The activity of HDAC8 depends on local and distal sequences of its peptide substrates

Biochemistry

Volumn 47, Issue 23, 2008, Pages 6242-6250

  Gurard Levin, Zachary A ^a   Mrksich, Milan ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; AMINO ACIDS; ASSAYS; BIOCHEMICAL ENGINEERING; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; PEPTIDES; PROTEINS; SELF ASSEMBLED MONOLAYERS;

ACETYL GROUPS; AMERICAN CHEMICAL SOCIETY (ACS); ARGININE (ARG); BIOCHEMICAL ACTIVITY; DEACETYLASE; DEACETYLATION (DD); GLYCINE (GLY); HISTONE DEACETYLASE (HDAC); LABEL FREE; N TERMINALS; PEPTIDE SUBSTRATES; SELF ASSEMBLED MONOLAYERS (SAMS);

SUBSTRATES;

ARGININE; GLYCINE; HISTONE DEACETYLASE 8; HISTONE H4; LYSINE; PEPTIDE DERIVATIVE;

ACETYLATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL ANALYSIS; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME SUBSTRATE; GENE EXPRESSION; MASS SPECTROMETRY; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEIN METHYLATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARGININE; ENZYMES, IMMOBILIZED; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCINE; HISTONE DEACETYLASES; HISTONES; HUMANS; KINETICS; MODELS, MOLECULAR; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; REPRESSOR PROTEINS; SUBSTRATE SPECIFICITY;

EID: 44949231404     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800053v     Document Type: Article

References (55)

