Impact of vitamin D depletion during development on mouse sperm DNA methylation

References

• Fox J, Kollenkirchen U. Normal plasma calcium, phosphate, and parathyroid hormone levels during 1,25(OH)2D3 infusions in rats. Am J Physiol. 1992 Jan;262(1 Pt 1):E126–9. PubMed PMID: 1733243.
   PubMedGoogle Scholar
• De Vizia B, Mansi A. Calcium and phosphorus metabolism in full-term infants. Monatsschrift Kinderheilkunde. 1992 Sep;140(9 Suppl 1):S8–12. PubMed PMID: 1435829.
   PubMedGoogle Scholar
• Wei R, Christakos S. Mechanisms underlying the regulation of innate and adaptive immunity by Vitamin D. Nutrients. 2015 Sep 24;7(10):8251–8260. PubMed PMID: 26404359; PubMed Central PMCID: PMC4632412.
   PubMed Web of Science ®Google Scholar
• Lugg ST, Howells PA, Thickett DR. Optimal Vitamin D supplementation levels for cardiovascular disease protection. Dis Markers. 2015;2015:864370. PubMed PMID: 26435569; PubMed Central PMCID: PMC4578836.
   PubMedGoogle Scholar
• Cui X, Gooch H, Groves NJ, et al. Vitamin D and the brain: key questions for future research. J Steroid Biochem Mol Biol. 2015 Apr;148:305–309. PubMed PMID: 25448739.
   PubMed Web of Science ®Google Scholar
• Blomberg Jensen M. Vitamin D and male reproduction. Nat Reviews Endocrinol. 2014 Mar;10(3):175–186. PubMed PMID: 24419359.
   PubMed Web of Science ®Google Scholar
• Fetahu IS, Hobaus J, Kallay E. Vitamin D and the epigenome. Front Physiol. 2014;5:164. PubMed PMID: 24808866; PubMed Central PMCID: PMC4010791.
   PubMed Web of Science ®Google Scholar
• Keane TM, Goodstadt L, Danecek P, et al. Mouse genomic variation and its effect on phenotypes and gene regulation. Nature. 2011 Sep 14;477(7364):289–294. PubMed PMID: 21921910; PubMed Central PMCID: PMC3276836.
   PubMed Web of Science ®Google Scholar
• Zhu H, Wang X, Shi H, et al. A genome-wide methylation study of severe vitamin D deficiency in African American adolescents. J Pediatr. 2013 May;162(5):1004–9 e1. PubMed PMID: 23219444; PubMed Central PMCID: PMC3935318.
   PubMed Web of Science ®Google Scholar
• Malinen M, Saramaki A, Ropponen A, et al. Distinct HDACs regulate the transcriptional response of human cyclin-dependent kinase inhibitor genes to Trichostatin A and 1alpha,25-dihydroxyvitamin D3. Nucleic Acids Res. 2008 Jan;36(1):121–132. PubMed PMID: 17999998; PubMed Central PMCID: PMC2248733.
   PubMed Web of Science ®Google Scholar
• Pereira F, Barbachano A, Silva J, et al. KDM6B/JMJD3 histone demethylase is induced by vitamin D and modulates its effects in colon cancer cells. Hum Mol Genet. 2011 Dec 1;20(23):4655–4665. PubMed PMID: 21890490.
   PubMed Web of Science ®Google Scholar
• Pereira F, Barbachano A, Singh PK, et al. Vitamin D has wide regulatory effects on histone demethylase genes. Cell Cycle. 2012 Mar 15;11(6):1081–1089. PubMed PMID: 22370479.
   PubMed Web of Science ®Google Scholar
• Padi SK, Zhang Q, Rustum YM, et al. MicroRNA-627 mediates the epigenetic mechanisms of vitamin D to suppress proliferation of human colorectal cancer cells and growth of xenograft tumors in mice. Gastroenterology. 2013 Aug;145(2):437–446. PubMed PMID: 23619147; PubMed Central PMCID: PMC3722307.
   PubMed Web of Science ®Google Scholar
• Seuter S, Pehkonen P, Heikkinen S, et al. Dynamics of 1alpha,25-dihydroxyvitamin D3-dependent chromatin accessibility of early vitamin D receptor target genes. Biochim Biophys Acta. 2013 Dec;1829(12):1266–1275. PubMed PMID: 24185200.
   PubMed Web of Science ®Google Scholar
• Seuter S, Heikkinen S, Carlberg C. Chromatin acetylation at transcription start sites and vitamin D receptor binding regions relates to effects of 1alpha,25-dihydroxyvitamin D3 and histone deacetylase inhibitors on gene expression. Nucleic Acids Res. 2013 Jan 07;41(1):110–124. PubMed PMID: 23093607; PubMed Central PMCID: PMC3592476.
