Biotin is not a natural histone modification

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1789, Issue 11-12, 2009, Pages 719-733

  Healy, Shannon ^a   Perez Cadahia, Beatriz ^b   Jia, Dongxin ^a   McDonald, Megan K ^a   Davie, James R ^b   Gravel, Roy A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Biotin; Histones; Immunoblot; Mass spectrometry; Post translational modification

Indexed keywords

ANTIBODY; AVIDIN; BIOTIN; HISTONE; NEUTRAVIDIN; SEPHAROSE; TRITIUM;

AMINO ACID SEQUENCE; ARTICLE; BIOTINYLATION; CHEMISTRY; CULTURE MEDIUM; GENE EXPRESSION REGULATION; GENETICS; HELA CELL; HUMAN; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN PROCESSING; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANTIBODIES; AVIDIN; BIOTIN; BIOTINYLATION; BLOTTING, WESTERN; CULTURE MEDIA; GENE EXPRESSION REGULATION; HELA CELLS; HISTONES; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN MODIFICATION, TRANSLATIONAL; SEPHAROSE; TRITIUM;

EID: 84859622095     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2009.09.003     Document Type: Article

References (74)

1. Wolf B. Disorders of biotin metabolism. The metabolic and molecular bases of inherited disease 2001, 2:3935-3962. McGraw-Hill, New York. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle, B. Childs, K.W. Kinsler, B. Vogelstein (Eds.).
2. Chapman-Smith A., Cronan J.E. The enzymatic biotinylation of proteins: a post-translational modification of exceptional specificity. Trends Biochem. Sci. 1999, 24:359.
3. Leon-Del-Rio A., Leclerc D., Akerman B., Wakamatsu N., Gravel R.A. Isolation of a cDNA encoding human holocarboxylase synthetase by functional complementation of a biotin auxotroph of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:4626.
4. Suzuki Y., Aoki Y., Ishida Y., Chiba Y., Iwamatsu A., Kishino T., Niikawa N., Matsubara Y., Narisawa K. Isolation and characterization of mutations in the human holocarboxylase synthetase cDNA. Nat. Genet. 1994, 8:122.
5. Wolf B., Grier R.E., Allen R.J., Goodman S.I., Kien C.L. Biotinidase deficiency: the enzymatic defect in late-onset multiple carboxylase deficiency. Clin. Chim. Acta 1983, 131:273.
6. Velazquez A. Biotin deficiency in protein-energy malnutrition: implications for nutritional homeostasis and individuality. Nutrition 1997, 13:991.
7. Mock D.M. Marginal biotin deficiency is common in normal human pregnancy and is highly teratogenic in mice. J. Nutr. 2009, 139:154.
8. Solorzano-Vargas R.S., Pacheco-Alvarez D., Leon-Del-Rio A. Holocarboxylase synthetase is an obligate participant in biotin-mediated regulation of its own expression and of biotin-dependent carboxylases mRNA levels in human cells. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:5325.
9. Pacheco-Alvarez D., Solorzano-Vargas R.S., Gonzalez-Noriega A., Michalak C., Zempleni J., Leon-Del-Rio A. Biotin availability regulates expression of the sodium-dependent multivitamin transporter and the rate of biotin uptake in HepG2 cells. Mol. Genet. Metab. 2005, 85:301.
10. Pacheco-Alvarez D., Solorzano-Vargas R.S., Gravel R.A., Cervantes-Roldan R., Velazquez A., Leon-Del-Rio A. Paradoxical regulation of biotin utilization in brain and liver and implications for inherited multiple carboxylase deficiency. J. Biol. Chem. 2004, 279:52312.
11. Velazquez-Arellano A., Hernandez-Esquivel M.L., Sanchez R.M., Ortega-Cuellar D., Rodriguez-Fuentes N., Cano S., Leon-Del-Rio A., Carvajal K. Functional and metabolic implications of biotin deficiency for the rat heart. Mol. Genet. Metab. 2008, 95:213.
