A Minimal Set of Tissue-Specific Hypomethylated CpGs Constitute Epigenetic Signatures of Developmental Programming

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Colaneri, Alejandro ^a,c   Wang, Tianyuan ^a   Pagadala, Vijayakanth ^a   Kittur, Jaya ^a   Staffa Jr , Nickolas G ^a   Peddada, Shyamal D ^a   Isganaitis, Elvira ^b   Patti, Mary Elizabeth ^b   Birnbaumer, Lutz ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL FUNCTION; CIS REGULATORY SEQUENCE; CONTROLLED STUDY; CPG ISLAND; DEVELOPMENT; DEVELOPMENTAL PROGRAMMING; DIET RESTRICTION; DNA METHYLATION; EPIGENETICS; EXON; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC DISTANCE; GENETIC IDENTIFICATION; GERM CELL; KIDNEY PARENCHYMA; LIVER; MALE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PROMOTER REGION; REGULATORY SEQUENCE; STRESS; TESTIS; TISSUE SPECIFIC DIFFERENTIALLY METHYLATED SITE; ZFP GENE;

ANIMALS; CPG ISLANDS; DNA METHYLATION; EPIGENOMICS; MALE; MICE; MICE, INBRED C57BL; TESTIS;

EID: 84884183305     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072670     Document Type: Article

References (57)