   PubMed Web of Science ®Google Scholar
• Anderson CM, Gillespie SL, Thiele DK, et al. Effects of maternal Vitamin D supplementation on the maternal and infant epigenome. Breastfeeding Med. 2018 Jun;13(5):371–380. PubMed PMID: 29782187.
   PubMed Web of Science ®Google Scholar
• Zhang H, Chu X, Huang Y, et al. Maternal vitamin D deficiency during pregnancy results in insulin resistance in rat offspring, which is associated with inflammation and Ikappabalpha methylation. Diabetologia. 2014 Oct;57(10):2165–2172. PubMed PMID: 24985146.
   PubMed Web of Science ®Google Scholar
• Meems LM, Mahmud H, Buikema H, et al. Parental vitamin D deficiency during pregnancy is associated with increased blood pressure in offspring via Panx1 hypermethylation. Am J Physiol Heart Circ Physiol. 2016 Dec 1;311(6):H1459–H1469. PubMed PMID: 27769995.
   PubMed Web of Science ®Google Scholar
• Wen J, Hong Q, Wang X, et al. The effect of maternal vitamin D deficiency during pregnancy on body fat and adipogenesis in rat offspring. Sci Rep. 2018 Jan 10;8(1):365. PubMed PMID: 29321608; PubMed Central PMCID: PMC5762667.
   PubMedGoogle Scholar
• Xue J, Schoenrock SA, Valdar W, et al. Maternal vitamin D depletion alters DNA methylation at imprinted loci in multiple generations. Clin Epigenetics. 2016;8:107. PubMed PMID: 27777636; PubMed Central PMCID: PMC5062906.
   PubMed Web of Science ®Google Scholar
• Jenkins TG, James ER, Alonso DF, et al. Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology. 2017 Nov;5(6):1089–1099. PubMed PMID: 28950428; PubMed Central PMCID: PMC5679018.
   PubMed Web of Science ®Google Scholar
• Wu H, Estill MS, Shershebnev A, et al. Preconception urinary phthalate concentrations and sperm DNA methylation profiles among men undergoing IVF treatment: a cross-sectional study. Hum Reproduction. 2017 Nov 1;32(11):2159–2169. PubMed PMID: 29024969.
   PubMed Web of Science ®Google Scholar
• Radford EJ, Ito M, Shi H, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science. 2014 Aug 15;345(6198):1255903. PubMed PMID: 25011554; PubMed Central PMCID: PMC4404520.
   PubMed Web of Science ®Google Scholar
• Santi D, De Vincentis S, Magnani E, et al. Impairment of sperm DNA methylation in male infertility: a meta-analytic study. Andrology. 2017 Jul;5(4):695–703. PubMed PMID: 28718528.
   PubMed Web of Science ®Google Scholar
• Denomme MM, McCallie BR, Parks JC, et al. Alterations in the sperm histone-retained epigenome are associated with unexplained male factor infertility and poor blastocyst development in donor oocyte IVF cycles. Hum Reproduction. 2017 Dec 1;32(12):2443–2455. PubMed PMID: 29087470.
   PubMed Web of Science ®Google Scholar
• Laqqan M, Solomayer EF, Hammadeh M. Aberrations in sperm DNA methylation patterns are associated with abnormalities in semen parameters of subfertile males. Reprod Biol. 2017 Sep;17(3):246–251. PubMed PMID: 28566207.
   PubMed Web of Science ®Google Scholar
• Consortium EP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012 Sep 6;489(7414):57–74. PubMed PMID: 22955616; PubMed Central PMCID: PMC3439153.
   PubMed Web of Science ®Google Scholar
• Zhao Z, Zhang F. Sequence context analysis in the mouse genome: single nucleotide polymorphisms and CpG island sequences. Genomics. 2006 Jan;87(1):68–74. PubMed PMID: 16316740.
   PubMed Web of Science ®Google Scholar
• Shea JM, Serra RW, Carone BR, et al. Genetic and epigenetic variation, but not diet, shape the sperm methylome. Dev Cell. 2015 Dec 21;35(6):750–758. PubMed PMID: 26702833; PubMed Central PMCID: PMC4691283.
   PubMed Web of Science ®Google Scholar
• Dallosso AR, Hancock AL, Szemes M, et al. Frequent long-range epigenetic silencing of protocadherin gene clusters on chromosome 5q31 in Wilms’ tumor. PLoS Genet. 2009 Nov;5(11):e1000745. PubMed PMID: 19956686; PubMed Central PMCID: PMC2776977.
   PubMed Web of Science ®Google Scholar
• Guibert S, Weber M. Functions of DNA methylation and hydroxymethylation in mammalian development. Curr Top Dev Biol. 2013;104:47–83. PubMed PMID: 23587238.
