Influence of high glucose in the expression of miRNAs and IGF1R signaling pathway in human myometrial explants.


Journal

Archives of gynecology and obstetrics
ISSN: 1432-0711
Titre abrégé: Arch Gynecol Obstet
Pays: Germany
ID NLM: 8710213

Informations de publication

Date de publication:
06 2021
Historique:
received: 20 04 2020
accepted: 15 12 2020
pubmed: 13 2 2021
medline: 7 10 2021
entrez: 12 2 2021
Statut: ppublish

Résumé

Several roles are attributed to the myometrium including sperm and embryo transport, menstrual discharge, control of uterine blood flow, and labor. Although being a target of diabetes complications, the influence of high glucose on this compartment has been poorly investigated. Both miRNAs and IGF1R are associated with diabetic complications in different tissues. Herein, we examined the effects of high glucose on the expression of miRNAs and IGF1R signaling pathway in the human myometrium. Human myometrial explants were cultivated for 48 h under either high or low glucose conditions. Thereafter, the conditioned medium was collected for biochemical analyses and the myometrial samples were processed for histological examination as well as miRNA and mRNA expression profiling by qPCR. Myometrial structure and morphology were well preserved after 48 h of cultivation in both high and low glucose conditions. Levels of lactate, creatinine, LDH and estrogen in the supernatant were similar between groups. An explorative screening by qPCR arrays revealed that 6 out of 754 investigated miRNAs were differentially expressed in the high glucose group. Data validation by single qPCR assays confirmed diminished expression of miR-215-5p and miR-296-5p, and also revealed reduced miR-497-3p levels. Accordingly, mRNA levels of IGF1R and its downstream mediators FOXO3 and PDCD4, which are potentially targeted by miR-497-3p, were elevated under high glucose conditions. In contrast, mRNA expression of IGF1, PTEN, and GLUT1 was unchanged. The human myometrium responds to short-term exposure (48 h) to high glucose concentrations by regulating the expression of miRNAs, IGF1R and its downstream targets.

Identifiants

pubmed: 33575847
doi: 10.1007/s00404-020-05940-5
pii: 10.1007/s00404-020-05940-5
pmc: PMC8087607
doi:

Substances chimiques

Apoptosis Regulatory Proteins 0
IGF1R protein, human 0
MIRN296 microRNA, human 0
MIRN497 microRNA, human 0
MicroRNAs 0
PDCD4 protein, human 0
RNA-Binding Proteins 0
Receptor, IGF Type 1 EC 2.7.10.1
Glucose IY9XDZ35W2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1513-1522

