation, estrogen receptor, and Pi3K proteins in rat ventral prostate. Journal of Andrology 33 854865. (https://doi.org/10.2164/jandrol.111.016089)

    • Search Google Scholar
    • Export Citation
  • RozancePJHayWW 2010 Neonatal hyperglycemia. NeoReviews 11 e632e639. (https://doi.org/10.1542/neo.11-11-e632)

  • RamelSRaoR 2020 Hyperglycemia in extremely preterm infants. NeoReviews 21 e89e97. (https://doi.org/10.1542/neo.21-2-e89)

  • SchalkenJ 2005 Androgen receptor mediated growth of prostate (cancer). European Urology Supplements 4 411. (https://doi.org/10.1016/j.eursup.2005.08.006)

    • Search Google Scholar
    • Export Citation
  • ShamhartPELutherDJAdapalaRKBryantJEPetersenKAMeszarosJGThodetiCK 2014 Hyperglycemia enhances function and differentiation of adult rat cardiac fibroblasts. Canadian Journal of Physiology and Pharmacology 92 598604. (https://doi.org/10.1139/cjpp-2013-0490)

    • Search Google Scholar
    • Export Citation
  • ŞimşekDGEcevitAHatipoğluNÇobanAArısoyAEBaşFMutluGYBideciAÖzekE 2018 Neonatal hyperglycemia, which threshold value, diagnostic approach and treatment?: Turkish neonatal and pediatric endocrinology and diabetes societies consensus report. Turk Pediatri Arsivi 53 (Supplement 1) S234S238. (https://doi.org/10.5152/TurkPediatriArs.2018.01821)

    • Search Google Scholar
    • Export Citation
  • SinghRSongRHAlaviNPegoraroAASinghAKLeeheyDJ 2001 High glucose decreases matrix metalloproteinase-2 activity in rat mesangial cells via transforming growth factor-β1. Nephron Experimental Nephrology 9 249257. (https://doi.org/10.1159/000052619)

    • Search Google Scholar
    • Export Citation
  • SugimuraYCunhaGRDonjacourAA 1986 Morphogenesis of ductal networks in the mouse prostate. Biology of Reproduction 34 961971. (https://doi.org/10.1095/biolreprod34.5.961)

    • Search Google Scholar
    • Export Citation
  • ThieleSGöbelARachnerTDFuesselSFroehnerMMudersMHBarettonGBBernhardtRJakobFGlüerCC et al. 2015 Wnt5A has anti‐prostate cancer effects in vitro and reduces tumor growth in the skeleton in vivo. Journal of Bone and Mineral Research 30 471480. (https://doi.org/10.1002/jbmr.2362)

    • Search Google Scholar
    • Export Citation
  • VilamaiorPSTabogaSRCarvalhoHF 2006 Postnatal growth of the ventral prostate in winstar rats: a stereological and morphometrical study. Anatomical Record Part A 288 885892. (https://doi.org/10.1002/ar.a.20363)

    • Search Google Scholar
    • Export Citation
  • WangBEWangXDErnstJAPolakisPGaoWQ 2008 Regulation of epithelial branching morphogenesis and cancer cell growth of the prostate by wnt signaling. PLoS ONE 3 e2186. (https://doi.org/10.1371/journal.pone.0002186)

    • Search Google Scholar
    • Export Citation
  • WangFReeceEAYangP 2013 Superoxide dismutase 1 overexpression in mice abolishes maternal diabetes – induced endoplasmic reticulum stress in diabetic embryopathy. American Journal of Obstetrics and Gynecology 209 345.e1345.e7. (https://doi.org/10.1016/j.ajog.2013.06.037)

    • Search Google Scholar
    • Export Citation
  • WangHSunLSuLRizoJLiuLWangLFWangFSWangX 2014 Mixed lineage kinase domain-like protein mlkl causes necrotic membrane disruption upon phosphorylation by RIP3. Molecular Cell 54 133146. (https://doi.org/10.1016/j.molcel.2014.03.003)

    • Search Google Scholar
    • Export Citation
  • WangTLiuXWangJ 2019 Upregulation of Wnt5a inhibits proliferation and migration of hepatocellular carcinoma cells. Journal of Cancer Research and Therapeutics 15 904908. (https://doi.org/10.4103/jcrt.JCRT_886_18)

    • Search Google Scholar
    • Export Citation
  • WeibelER 1974 Selection of the best method in stereology. Journal of Microscopy 100 261269. (https://doi.org/10.1111/j.1365-2818.1974.tb03938.x)

    • Search Google Scholar
    • Export Citation
  • XuYGaoHHuYFangYQiCHuangJCaiXWuHDingXZhangZ 2019 High glucose-induced apoptosis and necroptosis in podocytes is regulated by UCHL1 via RIPK1/RIPK3 pathway. Experimental Cell Research 382 111463. (https://doi.org/10.1016/j.yexcr.2019.06.008)

    • Search Google Scholar
    • Export Citation
  • ZhuHYuWJLeYWangWJLiFGuiTWangYMShiWDDingWLFanXQ 2012 High glucose levels increase the expression of neurotrophic factors associated with p-p42/p44 MAPK in Schwann cells in vitro. Molecular Medicine Reports 6 179184. (https://doi.org/10.1007/BF03402113)

    • Search Google Scholar
    • Export Citation
  • ZamirITorneviAAbrahamssonTAhlssonFEngströmEHallbergBHansen-PuppIStoltz SjöströmEDomellöfM 2018 Hyperglycemia in extremely preterm infants – insulin treatment, mortality and nutrient intakes. Journal of Pediatrics 200 104.e1110.e1. (https://doi.org/10.1016/j.jpeds.2018.03.049)

    • Search Google Scholar
    • Export Citation