Mechanistic analysis of a suicide inactivator of histone demethylase LSD1

Biochemistry

Volumn 46, Issue 23, 2007, Pages 6892-6902

  Szewczuk, Lawrence M ^a   Culhane, Jeffrey C ^a   Yang, Maojun ^b   Majumdar, Ananya ^c   Yu, Hongtao ^b   Cole, Philip A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MECHANISTIC ANALYSIS; SUICIDE INACTIVATORS;

AMINES; COVALENT BONDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; SPECTROSCOPIC ANALYSIS; TRANSCRIPTION;

ENZYME INHIBITION;

AMINE; AMINE OXIDASE (FLAVIN CONTAINING); AZIRIDINE DERIVATIVE; BIOTIN; CYCLOPROPANE DERIVATIVE; ENZYME INHIBITOR; FLAVINE NUCLEOTIDE; HISTONE DEMETHYLASE; HISTONE H3; HISTONE H4; IMINE; LYSINE; LYSINE SPECIFIC DEMETHYLASE 1; METHYL GROUP; PROPANE; PROPARGYLAMINE DERIVATIVE; PROPYLAMINE; REPRESSOR PROTEIN; SODIUM BOROHYDRIDE; UNCLASSIFIED DRUG;

ARTICLE; BIOTINYLATION; CARBON NUCLEAR MAGNETIC RESONANCE; CONJUGATE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME MODIFICATION; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEOMICS;

AMINO ACID SEQUENCE; BIOTINYLATION; ENZYME INHIBITORS; FLAVINS; GLUTATHIONE; HELA CELLS; HUMANS; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES, N-DEMETHYLATING; SPECTROPHOTOMETRY;

EID: 34250203607     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700414b     Document Type: Article

References (47)

