NMR-based detection of acetylation sites in peptides

Journal of Peptide Science

Volumn 16, Issue 8, 2010, Pages 414-423

  Smet Nocca, Caroline ^a,b   Wieruszeski, Jean Michel ^a   Melnyk, Oleg ^c   Benecke, Arndt ^b,d  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b CNRS   (France)

^c INSTITUT DE BIOLOGIE DE LILLE   (France)

^d INSTITUT DES HAUTES ÉTUDES SCIENTIFIQUES   (France)

Author keywords

Acetylation; Histone; NMR spectroscopy; Protein structure; Thymine DNA glycosylase

Indexed keywords

ACETAMIDE; ACETIC ACID DERIVATIVE; HISTONE H4; LYSINE; PEPTIDE; HISTONE;

ACETYLATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; CHEMISTRY; METABOLISM; PROCEDURES;

ACETYLATION; HISTONES; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES;

EID: 77957295910     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.1257     Document Type: Article

References (59)

1. Spange S, Wagner T, Heinzel T, Kramer OH. Acetylation of nonhistone proteins modulates cellular signalling at multiple levels. Int. J. Biochem. Cell Biol. 2009; 41: 185-198.
2. Kouzarides T. Acetylation: a regulatory modification to rival phosphorylation? EMBO J. 2000; 19: 1176-1179.
3. Mujtaba S, Zeng L, Zhou MM. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 2007; 26: 5521-5527.
4. Zeng L, Zhou MM. Bromodomain: an acetyl-lysine binding domain. FEBS Lett. 2002; 513: 124-128.
5. Timmermann S, Lehrmann H, Polesskaya A, Harel-Bellan A. Histone acetylation and disease. Cell. Mol. Life Sci. 2001; 58: 728-736.
6. Mottet D, Castronovo V. Histone deacetylases: target enzymes for cancer therapy. Clin. Exp. Metastasis 2008; 25: 183-189.
7. Selvi RB, Kundu TK. Reversible acetylation of chromatin: implication in regulation of gene expression, disease and therapeutics. Biotechnol. J. 2009; 4: 375-390.
8. Ocker M, Schneider-Stock R. Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int. J. Biochem. Cell Biol. 2007; 39: 1367-1374.
9. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett. 2008; 269: 7-17.
10. Iakoucheva LM, Radivojac P, Brown CJ, O'Connor TR, Sikes JG, Obradovic Z, Dunker AK. The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 2004; 32: 1037-1049. (Pubitemid 38854704)
11. Obradovic Z, Peng K, Vucetic S, Radivojac P, Brown CJ, Dunker AK. Predicting intrinsic disorder from amino acid sequence. Proteins 2003; 53(Suppl 6): 566-572.
12. Tompa P. Intrinsically unstructured proteins. Trends Biochem. Sci. 2002; 27: 527-533.
13. Radivojac P, Obradovic Z, Smith DK, Zhu G, Vucetic S, Brown CJ, Lawson JD, Dunker AK. Protein flexibility and intrinsic disorder. Protein Sci. 2004; 13: 71-80.
14. Fink AL. Natively unfolded proteins. Curr. Opin. Struct. Biol. 2005; 15: 35-41.
15. Haynes C, Oldfield CJ, Ji F, Klitgord N, Cusick ME, Radivojac P, Uversky VN, Vidal M, Iakoucheva LM. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput. Biol. 2006; 2: e100.
16. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK. Intrinsic disorder and functional proteomics. Biophys. J. 2007; 92: 1439-1456.
17. Uversky VN, Radivojac P, Iakoucheva LM, Obradovic Z, Dunker AK. Prediction of intrinsic disorder and its use in functional proteomics. Methods Mol. Biol. 2007; 408: 69-92.
18. Hansen JC, Lu X, Ross ED, Woody RW. Intrinsic protein disorder, amino acid composition, and histone terminal domains. J. Biol. Chem. 2006; 281: 1853-1856.
19. Bang E, Lee CH, Yoon JB, Lee DW, Lee W. Solution structures of the N-terminal domain of histone H4. J. Pept. Res. 2001; 58: 389-398.
