Use of pH and kinetic isotope effects to establish chemistry as rate-limiting in oxidation of a peptide substrate by LSD1

Biochemistry

Volumn 48, Issue 23, 2009, Pages 5440-5445

  Gaweska, Helena ^a   Pozzi, Michelle Henderson ^b   Schmidt, Dawn M Z ^c   McCafferty, Dewey G ^c   Fitzpatrick, Paul F ^d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c DUKE UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C-H BOND CLEAVAGE; DEMETHYLASE; DEUTERATION; DEUTERIUM KINETIC ISOTOPE EFFECT; HISTONE H3; HYDRIDE TRANSFERS; ISOTOPIC SUBSTITUTION; KINETIC ISOTOPE EFFECTS; MECHANISM OF OXIDATION; N-TERMINAL; PEPTIDE SUBSTRATES; PHYSIOLOGICAL PH; RATE LIMITING; STOPPED FLOW;

AMINES; AMINO ACIDS; CARRIER MOBILITY; CHEMICAL BONDS; DEUTERIUM; OXIDATION; RATE CONSTANTS; SUBSTRATES;

PH EFFECTS;

DEUTERIUM; FLAVOPROTEIN; HISTONE H3; ISOTOPE; LYSINE SPECIFIC DEMETHYLASE; QUERCETIN; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHEMICAL REACTION; ENZYME ASSAY; ENZYME SUBSTRATE COMPLEX; ISOTOPE ANALYSIS; OXIDATION; PEPTIDE SYNTHESIS; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION; SPECTROSCOPY; STEADY STATE;

BINDING SITES; DEUTERIUM; HUMANS; HYDROGEN-ION CONCENTRATION; ISOTOPES; KINETICS; OXIDATION-REDUCTION; OXIDOREDUCTASES, N-DEMETHYLATING; PEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 67049098986     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900499w     Document Type: Article

References (51)

1. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature389, 251-260. (Pubitemid 27406632)
2. Jenuwein, T., and Allis, C. D. (2001) Translating the histone code. Science293, 1074-1080. (Pubitemid 32758077)
3. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., and Casero, R. A. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell119, 941-953. (Pubitemid 40037608)
4. Metzger, E., Wissmann, M., Yin, N., Muller, J. M., Schneider, R., Peters, A. H. F. M., Gunther, T., Buettner, R., and Schule, R. (2005) LSD1 demethylates repressive histone marks to promote androgenreceptor- dependent transcription. Nature437, 436-439. (Pubitemid 41613508)
5. Huang, J., Sengupta, R., Espejo, A. B., Lee, M. G., Dorsey, J. A., Richter, M., Opravil, S., Shiekhattar, R., Bedford, M. T., Jenuwein, T., and Berger, S. L. (2007) p53 is regulated by the lysine demethylase LSD1. Nature449, 105-108. (Pubitemid 47373772)
6. Tsukada, Y.-i., 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. Nature439, 811-816.
7. Shilatifard, A. (2008) Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr. Opin. Cell Biol.20, 341-348.
8. Lee, M. G., Wynder, C., Schmidt, 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.
9. Schulte, J. H., Lim, S., Schramm, A., Friedrichs, N., Koster, J., Versteeg, R., Ora, I., Pajtler, K., Klein-Hitpass, L., Kuhfittig-Kulle, S., Metzger, E., Schule, R., Eggert, A., Buettner, R., and Kirfel, J. (2009) Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: Implications for therapy. Cancer Res.69, 2065-2071.
10. Kahl, P., Gullotti, L., Heukamp, L. C., Wolf, S., Friedrichs, N., Vorreuther, R., Solleder, G., Bastian, P. J., Ellinger, J., Metzger, E., Schule, R., and Buettner, R. (2006) Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res.66, 11341-11347. (Pubitemid 46009965)
11. Zhu, X., Wang, J., Ju, B. G., and Rosenfeld, M. G. (2007) Signaling and epigenetic regulation of pituitary development. Curr. Opin. Cell Biol.19, 605-611.
12. Su, S. T., Ying, H. Y., Chiu, Y. K., Lin, F. R., Chen, M. Y., and Lin, K. I. (2009) Involvement of histone demethylase LSD1 in Blimp- 1-mediated gene repression during plasma cell differentiation. Mol. Cell. Biol.29, 1421-1431.
13. Fraaije, M. W., and Mattevi, A. (2000) Flavoenzymes: Diverse catalysts with recurrent features. Trends Biochem. Sci.25, 126-132.
14. 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.
15. Fitzpatrick, P. F. (2001) Substrate dehydrogenation by flavoproteins. Acc. Chem. Res.34, 299-307.
16. Kurtz, K. A., Rishavy, M. A., Cleland, W. W., and Fitzpatrick, P. F. (2000) Nitrogen isotope effects as probes of the mechanism of D-amino acid oxidase. J. Am. Chem. Soc.122, 12896-12897.
17. 2, consistent with a hydride transfer mechanism. Biochemistry42, 15208-15214.
18. 15N kinetic isotope effects on alanine oxidation by an L-amino acid oxidase. Biochemistry45, 15844-15852.
19. Ralph, E. C., Hirschi, J. S., Anderson, M. A., Cleland, W. W., Singleton, D. A., and Fitzpatrick, P. F. (2007) Insights into the mechanism of flavoprotein-catalyzed amine oxidation from nitrogen isotope effects on the reaction of N-methyltryptophan oxidase. Biochemistry46, 7655-7664. (Pubitemid 46986389)
20. Fitzpatrick, P. F. (2007) Insights into the mechanisms of flavoprotein oxidases from kinetic isotope effects. J. Labelled Compd. Radiopharm. 50, 1016-1025.
21. Culhane, J. C., Szewczuk, L. M., Liu, X., Da, G., Marmorstein, R., and Cole, P. A. (2006) A mechanism-based inactivator for histone demethylase LSD1. J. Am. Chem. Soc.128, 4536-4537.
22. Szewczuk, L. M., Culhane, J. C., Yang, M., Majumdar, A., Yu, H., and Cole, P. A. (2007) Mechanistic analysis of a suicide inactivator of histone demethylase LSD1. Biochemistry46, 6892-6902. (Pubitemid 46906418)
23. Yang, M., Culhane, J. C., Szewczuk, L. M., Jalili, P., Ball, H. L., Machius, M., Cole, P. A., and Yu, H. (2007) Structural Basis for the Inhibition of the LSD1 Histone Demethylase by the Antidepressant trans-2- Phenylcyclopropylamine. Biochemistry46, 8058-8065. (Pubitemid 47051641)
24. Gooden, D. M., Schmidt, D. M. Z., Pollock, J. A., Kabadi, A. M., and McCafferty, D. G. (2008) Facile synthesis of substituted trans- 2-arylcyclopropylamine inhibitors of the human histone demethylase LSD1 and monoamine oxidases A and B. Bioorg. Med. Chem. Lett.18, 3047-3051.
25. Schmidt, D. M. Z., and McCafferty, D. G. (2007) trans-2- Phenylcyclopropylamine Is a Mechanism-Based Inactivator of the Histone Demethylase LSD1. Biochemistry46, 4408-4416. (Pubitemid 46559406)
26. 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.
27. 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.