12. Dakshinamurti K., Mistry S.P. Tissue and intracellular distribution of biotin-C-1400H in rats and chicks. J. Biol. Chem. 1963, 238:294.
13. Nakatani Y., Masudo K., Nozawa A., Inayama Y., Yamanaka S., Ito T., Kitamura H., Notohara K., Kashima K., Yokoyama S., Tsujimoto M., Tamai S., Abe Y., Resl M., Mark E.J. Biotin-rich, optically clear nuclei express estrogen receptor-beta: tumors with morules may develop under the influence of estrogen and aberrant beta-catenin expression. Hum. Pathol. 2004, 35:869.
14. Kimura Y., Kashima K., Daa T., Kondo Y., Yada K., Sasaki A., Matsumoto T., Kitano S., Kubo N., Yokoyama S. Biotin-rich intranuclear inclusions in morule-lacking adenocarcinoma of the gallbladder: a new category of "neoplastic/non-morular" lesions. Virchows Arch. 2005, 446:194.
15. Zempleni J. Uptake, localization, and noncarboxylase roles of biotin. Annu. Rev. Nutr. 2005, 25:175.
16. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389:251.
17. Davie J.R. Covalent modifications of histones: expression from chromatin templates. Curr. Opin. Genet. Dev. 1998, 8:173.
18. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074.
19. Mersfelder E.L., Parthun M.R. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res. 2006, 34:2653.
20. Stanley J.S., Griffin J.B., Zempleni J. Biotinylation of histones in human cells. Effects of cell proliferation, Eur. J. Biochem. 2001, 268:5424.
21. LaRochelle W.J. Detection of proteins on blots using avidin- or streptavidin-biotin. The protein protocols handbook, Springer 1996, 323-327. J.M. Walker (Ed.).
22. Brower M.S., Brakel C.L., Garry K. Immunodetection with streptavidin-acid phosphatase complex on Western blots. Anal. Biochem. 1985, 147:382.
23. Camporeale G., Chew Y.C., Kueh A., Sarath G., Zempleni J. Use of synthetic peptides for identifying biotinylation sites in human histones. Methods Mol. Biol. 2008, 418:139.
24. Kobza K., Camporeale G., Rueckert B., Kueh A., Griffin J.B., Sarath G., Zempleni J. K4, K9 and K18 in human histone H3 are targets for biotinylation by biotinidase. FEBS J. 2005, 272:4249.
25. Chew Y.C., Camporeale G., Kothapalli N., Sarath G., Zempleni J. Lysine residues in N-terminal and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. J. Nutr. Biochem. 2006, 17:225.
26. Camporeale G., Shubert E.E., Sarath G., Cerny R., Zempleni J. K8 and K12 are biotinylated in human histone H4. Eur. J. Biochem. 2004, 271:2257.
27. Kothapalli N., Sarath G., Zempleni J. Biotinylation of K12 in histone H4 decreases in response to DNA double-strand breaks in human JAr choriocarcinoma cells. J. Nutr. 2005, 135:2337.
28. Camporeale G., Oommen A.M., Griffin J.B., Sarath G., Zempleni J. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J. Nutr. Biochem. 2007, 18:760.
29. Hymes J., Fleischhauer K., Wolf B. Biotinylation of histones by human serum biotinidase: assessment of biotinyl-transferase activity in sera from normal individuals and children with biotinidase deficiency. Biochem. Mol. Med. 1995, 56:76.
30. Kobza K., Sarath G., Zempleni J. Prokaryotic BirA ligase biotinylates K4, K9, K18 and K23 in histone H3. BMB. Rep. 2008, 41:310.
31. Narang M.A., Dumas R., Ayer L.M., Gravel R.A. Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum. Mol. Genet. 2004, 13:15.
32. Hymes J., Fleischhauer K., Wolf B. Biotinylation of biotinidase following incubation with biocytin. Clin. Chim. Acta 1995, 233:39.
33. Healy S., Heightman T.D., Hohmann L., Schriemer D., Gravel R.A. Nonenzymatic biotinylation of histone H2A. Protein Sci. 2009, 18:314.
