Epigenetic silencing of nucleolar rRNA genes in Alzheimer's disease

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Pietrzak, Maciej ^a   Rempala, Grzegorz ^b   Nelson, Peter T ^c   Zheng, Jing Juan ^a   Hetman, Michal ^a  

^a University of Louisville School of Medicine   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; RIBOSOME DNA; RIBOSOME RNA;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN TISSUE; CHROMATIN; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; GENE LOSS; GENE MAPPING; GENE SILENCING; GENETIC STABILITY; HUMAN; HUMAN TISSUE; MALE; MILD COGNITIVE IMPAIRMENT; PARIETAL CORTEX; PROMOTER REGION; SENESCENCE; GENETIC EPIGENESIS; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOLUS; NUCLEOTIDE SEQUENCE;

AGED, 80 AND OVER; ALZHEIMER DISEASE; BASE SEQUENCE; CELL NUCLEOLUS; CPG ISLANDS; CYTOSINE; DNA METHYLATION; DNA, RIBOSOMAL; EPIGENESIS, GENETIC; FEMALE; GENE SILENCING; HUMANS; MALE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; RNA, RIBOSOMAL;

EID: 79960688688     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022585     Document Type: Article

References (38)

1. Szyf M, (2009) Epigenetics, DNA methylation, and chromatin modifying drugs. Annu Rev Pharmacol Toxicol 49: 243-263.
2. Suzuki MM, Bird A, (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9: 465-476.
3. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, et al. (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
4. Chouliaras L, Rutten BP, Kenis G, Peerbooms O, Visser PJ, et al. (2010) Epigenetic regulation in the pathophysiology of Alzheimer's disease. Prog Neurobiol 90: 498-510.
5. Siegmund KD, Connor CM, Campan M, Long TI, Weisenberger DJ, et al. (2007) DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2: e895.
6. Wang SC, Oelze B, Schumacher A, (2008) Age-specific epigenetic drift in late-onset Alzheimer's disease. PLoS One 3: e2698.
7. McStay B, Grummt I, (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol 24: 131-157.
8. McGowan PO, Sasaki A, Huang TC, Unterberger A, Suderman M, et al. (2008) Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS ONE 3: e2085.
9. Santoro R, Lienemann P, Fussenegger M, (2009) Epigenetic engineering of ribosomal RNA genes enhances protein production. PLoS One 4: e6653.
10. Guetg C, Lienemann P, Sirri V, Grummt I, Hernandez-Verdun D, et al. (2010) The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. Embo J 29: 2135-2146.
11. Honda K, Smith MA, Zhu X, Baus D, Merrick WC, et al. (2005) Ribosomal RNA in Alzheimer disease is oxidized by bound redox-active iron. J Biol Chem 280: 20978-20986.
12. Ding Q, Markesbery WR, Chen Q, Li F, Keller JN, (2005) Ribosome dysfunction is an early event in Alzheimer's disease. J Neurosci 25: 9171-9175.
13. Ding Q, Markesbery WR, Cecarini V, Keller JN, (2006) Decreased RNA, and Increased RNA Oxidation, in Ribosomes from Early Alzheimer's Disease. Neurochem Res 31: 705-710.
14. Nelson PT, Keller JN, (2007) RNA in brain disease: no longer just "the messenger in the middle". J Neuropathol Exp Neurol 66: 461-468.
15. Iacono D, O'Brien R, Resnick SM, Zonderman AB, Pletnikova O, et al. (2008) Neuronal hypertrophy in asymptomatic Alzheimer disease. J Neuropathol Exp Neurol 67: 578-589.
16. Iacono D, Markesbery WR, Gross M, Pletnikova O, Rudow G, et al. (2009) The Nun study: clinically silent AD, neuronal hypertrophy, and linguistic skills in early life. Neurology 73: 665-673.
17. Kalita K, Makonchuk D, Gomes C, Zheng JJ, Hetman M, (2008) Inhibition of nucleolar transcription as a trigger for neuronal apoptosis. J Neurochem 105: 2286-2299.
18. Parlato R, Kreiner G, Erdmann G, Rieker C, Stotz S, et al. (2008) Activation of an endogenous suicide response after perturbation of rRNA synthesis leads to neurodegeneration in mice. J Neurosci 28: 12759-12764.
