Imprinted gene alterations in the kidneys of growth restricted offspring may be mediated by a long non-coding RNA

References

• Doan TNA, Akison LK, Bianco-Miotto T. Epigenetic mechanisms responsible for the transgenerational inheritance of intrauterine growth restriction phenotypes. Front Endocrinol (Lausanne). 2022;13:838737. doi: 10.3389/fendo.2022.838737
   PubMed Web of Science ®Google Scholar
• Sharma D, Shastri S, Sharma P. Intrauterine growth restriction: antenatal and postnatal aspects. Clin Med Insights Pediatr. 2016;10:67–12. doi: 10.4137/CMPed.S40070
   PubMedGoogle Scholar
• Dalle Molle R, Bischoff AR, Portella AK, et al. The fetal programming of food preferences: current clinical and experimental evidence. J Dev Orig Health Dis. 2016;7(3):222–230. doi: 10.1017/S2040174415007187
   PubMed Web of Science ®Google Scholar
• Skinner MK, Manikkam M, Tracey R, et al. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med. 2013;11:228. doi: 10.1186/1741-7015-11-228
   PubMed Web of Science ®Google Scholar
• Skinner MK, Ben Maamar M, Sadler-Riggleman I, et al. Alterations in sperm DNA methylation, non-coding RNA and histone retention associate with DDT-induced epigenetic transgenerational inheritance of disease. Epigenet Chromatin. 2018;11(1):8. doi: 10.1186/s13072-018-0178-0
   PubMedGoogle Scholar
• Thorson JLM, Beck D, Ben Maamar M, et al. Ancestral plastics exposure induces transgenerational disease-specific sperm epigenome-wide association biomarkers. Environ Epigenet. 2021;7(1):dvaa023. doi: 10.1093/eep/dvaa023
   PubMed Web of Science ®Google Scholar
• Weber-Stadlbauer U, Richetto J, Zwamborn RAJ, et al. Transgenerational modification of dopaminergic dysfunctions induced by maternal immune activation. Neuropsychopharmacology. 2021;46(2):404–412. doi: 10.1038/s41386-020-00855-w
   PubMed Web of Science ®Google Scholar
• Goyal D, Limesand SW, Goyal R. Epigenetic responses and the developmental origins of health and disease. J Endocrinol. 2019;242(1):T105–T119. doi: 10.1530/joe-19-0009
   PubMed Web of Science ®Google Scholar
• Siklenka K, Erkek S, Godmann M, et al. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science. 2015;350(6261):aab2006. doi: 10.1126/science.aab2006
   PubMed Web of Science ®Google Scholar
• Lismer A, Siklenka K, Lafleur C, et al. Sperm histone H3 lysine 4 trimethylation is altered in a genetic mouse model of transgenerational epigenetic inheritance. Nucleic Acids Res. 2020;48(20):11380–11393. doi: 10.1093/nar/gkaa712
   PubMed Web of Science ®Google Scholar
• Briffa JF, Wlodek ME, Moritz KM. Transgenerational programming of nephron deficits and hypertension. Semin Cell Dev Biol. 2018;S1084-9521(17):30447–0. doi: 10.1016/j.semcdb.2018.05.025
   Google Scholar
• Doan TNA, Briffa JF, Phillips AL, et al. Epigenetic mechanisms involved in intrauterine growth restriction and aberrant kidney development and function. J Dev Orig Health Dis. 2021;12(6):952–962. doi: 10.1017/S2040174420001257
   PubMed Web of Science ®Google Scholar
• Gallo LA, Tran M, Cullen-McEwen LA, et al. Transgenerational programming of fetal nephron deficits and sex-specific adult hypertension in rats. Reprod Fertil Dev. 2014;26(7):1032–1043. doi: 10.1071/RD13133
   PubMed Web of Science ®Google Scholar
• Gallo LA, Tran M, Moritz KM, et al. Cardio-renal and metabolic adaptations during pregnancy in female rats born small: implications for maternal health and second generation fetal growth. Journal Of Physiology. 2012;590(3):617–630. doi: 10.1113/jphysiol.2011.219147
   PubMed Web of Science ®Google Scholar
• Master JS, Zimanyi MA, Yin KV, et al. Transgenerational left ventricular hypertrophy and hypertension in offspring after uteroplacental insufficiency in male rats. Clin Exp Pharmacol Physiol. 2014;41(11):884–890. doi: 10.1111/1440-1681.12303