34. Hymes J., Wolf B. Biotinidase and its roles in biotin metabolism. Clin. Chim. Acta 1996, 255:1.
35. Stanley C.M., Hymes J., Wolf B. Identification of alternatively spliced human biotinidase mRNAs and putative localization of endogenous biotinidase. Mol. Genet. Metab. 2004, 81:300.
36. Camporeale G., Giordano E., Rendina R., Zempleni J., Eissenberg J.C. Drosophila melanogaster holocarboxylase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan, and heat tolerance. J. Nutr. 2006, 136:2735.
37. Bailey L.M., Ivanov R.A., Wallace J.C., Polyak S.W. Artifactual detection of biotin on histones by streptavidin. Anal. Biochem. 2008, 373:71.
38. Smith E.M., Hoi J.T., Eissenberg J.C., Shoemaker J.D., Neckameyer W.S., Ilvarsonn A.M., Harshman L.G., Schlegel V.L., Zempleni J. Feeding Drosophila a biotin-deficient diet for multiple generations increases stress resistance and lifespan and alters gene expression and histone biotinylation patterns. J. Nutr. 2007, 137:2006.
39. Manthey K.C., Griffin J.B., 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.
40. Scheerger S.B., Zempleni J. Expression of oncogenes depends on biotin in human small cell lung cancer cells NCI-H69. Int. J. Vitam. Nutr. Res. 2003, 73:461.
41. Crisp S.E., Griffin J.B., White B.R., Toombs C.F., Camporeale G., Said H.M., Zempleni J. 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. Eur. J. Nutr. 2004, 43:23.
42. Chew Y.C., Sarath G., Zempleni J. An avidin-based assay for histone debiotinylase activity in human cell nuclei. J. Nutr. Biochem. 2007, 18:475.
43. Ballard T.D., Wolff J., Griffin J.B., Stanley J.S., van C.S., Zempleni J. Biotinidase catalyzes debiotinylation of histones. Eur. J. Nutr. 2002, 41:78.
44. Duhamel R.C., Whitehead J.S. Prevention of nonspecific binding of avidin. Methods Enzymol. 1990, 184:201.
45. Diamandis E.P., Christopoulos T.K. The biotin-(strept)avidin system: principles and applications in biotechnology. Clin. Chem. 1991, 37:625.
46. Villar-Garea A., Israel L., Imhof A. Analysis of histone modifications by mass spectrometry. Curr. Protoc. Protein Sci. 2008, Chapter 14. Unit.
47. Suormala T., Fowler B., Duran M., Burtscher A., Fuchshuber A., Tratzmuller R., Lenze M.J., Raab K., Baur B., Wick H., Baumgartner R. Five patients with a biotin-responsive defect in holocarboxylase formation: evaluation of responsiveness to biotin therapy in vivo and comparative biochemical studies in vitro. Pediatr. Res. 1997, 41:666.
48. Chadee D.N., Peltier C.P., Davie J.R. Histone H1(S)-3 phosphorylation in Ha-ras oncogene-transformed mouse fibroblasts. Oncogene 2002, 21:8397.
49. Sun J.M., Chen H.Y., Espino P.S., Davie J.R. Phosphorylated serine 28 of histone H3 is associated with destabilized nucleosomes in transcribed chromatin. Nucleic Acids Res. 2007, 35:6640.
50. Fischle W. In nucleo enzymatic assays for the identification and characterization of histone modifying activities. Methods 2005, 36:362.
51. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87:953.
52. Robinson B.H., Oei J., Saunders M., Gravel R. [3H]biotin-labeled proteins in cultured human skin fibroblasts from patients with pyruvate carboxylase deficiency. J. Biol. Chem. 1983, 258:6660.
53. Wolf B., Grier R.E., Secor M., Heard G.S. Biotinidase deficiency: a novel vitamin recycling defect. J. Inherit. Metab. Dis. 1985, 8 Suppl. 1:53.
54. Shriver B.J., Roman-Shriver C., Allred J.B. Depletion and repletion of biotinyl enzymes in liver of biotin-deficient rats: evidence of a biotin storage system. J. Nutr. 1993, 123:1140.