19. Rieker C, Engblom D, Kreiner G, Domanskyi A, Schober A, et al. (2011) Nucleolar Disruption in Dopaminergic Neurons Leads to Oxidative Damage and Parkinsonism through Repression of Mammalian Target of Rapamycin Signaling. J Neurosci 31: 453-460.
20. Kastner P, Mosgoeller W, Fang-Kircher S, Kitzmueller E, Kirchner L, et al. (2003) Deficient brain RNA polymerase and altered nucleolar structure persists until day 8 after perinatal asphyxia of the rat. Pediatr Res 53: 62-71.
21. Zafiropoulos A, Tsentelierou E, Linardakis M, Kafatos A, Spandidos DA, (2005) Preferential loss of 5S and 28S rDNA genes in human adipose tissue during ageing. Int J Biochem Cell Biol 37: 409-415.
22. Paredes S, Maggert KA, (2009) Expression of I-CreI endonuclease generates deletions within the rDNA of Drosophila. Genetics 181: 1661-1671.
23. Chan PP, Lowe TM, (2009) GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37: D93-97.
24. Speranca MA, Batista LM, Lourenco Rda S, Tavares WM, Bertolucci PH, et al. (2008) Can the rDNA methylation pattern be used as a marker for Alzheimer's disease? Alzheimers Dement 4: 438-442.
25. Kennedy BK, Gotta M, Sinclair DA, Mills K, McNabb DS, et al. (1997) Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S. cerevisiae. Cell 89: 381-391.
26. Gaubatz J, Prashad N, Cutler RG, (1976) Ribosomal RNA gene dosage as a function of tissue and age for mouse and human. Biochim Biophys Acta 418: 358-375.
27. Strehler BL, Chang MP, (1979) Loss of hybridizable ribosomal DNA from human post-mitotic tissues during aging: II. Age-dependent loss in human cerebral cortex-hippocampal and somatosensory cortex comparison. Mech Ageing Dev 11: 379-382.
28. Machwe A, Orren DK, Bohr VA, (2000) Accelerated methylation of ribosomal RNA genes during the cellular senescence of Werner syndrome fibroblasts. Faseb J 14: 1715-1724.
29. Swisshelm K, Disteche CM, Thorvaldsen J, Nelson A, Salk D, (1990) Age-related increase in methylation of ribosomal genes and inactivation of chromosome-specific rRNA gene clusters in mouse. Mutat Res 237: 131-146.
30. Oakes CC, Smiraglia DJ, Plass C, Trasler JM, Robaire B, (2003) Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats. Proc Natl Acad Sci U S A 100: 1775-1780.
31. Morgan AR, Hamilton G, Turic D, Jehu L, Harold D, et al. (2008) Association analysis of 528 intra-genic SNPs in a region of chromosome 10 linked to late onset Alzheimer's disease. Am J Med Genet B Neuropsychiatr Genet 147B: 727-731.
32. Guo JU, Su Y, Zhong C, Ming GL, Song H, (2011) Hydroxylation of 5-Methylcytosine by TET1 Promotes Active DNA Demethylation in the Adult Brain. Cell 145: 423-434.
33. Nelson PT, Jicha GA, Schmitt FA, Liu H, Davis DG, et al. (2007) Clinicopathologic correlations in a large Alzheimer disease center autopsy cohort: neuritic plaques and neurofibrillary tangles "do count" when staging disease severity. J Neuropathol Exp Neurol 66: 1136-1146.
34. Abdul HM, Sama MA, Furman JL, Mathis DM, Beckett TL, et al. (2009) Cognitive decline in Alzheimer's disease is associated with selective changes in calcineurin/NFAT signaling. J Neurosci 29: 12957-12969.
35. Singer-Sam J, Grant M, LeBon JM, Okuyama K, Chapman V, et al. (1990) Use of a HpaII-polymerase chain reaction assay to study DNA methylation in the Pgk-1 CpG island of mouse embryos at the time of X-chromosome inactivation. Mol Cell Biol 10: 4987-4989.
36. Kalita K, Makonchuk D, Gomes C, Zheng JJ, Hetman M, (2008) Inhibition of nucleolar transcription as a trigger for neuronal apoptosis. J Neurochem 105: 2286-2299.
37. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
38. Mokarram P, Kumar K, Brim H, Naghibalhossaini F, Saberi-firoozi M, et al. (2009) Distinct high-profile methylated genes in colorectal cancer. PLoS One 4: e7012.