Références

Abrahamsohn P (2005) The female reproductive system. In: Junqueira LC, Carneiro J (eds) Basic histology: text and atlas, 11th edn. McGraw Hill Medical, New York
Bulletti C, de Ziegler D, Polli V, Diotallevi L, Del Ferro E, Flamigni C (2000) Uterine contractility during the menstrual cycle. Hum Reprod 15(S1):81–89
pubmed: 10928421
Lyons EA, Taylor PJ, Zheng XH, Ballard G, Levi CS, Kredentser JV (1991) Characterization of subendometrial myometrial contractions throughout the menstrual cycle in normal fertile women. Fertil Steril 55:771–774
pubmed: 2010002
Brar HS, Platt LD, DeVore GR, Horenstein J, Medearis AL (1988) Qualitative assessment of maternal uterine and fetal umbilical artery blood flow and resistance in laboring patients by Doppler velocimetry. Am J Obstet Gynecol 158(4):952–956
pubmed: 2966588
Bulletti C, Ziegler DDE, Setti PL, Cicinelli E, Polli V, Flamigni C (2004) The patterns of uterine contractility in normal menstruating women: from physiology to pathology. Ann N Y Acad Sci 1034:64–83
pubmed: 15731300
Kovilam O, Khoury J, Miodovnik M, Chames M, Spinnoto J, Sibai B (2002) Spontaneous preterm delivery in the type 1 diabetic pregnancy: the role of glycemic control. J Matern Fetal Neonatal Med 11(4):245–248
pubmed: 12375678
Lepercq J, Coste J, Theau A, Dubois-Laforgue D, Timsit J (2004) Factors associated with preterm delivery in women with type 1 diabetes: a cohort study. Diabetes Care 27:2824–2828
pubmed: 15562192
Al-Qahtani S, Heath A, Quenby S, Dawood F, Floyd R, Burdyga T, Wray S (2012) Diabetes is associated with impairment of uterine contractility and high caesarean section rate. Diabetologia 55(2):489–498
pubmed: 22101974
Mayer-Davis EJ, Lawrence JM, Dabelea D et al (2017) Incidence trends of type 1 and type 2 diabetes among youths, 2002–2012. N Engl J Med 376(15):1419–1429
pubmed: 28402773 pmcid: 28402773
American-Diabetes-Association (2011) Diagnosis and classification of diabetes mellitus. Diabetes Care 34(S1):S62–S69
pmcid: 3006051
Kaya T, Cetin A, Cetin M, Sarioglu Y (1999) Effects of endothelin-1 and calcium channel blockers on contractions in human myometrium. A study on myometrial strips from normal and diabetic pregnant women. J Reprod Med 44(2):115–121
pubmed: 10853442
McMurtrie EM, Ginsberg GG, Frederick GT, Kirkland JL, Stancel GM, Gardner RM (1985) Effect of a diabetic state on myometrial ultrastructure and isolated uterine contractions in the rat. Proc Soc Exp Biol Med 180:497–504
pubmed: 4080698
Jawerbaum A, Catafau JR, Gonzalez ET, Novaro V, Gomez G, Gelpi E, Gimeno MA (1996) Eicosanoid production, metabolism and contractile activity in the isolated uterus from non-insulin-dependent diabetic rats during late pregnancy. Prostaglandins 51:307–320
pubmed: 8792441
Spiegl G, Zupko I, Minorics R, Csik G, Csonka D, Falkay G (2009) Effects of experimentally induced diabetes mellitus on pharmacologically and electrically elicited myometrial contractility. Clin Exp Pharmacol Physiol 36(9):884–891
pubmed: 19298542
Favaro RR, Raspantini PR, Salgado RM, Fortes ZB, Zorn TMT (2015) Long-term type 1 diabetes alters the deposition of collagens and proteoglycans in the early pregnant myometrium of mice. Histol Histopathol 30(4):435–444
pubmed: 25196145
Favaro RR, Salgado RM, Raspantini PR, Fortes ZB, Zorn TMT (2010) Effects of long-term diabetes on the structure and cell proliferation of the myometrium in the early pregnancy of mice. Int J Exp Pathol 91(5):426–435
