A novel, enigmatic histone modification: biotinylation of histones by holocarboxylase synthetase.

Holocarboxylase synthetase catalyzes the covalent binding of biotin to histones in humans and other eukaryotes. Eleven biotinylation sites have been identified in histones H2A, H3, and H4. K12-biotinylated histone H4 is enriched in heterochromatin, repeat regions, and plays a role in gene repression. About 30% of the histone H4 molecules are biotinylated at K12 in histone H4 in human fibroblast telomeres. The abundance of biotinylated histones at distinct genomic loci depends on biotin availability. Decreased histone biotinylation decreases life span and stress resistance in Drosophila. Low enrichment of biotinylated histones at transposable elements impairs repression of these elements.

[1]  Janos Zempleni,et al.  Biotinylation of histones represses transposable elements in human and mouse cells and cell lines and in Drosophila melanogaster. , 2008, The Journal of nutrition.

[2]  J. Zempleni,et al.  Epigenetic regulation of chromatin structure and gene function by biotin: are biotin requirements being met? , 2008, Nutrition reviews.

[3]  J. Zempleni,et al.  Holocarboxylase synthetase regulates expression of biotin transporters by chromatin remodeling events at the SMVT locus. , 2008, The Journal of nutritional biochemistry.

[4]  J. Zempleni,et al.  Prokaryotic BirA ligase biotinylates K4, K9, K18 and K23 in histone H3. , 2008, BMB reports.

[5]  Toshiaki Watanabe,et al.  Biotin deficiency affects the proliferation of human embryonic palatal mesenchymal cells in culture. , 2008, The Journal of nutrition.

[6]  J. Wallace,et al.  Artifactual detection of biotin on histones by streptavidin. , 2008, Analytical biochemistry.

[7]  J. Zempleni,et al.  Prokaryotic BirA ligase biotinylates K 4 , K 9 , K 18 and K 23 in histone H 3 † , 2008 .

[8]  J. Zempleni,et al.  Feeding Drosophila a biotin-deficient diet for multiple generations increases stress resistance and lifespan and alters gene expression and histone biotinylation patterns. , 2007, The Journal of nutrition.

[9]  J. Zempleni,et al.  An avidin-based assay for histone debiotinylase activity in human cell nuclei. , 2007, The Journal of nutritional biochemistry.

[10]  J. Zempleni,et al.  Vitamin-Dependent Modifications of Chromatin: Epigenetic Events and Genomic Stability , 2007 .

[11]  J. Zempleni,et al.  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. , 2007, The Journal of nutrition.

[12]  B. Ames,et al.  Biotin deficiency inhibits heme synthesis and impairs mitochondria in human lung fibroblasts. , 2007, The Journal of nutrition.

[13]  J. Zempleni,et al.  Drosophila melanogaster holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan, and heat tolerance. , 2006, The Journal of nutrition.

[14]  E. Barnard,et al.  Increased susceptibility to ATP via alteration of P2X receptor function in dystrophic mdx mouse muscle cells , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[15]  Janos Zempleni,et al.  Lysine residues in N-terminal and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. , 2006, The Journal of nutritional biochemistry.

[16]  J. Zempleni,et al.  Biotinylation of K8 and K12 co‐occurs with acetylation and mono‐methylation in human histone H4 , 2006 .

[17]  Y. Matsubara,et al.  Mutations in the holocarboxylase synthetase gene HLCS , 2005, Human mutation.

[18]  Janos Zempleni,et al.  K4, K9 and K18 in human histone H3 are targets for biotinylation by biotinidase , 2005, The FEBS journal.

[19]  J. Zempleni,et al.  Roles for nutrients in epigenetic events. , 2005, The Journal of nutritional biochemistry.

[20]  J. Zempleni,et al.  Biotin deficiency decreases life span and fertility but increases stress resistance in Drosophila melanogaster. , 2004, The Journal of nutritional biochemistry.

[21]  Janos Zempleni,et al.  K8 and K12 are biotinylated in human histone H4. , 2004, European journal of biochemistry.

[22]  J. Zempleni,et al.  Biotin supply affects rates of cell proliferation, biotinylation of carboxylases and histones, and expression of the gene encoding the sodium-dependent multivitamin transporter in JAr choriocarcinoma cells , 2004, European journal of nutrition.