20. Cary PD, Crane-Robinson C, Bradbury EM, Dixon GH. Effect of acetylation on the binding of N-terminal peptides of histone H4 to DNA. Eur. J. Biochem. 1982; 127: 137-143.
21. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403: 41-45.
22. Eberharter A, Becker PB. Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep. 2002; 3: 224-229.
23. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006; 311: 844-847. (Pubitemid 43228847)
24. Shogren-Knaak M, Peterson CL. Switching on chromatin: mechanistic role of histone H4-K16 acetylation. Cell Cycle 2006; 5: 1361-1365. (Pubitemid 44153640)
25. Kurdistani SK, Tavazoie S, Grunstein M. Mapping global histone acetylation patterns to gene expression. Cell 2004; 117: 721-733. (Pubitemid 38748889)
26. Schubeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, Gottschling DE, O'Neill LP, Turner BM, Delrow J, Bell SP, Groudine M. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004; 18: 1263-1271. (Pubitemid 38720594)
27. Ura K, Kurumizaka H, Dimitrov S, Almouzni G, Wolffe AP. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone-dependent transcriptional repression. EMBO J. 1997; 16: 2096-2107. (Pubitemid 27170970)
28. Benecke A. Chromatin code, local non-equilibrium dynamics, and the emergence of transcription regulatory programs. Eur. Phys. J. E Softmatter 2006; 19: 353-366.
29. Lau OD, Kundu TK, Soccio RE, Ait-Si-Ali S, Khalil EM, Vassilev A, Wolffe AP, Nakatani Y, Roeder RG, Cole PA. HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol. Cell 2000; 5: 589-595.
30. Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996; 87: 953-959. (Pubitemid 26404293)
31. Schiltz RL, Mizzen CA, Vassilev A, Cook RG, Allis CD, Nakatani Y. Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J. Biol. Chem. 1999; 274: 1189-1192.
32. Tini M, Benecke A, Um SJ, Torchia J, Evans RM, Chambon P. Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription. Mol. Cell 2002; 9: 265-277. (Pubitemid 34195553)
33. Smith CM. Quantification of acetylation at proximal lysine residues using isotopic labeling and tandem mass spectrometry. Methods 2005; 36: 395-403.
34. Smith CM, Gafken PR, Zhang Z, Gottschling DE, Smith JB, Smith DL. Mass spectrometric quantification of acetylation at specific lysines within the amino-terminal tail of histone H4. Anal. Biochem. 2003; 316: 23-33.
35. Brownell JE, Allis CD. Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr. Opin. Genet. Dev. 1996; 6: 176-184.
36. Chen D, Lucey MJ, Phoenix F, Lopez-Garcia J, Hart SM, Losson R, Buluwela L, Coombes RC, Chambon P, Schar P, Ali S. T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor alpha. J. Biol. Chem. 2003; 278: 38586-38592.
37. Gallinari P, Jiricny J. A new class of uracil-DNA glycosylases related to human thymine-DNA glycosylase. Nature 1996; 383: 735-738. (Pubitemid 26360653)
38. Hardeland U, Bentele M, Jiricny J, Schar P. Separating substrate recognition from base hydrolysis in human thymine DNA glycosylase by mutational analysis. J. Biol. Chem. 2000; 275: 33449-33456.
39. Hardeland U, Bentele M, Jiricny J, Schar P. The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res. 2003; 31: 2261-2271.
40. Lucey MJ, Chen D, Lopez-Garcia J, Hart SM, Phoenix F, Al-Jehani R, Alao JP, White R, Kindle KB, Losson R, Chambon P, Parker MG, Schar P, Heery DM, Buluwela L, Ali S. T:G mismatch-specific thymine-DNA glycosylase (TDG) as a coregulator of transcription interacts with SRC1 family members through a novel tyrosine repeat motif. Nucleic Acids Res. 2005; 33: 6393-6404. (Pubitemid 41742576)