   PubMed Web of Science ®Google Scholar
• Tran M, Gallo LA, Jefferies AJ, et al. Transgenerational metabolic outcomes associated with uteroplacental insufficiency. J Endocrinol. 2013;217(1):105–118. doi: 10.1530/JOE-12-0560
   PubMed Web of Science ®Google Scholar
• Wadley GD, Siebel AL, Cooney GJ, et al. Uteroplacental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sex-specific manner in the adult rat. Am J Physiol Endocrinol Metab. 2008;294(5):E861–E869. doi: 10.1152/ajpendo.00037.2008
   PubMed Web of Science ®Google Scholar
• Horsthemke B. A critical view on transgenerational epigenetic inheritance in humans. Nat Commun. 2018;9(1):2973. doi: 10.1038/s41467-018-05445-5
   PubMedGoogle Scholar
• Cordeiro A, Neto AP, Carvalho F, et al. Relevance of genomic imprinting in intrauterine human growth expression of CDKN1C, H19, IGF2, KCNQ1 and PHLDA2 imprinted genes. J Assist Reprod Genet. 2014;31(10):1361–1368. doi: 10.1007/s10815-014-0278-0
   PubMed Web of Science ®Google Scholar
• Saha P, Verma S, Pathak RU, et al. Long noncoding RNAs in mammalian development and diseases. Adv Exp Med Biol. 2017;1008:155–198. doi: 10.1007/978-981-10-5203-3_6
   PubMed Web of Science ®Google Scholar
• Wlodek ME, Westcott K, Siebel AL, et al. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008;74(2):187–195. doi: 10.1038/ki.2008.153
   PubMed Web of Science ®Google Scholar
• Wlodek ME, Mibus A, Tan A, et al. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J Am Soc Nephrol. 2007;18(6):1688–1696. doi: 10.1681/asn.2007010015
   PubMed Web of Science ®Google Scholar
• Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215. doi: 10.1093/nar/16.3.1215
   PubMed Web of Science ®Google Scholar
• Suchiman HE, Slieker RC, Kremer D, et al. Design, measurement and processing of region-specific DNA methylation assays: the mass spectrometry-based method EpiTYPER. Front Genet. 2015;6:287. doi: 10.3389/fgene.2015.00287
   PubMed Web of Science ®Google Scholar
• R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available from: http://www.R-project.org/
   Google Scholar
• Team R. RStudio: integrated development for R. Boston, MA: RStudio, PBC; 2020. Available from: http://www.rstudio.com/
   Google Scholar
• Øyvind H, David ATH, Paul DR. PAST: Paleontological statistics software package for education and data analysis. Palaeont Electr. 2001;4(1):1–9.
   Google Scholar
• Fitzpatrick GV, Pugacheva EM, Shin JY, et al. Allele-specific binding of CTCF to the multipartite imprinting control region KvDMR1. Mol Cell Biol. 2007;27(7):2636–2647. doi: 10.1128/mcb.02036-06
   PubMed Web of Science ®Google Scholar
• Shin JY, Fitzpatrick GV, Higgins MJ. Two distinct mechanisms of silencing by the KvDMR1 imprinting control region. EMBO J. 2008;27(1):168–178. doi: 10.1038/sj.emboj.7601960
   PubMed Web of Science ®Google Scholar
• Mancini-DiNardo D, Steele SJS, Ingram RS, et al. A differentially methylated region within the gene Kcnq1 functions as an imprinted promoter and silencer. Hum Mol Genet. 2003;12(3):283–294. doi: 10.1093/hmg/ddg024
   PubMed Web of Science ®Google Scholar
• Abugessaisa I, Noguchi S, Hasegawa A, et al. refTSS: a reference data set for human and mouse transcription start sites. J Mol Biol. 2019;431(13):2407–2422. doi: 10.1016/j.jmb.2019.04.045
   PubMed Web of Science ®Google Scholar
• Tsunoda T, Takagi T. Estimating transcription factor bindability on DNA. Bioinformatics. 1999;15(7–8):622–30. doi: 10.1093/bioinformatics/15.7.622
   PubMed Web of Science ®Google Scholar
