Ribosomal DNA Copy Number Variation is Coupled with DNA Methylation Changes at the 45S rDNA Locus

References

• Henderson AS, Warburton D, Atwood KC. Location of ribosomal DNA in the human chromosome complement. Proc Natl Acad Sci U S A. 1972;69(11):3394–13. doi: 10.1073/pnas.69.11.3394
   PubMed Web of Science ®Google Scholar
• Henderson AS, Warburton D, Atwood KC. Letter: ribosomal DNA connectives between human acrocentric chromosomes. Nature. 1973;245:95–97.
   PubMed Web of Science ®Google Scholar
• Rabl J, Leibundgut M, Ataide SF, et al. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science. 2011;331(6018):730–736. doi: 10.1126/science.1198308
   PubMed Web of Science ®Google Scholar
• Doudna JA, Rath VL. Structure and function of the eukaryotic ribosome: the next frontier. Cell. 2002;109(2):153–156. doi: 10.1016/S0092-8674(02)00725-0
   PubMed Web of Science ®Google Scholar
• Tahmasebi S, Khoutorsky A, Mathews MB, et al. Translation deregulation in human disease. Nat Rev Mol Cell Biol. 2018;19(12):791–807. doi: 10.1038/s41580-018-0034-x
   PubMed Web of Science ®Google Scholar
• Saba JA, Liakath-Ali K, Green R, et al. Translational control of stem cell function. Nat Rev Mol Cell Biol. 2021;22(10):671–690. doi: 10.1038/s41580-021-00386-2
   PubMed Web of Science ®Google Scholar
• Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood. 2010;115(16):3196–3205. doi: 10.1182/blood-2009-10-178129
   PubMed Web of Science ®Google Scholar
• Kobayashi T. Ribosomal RNA gene repeats, their stability and cellular senescence. Proc Jpn Acad Ser B Phys Biol Sci. 2014;90:119–129. doi: 10.2183/pjab.90.119
   PubMed Web of Science ®Google Scholar
• Stochaj U, Weber SC. Nucleolar organization and functions in health and disease. Cells. 2020;9(3):526. doi: 10.3390/cells9030526
   PubMed Web of Science ®Google Scholar
• Potabattula R, Zacchini F, Ptak GE, et al. Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline. Aging Cell. 2020;19(8):e13181. doi: 10.1111/acel.13181
   PubMed Web of Science ®Google Scholar
• Salameh Y, Bejaoui Y, El Hajj N. DNA methylation biomarkers in aging and age-related diseases. Front Genet. 2020;11:171. doi: 10.3389/fgene.2020.00171
   PubMed Web of Science ®Google Scholar
• Wang M, Lemos B. Ribosomal DNA harbors an evolutionarily conserved clock of biological aging. Genome Res. 2019;29(3):325–333. doi: 10.1101/gr.241745.118
   PubMed Web of Science ®Google Scholar
• Antonarakis SE. Short arms of human acrocentric chromosomes and the completion of the human genome sequence. Genome Res. 2022;32(4):599–607. doi: 10.1101/gr.275350.121
   PubMed Web of Science ®Google Scholar
• Nurk S, Koren S, Rhie A, et al. The complete sequence of a human genome. Science. 2022;376(6588):44–53. doi: 10.1126/science.abj6987
   PubMed Web of Science ®Google Scholar
• Lewis JD, Tollervey D. Like attracts like: getting RNA processing together in the nucleus. Science. 2000;288(5470):1385–1389. doi: 10.1126/science.288.5470.1385
   PubMed Web of Science ®Google Scholar
• Warner JR. The economics of ribosome biosynthesis in yeast. Trends Biochem Sci. 1999;24(11):437–440. doi: 10.1016/S0968-0004(99)01460-7
   PubMed Web of Science ®Google Scholar
• Pederson T. The plurifunctional nucleolus. Nucleic Acids Res. 1998;26(17):3871–3876. doi: 10.1093/nar/26.17.3871
   PubMed Web of Science ®Google Scholar
• Gonzalez IL, Sylvester JE. Complete sequence of the 43-kb human ribosomal DNA repeat: analysis of the intergenic spacer. Genomics. 1995;27(2):320–328. doi: 10.1006/geno.1995.1049
   PubMed Web of Science ®Google Scholar
• Moss T, Langlois F, Gagnon-Kugler T, et al. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol Life Sci. 2007;64(1):29–49. doi: 10.1007/s00018-006-6278-1
   PubMed Web of Science ®Google Scholar
• Hillis DM, Dixon MT. Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol. 1991;66(4):411–453. doi: 10.1086/417338
   PubMed Web of Science ®Google Scholar
• Learned RM, Learned TK, Haltiner MM, et al. Human rRNA transcription is modulated by the coordinate binding of two factors to an upstream control element. Cell. 1986;45(6):847–857. doi: 10.1016/0092-8674(86)90559-3
   PubMed Web of Science ®Google Scholar
• Gibbons JG, Branco AT, Yu S, et al. Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat Commun. 2014;5(1):4850. doi: 10.1038/ncomms5850
   PubMedGoogle Scholar
• Santoro R, Grummt I. Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell. 2001;8(3):719–725. doi: 10.1016/S1097-2765(01)00317-3
   PubMed Web of Science ®Google Scholar
• Porokhovnik L. Individual copy number of ribosomal genes as a factor of mental retardation and autism risk and severity. Cells. 2019;8(10):1151. doi: 10.3390/cells8101151
   PubMed Web of Science ®Google Scholar
• Hall AN, Turner TN, Queitsch C. Thousands of high-quality sequencing samples fail to show meaningful correlation between 5S and 45S ribosomal DNA arrays in humans. Sci Rep. 2021;11(1):449. doi: 10.1038/s41598-020-80049-y
   PubMed Web of Science ®Google Scholar
• Chestkov IV, Jestkova EM, Ershova ES, et al. Abundance of ribosomal RNA gene copies in the genomes of schizophrenia patients. Schizophr Res. 2018;197:305–314. doi: 10.1016/j.schres.2018.01.001
   PubMed Web of Science ®Google Scholar
• Veiko NN, Egolina NA, Radzivil GG, et al. Quantitative analysis of repetitive sequences in human genomic DNA and detection of an elevated ribosomal repeat copy number in patients with schizophrenia (the results of molecular and cytogenetic analysis). Mol Biol (Mosk). 2003;37:409–419. NA.
