Chromatin measurements reveal contributions of synthesis and decay to steady-state mRNA levels

Molecular Systems Biology

Volumn 8, Issue , 2012, Pages

  Tippmann, Sylvia C ^a,b,c   Ivanek, Robert ^a   Gaidatzis, Dimos ^a,c   Schöler, Anne ^a,b,c   Hoerner, Leslie ^a   Van Nimwegen, Erik ^d   Stadler, Peter F ^e,f,g,h,i,j   Stadler, Michael B ^a,c   Schübeler, Dirk ^a,b  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

^e UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF LEIPZIG   (Germany)

^g MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

^h FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

ⁱ UNIVERSITY OF COPENHAGEN   (Denmark)

^j SANTA FE INSTITUTE   (United States)

more..

Author keywords

chromatin; histone modifications; microRNA; RNA decay; transcriptional regulation

Indexed keywords

HISTONE H3; MESSENGER RNA; MICRORNA; GLUTAMIC ACID;

ARTICLE; CHROMATIN; EXPERIMENTAL MOUSE; GENE EXPRESSION; HALF LIFE TIME; HISTONE MODIFICATION; HOUSEKEEPING GENE; HUMAN; MEASUREMENT; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA DECAY; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSCRIPTION; STEADY STATE; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; METHODOLOGY; MOUSE; NERVE CELL; PHYSIOLOGY; PLURIPOTENT STEM CELL; RNA PROCESSING; RNA STABILITY; SEQUENCE ANALYSIS;

EUKARYOTA;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GLUTAMIC ACID; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICE; MICRORNAS; MODELS, BIOLOGICAL; NEURONS; PLURIPOTENT STEM CELLS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC;

EID: 84864216831     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2012.23     Document Type: Article

References (74)