55. Rodriguez-Melendez R., Perez-Andrade M.E., Diaz A., Deolarte A., Camacho-Arroyo I., Ciceron I., Ibarra I., Velazquez A. Differential effects of biotin deficiency and replenishment on rat liver pyruvate and propionyl-CoA carboxylases and on their mRNAs. Mol. Genet. Metab. 1999, 66:16.
56. Kawahara T.L., Michishita E., Alder A.S., Damian M., Berber E., Lin M., McCord R.A., Onqaiqui K.C., Boxer L.D., Chang H.Y., Chua K.F. SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 2009, 136:62.
57. Tamaru H., Zhang X., McMillen D., Singh P.B., Nakayama J., Grewal S.I., Allis C.D., Cheng X., Selker E.U. Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat. Genet. 2003, 34:75.
58. Decluve G.P., Davie J.R. Chromatin structure of erythroid-specific genes of immature and mature chicken erythrocytes. Biochem. J. 1989, 263:179.
59. Hassan Y.I., Zempleni J. A novel, enigmatic histone modification: biotinylation of histones by holocarboxylase synthetase. Nutr. Rev. 2008, 66:721.
60. Shahbazian M.D., Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 2007, 76:75.
61. Peterson C.L., Laniel M.A. Histones and histone modifications. Curr. Biol. 2004, 14:R546-R551.
62. Walter T.S., Meier C., Assenberg R., Au K.F., Ren J., Verma A., Nettleship J.E., Owens R.J., Stuart D.I., Grimes J.M. Lysine methylation as a routine rescue strategy for protein crystallization. Structure 2006, 14:1617.
63. Lee B.S., Krisnanchettiar S., Lateef S.S., Gupta S. Mass spectrometric detection of biotinylated peptides captured by avidin functional affinity electrophoresis. Rapid Commun. Mass Spectrom. 2005, 19:886.
64. Schriemer D.C., Li L. Combining avidin-biotin chemistry with matrix-assisted laser desorption/ionization mass spectrometry. Anal. Chem. 1996, 68:3382.
65. Schriemer D.C., Yalcin T., Li L. MALDI mass spectrometry combined with avidin-biotin chemistry for analysis of protein modifications. Anal. Chem. 1998, 70:1569.
66. Peters D.M., Griffin J.B., Stanley J.S., Beck M.M., Zempleni J. Exposure to UV light causes increased biotinylation of histones in Jurkat cells. Am. J. Physiol. Cell Physiol. 2002, 283:C878-C884.
67. Perez-Monjaras A., Cervantes-Roldan R., Meneses-Morales I., Gravel R.A., Reyes-Carmona S., Solorzano-Vargas S., Gonzalez-Noriega A., Leon-Del-Rio A. Impaired biotinidase activity disrupts holocarboxylase synthetase expression in late onset multiple carboxylase deficiency. J. Biol. Chem. 2008, 283:34150.
68. Stanley J.S., Mock D.M., Griffin J.B., Zempleni J. Biotin uptake into human peripheral blood mononuclear cells increases early in the cell cycle, increasing carboxylase activities. J. Nutr. 2002, 132:1854.
69. Martin C., Zhang Y. The diverse functions of histone lysine methylation. Nat. Rev., Mol. Cell Biol. 2005, 6:838.
70. Davie J.R., Saunders C.A., Walsh J.M., Weber S.C. Histone modifications in the yeast S. cerevisiae. Nucleic Acids Res. 1981, 9:3205.
71. Takechi R., Taniguchi A., Ebara S., Fukui T., Watanabe T. Biotin deficiency affects the proliferation of human embryonic palatal mesenchymal cells in culture. J. Nutr. 2008, 138:680.
72. Beckett D. Biotin sensing: universal influence of biotin status on transcription. Annu. Rev. Genet. 2007, 41:443.
73. Rodriguez-Melendez R., Cano S., Mendez S.T., Velazquez A. Biotin regulates the genetic expression of holocarboxylase synthetase and mitochondrial carboxylases in rats. J. Nutr. 2001, 131:1909.
74. Leon-Del-Rio A. Biotin-dependent regulation of gene expression in human cells. J. Nutr. Biochem. 2005, 16:432.