The Journal of Nutritional Biochemistry
Volume 22, Issue 4 , Pages 328-333 , April 2011

Novel histone biotinylation marks are enriched in repeat regions and participate in repression of transcriptionally competent genes

Received 25 November 2009 ,Revised 14 February 2010 ,Accepted 23 February 2010.

References 

  1. Wolffe A. Chromatin. 3th ed.. San Diego (Calif): Academic Press; 1998;
  2. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 1997;389:251–260
  3. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705
  4. Cheung P, Tanner KG, Cheung WL, Sassone-Corsi P, Denu JM, Allis CD. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell. 2000;5:905–915
  5. Clayton AL, Mahadevan LC. MAP kinase-mediated phosphoacetylation of histone H3 and inducible gene regulation. FEBS Lett. 2003;546:51–58
  6. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol. 2003;13:1192–1200
  7. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 2005;24:800–812
  8. Stanley JS, Griffin JB, Zempleni J. Biotinylation of histones in human cells: effects of cell proliferation. Eur J Biochem. 2001;268:5424–5429
  9. Camporeale G, Shubert EE, Sarath G, Cerny R, Zempleni J. K8 and K12 are biotinylated in human histone H4. Eur J Biochem. 2004;271:2257–2263
  10. Kobza K, Camporeale G, Rueckert B, Kueh A, Griffin JB, Sarath G, et al. K4, K9, and K18 in human histone H3 are targets for biotinylation by biotinidase. FEBS J. 2005;272:4249–4259
  11. Chew YC, Camporeale G, Kothapalli N, Sarath G, Zempleni J. Lysine residues in N- and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. J Nutr Biochem. 2006;17:225–233
  12. Kobza K, Sarath G, Zempleni J. Prokaryotic BirA ligase biotinylates K4, K9, K18 and K23 in histone H3. BMB Rep. 2008;41:310–315
  13. Camporeale G, Giordano E, Rendina R, Zempleni J, Eissenberg JC. Drosophila holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan and heat tolerance. J Nutr. 2006;136:2735–2742
  14. Camporeale G, Zempleni J, Eissenberg JC. Susceptibility to heat stress and aberrant gene expression patterns in holocarboxylase synthetase-deficient Drosophila melanogaster are caused by decreased biotinylation of histones, not of carboxylases. J Nutr. 2007;137:885–889
  15. Chew YC, Raza AS, Sarath G, Zempleni J. Biotinylation of K8 and K12 co-occurs with acetylation and mono-methylation in human histone H4. FASEB J. 2006;20:A610;[abstract]
  16. Camporeale G, Oommen AM, Griffin JB, Sarath G, Zempleni J. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J Nutr Biochem. 2007;18:760–768
  17. Wijeratne SS, Camporeale G, Zempleni J. K12-biotinylated histone H4 is enriched in telomeric repeats from human lung IMR-90 fibroblasts. J Nutr Biochem. 2010;21:310–316
  18. Chew YC, West JT, Kratzer SJ, Ilvarsonn AM, Eissenberg JC, Dave BJ, et al. Biotinylation of histones represses transposable elements in human and mouse cells and cell lines, and in Drosophila melanogaster. J Nutr. 2008;138:2316–2322
  19. Gralla M, Camporeale G, Zempleni J. Holocarboxylase synthetase regulates expression of biotin transporters by chromatin remodeling events at the SMVT locus. J Nutr Biochem. 2008;19:400–408
  20. Manthey KC, Griffin JB, Zempleni J. Biotin supply affects expression of biotin transporters, biotinylation of carboxylases, and metabolism of interleukin-2 in Jurkat cells. J Nutr. 2002;132:887–892
  21. Mascher B, Sclenke P, Seyfarth M. Expression and kinetics of cytokines determined by intracellular staining using flow cytometry. J Immunol Methods. 1999;223:115–121
  22. Camporeale G, Zempleni J. Biotin. In:  Bowman BA,  Russell RM editor. Present Knowledge in Nutrition. vol. 1:Washington, DC: International Life Sciences Institute; 2006;p. 314–326
  23. Healy S, Perez-Cadahia B, Jia D, McDonald MK, Davie JR, Gravel RA. Biotin is not a natural histone modification. Biochim Biophys Acta. 2009;1789:719–733
  24. Kouzarides T, Berger SL. Chromatin modifications and their mechanism of action. In:  Allis CD,  Jenuwein T,  Reinberg D editor. Epigenetics. Cold Spring Harbor (NY): Cold Spring Harbor Press; 2007;p. 191–209
  25. Dahl JA, Collas P. A rapid micro chromatin immunoprecipitation assay (microChIP). Nat Protoc. 2008;3:1032–1045
  26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 2001;25:402–408
  27. Blanchard R, Gu X, Burnette A, Huang J, Zeng X. Genome-wide, promoter-tilling, real-time PCR assays for analyzing chromatin immunoprecipitation samples. http://www.sabiosciences.com/support_posters.php2007;[accessed 11/23/2009]
  28. Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M. Chromatin immunoprecipitation: optimization, quantitative analysis and data normalization. Plant Methods. 2007;3:11
  29. SAS Institute . StatView Reference. 3rd ed.. Cary (NC): SAS Publishing; 1999;
  30. Hassan YI, Zempleni J. A novel, enigmatic histone modification: biotinylation of histones by holocarboxylase synthetase. Nutr Rev. 2008;66:721–725
  31. Mock DM, Lankford GL, Mock NI. Biotin accounts for only half of the total avidin-binding substances in human serum. J Nutr. 1995;125:941–946
  32. Zempleni J, Helm RM, Mock DM. In vivo biotin supplementation at a pharmacologic dose decreases proliferation rates of human peripheral blood mononuclear cells and cytokine release. J Nutr. 2001;131:1479–1484
  33. Bailey LM, Ivanov RA, Wallace JC, Polyak SW. Artifactual detection of biotin on histones by streptavidin. Anal Biochem. 2008;373:71–77
  34. Li E, Bird A. DNA methylation in mammals. In:  Allis CD,  Jenuwein T,  Reinberg D editor. Epigenetics. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2007;p. 341–356
  35. Cheung WL, Ajiro K, Samejima K, Kloc M, Cheung P, Mizzen CA, et al. Apoptotic phosphorylation of histone H2B is mediated by mammalian sterile twenty kinase. Cell. 2003;113:507–517

 A contribution of the University of Nebraska Agricultural Research Division, supported in part by funds provided through the Hatch Act. Additional support was provided by NIH grants DK063945, DK077816, DK082476 and ES015206; USDA CSREES grant 2006-35200-17138; and NSF grant EPS 0701892.

PII: S0955-2863(10)00069-0

doi: 10.1016/j.jnutbio.2010.02.011

The Journal of Nutritional Biochemistry
Volume 22, Issue 4 , Pages 328-333 , April 2011