1. Allfrey, V. G., Faulkner, R., and Mirsky, A. E. (1964) Acetylation 4- Methylation of Histones + Their Possible Role in Regulation of RNA Synthesis. Proc. Natl. Acad. Sci. U.S.A. 51, 786-794.
2. Jenuwein, T., and Allis, C. D. (2001) Translating the histone code. Science 293, 1074-1080.
3. Shahbazian, M. D., and Grunstein, M. (2007) Functions of site-specific histone acerylation and deacetylation. Annu. Rev. Biochem. 76, 75-100.
4. Dhalluin, C., Carlson, J. E., Zeng, L., He, C., Aggarwal, A. K., and Zhou, M. M. (1999) Structure and ligand of a histone acetyltransferase bromodomain. Nature 399, 491-496.
5. Pazin, M. J., and Kadonaga, J. T. (1997) What's up and down with histone deacetylation and transcription? Cell 89, 325-328.
6. Peterson, C. L., and Laniel, M. A. (2004) Histones and histone modifications. Curr. Biol. 14, R546-R551.
7. Sterner, D. E., and Berger, S. L. (2000) Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64, 435-459.
8. Kolle, D., Brosch, G., Lechner, T., Lusser, A., and Loidl, P. (1998) Biochemical methods for analysis of histone deacetylases. Methods 15, 323-331.
9. DarkinRattray, S. J., Gurnett, A. M., Myers, R. W., Dulski, P. M., Crumley, T. M., Allocco, J. J., Cannova, C., Meinke, P. T., Colletti, S. L., Bednarek, M. A., Singh, S. B., Goetz, M. A., Dombrowski, A. W., Polishook, J. D., and Schmatz, D. M. (1996) Apicidin: A novel antiprotozoal agent that inhibits parasite histone deacetylase. Proc. Natl. Acad. Sci. U.S.A. 93, 13143-13147.
10. Heltweg, B., Trapp, J., and Jung, M. (2005) In vitro assays for the determination of histone deacetylase activity. Methods 36, 332-337.
11. Wegener, D., Hildmann, C., and Schwienhorst, A. (2003) Recent progress in the development of assays suited for histone deacetylase inhibitor screening. Mol. Genet. Metab. 80, 138-147.
12. Frank, R. (1992) Spot-Synthesis: An Easy Technique for the Positionally Addressable, Parallel Chemical Synthesis on a Membrane Support. Tetrahedron 48, 9217-9232.
13. Clemente, S., Franco, L., and Lopez-Rodas, G. (2001) Distinct site specificity of two pea histone deacetylase complexes. Biochemistry 40, 10671-10676.
14. Riester, D., Hildmann, C., Schwienhorst, A., and Meyer-Almes, F. J. (2007) Histone deacetylase inhibitor assay based on fluorescence resonance energy transfer. Anal. Biochem. 362, 136-141.
15. Su, J., Rajapaksha, T. W., Peter, M. E., and Mrksich, M. (2006) Assays of endogenous caspase activities: A comparison of mass spectrometry and fluorescence formats. Anal. Chem. 78, 4945-4951.
16. Garske, A. L., and Denu, J. M. (2006) SIRT1 top 40 hits: Use of one-bead, one-compound acetyl-peptide libraries and quantum dots to probe deacetylase specificity. Biochemistry 45, 94-101.
17. Blander, G., Olejnik, J., Olejnik, E. K., Mcdonagh, T., Haigis, M., Yaffe, M. B., and Guarente, L. (2005) SIRT1 shows no substrate specificity in vitro. J. Biol. Chem. 280, 9780-9785.
18. Yin, Y. L., Liu, C. D., Tsai, S. N., Zhou, B., Ngai, S. M., and Zhu, G. (2005) SET8 recognizes the sequence (RHRKVLRDN)-V-20 within the N terminus of histone H4 and mono-methylates lysine 20. J. Biol. Chem. 280, 30025-30031.
19. Chin, H. G., Pradhan, M., Esteve, P. O., Patnaik, D., Evans, T. C., and Pradhan, S. (2005) Sequence specificity and role of proximal amino acids of the histone H3 tail on catalysis of murine G9a lysine 9 histone H3 methyltransferase. Biochemistry 44, 12998-13006.
20. Forneris, F., Binda, C., Dall'Aglio, A., Fraaije, M. W., Battaglioli, E., and Mattevi, A. (2006) A highly specific mechanism of histone H3-K4 recognition by histone demethylase LSD1. J. Biol. Chem. 281, 35289-35295.
21. Clements, A., Poux, A. N., Lo, W. S., Pillus, L., Berger, S. L., and Marmorstein, R. (2003) Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol. Cell 12, 461-473.
22. Zhao, K. H., Chai, X. M., and Marmorstein, R. (2003) Structure of the yeast Hst2 protein deacetylase in ternary complex with 2′-O-acetyl ADP ribose and histone peptide. Structure 11, 1403-1411.
23. Vannini, A., Volpari, C., Gallinari, P., Jones, P., Mattu, M., Carfi, A., De Francesco, R., Steinkuhler, C., and Di Marco, S. (2007) Substrate binding to histone deacetylases as shown by the crystal structure of the HDAC8-substrate complex. EMBO Rep. 8, 879-884.
24. Thieriet, N., Alsina, J., Giralt, E., Guibe, F., and Albericio, F. (1997) Use of Alloc-amino acids in solid-phase peptide synthesis. Tandem deprotection-coupling reactions using neutral conditions. Tetrahedron Lett. 38, 7275-7278.
25. Houseman, B. T., Gawalt, E. S., and Mrksich, M. (2003) Maleimide-functionalized self-assembled monolayers for the preparation of peptide and carbohydrate biochips. Langmuir 19, 1522-1531.
26. Gurard-Levin, Z. A., and Mrksich, M. (2008) Combining Self-Assembled Monolayers and Mass Spectrometry for Applications in Biochips. Annu. Rev. Anal. Chem. 1. (in press).
27. Min, D. H., Tang, W. J., and Mrksich, M. (2004) Chemical screening by mass spectrometry to identify inhibitors of anthrax lethal factor. Nat. Biotechnol. 22, 717-723.
28. Min, D. H., Su, J., and Mrksich, M. (2004) Profiling kinase activities by using a peptide chip and mass spectrometry. Angew. Chem., Int. Ed. 43, 5973-5977.