pubmed: 20586816 pmcid: 3003840
Siddle K (2011) Signalling by insulin and IGF receptors: supporting acts and new players. J Mol Endocrinol 47(1):R1-10
pubmed: 21498522
Riedemann J, Macaulay VM (2006) IGF1R signalling and its inhibition. Endocr Relat Cancer 13(S1):S33-43
pubmed: 17259557
White V, Jawerbaum A, Mazzucco MB, Gauster M, Desoye G, Hiden U (2015) Diabetes-associated changes in the fetal insulin/insulin-like growth factor system are organ specific in rats. Pediatr Res 77(1–1):48–55
pubmed: 25268143
Morris BJ, Willcox DC, Donlon TA, Willcox BJ (2015) FOXO3: a major gene for human longevity—a mini-review. Gerontology 61(6):515–525
pubmed: 25832544 pmcid: 5403515
Lankat-Buttgereit B, Goke R (2009) The tumour suppressor Pdcd4: recent advances in the elucidation of function and regulation. Biol Cell 101(6):309–317
pubmed: 19356152
Jonas S, Izaurralde E (2015) Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet 16(7):421–433
pubmed: 26077373
Slezak-Prochazka I, Durmus S, Kroesen BJ, van den Berg A (2010) MicroRNAs, macrocontrol: regulation of miRNA processing. RNA 16(6):1087–1095
pubmed: 20423980 pmcid: 2874160
Kato M, Castro NE, Natarajan R (2013) MicroRNAs: potential mediators and biomarkers of diabetic complications. Free Radic Biol Med 64:85–94
pubmed: 23770198 pmcid: 3762900
Morales-Prieto DM, Ospina-Prieto S, Schmidt A, Chaiwangyen W, Markert UR (2014) Elsevier trophoblast research award lecture: origin, evolution and future of placenta miRNAs. Placenta 35(Suppl):S39-45
pubmed: 24378039
Morales-Prieto DM, Chaiwangyen W, Ospina-Prieto S, Schneider U, Herrmann J, Gruhn B, Markert UR (2012) MicroRNA expression profiles of trophoblastic cells. Placenta 33(9):725–734
pubmed: 22721760
Ackerman WE 4th, Buhimschi IA, Brubaker D, Maxwell S, Rood KM, Chance MR, Jing H, Mesiano S, Buhimschi CS (2018) Integrated microRNA and mRNA network analysis of the human myometrial transcriptome in the transition from quiescence to labor. Biol Reprod 98(6):834–845
pubmed: 29447339 pmcid: 5991200
Georgieva B, Milev I, Minkov I, Dimitrova I, Bradford AP, Baev V (2012) Characterization of the uterine leiomyoma microRNAome by deep sequencing. Genomics 99(5):275–281
pubmed: 22446413
Tang Y, Ji H, Liu H, Gu W, Li X, Peng T (2015) Identification and functional analysis of microRNA in myometrium tissue from spontaneous preterm labor. Int J Clin Exp Pathol 8(10):12811–12819
pubmed: 26722471 pmcid: 4680416
Cook JR, MacIntyre DA, Samara E, Kim SH, Singh N, Johnson MR, Bennett PR, Terzidou V (2015) Exogenous oxytocin modulates human myometrial microRNAs. Am J Obstet Gynecol 213:65.e1–9
Tang X, Muniappan L, Tang G, Ozcan S (2009) Identification of glucose-regulated miRNAs from pancreatic beta cells reveals a role for miR-30d in insulin transcription. RNA 15(2):287–293
pubmed: 19096044 pmcid: 2648717
Mu J, Pang Q, Guo YH, Chen JG, Zeng W, Huang YJ, Zhang J, Feng B (2013) Functional implications of microRNA-215 in TGF-beta1-induced phenotypic transition of mesangial cells by targeting CTNNBIP1. PLoS ONE 8(3):e58622
pubmed: 23554908 pmcid: 3595285
Tang XM, Rossi MJ, Masterson BJ, Chegini N (1994) Insulin-like growth factor I (IGF-I), IGF-I receptors, and IGF binding proteins 1–4 in human uterine tissue: tissue localization and IGF-I action in endometrial stromal and myometrial smooth muscle cells in vitro. Biol Reprod 50(5):1113–1125
pubmed: 7517700