1. Cantone I, Fisher AG, (2013) Epigenetic programming and reprogramming during development. Nat Struct Mol Biol 20: 282-289 doi:10.1038/nsmb.2489.
2. Bergman Y, Cedar H, (2013) DNA methylation dynamics in health and disease. Nat Struct Mol Biol 20: 274-281 doi:10.1038/nsmb.2518.
3. Ji H, Ehrlich LIR, Seita J, Murakami P, Doi A, et al. (2010) Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467: 338-342 doi:10.1038/nature09367.
4. Jirtle RL, Skinner MK, (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8: 253-262 doi:10.1038/nrg2045.
5. Cortessis VK, Thomas DC, Levine AJ, Breton CV, Mack TM, et al. (2012) Environmental epigenetics: prospects for studying epigenetic mediation of exposure-response relationships. Hum Genet 131: 1565-1589 doi:10.1007/s00439-012-1189-8.
6. Harris RA, Nagy-Szakal D, Kellermayer R, (2013) Human metastable epiallele candidates link to common disorders. Epigenetics 8: 157-163 doi:10.4161/epi.23438.
7. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmühl Y, et al. (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12: 0 doi:10.1038/nn.2436.
8. Gluckman PD, (2011) Epigenetics and metabolism in 2011: Epigenetics, the life-course and metabolic disease. Nat Rev Endocrinol 8: 74-76 doi:10.1038/nrendo.2011.226.
9. Blackledge NP, Klose RJ, (2011) CpG island chromatin: A platform for gene regulation. Epigenetics 6.
10. Bird AP, (1986) CpG-rich islands and the function of DNA methylation. Nature 321: 209-213 doi:10.1038/321209a0.
11. Illingworth RS, Gruenewald-Schneider U, Webb S, Kerr ARW, James KD, et al. (2010) Orphan CpG Islands Identify Numerous Conserved Promoters in the Mammalian Genome. PLoS Genet 6: e1001134 doi:10.1371/journal.pgen.1001134.
12. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, et al. (2010) Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466: 253-257 doi:10.1038/nature09165.
13. Illingworth R, Kerr A, Desousa D, Jørgensen H, Ellis P, et al. (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6: e22 doi:10.1371/journal.pbio.0060022.
14. Deaton AM, Webb S, Kerr ARW, Illingworth RS, Guy J, et al. (2011) Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Research 21: 1074-1086 doi:10.1101/gr.118703.110.
15. Colaneri A, Staffa N, Fargo DC, Gao Y, Wang T, et al. (2011) Expanded methyl-sensitive cut counting reveals hypomethylation as an epigenetic state that highlights functional sequences of the genome. Proc Natl Acad Sci USA 108: 9715-9720 doi:10.1073/pnas.1105713108.
16. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. nature pp. 6 doi:10.1038/nature10716.
17. Song F, Mahmood S, Ghosh S, Liang P, Smiraglia DJ, et al. (2009) Tissue specific differentially methylated regions (TDMR): Changes in DNA methylation during development. Genomics 93: 130-139 doi:10.1016/j.ygeno.2008.09.003.
18. Liang P, Song F, Ghosh S, Morien E, Qin M, et al. (2011) Genome-wide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. BMC Genomics 12: 231 doi:10.1186/1471-2164-12-231.
19. Heyn H, Esteller M, (2012) DNA methylation profiling in the clinic: applications and challenges. Nat Rev Genet 13: 679-692 doi:10.1038/nrg3270.
20. Campión J, Milagro FI, Martínez JA, (2009) Individuality and epigenetics in obesity. Obes Rev 10: 383-392 doi:10.1111/j.1467-789X.2009.00595.x.
21. Kim MS, Lee J, Sidransky D, (2010) DNA methylation markers in colorectal cancer. Cancer Metastasis Rev 29: 181-206 doi:10.1007/s10555-010-9207-6.
22. Jimenez-Chillaron JC, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, et al. (2008) Intergenerational Transmission of Glucose Intolerance and Obesity by In Utero Undernutrition in Mice. Diabetes 58: 460-468 doi:10.2337/db08-0490.
23. Jimenez-Chillaron JC, Hernandez-Valencia M, Lightner A, Faucette RR, Reamer C, et al. (2006) Reductions in caloric intake and early postnatal growth prevent glucose intolerance and obesity associated with low birthweight. Diabetologia 49: 1974-1984 doi:10.1007/s00125-006-0311-7.
24. Eaves HL, Gao Y, (2009) MOM: maximum oligonucleotide mapping. Bioinformatics 25: 969-970 doi:10.1093/bioinformatics/btp092.
25. Guo W, Sarkar SK, Peddada SD, (2009) Controlling False Discoveries in Multidimensional Directional Decisions, with Applications to Gene Expression Data on Ordered Categories. Biometrics 66: 485-492 doi:10.1111/j.1541-0420.2009.01292.x.
26. Takai D, Jones PA, (2002) Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci USA 99: 3740-3745 doi:10.1073/pnas.052410099.
27. Gardiner-Garden M, Frommer M, (1987) CpG islands in vertebrate genomes. Journal of Molecular Biology 196: 261-282.
28. Bock C, Walter J, Paulsen M, Lengauer T, (2007) CpG island mapping by epigenome prediction. PLoS Comput Biol 3: e110 doi:10.1371/journal.pcbi.0030110.
29. Hackenberg M, Previti C, Luque-Escamilla PL, Carpena P, Martínez-Aroza J, et al. (2006) CpGcluster: a distance-based algorithm for CpG-island detection. BMC Bioinformatics 7: 446 doi:10.1186/1471-2105-7-446.