   PubMed Web of Science ®Google Scholar
• Anilkumar TR, Devi AN, Pillai SM, et al. Expression of protocadherin 11Yb (PCDH11Yb) in seminal germ cells is correlated with fertility status in men. Reprod Fertil Dev. 2017 Oct;29(11):2100–2111. PubMed PMID: 28241900.
   PubMed Web of Science ®Google Scholar
• Koch S, Acebron SP, Herbst J, et al. Post-transcriptional Wnt signaling governs epididymal sperm maturation. Cell. 2015 Nov 19;163(5):1225–1236. PubMed PMID: 26590424.
   PubMed Web of Science ®Google Scholar
• Miller D, Brinkworth M, Iles D. Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction. 2010 Feb;139(2):287–301. PubMed PMID: 19759174.
   PubMed Web of Science ®Google Scholar
• Marchal R, Chicheportiche A, Dutrillaux B, et al. DNA methylation in mouse gametogenesis. Cytogenet Genome Res. 2004;105(2–4):316–324. PubMed PMID: 15237219.
   PubMed Web of Science ®Google Scholar
• McLay DW, Clarke HJ. Remodelling the paternal chromatin at fertilization in mammals. Reproduction. 2003 May;125(5):625–633. PubMed PMID: 12713425; PubMed Central PMCID: PMC5123868.
   PubMed Web of Science ®Google Scholar
• Katz TA, Liao SG, Palmieri VJ, et al. Targeted DNA methylation screen in the mouse mammary genome reveals a parity-induced hypermethylation of Igf1r that persists long after parturition. Cancer Prev Res. 2015 Oct;8(10):1000–1009. PubMed PMID: 26290394; PubMed Central PMCID: PMC4677681.
   PubMed Web of Science ®Google Scholar
• Welsh CE, Miller DR, Manly KF, et al. Status and access to the collaborative cross population. Mamm genome. 2012 Oct;23(9–10):706–712. PubMed PMID: 22847377; PubMed Central PMCID: PMC3463789.
   PubMed Web of Science ®Google Scholar
• Bartolomei MS, Webber AL, Brunkow ME, et al. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 1993 Sep;7(9):1663–1673. PubMed PMID: 7690336.
   PubMed Web of Science ®Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014 Aug 01;30(15):2114–2120. PubMed PMID: 24695404; PubMed Central PMCID: PMC4103590.
   PubMed Web of Science ®Google Scholar
• Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011 Jun 01;27(11):1571–1572. PubMed PMID: 21493656; PubMed Central PMCID: PMC3102221.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012 Mar 04;9(4):357–359. PubMed PMID: 22388286; PubMed Central PMCID: PMC3322381.
   PubMed Web of Science ®Google Scholar
• Akalin A, Kormaksson M, Li S, et al. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 2012 Oct 03;13(10):R87. PubMed PMID: 23034086; PubMed Central PMCID: PMC3491415.
   PubMed Web of Science ®Google Scholar
• R Core Team. R: A language and environment for statistical computing R foundation for statistical computing. Vienna, Austria; 2015. Available from: https://www.R-project.org/
   Google Scholar
• Wang HQ, Tuominen LK, Tsai CJ. SLIM: a sliding linear model for estimating the proportion of true null hypotheses in datasets with dependence structures. Bioinformatics. 2011 Jan 15;27(2):225–231. PubMed PMID: 21098430.
   PubMed Web of Science ®Google Scholar
• Sherry ST, Ward MH, Kholodov M, et al. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 2001 Jan 1;29(1):308–311. PubMed PMID: 11125122; PubMed Central PMCID: PMC29783.
   PubMed Web of Science ®Google Scholar
• Mi H, Huang X, Muruganujan A, et al. PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Res. 2017 Jan 4;45(D1):D183–D189. PubMed PMID: 27899595; PubMed Central PMCID: PMC5210595.
   PubMed Web of Science ®Google Scholar
• Mi H, Thomas P. PANTHER pathway: an ontology-based pathway database coupled with data analysis tools. Methods Mol Biol. 2009;563:123–140. PubMed PMID: 19597783.
   PubMedGoogle Scholar
• Mi H, Muruganujan A, Casagrande JT, et al. Large-scale gene function analysis with the PANTHER classification system. Nat Protoc. 2013 Aug;8(8):1551–1566. PubMed PMID: 23868073.
   PubMed Web of Science ®Google Scholar
• Dunn OJ. Multiple comparison among means. J Am Stat Assoc. 1961;56:52–64.
   Web of Science ®Google Scholar
• Hochberg Y, Ba Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol. 1995;57:289–300.
   Google Scholar