Wang J, Niu W, Nikiforov Y, Naito S, Chernausek S, Witte D, LeRoith D, Strauch A, Fagin JA (1997) Targeted overexpression of IGF-I evokes distinct patterns of organ remodeling in smooth muscle cell tissue beds of transgenic mice. J Clin Invest 100(6):1425–1439
pubmed: 9294108 pmcid: 508321
Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellve AR, Efstratiadis A (1996) Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 10(7):903–918
pubmed: 8813730
Shynlova O, Tsui P, Dorogin A, Langille BL, Lye SJ (2007) Insulin-like growth factors and their binding proteins define specific phases of myometrial differentiation during pregnancy in the rat. Biol Reprod 76(4):571–578
pubmed: 17123939
Hayati AR, Cheah FC, Tan AE, Tan GC (2007) Insulin-like growth factor-1 receptor expression in the placentae of diabetic and normal pregnancies. Early Hum Dev 83(1):41–46
pubmed: 16750336
Gerhardinger C, McClure KD, Romeo G, Podestà F, Lorenzi M (2001) IGF-I mRNA and signaling in the diabetic retina. Diabetes 50(1):175–183
pubmed: 11147784
Ma W, Kang Y, Ning L, Tan J, Wang H, Ying Y (2017) Identification of microRNAs involved in gefitinib resistance of non-small-cell lung cancer through the insulin-like growth factor receptor 1 signaling pathway. Exp Ther Med 14(4):2853–2862
pubmed: 28912847 pmcid: 5585727
Wang L, Su W, Du W, Xu Y, Wang L, Kong D, Han Z, Zheng G, Li Z (2015) Gene and MicroRNA profiling of human induced pluripotent stem cell-derived endothelial cells. Stem Cell Rev 11(2):219–227
Choi SY, Yun J, Lee OJ, Han HS, Yeo MK, Lee MA, Suh KS (2013) MicroRNA expression profiles in placenta with severe preeclampsia using a PNA-based microarray. Placenta 34(9):799–804
pubmed: 23830491
Cazanave SC, Mott JL, Elmi NA, Bronk SF, Masuoka HC, Charlton MR, Gores GJ (2011) A role for miR-296 in the regulation of lipoapoptosis by targeting PUMA. J Lipid Res 52(8):1517–1525
pubmed: 21633093 pmcid: 3137017
Savi F, Forno I, Faversani A, Luciani A, Caldiera S, Gatti S, Foa P, Ricca D, Bulfamante G, Vaira V, Bosari S (2014) miR-296/Scribble axis is deregulated in human breast cancer and miR-296 restoration reduces tumour growth in vivo. Clin Sci 127(4):233–242
Lee KH, Lin FC, Hsu TI, Lin JT, Guo JH, Tsai CH, Lee YC, Lee YC, Chen CL, Hsiao M, Lu PJ (2014) MicroRNA-296-5p (miR-296-5p) functions as a tumor suppressor in prostate cancer by directly targeting Pin1. Biochim Biophys Acta 1843(9):2055–2066
pubmed: 24915000
Xu C, Li S, Chen T, Hu H, Ding C, Xu Z, Chen J, Liu Z, Lei Z, Zhang HT, Li C, Zhao J (2016) miR-296-5p suppresses cell viability by directly targeting PLK1 in non-small cell lung cancer. Oncol Rep 35(1):497–503
pubmed: 26549165
Li T, Lu YY, Zhao XD, Guo HQ, Liu CH, Li H, Zhou L, Han YN, Wu KC, Nie YZ, Shi YQ, Fan DM (2014) MicroRNA-296-5p increases proliferation in gastric cancer through repression of Caudal-related homeobox 1. Oncogene 33(6):783–793
pubmed: 23353818
Vychytilova-Faltejskova P, Merhautova J, Machackova T, Gutierrez-Garcia I, Garcia-Solano J, Radova L, Brchnelova D, Slaba K, Svoboda M, Halamkova J, Demlova R, Kiss I, Vyzula R, Conesa-Zamora P, Slaby O (2017) MiR-215-5p is a tumor suppressor in colorectal cancer targeting EGFR ligand epiregulin and its transcriptional inducer HOXB9. Oncogenesis 6(11):399
pubmed: 29199273 pmcid: 5868056
Wang C, Chen Q, Li S, Li S, Zhao Z, Gao H, Wang X, Li B, Zhang W, Yuan Y, Ming L, He H, Tao B, Zhong J (2017) Dual inhibition of PCDH9 expression by miR-215-5p up-regulation in gliomas. Oncotarget 8(6):10287–10297