30. Wu H, Caffo B, Jaffee HA, Irizarry RA, Feinberg AP, (2010) Redefining CpG islands using hidden Markov models. Biostatistics (Oxford, England) doi:10.1093/biostatistics/kxq005.
31. McCall MN, Uppal K, Jaffee HA, Zilliox MJ, Irizarry RA, (2010) The Gene Expression Barcode: leveraging public data repositories to begin cataloging the human and murine transcriptomes. Nucleic Acids Res 39: D1011-D1015 doi:10.1093/nar/gkq1259.
32. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, et al. (2012) A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120 doi:10.1038/nature11243.
33. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z, (2009) GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48 doi:10.1186/1471-2105-10-48.
34. de Hoon MJL, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454 doi:10.1093/bioinformatics/bth078.
35. Saldanha AJ, (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248 doi:10.1093/bioinformatics/bth349.
36. Suzuki M, Jing Q, Lia D, Pascual M, McLellan A, et al. (2010) Optimized design and data analysis of tag-based cytosine methylation assays. Genome Biol 11: R36 doi:10.1186/gb-2010-11-4-r36.
37. Ball MP, Li JB, Gao Y, Lee J-H, LeProust EM, et al. (2009) Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. Nat Biotechnol 27: 361-368 doi:10.1038/nbt.1533.
38. Colaneri AC, Jones AM, (2013) Genome-wide quantitative identification of DNA differentially methylated sites in Arabidopsis seedlings growing at different water potential. PLoS ONE 8: e59878 doi:10.1371/journal.pone.0059878.
39. Straussman R, Nejman D, Roberts D, Steinfeld I, Blum B, et al. (2009) Developmental programming of CpG island methylation profiles in the human genome. Nat Struct Mol Biol 16: 564-571 doi:10.1038/nsmb.1594.
40. Deaton AM, Bird A, (2011) CpG islands and the regulation of transcription. Genes Dev 25: 1010-1022 doi:10.1101/gad.2037511.
41. Doi A, Park I-H, Wen B, Murakami P, Aryee MJ, et al. (2009) Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 41: 1350-1353 doi:10.1038/ng.471.
42. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, et al. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41: 178-186 doi:10.1038/ng.298.
43. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29 doi:10.1038/75556.
44. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57 doi:10.1038/nprot.2008.211.
45. Huang DW, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13 doi:10.1093/nar/gkn923.
46. Shen L, Kondo Y, Guo Y, Zhang J, Zhang L, et al. (2007) Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet 3: 2023-2036 doi:10.1371/journal.pgen.0030181.
47. Suzuki M, Sato S, Arai Y, Shinohara T, Tanaka S, et al. (2007) A new class of tissue-specifically methylated regions involving entire CpG islands in the mouse. Genes to Cells 12: 1305-1314 doi:10.1111/j.1365-2443.2007.01136.x.
48. Sakamoto H, Suzuki M, Abe T, Hosoyama T, Himeno E, et al. (2007) Cell type-specific methylation profiles occurring disproportionately in CpG-less regions that delineate developmental similarity. Genes Cells 12: 1123-1132 doi:10.1111/j.1365-2443.2007.01120.x.
49. Huang R-L, Chang C-C, Su P-H, Chen Y-C, Liao Y-P, et al. (2012) Methylomic analysis identifies frequent DNA methylation of zinc finger protein 582 (ZNF582) in cervical neoplasms. PLoS ONE 7: e41060 doi:10.1371/journal.pone.0041060.
50. O'Geen H, Squazzo SL, Iyengar S, Blahnik K, Rinn JL, et al. (2007) Genome-Wide Analysis of KAP1 Binding Suggests Autoregulation of KRAB-ZNFs. PLoS Genet 3: e89 doi:10.1371/journal.pgen.0030089.st004.
51. Bell O, Wirbelauer C, Hild M, Scharf AND, Schwaiger M, et al. (2007) Localized H3K36 methylation states define histone H4K16 acetylation during transcriptional elongation in Drosophila. EMBO J 26: 4974-4984 doi:10.1038/sj.emboj.7601926.
52. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, et al. (2009) Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41: 376-381 doi:10.1038/ng.322.
53. Schwartz S, Meshorer E, Ast G, (2009) Chromatin organization marks exon-intron structure. Nat Struct Mol Biol 16: 990-995 doi:10.1038/nsmb.1659.
54. Hahn MA, Wu X, Li AX, Hahn T, Pfeifer GP, (2011) Relationship between Gene Body DNA Methylation and Intragenic H3K9me3 and H3K36me3 Chromatin Marks. PLoS ONE 6: e18844 doi:10.1371/journal.pone.0018844.s006.
55. Quach JM, Walker EC, Allan E, Solano M, Yokoyama A, et al. (2011) Zinc Finger Protein 467 Is a Novel Regulator of Osteoblast and Adipocyte Commitment. Journal of Biological Chemistry 286: 4186-4198 doi:10.1074/jbc.M110.178251.
56. Wiench M, John S, Baek S, Johnson TA, Sung M-H, et al. (2011) DNA methylation status predicts cell type-specific enhancer activity. EMBO J 30: 3028-3039 doi:10.1038/emboj.2011.210.
57. Feinberg AP, (2010) Epigenomics reveals a functional genome anatomy and a new approach to common disease. Nat Biotechnol 28: 1049-1052 doi:10.1038/nbt1010-1049.