   PubMed Web of Science ®Google Scholar
• Ershova ES, Malinovskaya EM, Golimbet VE, et al. Copy number variations of satellite III (1q12) and ribosomal repeats in health and schizophrenia. Schizophr Res. 2020;223:199–212. doi: 10.1016/j.schres.2020.07.022
   PubMed Web of Science ®Google Scholar
• Haertle L, Muller T, Lardenoije R, et al. Methylomic profiling in trisomy 21 identifies cognition- and Alzheimer’s disease-related dysregulation. Clin Epigenetics. 2019;11(1):195. doi: 10.1186/s13148-019-0787-x
   PubMed Web of Science ®Google Scholar
• Schneider E, Dittrich M, Bock J, et al. CpG sites with continuously increasing or decreasing methylation from early to late human fetal brain development. Gene. 2016;592(1):110–118. doi: 10.1016/j.gene.2016.07.058
   PubMed Web of Science ®Google Scholar
• Schneider E, El Hajj N, Richter S, et al. Widespread differences in cortex DNA methylation of the “language gene” CNTNAP2 between humans and chimpanzees. Epigenetics. 2014;9(4):533–545. doi: 10.4161/epi.27689
   PubMed Web of Science ®Google Scholar
• Vogel Ciernia A, LaSalle J. The landscape of DNA methylation amid a perfect storm of autism aetiologies. Nat Rev Neurosci. 2016;17(7):411–423. doi: 10.1038/nrn.2016.41
   PubMed Web of Science ®Google Scholar
• Morton EA, Hall AN, Kwan E, et al. Challenges and approaches to genotyping repetitive dna. g3 (bethesda. G3: Genes | Genomes | Genetics. 2020;10(1):417–430. doi: 10.1534/g3.119.400771
   Web of Science ®Google Scholar
• Stults DM, Killen MW, Pierce HH, et al. Genomic architecture and inheritance of human ribosomal RNA gene clusters. Genome Res. 2008;18(1):13–18. doi: 10.1101/gr.6858507
   PubMed Web of Science ®Google Scholar
• Hori Y, Shimamoto A, Kobayashi T. The human ribosomal DNA array is composed of highly homogenized tandem clusters. Genome Res. 2021;31(11):1971–1982. doi: 10.1101/gr.275838.121
   PubMed Web of Science ®Google Scholar
• Rhoads A, Au KF. PacBio sequencing and its applications. Genom Proteom Bioinformat. 2015;13(5):278–289. doi: 10.1016/j.gpb.2015.08.002
   PubMed Web of Science ®Google Scholar
• Yoshimura J, Ichikawa K, Shoura MJ, et al. Recompleting the Caenorhabditis elegans genome. Genome Res. 2019;29(6):1009–1022. doi: 10.1101/gr.244830.118
   PubMed Web of Science ®Google Scholar
• Gibbons JG, Branco AT, Godinho SA, et al. Concerted copy number variation balances ribosomal DNA dosage in human and mouse genomes. Proc Natl Acad Sci U S A. 2015;112(8):2485–2490. doi: 10.1073/pnas.1416878112
   PubMed Web of Science ®Google Scholar
• Wang M, Lemos B, Eng C. Ribosomal DNA copy number amplification and loss in human cancers is linked to tumor genetic context, nucleolus activity, and proliferation. PLoS Genet. 2017;13(9):e1006994. doi: 10.1371/journal.pgen.1006994
   PubMed Web of Science ®Google Scholar
• Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27(11):1571–1572. doi: 10.1093/bioinformatics/btr167
   PubMed Web of Science ®Google Scholar
• Jeong H, Mendizabal I, Berto S, et al. Evolution of DNA methylation in the human brain. Nat Commun. 2021;12(1):2021. doi: 10.1038/s41467-021-21917-7
   PubMed Web of Science ®Google Scholar
• Mendizabal I, Berto S, Usui N, et al. Cell type-specific epigenetic links to schizophrenia risk in the brain. Genome Biol. 2019;20(1):135. doi: 10.1186/s13059-019-1747-7
   PubMedGoogle Scholar
• Dunaway KW, Islam MS, Coulson RL, et al. Cumulative impact of polychlorinated biphenyl and large chromosomal duplications on DNA methylation, chromatin, and expression of autism candidate genes. Cell Rep. 2016;17(11):3035–3048. doi: 10.1016/j.celrep.2016.11.058
   PubMed Web of Science ®Google Scholar