[23]  M. Narang,et al.  Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. , 2003, Human molecular genetics.

[24]  P. Olive Detection of DNA damage in individual cells by analysis of histone H2AX phosphorylation. , 2004, Methods in cell biology.

[25]  J. Zempleni,et al.  Expression of oncogenes depends on biotin in human small cell lung cancer cells NCI-H69. , 2003, International journal for vitamin and nutrition research. Internationale Zeitschrift fur Vitamin- und Ernahrungsforschung. Journal international de vitaminologie et de nutrition.

[26]  Jonathan Chernoff,et al.  Apoptotic Phosphorylation of Histone H2B Is Mediated by Mammalian Sterile Twenty Kinase , 2003, Cell.

[27]  C. Allis,et al.  Histone and chromatin cross-talk. , 2003, Current opinion in cell biology.

[28]  T. Richmond,et al.  Chromatin fiber folding: requirement for the histone H4 N-terminal tail. , 2003, Journal of molecular biology.

[29]  J. Zempleni,et al.  Biotin supply affects expression of biotin transporters, biotinylation of carboxylases and metabolism of interleukin-2 in Jurkat cells. , 2002, The Journal of nutrition.

[30]  J. Zempleni,et al.  Biotinidase catalyzes debiotinylation of histones , 2002, European journal of nutrition.

[31]  J. Zempleni,et al.  Biotinylation of histones in human cells , 2001 .

[32]  K. Kawasaki,et al.  Structure of human holocarboxylase synthetase gene and mutation spectrum of holocarboxylase synthetase deficiency , 2001, Human Genetics.

[33]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[34]  S. Méndez,et al.  Biotin regulates the genetic expression of holocarboxylase synthetase and mitochondrial carboxylases in rats. , 2001, The Journal of nutrition.

[35]  J. Zempleni,et al.  Biotinylation of histones in human cells. Effects of cell proliferation. , 2001, European journal of biochemistry.

[36]  T. Suormala,et al.  Relationship between Kinetic Properties of Mutant Enzyme and Biochemical and Clinical Responsiveness to Biotin in Holocarboxylase Synthetase Deficiency , 1999, Pediatric Research.

[37]  B. Wolf,et al.  Human biotinidase isn't just for recycling biotin. , 1999, The Journal of nutrition.

[38]  T. Suormala,et al.  Inherited defects of biotin metabolism , 1999, BioFactors.

[39]  M. Hiratsuka,et al.  Identification of holocarboxylase synthetase (HCS) proteins in human placenta. , 1998, Biochimica et biophysica acta.

[40]  G. Herman,et al.  Clustering of mutations in the biotin-binding region of holocarboxylase synthetase in biotin-responsive multiple carboxylase deficiency. , 1996, Human molecular genetics.

[41]  B. Wolf,et al.  Biotinylation of histones by human serum biotinidase: assessment of biotinyl-transferase activity in sera from normal individuals and children with biotinidase deficiency. , 1995, Biochemical and molecular medicine.

[42]  D. Leclerc,et al.  Isolation of a cDNA encoding human holocarboxylase synthetase by functional complementation of a biotin auxotroph of Escherichia coli. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[43]  N. Niikawa,et al.  Isolation and characterization of mutations in the human holocarboxylase synthetase cDNA , 1994, Nature Genetics.

[44]  Y. Suzuki,et al.  Purification and properties of bovine liver holocarboxylase synthetase. , 1994, Archives of biochemistry and biophysics.

[45]  B. Wolf,et al.  Biotinidase Deficiency a , 1985, Advances in pediatrics.

[46]  T. Boulikas,et al.  Increase in histone poly (ADP-ribosylation) in mitogen-activated lymphoid cells. , 1990, Experimental cell research.

[47]  J. Cronan The E. coli bio operon: Transcriptional repression by an essential protein modification enzyme , 1989, Cell.

[48]  T. Boulikas At least 60 ADP‐ribosylated variant histones are present in nuclei from dimethylsulfate‐treated and untreated cells. , 1988, The EMBO journal.

[49]  D. Balnave Clinical symptoms of biotin deficiency in animals. , 1977, The American journal of clinical nutrition.