1. Ambros V (2004) The functions of animal microRNAs. Nature 431: 350-355 (Pubitemid 39265675)
2. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R (2008) Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes Dev 22: 2773-2785
3. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837 (Pubitemid 46802390)
4. Beitzinger M, Peters L, Zhu JY, Kremmer E, Meister G (2007) Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol 4: 76-84
5. Bell O, Schwaiger M, Oakeley EJ, Lienert F, Beisel C, Stadler MB, Schubeler D (2010) Accessibility of the Drosophila genome discriminates PcG repression, H4K16 acetylation and replication timing. Nat StructMol Biol 17: 894-900
6. Bell O, Wirbelauer C, Hild M, Scharf AN, Schwaiger M, MacAlpine DM, Zilbermann F, van Leeuwen F, Bell SP, Imhof A, Garza D, Peters AH, Schübeler D (2007) Localized H3K36 methylation states define histone H4K16 acetylation during transcriptional elongation in Drosophila. EMBOJ26: 4974-4984 (Pubitemid 350261289)
7. Bibel M, Richter J, Lacroix E, Barde Y-A (2007) Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2: 1034-1043 (Pubitemid 46901284)
8. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21 (Pubitemid 34049633)
9. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353 (Pubitemid 44050199)
10. Buratowski S, Kim T (2010) The role of cotranscriptional histone methylations. Cold Spring Harb Symp Quan Biol 75: 95-102
11. Cheng C, Gerstein M (2011) Modeling the relative relationship of transcription factor binding and histone modifications to gene expression levels in mouse embryonic stem cells. Nucleic Acids Res 40: 553-568
12. Chi SW, Zang JB, Mele A, Darnell RB (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486
13. Deal RB, Henikoff JG, Henikoff S (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science (New York, NY) 328: 1161-1164
14. Di Giammartino DC, Nishida K, Manley JL (2011) Mechanisms and consequences of alternative polyadenylation. Mol Cell 43: 853-866
15. Dölken L, Ruzsics Z, Rädle B, Friedel CC, Zimmer R, Mages J, Hoffmann R, Dickinson P, Forster T, Ghazal P, Koszinowski UH (2008) High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay RNA (New York, NY) 14: 1959-1972
16. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, Burton J, Cox TV, Davies R, Down TA, Haefliger C, Horton R, Howe K, Jackson DK, Kunde J, Koenig C, Liddle J, Niblett D, Otto T, Pettett R et al (2006) DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38: 1378-1385 (Pubitemid 44837559)
17. Edmunds JW, Mahadevan LC, Clayton AL (2008) Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27: 406-420 (Pubitemid 351161656)
18. Eisenberg E, Levanon EY (2003) Human housekeeping genes are compact. Trends Genet 19: 362-365 (Pubitemid 36794535)
19. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5: R1
20. Gaidatzis D, van Nimwegen E, Hausser J, Zavolan M (2007) Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 8: 69
21. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88 (Pubitemid 47031323)
22. Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840
23. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano Jr M, Jungkamp AC, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141
24. Hon G, Wang W, Ren B (2009) Discovery and annotation of functional chromatin signatures in the human genome. PLoS Comput Biol 5: e1000566
25. Hutvágner G, McLachlan J, Pasquinelli AE, Bálint E, Tuschl T, Zamore PD (2001) A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science (New York, NY) 293: 834-838
26. Joshi AA, Struhl K (2005) Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol Cell 20: 971-978 (Pubitemid 41814885)
27. Karlic R, Chung H-R, Lasserre J, Vlahovicek K, Vingron M (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci USA 107: 2926-2931
28. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ (2005) Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605 (Pubitemid 41608463)
29. Kizer KO, Phatnani HP, Shibata Y Hall H, Greenleaf AL, Strahl BD (2005) A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol 25: 3305-3316 (Pubitemid 40464330)
30. Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98: 285-294 (Pubitemid 29380564)
31. Kouzarides T (2007) Chromatin modifications and their function. Cell 128: 693-705 (Pubitemid 46273577)
32. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N (2005) Combinatorial microRNA target predictions. Nat Genet 37: 495-500 (Pubitemid 40617277)
33. Krogan NJ, Kim M, Tong A, Golshani A, Cagney G, Canadien V, Richards DP, Beattie BK, Emili A, Boone C, Shilatifard A, Buratowski S, Greenblatt J (2003) Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol Cell Biol 23: 4207-4218 (Pubitemid 36666424)
34. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, Dinic L Ojo T, Hafner M, Zavolan M, Tuschl T (2008) Molecular characterization of human Argonaute-containing ribonucleo-protein complexes and their bound target mRNAs. RNA (New York, NY) 14: 2580-2596
35. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. GenomeBiol 10: R25
36. Lewis BP, Shih I-H, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115: 787-798 (Pubitemid 38058492)
37. Li B, Howe L, Anderson S, Yates JR, Workman JL (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. JBiol Chem 278: 8897-8903 (Pubitemid 36800365)
38. Li J, Moazed D, Gygi SP (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J Biol Chem 277: 49383-49388 (Pubitemid 36014370)
