Nonenzymatic biotinylation of histone H2A

Protein Science

Volumn 18, Issue 2, 2009, Pages 314-328

  Healy, Shannon ^a   Heightman, Tom D ^b   Hohmann, Laura ^c   Schriemer, David ^a   Gravel, Roy A ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

Biotin; Histones; Holocarboxylase synthetase; Mass spectrometry; Nonenzymatic

Indexed keywords

BIOTIN; HISTONE H2A; HOLOCARBOXYLASE SYNTHETASE; PROTEIN; PROTEIN BIRA; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BIOTINYLATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN MODIFICATION;

ADENOSINE MONOPHOSPHATE; BIOTIN; CARBON-CARBON LIGASES; CARBON-NITROGEN LIGASES; ESCHERICHIA COLI; HISTONES; HUMANS; LYSINE; MODELS, MOLECULAR; PEPTIDE MAPPING; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EUKARYOTA; PROKARYOTA;

EID: 59949084113     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.37     Document Type: Article

References (45)

1. Wood HG, Barden RE (1977) Biotin enzymes. Annu Rev Biochem 46: 385-413.
2. Chapman-Smith A, Cronan JE Jr (1999) In vivo enzymatic protein biotinylation. Biomol Eng 16: 119-125.
3. Pacheco-Alvarez D, Solorzano-Vargas RS, Del Rio AL (2002) Biotin in metabolism and its relationship to human disease. Arch Med Res 33: 439-447.
4. Streit WR, Entcheva P (2003) Biotin in microbes, the genes involved in its biosynthesis, its biochemical role and perspectives for biotechnological production. Appl Microbiol Biotechnol 61: 21-31.
5. Leon-Del-Rio A, Leclerc D, Akerman B, Wakamatsu N, Gravel RA (1995) Isolation of a cDNA encoding human holocarboxylase synthetase by functional complementation of a biotin auxotroph of Escherichia coli. Proc Natl Acad Sci USA 92: 4626-4630.
6. Suzuki Y, Aoki Y, Ishida Y, Chiba Y, Iwamatsu A, Kishino T, Niikawa N, Matsubara Y, Narisawa K (1994) Isolation and characterization of mutations in the human holocar- boxylase synthetase cDNA. Nat Genet 8: 122-128.
7. Eisenberg MA, Prakash O, Hsiung SC (1982) Purification and properties of the biotin repressor. A bifunctional protein. J Biol Chem 257: 15167-15173.
8. Wolf B, Grier RE, Secor M Jr, Heard GS (1985) Biotini-dase deficiency: a novel vitamin recycling defect. J Inherit Metab Dis 8 Suppl 1: 53-58.
9. Dakshinamurti K, Mistry SP (1963) Tissue and intracellu- lar distribution of biotin-C-1400H in rats and chicks. J Biol Chem 238: 294-296.
10. Hasegawa Y, Ishida Y, Kato K, Ijiri R, Miyake T, Nishi- mata S, Watanabe T, Namba I, Hayabuchi Y, Kigasawa H, Tanaka Y (2003) Pancreatoblastoma. A case report with special emphasis on squamoid corpuscles with optically clear nuclei rich in biotin. Acta Cytol 47: 679-684.
11. Nakatani Y, Kitamura H, Inayama Y, Ogawa N (1994) Pulmonary endodermal tumor resembling fetal lung. The optically clear nucleus is rich in biotin. Am J Surg Pathol 18: 637-642.
12. Yokoyama S, Kashima K, Inoue S, Daa T, Nakayama I, Moriuchi A (1993) Biotin-containing intranuclear inclusions in endometrial glands during gestation and puerpe- rium. Am J Clin Pathol 99: 13-17.
13. 4. Eur J Biochem 271: 2257-2263.
14. Chew YC, Camporeale G, Kothapalli N, Sarath G, Zempleni J (2006) Lysine residues in N-terminal and C-terminal regions of human histone H2A are targets for biotinylation by biotini- dase. J Nutr Biochem 17: 225-233.
15. Kobza K, Camporeale G, Rueckert B, Kueh A, Griffin JB, Sarath G, Zempleni J (2005) K4, K9 and K18 in human histone H3 are targets for biotinylation by biotinidase. FEBS J 272: 4249-4259.
16. Davie JR (1998) Covalent modifications of histones: expression from chromatin templates.Curr Opin Genet Dev 8: 173-178.
17. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074-1080.
18. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
19. Streaker ED, Beckett D (2006) Nonenzymatic biotinylation of a biotin carboxyl carrier protein: unusual reactivity of the physiological target lysine. Protein Sci 15: 1928-1935.
20. Narang MA, Dumas R, Ayer LM, Gravel RA (2004) Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum Mol Genet 13: 15-23.
21. Tanaka Y, Tawaramoto-Sasanuma M, Kawaguchi S, Ohta T, Yoda K, Kurumizaka H, Yokoyama S (2004) Expression and purification of recombinant human histones. Methods 33: 3-11.