• Baribault C, Ehrlich KC, Ponnaluri VKC, et al. Developmentally linked human DNA hypermethylation is associated with down-modulation, repression, and upregulation of transcription. Epigenetics. 2018;13(3):275–289. doi: 10.1080/15592294.2018.1445900
   PubMed Web of Science ®Google Scholar
• Kao C-Y, Xu M, Wang L, et al. Elevated COUP-TFII expression in dopaminergic neurons accelerates the progression of Parkinson’s disease through mitochondrial dysfunction. PLoS Genet. 2020;16(6):e1008868. doi: 10.1371/journal.pgen.1008868
   PubMed Web of Science ®Google Scholar
• Li L, Galichon P, Xiao X, et al. Orphan nuclear receptor COUP-TFII enhances myofibroblast glycolysis leading to kidney fibrosis. EMBO Rep. 2021;22(6):e51169. doi: 10.15252/embr.202051169
   PubMed Web of Science ®Google Scholar
• Ishii S, Koibuchi N. COUP-TFII in kidneys, from embryos to sick adults. Diagnostics. 2022;12(5). doi: 10.3390/diagnostics12051181
   Web of Science ®Google Scholar
• Estrela GR, Freitas-Lima LC, Budu A, et al. Chronic kidney disease induced by Cisplatin, folic acid and renal ischemia reperfusion induces anemia and promotes GATA-2 activation in mice. Biomedicines. 2021;9(7):769. doi: 10.3390/biomedicines9070769
   PubMed Web of Science ®Google Scholar
• Yang X, Mei C, Nie H, et al. Expression profile and prognostic values of GATA family members in kidney renal clear cell carcinoma. Aging. 2023;15(6):2170–2188. doi: 10.18632/aging.204607
   PubMedGoogle Scholar
• Liu Z, Zhang J, Gao Y, et al. Large-scale characterization of DNA methylation changes in human gastric carcinomas with and without metastasis. Clin Cancer Res. 2014;20(17):4598–4612. doi: 10.1158/1078-0432.CCR-13-3380
   PubMed Web of Science ®Google Scholar
• Zhao L, Li C, Guan C, et al. Serum response factor, a novel early diagnostic biomarker of acute kidney injury. Aging. 2021 Jan 5;13(2):2885–2894. doi: 10.18632/aging.202381
   PubMedGoogle Scholar
• Drake KA, Chaney C, Patel M, et al. Transcription factors YAP/TAZ and SRF cooperate to specify renal myofibroblasts in the developing mouse kidney. J Am Soc Nephrol. 2022;33(9):1694–1707. doi: 10.1681/asn.2021121559
   PubMed Web of Science ®Google Scholar
• Makhov PB, Golovine KV, Kutikov A, et al. Reversal of epigenetic silencing of AP-2alpha results in increased zinc uptake in DU-145 and LNCaP prostate cancer cells. Carcinogenesis. 2011;32(12):1773–1781. doi: 10.1093/carcin/bgr212
   PubMed Web of Science ®Google Scholar
• Lamontagne JO, Zhang H, Zeid AM, et al. Transcription factors AP-2α and AP-2β regulate distinct segments of the distal nephron in the mammalian kidney. Nat Commun. 2022;13(1):2226. doi: 10.1038/s41467-022-29644-3
   PubMed Web of Science ®Google Scholar
• Simmers MD, Hudson KM, Baptissart M, et al. Epigenetic control of the imprinted growth regulator Cdkn1c in cadmium-induced placental dysfunction. Epigenetics. 2022;18:1–17. doi: 10.1080/15592294.2022.2088173
   Google Scholar
• Chen S, Sun FZ, Huang X, et al. Assisted reproduction causes placental maldevelopment and dysfunction linked to reduced fetal weight in mice. Sci Rep. 2015;5:10596. doi: 10.1038/srep10596
   PubMed Web of Science ®Google Scholar
• Fitzpatrick GV, Soloway PD, Higgins MJ. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nature Genet. 2002;32(3):426–431. doi: 10.1038/ng988
   PubMed Web of Science ®Google Scholar
• Mancini-Dinardo D, Steele SJS, Levorse JM, et al. Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev. 2006;20(10):1268–1282. doi: 10.1101/gad.1416906
   PubMed Web of Science ®Google Scholar
• Cytrynbaum C, Chong K, Hannig V, et al. Genomic imbalance in the centromeric 11p15 imprinting center in three families: further evidence of a role for IC2 as a cause of Russell–Silver syndrome. Am J Med Genet A. 2016;170(10):2731–2739. doi: 10.1002/ajmg.a.37819