39. Lienert F, Mohn F, Tiwari VK, Baubec T, Roloff TC, Gaidatzis D, Stadler MB, Schübeler D (2011) Genomic prevalence of heterochromatic H3K9me2 and transcription do not discriminate pluripotent from terminally differentiated cells. PLoS Genet 7: e1002090
40. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C et al (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560 (Pubitemid 47206934)
41. Millevoi S, Vagner S (2010) Molecular mechanisms of eukaryotic pre-mRNA 3' end processing regulation. Nucleic Acids Res 38: 2757-2774
42. Min IM, Waterfallzzz JJ, Core LJ, Munroe RJ, Schimenti J, Lis JT (2011) Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev 25: 742-754
43. Mohn F, Schübeler D (2009) Genetics and epigenetics: stability and plasticity during cellular differentiation. Trends Genet 25: 129-136
44. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, Stadler MB, Bibel M, Schübeler D (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol Cell 30: 755-766
45. Mukherji S, Ebert MS, Zheng GXY, Tsang JS, Sharp PA, van Oudenaarden A (2011) MicroRNAs can generate thresholds in target gene expression. Nat Genet 43: 854-859
46. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci USA 102: 12135-12140 (Pubitemid 41291141)
47. Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463
48. Ouyang Z, Zhou Q, Wong WH (2009) ChIP-Seq of transcription factors predicts absolute and differential gene expression in embryonic stem cells. Proc Natl Acad Sci USA 106: 21521-21526
49. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, Bell GW, Walker K, Rolfe PA, Herbolsheimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527 (Pubitemid 41191151)
50. Rabani M, Levin JZ, Fan L, Adiconis X, Raychowdhury R, Garber M, Gnirke A, Nusbaum C, Hacohen N, Friedman N, Amit I, Regev A (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 29: 436-442
51. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA (2010) c-Myc regulates transcriptional pause release. Cell 141: 432-445
52. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517 (Pubitemid 39288185)
53. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473: 337-342
54. Segal E, Widom J (2009) From DNA sequence to transcriptional behaviour: a quantitative approach. NatRev Genet 10: 443-456
55. Sharova LV, Sharov AA, Nedorezov T, Piao Y Shaik N, Ko MSH (2009) Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res 16: 45-58
56. She X, Rohl CA, Castle JC, Kulkarni AV, Johnson JM, Chen R (2009) Definition, conservation and epigenetics of housekeeping and tissue-enriched genes. BMC Genomics 10: 269
57. Sinkkonen L, Hugenschmidt T, Berninger P, Gaidatzis D, Mohn F, Artus-Revel CG, Zavolan M, Sinkkonen L, Hugenschmidt T, Berninger P, Gaidatzis D, Mohn F, Artus-Revel CG, Zavolan M, Svoboda P, Filipowicz W (2008) MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat StructMol Biol 15: 259-267 (Pubitemid 351654045)
58. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM (2005) Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 123: 1133-1146 (Pubitemid 41785426)
59. Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, Allis CD (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 22: 1298-1306 (Pubitemid 34150767)
60. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang JSoden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101: 6062-6067 (Pubitemid 38520528)
61. Sun XJ (2005) Identification and characterization of a novel human histone H3 lysine 36-specific methyltransferase. J Biol Chem 280: 35261-35271
62. Team RDC (2011)) . R: A Language and Environment for Statistical Computing. Retrieved from http://www.R-project.org
63. Tiwari VK, Stadler MB, Wirbelauer C, Paro R, Schubeler D, Beisel C (2012) A chromatin-modifying function of JNK during stem cell differentiation. Nat Genet 44: 94-100
64. Vakoc CR, Sachdeva MM, Wang H, Blobel GA (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol CellBiol 26: 9185-9195 (Pubitemid 44904415)
65. van Dongen S, Abreu-Goodger C, Enright A (2008) Detecting microRNA binding and siRNA off-target effects from expression data. Nat Methods 5: 1023-1025
66. Vinogradov AE (2004) Compactness of human housekeeping genes: selection for economy or genomic design?. Trends Genet 20: 248-253 (Pubitemid 38510438)
67. Wagner EJ, Carpenter PB (2012) Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13: 115-126
68. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, Schübeler D (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39: 457-466 (Pubitemid 46514772)
69. Wirbelauer C, Bell O, Schubeler D (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev 19: 1761-1766 (Pubitemid 41126914)
70. Wyrick JJ, Holstege FC, Jennings EG, Causton HC, Shore D, Grunstein M, Lander ES, Young RA (1999) Chromosomal landscape of nucleosome-dependent gene expression and silencing in yeast. Nature 402: 418-421 (Pubitemid 129544830)
71. Xiao T, Hall H, Kizer KO, Shibata Y, Hall MC, Borchers CH, Strahl BD (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev 17: 654-663 (Pubitemid 36307549)
72. Young MD, Willson TA, Wakefield MJ, Trounson E, Hilton DJ, Blewitt ME, Oshlack A, Majewski IJ (2011) ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res 39: 7415-7427
73. Yuan W,XieJ, Long C, Erdjument-Bromage H, Ding X, Zheng Y Tempst P, Chen S, Zhu B, Reinberg D (2009) Heterogeneous nuclear ribonucleoprotein L Is a subunit of human KMT3a/Set2 complex required for H3 Lys-36 trimethylation activity in vivo. J Biol Chem 284: 15701-15707
74. Zhu J, He F, Song S, Wang J, Yu J (2008) How many human genes can be defined as housekeeping with current expression data?. BMC Genomics9: 172