28. Huang, Z.-P., Du, J.-T., Zhao, Y.-F., and Li, Y.-M. (2006) Synthesis of Site-Specifically Dimethylated and Trimethylated Peptides Derived from Histone H3 N-Terminal Tail. Int. J. Pept. Protein Res.12, 187-193.
29. Ellis, K. J., and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes. Methods Enzymol.87, 405-426.
30. Cook, P. F., and Cleland, W. W. (1981) pH variation of isotope effects in enzyme-catalyzed reactions. 1. Isotope- and pH-dependent steps the same. Biochemistry20, 1797-1805.
31. Jencks, W. P. (1969) Catalysis in chemistry and enzymology, McGraw- Hill Books, Inc., New York.
32. Denu, J. M., and Fitzpatrick, P. F. (1992) pH and kinetic isotope effects on the reductive half-reaction of D-amino acid oxidase. Biochemistry31, 8207-8215.
33. Emanuele, J. J. Jr., and Fitzpatrick, P. F. (1995) Mechanistic studies of the flavoprotein tryptophan 2-monooxygenase. 2. pH and kinetic isotope effects. Biochemistry34, 3716-3723.
34. Silverman, R. B. (1995) Radical ideas about monoamine oxidase. Acc. Chem. Res.28, 335-342.
35. McCann, A. E., and Sampson, N. S. (2000) A C6-flavin adduct is the major product of irreversible inactivation of cholesterol oxidase by 2a,3a-cyclopropano-5a-cholestan-3b-ol. J. Am. Chem. Soc.122, 35-39.
36. Chen, Z. W., Zhao, G., Martinovic, S., Jorns, M. S., and Mathews, F. S. (2005) Structure of the sodium borohydride-reduced N-(cyclopropyl) glycine adduct of the flavoenzyme monomeric sarcosine oxidase. Biochemistry44, 15444-15450. (Pubitemid 41706127)
37. Henderson Pozzi, M., Gawandi, V., and Fitzpatrick, P. F. (2009) pH Dependence of a Mammalian Polyamine Oxidase: Insights into Substrate Specificity and the Role of Lysine 315. Biochemistry48, 1508-1516.
38. Ralph, E. C., and Fitzpatrick, P. F. (2005) pH and kinetic isotope effects on sarcosine oxidation by N-methyltryptophan oxidase. Biochemistry44, 3074-3081. (Pubitemid 40293682)
39. Dunn, R. V., Marshall, K. R., Munro, A. W., and Scrutton, N. S. (2008) The pH dependence of kinetic isotope effects in monoamine oxidase A indicates stabilization of the neutral amine in the enzymesubstrate complex. FEBS J.275, 3850-3858. (Pubitemid 351990950)
40. Pawelek, P. D., Cheah, J., Coulombe, R., Macheroux, P., Ghisla, S., and Vrielink, A. (2000) The structure of L-amino acid oxidase reveals the substrate trajectory into an enantiomerically conserved active site. EMBO J.19, 4204-4215. (Pubitemid 30623731)
41. Binda, C., Coda, A., Angelini, R., Federico, R., Ascenzi, P., and Mattevi, A. (1999) A 30 Å long U-shaped catalytic tunnel in the crystal structure of polyamine oxidase. Structure7, 265-276. (Pubitemid 29159686)
42. Huang, Q., Liu, Q., and Hao, Q. (2005) Crystal structures of Fms1 and its complex with spermine reveal substrate specificity. J. Mol. Biol.348, 951-959.
43. Binda, C., Newton-Vinson, P., Hubalek, F., Edmondson, D. E., and Mattevi, A. (2002) Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders. Nat. Struct. Biol.9, 22-26.
44. Ma, J., Yoshimura, M., Yamashita, E., Nakagawa, A., Ito, A., and Tsukihara, T. (2004) Structure of rat monoamine oxidase A and its specific recognitions for substrates and inhibitors. J. Mol. Biol.338, 103-114.
45. Lee, M. B., Winder, C., Cooch, H., and Shiekhattar, R. (2005) An essential role for CoREST in nucleosomal histone3 lysine4 demethylation. Nature437, 432-435. (Pubitemid 41613507)
46. Polticelli, F., Basran, J., Faso, C., Cona, A., Minervini, G., Angelini, R., Federico, R., Scrutton, N. S., and Tavladoraki, P. (2005) Lys300 plays a major role in the catalytic mechanism of maize polyamine oxidase. Biochemistry44, 16108-16120. (Pubitemid 41785809)
47. Massey, V., and Gibson, Q. H. (1964) Role of semiquinones in flavoprotein catalysis. Fed. Proc.23, 18-29.
48. Massey, V., and Curti, B. (1967) On the reaction mechanism of Crotalus adamanteus L-amino acid oxidase. J. Biol. Chem.242, 1259-1264.
49. Walker, M. C., and Edmondson, D. E. (1994) Structure-activity relationships in the oxidation of benzylamine analogues by bovine liver mitochondrial monoamine oxidase B. Biochemistry33, 7088-7098. (Pubitemid 24208745)
50. Emanuele, J. J. Jr., and Fitzpatrick, P. F. (1995) Mechanistic studies of the flavoprotein tryptophan 2-monooxygenase. 1. Kinetic mechanism. Biochemistry34, 3710-3715.
51. Basran, J., Bhanji, N., Basran, A., Nietlispach, D., Mistry, S., Meskys, R., and Scrutton, N. S. (2002) Mechanistic aspects of the covalent flavoprotein dimethylglycine oxidase of Arthrobacter globiformis studied by stopped-flow spectrophotometry. Biochemistry41, 4733-4743. (Pubitemid 34275674)