1. Schreiber, S. L., and Bernstein, B. E. (2002) Signaling network model of chromatin, Cell 111, 771-778.
2. Jenuwein, T., and Allis, C. D. (2001) Translating the histone code. Science 293, 1074-1080.
3. Olins, D. E., and Olins, A. L. (2003) Chromatin history: Our view from the bridge, Nat. Rev. Mol. Cell Biol. 4, 809-814.
4. Martin, C., and Zhang, Y. (2005) The diverse functions of histone lysine modification, Nat. Rev. Mol. Cell Biol. 6, 838-849.
5. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A., and Shi, Y. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1, Cell 119, 941-953.
6. Shi, Y., and Whetstine, J. R. (2007) Dynamic regulation of histone lysine methylation by demethylases, Mol. Cell 25, 1-14.
7. Tsukada, T., Fang, J., Erdjument-Bromage, H., Warren, M. E., Borchers, C. H., Tempst, P., and Zhang, Y. (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439, 811-816.
8. Whetstine, J. R., Nottke, A., Lan, F., Huarte, M., Smolikov, S., Chen, Z., Spooner, E., Li, E., Zhang, G., Colaiacovo, M., and Shi, Y. (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases, Cell 125, 467-481.
9. Binda, C., Mattevi, A., and Edmonson, D. E. (2002) Structure-function relationships in flavoenzyme-dependent amine oxidations: A comparison of polyamine oxidase and monoamine oxidase, J. Biol. Chem. 277, 23973-23976.
10. Lee, M. G., Wynder, C., Cooch, N., and Shiekhattar, R. (2005) An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation, Nature 437, 432-435.
11. Shi, Y. J., Matson, C., Lan, F., Iwase, S., Baba, T., and Shi, Y. (2005) Regulation of LSD1 histone demethylase activity by its associated factors, Mol. Cell 19, 857-864.
12. Yang, M., Gocke, C. B., Luo, X., Borek, D., Tomchick, D. R., Machius, M., Otwinowski, Z., and Yu, H. (2006) Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol. Cell 23, 377-387.
13. Chen, Y., Yang, Y., Wang, F., Wan, K., Yamane, K., Zhang, Y., and Lei, M. (2006) Crystal structure of human histone lysine-specific demethylase 1 (LSD1), Proc. Natl. Acad. Sci. U.S.A. 103, 13956-13961.
14. Stavropoulos, P., Blobel, G., and Hoelz, A. (2006) Crystal structure and mechanism of human lysine-specific demethylase-1, Nat. Struct. Mol. Biol. 13, 626-632.
15. Culhane, J. C., Szewczuk, L. M., Liu, X., Da, G., Marmorstein, R., and Cole, P. A. (2006) A mechanism-based inactivator for hisone demethylase LSD1, J. Am. Chem. Soc. 128, 4536-4537.
16. Lee, M. G., Wynder, C., Scmidt, D. M., McCafferty, D. G., and Shiekhattar, R. (2006) Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications, Chem. Biol. 13, 563-567.
17. Edmondson, D. E., Mattevi, A., Binda, C., Li, M., and Hubalek, F. (2004) Structure and mechanism of monoamine oxidase, Curr. Med. Chem. 11, 1983-1993.
18. Walsh, C. T. (1984) Suicide substrates, mechanism-based enzyme inactivators: Recent developments, Annu. Rev. Biochem. 53, 493-535.
19. Silverman, R. B. (1995) Mechanism-based enzyme inactivators, Methods Enzymol. 249, 240-283.
20. Hellerman, L., and Erwin, V. G. (1968) Mitochondrial monoamine oxidase. II. Action of various inhibitors for the bovine kidney enzyme. Catalytic mechanism, J. Biol. Chem. 243, 5234-5243.
21. Maycock, A. L., Abeles, R. H., Salach, J. I., and Singer, T. P. (1976) The structure of the covalent adduct formed by the interaction of 3-dimethylamino-1-propyne and the flavine of mitochondrial amine oxidase, Biochemistry 15, 114-125.
22. Binda, C., Hubalek, F., Li, M., Herzig, Y., Sterling, J., Edmondson, D. E., and Mattevi, A. (2005) Binding of rasagiline-related inhibitors to human monoamine oxidases: A kinetic and crystallography analysis, J. Med. Chem. 48, 8148-8154.
23. Forneris, F., Binda, C., Vanoni, M. A., Battaglioli, E., and Mattevi, A. (2005) Human histone demethylase LSD1 reads the histone code, J. Biol. Chem. 280, 41360-41365.
24. Copeland, R. A. (2000) Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis, 2nd ed., Wiley-VCH, New York.
25. Kitz, R., and Wilson, I. B. (1962) Esters of methanesulfonic acid as irreversible inhibitors of acetylcholinesterase, J. Biol. Chem. 237, 3245-3249.