• Vogel Ciernia A, Laufer BI, Hwang H, et al. Epigenomic convergence of neural-immune risk factors in neurodevelopmental disorder cortex. Cereb Cortex. 2020;30(2):640–655. doi: 10.1093/cercor/bhz115
   PubMed Web of Science ®Google Scholar
• Korthauer K, Chakraborty S, Benjamini Y, et al. Detection and accurate false discovery rate control of differentially methylated regions from whole genome bisulfite sequencing. Biostatistics. 2019;20(3):367–383. doi: 10.1093/biostatistics/kxy007
   PubMed Web of Science ®Google Scholar
• Schultz MD, He Y, Whitaker JW, et al. Human body epigenome maps reveal noncanonical DNA methylation variation. Nature. 2015;523(7559):212–216. doi: 10.1038/nature14465
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–359. doi: 10.1038/nmeth.1923
   PubMed Web of Science ®Google Scholar
• Aird D, Ross MG, Chen WS, et al. Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries. Genome Biol. 2011;12(2):R18. doi: 10.1186/gb-2011-12-2-r18
   PubMed Web of Science ®Google Scholar
• James SA, O’Kelly MJ, Carter DM, et al. Repetitive sequence variation and dynamics in the ribosomal DNA array of Saccharomyces cerevisiae as revealed by whole-genome resequencing. Genome Res. 2009;19(4):626–635. doi: 10.1101/gr.084517.108
   PubMed Web of Science ®Google Scholar
• Lyckegaard EM, Clark AG. Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1989;86(6):1944–1948. doi: 10.1073/pnas.86.6.1944
   PubMed Web of Science ®Google Scholar
• Lu KL, Nelson JO, Watase GJ, et al. Transgenerational dynamics of rDNA copy number in Drosophila male germline stem cells. Elife. 2018;7. doi: 10.7554/eLife.32421
   Web of Science ®Google Scholar
• Johnson LK, Johnson RW, Strehler BL. Cardiac hypertrophy, aging and changes in cardiac ribosomal RNA gene dosage in man. J Mol Cell Cardiol. 1975;7(2):125–133. doi: 10.1016/0022-2828(75)90014-0
   PubMed Web of Science ®Google Scholar
• Strehler BL, Chang MP, Johnson LK. Loss of hybridizable ribosomal DNA from human post-mitotic tissues during aging: i. Age-dependent loss in human myocardium. Mech Ageing Dev. 1979;11(5–6):371–378. doi: 10.1016/0047-6374(79)90012-5
   PubMed Web of Science ®Google Scholar
• Zafiropoulos A, Tsentelierou E, Linardakis M, et al. Preferential loss of 5S and 28S rDNA genes in human adipose tissue during ageing. Int J Biochem Cell Biol. 2005;37(2):409–415. doi: 10.1016/j.biocel.2004.07.007
   PubMed Web of Science ®Google Scholar
• Hallgren J, Pietrzak M, Rempala G, et al. Neurodegeneration-associated instability of ribosomal DNA. Biochim Biophys Acta. 2014;1842(6):860–868. doi: 10.1016/j.bbadis.2013.12.012
   PubMed Web of Science ®Google Scholar
• Watada E, Li S, Hori Y, et al. Age-dependent ribosomal DNA variations in mice. Mol Cell Biol. 2020;40(22):40. doi: 10.1128/MCB.00368-20
   Web of Science ®Google Scholar
• Peterson CR, Cryar JR, Gaubatz JW. Constancy of ribosomal RNA genes during aging of mouse heart cells and during serial passage of WI-38 cells. Arch Gerontol Geriatr. 1984;3(2):115–125. doi: 10.1016/0167-4943(84)90004-9
   PubMed Web of Science ®Google Scholar
• Kampen KR, Sulima SO, Vereecke S, et al. Hallmarks of ribosomopathies. Nucleic Acids Res. 2020;48(3):1013–1028. doi: 10.1093/nar/gkz637
   PubMed Web of Science ®Google Scholar
• Rodriguez-Algarra F, Seaborne RAE, Danson AF, et al. Genetic variation at mouse and human ribosomal DNA influences associated epigenetic states. Genome Biol. 2022;23(1):54. doi: 10.1186/s13059-022-02617-x
   PubMed Web of Science ®Google Scholar
• Lopez FB, Fort A, Tadini L, et al. Gene dosage compensation of rRNA transcript levels in Arabidopsis thaliana lines with reduced ribosomal gene copy number. Plant Cell. 2021;33(4):1135–1150. doi: 10.1093/plcell/koab020
   PubMed Web of Science ®Google Scholar