41. Neddermann P, Gallinari P, Lettieri T, Schmid D, Truong O, Hsuan JJ, Wiebauer K, Jiricny J. Cloning and expression of human G/T mismatch-specific thymine-DNA glycosylase. J. Biol. Chem. 1996; 271: 12767-12774.
42. Piotto M, Saudek V, Sklenar V.Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 1992; 2: 661-665.
43. Wishart DS, Sykes BD, Richards FM. The chemical shift index : a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 1992; 31: 1647-1651.
44. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 1995; 5: 67-81.
45. Marsh JA, Singh VK, Jia Z, Forman-Kay JD. Sensitivity of secondary structure propensities to sequence differences between alpha- and gamma-synuclein : implications for fibrillation. Prot. Sci. 2006; 15: 2795-2804.
46. Smet-Nocca C, Wieruszeski J-M, Chaar V, Leroy A, Benecke A. The Thymine-DNA Glycosylase regulatory domain: residual structure and DNA binding. Biochemistry 2008; 47: 6519-6530. (Pubitemid 351874279)
47. Iwahara J, Jung YS, Clore GM. Heteronuclear NMR spectroscopy for lysine NH(3) groups in proteins: unique effect of water exchange on (15)N transverse relaxation. J. Am. Chem. Soc. 2007; 129: 2971-2980.
48. Bussell R, Jr, Eliezer D. Residual structure and dynamics in Parkinson's disease-associated mutants of alpha-synuclein. J. Biol. Chem. 2001; 276: 45996-46003.
49. Lippens G, Sillen A, Smet C, Wieruszeski JM, Leroy A, Buee L, Landrieu I. Studying the natively unfolded neuronal Tau protein by solution NMR spectroscopy. Protein Pept. Lett. 2006; 13: 235-246.
50. Smet C, Leroy A, Sillen A, Wieruszeski JM, Landrieu I, Lippens G. Accepting its random coil nature allows a partial NMR assignment of the neuronal Tau protein. ChemBioChem 2004; 5: 1639-1646. (Pubitemid 39664673)
51. Sung YH, Eliezer D. Residual structure, backbone dynamics, and interactions within the synuclein family. J. Mol. Biol. 2007; 372: 689-707.
52. Wang X, Hayes JJ. Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol. Cell. Biol. 2008; 28: 227-236.
53. Shogren-Knaak MA, Fry CJ, Peterson CL. A native peptide ligation strategy for deciphering nucleosomal histone modifications. J. Biol. Chem. 2003; 278: 15744-15748.
54. Shogren-Knaak MA, Peterson CL. Creating designer histones by native chemical ligation. Methods Enzymol. 2004; 375: 62-76. (Pubitemid 38124860)
55. Muir TW. Semisynthesis of proteins by expressed protein ligation. Annu. Rev. Biochem. 2003; 72: 249-289.
56. Muralidharan V, Muir TW. Protein ligation: an enabling technology for the biophysical analysis of proteins. Nat. Methods 2006; 3: 429-438. (Pubitemid 43811554)
57. Otomo T, Ito N, Kyogoku Y, Yamazaki T. NMR observation of selected segments in a larger protein: central-segment isotope labeling through intein-mediated ligation. Biochemistry 1999; 38: 16040-16044. (Pubitemid 129520524)
58. Landrieu I, Lacosse L, Leroy A, Wieruszeski JM, Trivelli X, Sillen A, Sibille N, Schwalbe H, Saxena K, Langer T, Lippens G. NMR analysis of a Tau phosphorylation pattern. J. Am. Chem. Soc. 2006; 128: 3575-3583.
59. Landrieu I, Leroy A, Smet-Nocca C, Huvent I, Amniai L, Hamdane M, Sibille N, Buée L, Wieruszeski J-M, Lippens G. Nuclear Magnetic Resonance Spectroscopy of the neuronal Tau protein: normal function and implication in Alzheimer's disease. Biochem. Soc. Trans. 2010; 38 (in press) .