26. McEwen, C. M., Sasaki, G., and Jones, D. C. (1969) Human liver mitochondrial monoamine oxidase. 3. Kinetic studies concerning time-dependent inhibitions, Biochemistry 8, 3963-3972.
27. Paech, C., Salach, J. I., and Singer, T. P. (1980) Suicide inactivation of monoamine oxidase by trans-phenylcyclopropylamine, J. Biol. Chem. 255, 2700-2704.
28. Gartner, B., Hemmerich, P., and Zeller, E. A. (1976) Structure of flavin adducts with acetylenic substrates. Chemistry of monoamine oxidase and lactate oxidase inhibition, Eur. J. Biochem. 63, 211-221.
29. Hubalek, F., Binda, C., Li, M., Herzig, Y., Sterling, J., Youdim, M. B. H., Mattevi, A., and Edmondson, D. E. (2004) Inactivation of purified human recombinant monoamine oxidases A and B by rasagiline and its analogues, J. Med. Chem. 47, 1760-1766.
30. Mitchell, D. J., Nikolic, D., Rivera, E., Sablin, S. O., Choi, S., van Breeman, R. B., Singer, T. P., and Silverman, R. B. (2001) Spectrometric evidence for the flavin-1-phenylcyclopropylamine inactivator adduct with monoamine oxidase N, Biochemistry 40, 5447-5456.
31. Woo, J. C. G., and Silverman, R. B. (1994) Observation of two different chromophores in the resting state of monoamine oxidase B by fluorescence spectroscopy, Biochem. Biophys. Res. Commun. 202, 1574-1578.
32. Ghisla, S., Ogata, H., Massey, V., Schonbrunn, A., Abeles, R. H., and Walsh, C. T. (1976) Kinetic studies on the inactivation of L-lactate oxidase by [the acetylenic suicide substrate] 2-hydroxy-3-butynoate. Biochemistry 15, 1791-1797.
33. Sablin, S. O., Yankovskaya, V., Bernard, S., Cronin, C. N., and Singer, T. P. (1998) Isolation and characterization of an evolutionary precursor of human monoamine oxidases A and B, Eur. J. Biochem. 253, 270-279.
34. Vuister, G. W., and Bax, A. (1992) Resolution enhancement and spectral editing of uniformly C-13-enriched proteins by homonuclear broad-band C-13 decoupling, J. Magn. Reson. 98, 428-435.
35. Eggenberger, U., Karimi-Nejad, Y., Thuering, H., Rüterjans, H., and Griesinger, C. (1992) Determination of H-α, H-β and H-β, C coupling-constants in C-13 labeled proteins, J. Biomol. NMR 2, 583-590.
36. 3J coupling-constants, Biochemistry 33, 5481-5492.
37. Bax, A., and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy, J. Magn. Reson. 63, 207-213.
38. Schmidt, D. M. Z., and McCafferty, D. G. (2007) trans-2- Phenylcyclopropylamine is a mechanism-based inactivator of the histone demethylase LSD1, Biochemistry 46, 4408-4416.
39. 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.
40. Sieber, S. A., Niessen, S., Hoover, H. S., and Cravatt, B. F. (2006) Proteomic profiling of metalloprotease activities with cocktails of active-site probes, Nat. Chem. Biol. 2, 274-281.
41. Blum, G., Mullins, S. R., Keren, K., Fonovic, M., Jedeszko, C., Rice, M. J., Sloane, B. F., and Bogyo, M. (2005) Dynamic imaging of protease activity with fluorescently quenched activity-based probes, Nat. Chem. Biol. 1, 203-209.
42. Kumar, S., Zhou, B., Liang, F., Wang, W. Q., Huang, Z., and Zhang, Z. Y. (2004) Activity-based probes for protein tyrosine phosphatases, Proc. Natl. Acad. Sci. U.S.A. 101, 7943-7948.
43. Luo, Y., Knuckley, B., Bhatia, M., Pellechia, P. J., and Thompson, P. R. (2006) Activity-based protein profiling reagents for protein arginine deiminase 4 (PAD4): Synthesis and in vitro evaluation of a fluorescently labeled probe, J. Am. Chem. Soc. 128, 14468-14469.
44. Kolb, H. C., Finn, M. G., and Sharpless, K. B. (2001) Click Chemistry: Diverse Chemical Function from a Few Good Reactions, Angew. Chem., Int. Ed. 40, 2004-2021.
45. Lewis, W. G., Green, L. G., Grynszpan, F., Radic, Z., Carlier, P. R., Taylor, P., Finn, M. G., and Sharpless, K. B. (2002) Click chemistry in situ: Acetylcholinesterase as a reaction vessel for the selective assembly of a femtomolar inhibitor from an array of building blocks, Angew. Chem., Int. Ed. 41, 1053-1057.
46. Muir, T. W., Sondhi, D., and Cole, P. A. (1998) Expressed protein ligation: A general method for protein engineering, Proc. Natl. Acad. Sci. U.S.A. 95, 6705-6710.
47. Wang, L., Brock, A., Herberich, B., and Schultz, P. G. (2001) Expanding the genetic code of Escherichia coli. Science 292, 498-500.