Acta Biotheoretica

, Volume 64, Issue 2, pp 121–132 | Cite as

Combinations of Histone Modifications for Pattern Genes

Regular Article
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Abstract

Histone post-translational modifications play important roles in transcriptional regulation. It is known that multiple histone modifications can act in a combinatorial manner. In this study, we investigated the effects of multiple histone modifications on expression levels of five gene categories (four kinds of pattern genes and non-pattern genes) in coding regions. The combinatorial patterns of modifications for the five gene categories were also studied in the regions. Our results indicated that the differences in the expression levels between any two gene categories were significant. There were some corresponding differences in multiple histone modification levels among the five gene categories. Multiple histone modifications jointly impacted expression levels of every gene category. Four mutual combinations of histone modifications were found and analyzed.

Keywords

Histone Histone code Acetylation Methylation Protein coding region 
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Notes

Acknowledgments

Thanks are due to Richard A. Rothery for grammatical correctness. This work was supported by the National Natural Science Foundation of China (Grant No. 31260274) and the Inner Mongolia Natural Science Foundation of China (Grant No. 2012MS0517).

Supplementary material

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References

  1. Bannister AJ, Kouzarides T (2005) Reversing histone methylation. Nature 436:1103–1106CrossRefGoogle Scholar
  2. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Holko M, Ayanbule O, Yefanov A, Soboleva A (2011) NCBI GEO: archive for functional genomics data sets—10 years on. Nucleic Acids Res 39:D1005–D1010CrossRefGoogle Scholar
  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. Cell 129:823–837CrossRefGoogle Scholar
  4. Butte AJ, Dzau VJ, Glueck SB (2001) Further defining housekeeping, or “maintenance,” genes focus on “a compendium of gene expression in normal human tissues”. Physiol Genomics 7:95–96Google Scholar
  5. Cheng C, Yan KK, Yip KY, Rozowsky J, Alexander R, Shou C, Gerstein M (2011) A statistical framework for modeling gene expression using chromatin features and application to modENCODE datasets. Genome Biol 12:R15CrossRefGoogle Scholar
  6. Eisenberg E, Levanon EY (2003) Human housekeeping genes are compact. Trends Genet 19:362–365CrossRefGoogle Scholar
  7. Fischer JJ, Toedling J, Krueger T, Schueler M, Huber W, Sperling S (2008) Combinatorial effects of four histone modifications in transcription and differentiation. Genomics 91:41–51CrossRefGoogle Scholar
  8. Fuchs SM, Laribee RN, Strahl BD (2009) Protein modifications in transcription elongation. Biochim Biophys Acta 1789:26–36CrossRefGoogle Scholar
  9. Fuchs SM, Krajewski K, Baker RW, Miller VL, Strahl BD (2011) Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr Biol 21:53–58CrossRefGoogle Scholar
  10. Greer S, Honeywell R, Geletu M, Arulanandam R, Raptis L (2010) Housekeeping genes; expression levels may change with density of cultured cells. J Immunol Methods 355:76–79CrossRefGoogle Scholar
  11. Guan X, Rastogi N, Parthun MR, Freitas MA (2013) Discovery of histone modification crosstalk networks by stable isotope labeling of amino acids in cell culture mass spectrometry (SILAC MS). Mol Cell Proteomics 12:2048–2059CrossRefGoogle Scholar
  12. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88CrossRefGoogle Scholar
  13. Hayter AJ (1986) The maximum familywise error rate of Fisher’s least significant difference test. J Am Stat Assoc 81:1000–1004CrossRefGoogle Scholar
  14. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B (2009) Histone modifications at human enhancers reflect global cell-typespecific gene expression. Nature 459:108–112CrossRefGoogle Scholar
  15. Jaschek R, Tanay A (2009) Spatial clustering of multivariate genomic and epigenomic information. In: Proceedings of the 13th annual international conference on research in computational molecular biology, SpringerGoogle Scholar
  16. Karlic R, Chung HR, Vlahovicek K, Vingron M (2010) Histone modification levels are predictive for gene expression. Proc Natl Acad Sci USA 107:2926–2931CrossRefGoogle Scholar
  17. Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–294CrossRefGoogle Scholar