pubmed: 28055966
Zhao J, Xu J, Zhang R (2018) SRPX2 regulates colon cancer cell metabolism by miR-192/215 via PI3K-Akt. Am J Transl Res 10(2):483–490
pubmed: 29511442 pmcid: 5835813
Han J, Zhang L, Guo H, Wysham WZ, Roque DR, Willson AK, Sheng X, Zhou C, Bae-Jump VL (2015) Glucose promotes cell proliferation, glucose uptake and invasion in endometrial cancer cells via AMPK/mTOR/S6 and MAPK signaling. Gynecol Oncol 138(3):668–675
pubmed: 26135947 pmcid: 4672629
Jie W, Wang X, Zhang Y, Guo J, Kuang D, Zhu P, Wang G, Ao Q (2010) SDF-1alpha/CXCR4 axis is involved in glucose-potentiated proliferation and chemotaxis in rat vascular smooth muscle cells. Int J Exp Pathol 91(5):436–444
pubmed: 20586815 pmcid: 3003841
Carstensen B, Read SH, Friis S, Sund R, Keskimaki I, Svensson AM, Ljung R, Wild SH, Kerssens JJ, Harding JL, Magliano DJ, Gudbjörnsdottir S, Diabetes and Cancer Research Consortium (2016) Cancer incidence in persons with type 1 diabetes: a five-country study of 9000 cancers in type 1 diabetic individuals. Diabetologia 59(5):980–988
pubmed: 26924393 pmcid: 4826427
Peng L, Wen Y, Han Y, Wei A, Shi G, Mizuguchi M, Lee P, Hernando E, Mittal K, Wei JJ (2009) Expression of insulin-like growth factors (IGFs) and IGF signaling: molecular complexity in uterine leiomyomas. Fertil Steril 91(6):2664–2675
pubmed: 18439583
Hou P, Zhao L, Li Y, Luo F, Wang S, Song J, Bai J (2014) Comparative expression of thioredoxin-1 in uterine leiomyomas and myometrium. Mol Hum Reprod 20(2):148–154
pubmed: 24130091
Fitzgerald JB, Chennathukuzhi V, Koohestani F, Nowak RA, Christenson LK (2012) Role of microRNA-21 and programmed cell death 4 in the pathogenesis of human uterine leiomyomas. Fertil Steril 98(3):726-734.e722
pubmed: 22728051 pmcid: 3432744
Baird DD, Travlos G, Wilson R, Dunson DB, Hill MC, D’Aloisio AA, London SJ, Schectman JM (2009) Uterine leiomyomata in relation to insulin-like growth factor-I, insulin, and diabetes. Epidemiology 20(4):604–610
pubmed: 19305350 pmcid: 2856640
Radin RG, Palmer JR, Rosenberg L, Kumanyika SK, Wise LA (2010) Dietary glycemic index and load in relation to risk of uterine leiomyomata in the Black Women’s Health Study. Am J Clin Nutr 91(5):1281–1288
pubmed: 20200259 pmcid: 2854903

Auteurs

Rodolfo R Favaro (RR)

Placenta Lab, Department of Obstetrics, Jena University Hospital, Jena, Germany. rodolfo.favaro@med.uni-jena.de.
Laboratory of Reproductive and Extracellular Matrix Biology, Department of Cell and Developmental Biology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil. rodolfo.favaro@med.uni-jena.de.

Diana M Morales-Prieto (DM)

Placenta Lab, Department of Obstetrics, Jena University Hospital, Jena, Germany.

Jörg Herrmann (J)

Department of Gynecology and Obstetrics, Hufeland Klinikum, Weimar, Germany.

Jürgen Sonnemann (J)

Department of Pediatric Hematology and Oncology, Children's Clinic, Jena University Hospital, Jena, Germany.

Ekkehard Schleussner (E)

Placenta Lab, Department of Obstetrics, Jena University Hospital, Jena, Germany.

Udo R Markert (UR)

Placenta Lab, Department of Obstetrics, Jena University Hospital, Jena, Germany.

Telma M T Zorn (TMT)

Laboratory of Reproductive and Extracellular Matrix Biology, Department of Cell and Developmental Biology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.

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