   PubMed Web of Science ®Google Scholar
• Bonaldi A, Mazzeu JF, Costa SS, et al. Microduplication of the ICR2 domain at chromosome 11p15 and familial Silver–Russell syndrome. Am J Med Genet A. 2011;155(10):2479–2483. doi: 10.1002/ajmg.a.34023
   Google Scholar
• Mio C, Allegri L, Passon N, et al. A paternally inherited 1.4 kb deletion of the 11p15.5 imprinting center 2 is associated with a mild familial Silver–Russell syndrome phenotype. Eur J Hum Genet. 2021;29(3):447–454. doi: 10.1038/s41431-020-00753-1
   PubMed Web of Science ®Google Scholar
• Passaretti F, Pignata L, Vitiello G, et al. Different mechanisms cause hypomethylation of both H19 and KCNQ1OT1 imprinted differentially methylated regions in two cases of Silver-Russell syndrome spectrum. Genes. 2022;13(10):1875. doi: 10.3390/genes13101875
   PubMed Web of Science ®Google Scholar
• López-Abad M, Iglesias-Platas I, Monk D. Epigenetic characterization of CDKN1C in placenta samples from non-syndromic intrauterine growth restriction. Front Genet. 2016;7:62. doi: 10.3389/fgene.2016.00062
   PubMed Web of Science ®Google Scholar
• Caniçais C, Vasconcelos S, Ramalho C, et al. Deregulation of imprinted genes expression and epigenetic regulators in placental tissue from intrauterine growth restriction. J Assist Reprod Genet. 2021;38(4):791–801. doi: 10.1007/s10815-020-02047-3
   PubMed Web of Science ®Google Scholar
• Guo L, Choufani S, Ferreira J, et al. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biology. 2008;320(1):79–91. doi: 10.1016/j.ydbio.2008.04.025
   PubMed Web of Science ®Google Scholar
• Bourque DK, Avila L, Peñaherrera M, et al. Decreased placental methylation at the H19/IGF2 imprinting control region is associated with normotensive intrauterine growth restriction but not preeclampsia. Placenta. 2010;31(3):197–202. doi: 10.1016/j.placenta.2009.12.003
   PubMed Web of Science ®Google Scholar
• Al-Awqati Q, Oliver JA. Stem cells in the kidney. Kidney Int. 2002;61(2):387–395. doi: 10.1046/j.1523-1755.2002.00164.x
   PubMed Web of Science ®Google Scholar
• Park J, Shrestha R, Qiu C, et al. Single-cell transcriptomics of the mouse kidney reveals potential cellular targets of kidney disease. Science. 2018;360(6390):758–763. doi: 10.1126/science.aar2131
   PubMed Web of Science ®Google Scholar
• Ransick A, Lindström NO, Liu J, et al. Single-cell Profiling Reveals sex, lineage, and regional diversity in the mouse kidney. Dev Cell. 2019;51(3):399–413.e7. doi: 10.1016/j.devcel.2019.10.005
   PubMed Web of Science ®Google Scholar
• Ding F, Tian X, Mo J, et al. Determination of the dynamic cellular transcriptional profiles during kidney development from birth to maturity in rats by single-cell RNA sequencing. Cell Death Discov. 2021;7(1):162. doi: 10.1038/s41420-021-00542-9
   PubMed Web of Science ®Google Scholar
• Bhogal B, Arnaudo A, Dymkowski A, et al. Methylation at mouse Cdkn1c is acquired during postimplantation development and functions to maintain imprinted expression. Genomics. 2004;84(6):961–970. doi: 10.1016/j.ygeno.2004.08.004
   PubMed Web of Science ®Google Scholar
• Guo T, Luo F, Lin Q. You are affected by what your parents eat: diet, epigenetics, transgeneration and intergeneration. Trends Food Sci Technol. 2020;100:248–261. doi: 10.1016/j.tifs.2020.04.021
   Web of Science ®Google Scholar
• Salmeri N, Carbone IF, Cavoretto PI, et al. Epigenetics beyond fetal growth restriction: a comprehensive overview. Mol Diagn Ther. 2022;26(6):607–626. doi: 10.1007/s40291-022-00611-4
   PubMed Web of Science ®Google Scholar
• Basak T, Ain R. Long non-coding RNAs in placental development and disease. Non-Cod RNA Investgat. 2019;3. doi: 10.21037/ncri.2019.03.01
   Google Scholar