  18. Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global Histone acetylation patterns to gene expression. Cell 117:721–733CrossRefGoogle Scholar
  19. Lee KK, Workman JL (2007) Histone acetyltransferase complexes: one size doesn’t fit all. Nat Rev Mol Cell Biol 8:284–295CrossRefGoogle Scholar
  20. Liang S, Li Y, Be X, Howes S, Liu W (2006) Detecting and profiling tissue-selective genes. Physiol Genomics 26:158–162CrossRefGoogle Scholar
  21. Liu X, Chen X, Yu X, Tao Y, Bode AM, Dong Z, Cao Y (2013) Regulation of microRNAs by epigenetics and their interplay involved in cancer. J Exp Clin Cancer Res 32:96CrossRefGoogle Scholar
  22. Lui JC, Chen W, Cheung CS, Baron J (2014) Broad shifts in gene expression during early postnatal life are associated with shifts in histone methylation patterns. PLoS one 28:e86957CrossRefGoogle Scholar
  23. Modena P, Lualdi E, Facchinetti F, Galli L, Teixeira MR, Pilotti S, Sozzi G (2005) SMARCB1/INI1 tumor suppressor gene is frequently inactivated in epithelioid sarcomas. Cancer Res 65:4012–4019CrossRefGoogle Scholar
  24. Ooga M, Inoue A, Kageyama S, Akiyama T, Nagata M, Aoki F (2008) Changes in H3K79 methylation during preimplantation development in mice. Biol Reprod 78:413–424CrossRefGoogle Scholar
  25. Pan JB, Hu SC, Wang H, Zou Q, Ji ZL (2012) PaGeFinder: quantitative identification of spatiotemporal pattern genes. Bioinformatics 28:1544–1545CrossRefGoogle Scholar
  26. Pan JB, Hu SC, Shi D, Cai MC, Li YB, Zou Q, Ji ZL (2013) PaGenBase: a pattern gene database for the global and dynamic understanding of gene function. PLoS one 8:e80747CrossRefGoogle Scholar
  27. Parkinson H, Sarkans U, Kolesnikov N, Abeygunawardena N, Burdett T, Dylag M, Emam I, Farne A, Hastings E, Holloway E, Kurbatova N, Lukk M, Malone J, Mani R, Pilicheva E, Rustici G, Sharma A, Williams E, Adamusiak T, Brandizi M, Sklyar N, Brazma A (2011) ArrayExpress update–an archive of microarray and high-throughput sequencing-based functional genomics experiments. Nucleic Acids Res 39:D1002–D1004CrossRefGoogle Scholar
  28. Schones DE, Zhao K (2008) Genome-wide approaches to studying chromatin modifications. Nat Rev Genet 9:179–191CrossRefGoogle Scholar
  29. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45CrossRefGoogle Scholar
  30. Teng S, Yang JY, Wang L (2013) Genome-wide prediction and analysis of human tissue-selective genes using microarray expression data. BMC Med Genomics 6:S10CrossRefGoogle Scholar
  31. Thorrez L, Laudadio I, Van Deun K, Quintens R, Hendrickx N, Granvik M, Lemaire K, Schraenen A, Van Lommel L, Lehnert S, Aguayo-Mazzucato C, Cheng-Xue R, Gilon P, Van Mechelen I, Bonner-Weir S, Lemaigre F, Schuit F (2011) Tissue-specific disallowance of housekeeping genes: the other face of cell differentiation. Genome Res 21:95–105CrossRefGoogle Scholar
  32. Ucar D, Hu Q, Tan K (2011) Combinatorial chromatin modification patterns in the human genome revealed by subspace clustering. Nucleic Acids Res 39:1–13CrossRefGoogle Scholar
  33. Wang ZB, Zang CZ, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40:897–903CrossRefGoogle Scholar
  34. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW 3rd, Su AI (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10:R130CrossRefGoogle Scholar
  35. Xiao SJ, Zhang C, Zou Q, Ji ZL (2010) TiSGeD: a database for tissue-specific genes. Bioinformatics 26:1273–1275CrossRefGoogle Scholar
  36. Yu H, Zhu S, Zhou B, Xue H, Han JD (2008) Inferring causal relationships among different histone modifications and gene expression. Genome Res 18:1314–1324CrossRefGoogle Scholar
  37. Zhang Y, Reinberg D (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 15:2343–2360CrossRefGoogle Scholar
  38. Zhang Y, Lv J, Liu H, Zhu J, Su J, Wu Q, Qi Y, Wang F, Li X (2010) HHMD: the human histone modification database. Nucleic Acids Res 38:D149–D154CrossRefGoogle Scholar
  39. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, Oliviero S (2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138:1122–1136CrossRefGoogle Scholar
  40. Zou Q, Li J, Hong Q, Lin Z, Wu Y, Shi H, Ju Y (2015) Prediction of microRNA-disease associations based on social network analysis methods. Biomed Res Int 2015:810514Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.School of Mathematics, Physics and Biological EngineeringInner Mongolia University of Science and TechnologyBaotouChina

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