22. Leon-Del-Rio A, Gravel RA (1994) Sequence requirements for the biotinylation of carboxyl-terminal fragments of human propionyl-CoA carboxylase alpha subunit expressed in Esche- richia coli. J Biol Chem 269: 22964-22968.
23. Inouye S, Nakamura M (2003) Identification of biotinyl- ated lysine residues in the photoprotein aequorin by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry peptide mapping after lysine-specific endopeptidase digestion. Anal Biochem 316: 216-222.
24. Mersfelder EL, Parthun MR (2006) The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res 34: 2653-2662.
25. Kim JY, Kim KW, Kwon HJ, Lee DW, Yoo JS (2002) Probing lysine acetylation with a modification-specific marker ion using high-performance liquid chromatogra- phy/electrospray-mass spectrometry with collision- induced dissociation. Anal Chem 74: 5443-5449.
26. Zempleni J (2005) Uptake, localization, and noncarboxy- lase roles of biotin. Annu Rev Nutr 25: 175-196.
27. Kobza K, Sarath G, Zempleni J (2008) Prokaryotic BirA ligase biotinylates K4, K9, K18 and K23 in histone H3. BMB Rep 41: 310-315.
28. Lacey JC Jr, Pruitt KM (1975) Drug-biomolecule interactions: interactions of mononucleotides and polybasic amino acids. J Pharm Sci 64: 473-477.
29. Schott H, Eckstein H (1980) Studies on interactions between immobilized lysine residues and oligomers of thymidylic and deoxyadenylic acids. Eur J Biochem 104: 79-84.
30. Agou F, Yang Y, Gesquiere JC, Waller JP, Guittet E (1995) Polyanion-induced alpha-helical structure of a synthetic 23-residue peptide representing the lysine-rich segment of the N-terminal extension of yeast cytoplasmic aspartyl-tRNA synthetase. Biochemistry 34: 569-576.
31. Wang X, Moore SC, Laszckzak M, Ausio J (2000) Acety- lation increases the alpha-helical content of the histone tails of the nucleosome. J Biol Chem 275: 35013-35020.
32. Atkins P (2001) Consequences of equilibrium. In: The Elements of Physical Chemistry, 3rd ed. New York: W.H. Freeman and Company, pp 167-185.
33. Bagautdinov B, Matsuura Y, Bagautdinova S, Kunishima N (2008) Protein biotinylation visualized by a complex structure of biotin protein ligase with a substrate. J Biol Chem 283: 14739-14750.
34. Westheimer FH (1995) Coincidences, decarboxylation, and electrostatic effects. Tetrahedron 51: 3-20.
35. Highbarger LA, Gerlt JA, Kenyon GL (1996) Mechanism of the reaction catalyzed by acetoacetate decarboxylase. Importance of lysine 116 in determining the pKa of active-site lysine 115. Biochemistry 35: 41-46.
36. Johnsson K, Allemann RK, Widmer H, Benner SA (1993) Synthesis, structure and activity of artificial, rationally designed catalytic polypeptides. Nature 365: 530-532.
37. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319: 1097-1113.
38. Badri KR, Zhou Y, Dhru U, Aramgam S, Schuger L (2008) Effects of the SANT domain of tension-induced/ inhibited proteins (TIPs), novel partners of the histone acetyltransferase p300, on p300 activity and TIP-6- induced adipogenesis. Mol Cell Biol 28: 6358-6372.
39. Camporeale G, Giordano E, Rendina R, Zempleni J, Eis- senberg JC (2006) Drosophila melanogaster holocarboxy- lase synthetase is a chromosomal protein required for normal histone biotinylation, gene transcription patterns, lifespan, and heat tolerance. J Nutr 136: 2735-2742.
40. Bailey LM, Ivanov RA, Wallace JC, Polyak SW (2008) Artifactual detection of biotin on histones by streptavi- din. Anal Biochem 373: 71-77.
41. Lane MD, Rominger KL, Young DL, Lynen F (1964) The enzymatic synthesis of holotranscarboxylase from apo- transcarboxylase and (+)-biotin. II. Investigation of the reaction mechanism. J Biol Chem 239: 2865-2871.
42. Nenortas E, Beckett D (1996) Purification and characterization of intact and truncated forms of the Escherichia coli biotin carboxyl carrier subunit of acetyl-CoA carbox- ylase. J Biol Chem 271: 7559-7567.
43. Wilkins MR, Gasteiger E, Gooley AA, Herbert BR, Molloy MP, Binz PA, Ou K, Sanchez JC, Bairoch A, Williams KL, Hochstrasser DF (1999) High-throughput mass spectro- metric discovery of protein post-translational modifications. J Mol Biol 289: 645-657.
44. Yates JR III, Eng JK, McCormack AL, Schieltz D (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67: 1426-1436.
45. Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.