29. Houseman, B. T., and Mrksich, M. (1999) The role of ligand density in the enzymatic glycosylation of carbohydrates presented on self-assembled monolayers of alkanethiolates on gold. Angew. Chem., Int. Ed. 38, 782-785.
30. Min, D. H., Yeo, W. S., and Mrksich, M. (2004) A method for connecting solution-phase enzyme activity assays with immobilized format analysis by mass spectrometry. Anal. Chem. 76, 3923-3929.
31. Houseman, B. T., and Mrksich, M. (2002) Towards quantitative assays with peptide chips: A surface engineering approach. Trends Biotechnol. 20, 279-281.
32. Mrksich, M., and Whitesides, G. M. (1997) Using self-assembled monolayers that present oligo(ethylene glycol) groups to control the interactions of proteins with surfaces. ACS Symp. Ser. 680, 361-373.
33. Somoza, J. R., Skene, R. J., Katz, B. A., Mol, C., Ho, J. D., Jennings, A. J., Luong, C., Arvai, A., Buggy, J. J., Chi, E., Tang, J., Sang, B. C., Verner, E., Wynands, R., Leahy, E. M., Dougan, D. R., Snell, G., Navre, M., Knuth, M. W., Swanson, R. V., McRee, D. E., and Tari, L. W. (2004) Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure 12, 1325-1334.
34. Dion, M. F., Altschuler, S. J., Wu, L. F., and Rando, O. J. (2005) Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. U.S.A. 102, 5501-5506.
35. Zhang, Y., and Reinberg, D. (2001) Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 15, 2343-2360.
36. Overall, C. M. (2001) Matrix metalloproteinase substrate binding domains, modules and exosites: Overview and experimental strategies. Methods Mol. Biol. 151, 79-120.
37. Biondi, R. M., and Nebreda, A. R. (2003) Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem. J. 372, 1-13.
38. Krishnaswamy, S. (2005) Exosite-driven substrate specificity and function in coagulation. J. Thromb. Haemostasis 3, 54-67.
39. Sauve, A. A., Wolberger, C., Schramm, V. L., and Boeke, J. D. (2006) The biochemistry of sirtuins. Annu. Rev. Biochem. 75, 435-465.
40. Howitz, K. T., Bitterman, K. J., Cohen, H. Y., Lamming, D. W., Lavu, S., Wood, J. G., Zipkin, R. E., Chung, P., Kisielewski, A., Zhang, L. L., Scherer, B., and Sinclair, D. A. (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425, 191-196.
41. Holbert, M. A., and Marmorstein, R. (2005) Structure and activity of enzymes that remove histone modifications. Curr. Opin. Struct. Biol. 15, 673-680.
42. Strahl, B. D., and Allis, C. D. (2000) The language of covalent histone modifications. Nature 403, 41-45.
43. Fischle, W., Wang, Y. M., and Allis, C. D. (2003) Binary switches and modification cassettes in histone biology and beyond. Nature 425, 475-479.
44. Nishioka, K., Rice, J. C., Sarma, K., Erdjument-Bromage, H., Werner, J., Wang, Y. M., Chuikov, S., Valenzuela, P., Tempst, P., Steward, R., Lis, J. T., Allis, C. D., and Reinberg, D. (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol. Cell 9, 1201-1213.
45. Latham, J. A., and Dent, S. Y. R. (2007) Cross-regulation of histone modifications. Nat. Struct. Mol. Biol. 14, 1017-1024.
46. Sarg, B., Helliger, W., Talasz, H., Koutzamani, E., and Lindner, H. H. (2004) Histone H4 hyperacetylation precludes histone H4 lysine 20 trimethylation. J. Biol. Chem. 279, 53458-53464.
47. Deng, S. J., Bickett, D. M., Mitchell, J. L., Lambert, M. H., Blackburn, R. K., Carter, H. L., Neugebauer, J., Pahel, G., Weiner, M. P., and Moss, M. L. (2000) Substrate specificity of human collagenase 3 assessed using a phage-displayed peptide library. J. Biol. Chem. 275, 31422-31427.
48. Harris, J. L., Backes, B. J., Leonetti, F., Mahrus, S., Ellman, J. A., and Craik, C. S. (2000) Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries. Proc. Natl. Acad. Sci. U.S.A. 97, 7754-7759.
49. Nazif, T., and Bogyo, M. (2001) Global analysis of proteasomal substrate specificity using positional-scanning libraries of covalent inhibitors. Proc. Natl. Acad. Sci. U.S.A. 98, 2967-2972.
50. Turk, B. E., Huang, L. L., Piro, E. T., and Cantley, L. C. (2001) Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat. Biotechnol. 19, 661-667.
51. Liu, C. L., Kaplan, T., Kim, M., Buratowski, S., Schreiber, S. L., Friedman, N., and Rando, O. J. (2005) Single-nucleosome mapping of histone modifications in S-cerevisiae. PLoS Biol. 3, 1753-1769.
52. Zhang, K. L., Williams, K. E., Huang, L., Yau, P., Siino, J. S., Bradbury, E. M., Jones, P. R., Minch, M. J., and Burlingame, A. L. (2002) Histone acetylation and deacetylation: Identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry. Mol. Cell. Proteomics 1, 500-508.
53. Su, X. D., Zhang, L. W., Lucas, D. M., Davis, M. E., Knapp, A. R., Green-Church, K. B., Marcucci, G., Parthun, M. R., Byrd, J. C., and Freitas, M. A. (2007) Histone H4 acetylation dynamics determined by stable isotope labeling with amino acids in cell culture and mass spectrometry. Anal. Biochem. 363, 22-34.
54. Thomas, C. E., Kelleher, N. L., and Mizzen, C. A. (2006) Mass spectrometric characterization of human histone H3: A bird's eye view. J. Proteome Res. 5, 240-247.
55. Seibert, C., Cadene, M., Sanfiz, A., Chait, B. T., and Sakmar, T. P. (2002) Tyrosine sulfation of CCR5 N-terminal peptide by tyrosyl-protein sulfotransferases 1 and 2 follows a discrete pattern and temporal sequence. Proc. Natl. Acad. Sci. U.S.A. 99, 11031-11036.