Structures and mechanism of the monoamine oxidase family

Biomolecular Concepts

Volumn 2, Issue 5, 2011, Pages 365-377

  Gaweska, Helena ^a   Fitzpatrick, Paul F ^a  

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

Author keywords

enzyme mechanism; flavoproteins; L amino acid oxidase; lysine specific demethylase; monoamine oxidase; polyamine oxidase; protein structure; spermine oxidase

Indexed keywords

EID: 84873727681     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/BMC.2011.030     Document Type: Review

References (115)

1. Wierenga RK, de Jong RJ, Kalk K.H., Hol WGJ, Drenth J. Crystal structure of p-hydroxybenzoate hydroxylase. J Mol Biol 1979; 131: 55-73.
2. Schreuder HA, van der Laan JM, Hol WGJ, Drenth J. Crystal structure of p-hydroxybenzoate hydroxylase complexed with its reaction product 3,4-dihydroxybenzoate. J Mol Biol 1988; 199: 637-48.
3. Silverman RB, Hoffman SJ, Catus WB. A mechanism for mitochondrial monoamine oxidase catalyzed amine oxidation. J Am Chem Soc 1980; 102: 7126-8.
4. Edmondson D.E. Aminium cation radical mechanism proposed for monoamine oxidase B catalysis: are there alternatives? Xenobiotica 1995; 25: 735-53.
5. Kim J-M, Bogdan M.A., Mariano PS. Mechanistic analysis of the 3-methyllumiflavin-promoted oxidative deamination of benzylamine. A potential model for monoamine oxidase catalysis. J Am Chem Soc 1993; 115: 10591-5.
6. Fitzpatrick PF. Oxidation of amines by flavoproteins. Arch Biochem Biophys 2010; 493: 13-25.
7. Walker MC, Edmondson D.E. Structure-activity relationships in the oxidation of benzylamine analogues by bovine liver mitochondrial monoamine oxidase B. Biochemistry 1994; 33: 7088-98.
8. Edmondson D.E., Bhattacharyya AK, Walker MC. Spectral and kinetic studies of imine product formation in the oxidation of p-(N, N-dimethylamino) benzylamine analogues by monoamine oxidase B. Biochemistry 1993; 32: 5196-202.
9. Bach AW, Lan NC, Johnson DL, Abell CW, Bembenek ME, Kwan SW, Seeburg PH, Shih JC. cDNA cloning of human liver monoamine oxidase A and B: molecular basis of differences in enzymatic properties. Proc Natl Acad Sci USA 1988; 85: 4934-8.
10. Fowler CJ, Benedetti MS. The metabolism of dopamine by both forms of monoamine oxidase in the rat brain and its inhibition by cimoxatone. J Neurochem 1983; 40: 1534-41.
11. McCauley R, Racker E. Separation of two monoamine oxidases from bovine bran. Mol Cell Biochem 1973; 1: 73-81.
12. Yang H-TT, Neff NH. b-Phenethylamine: a specific substrate for type B monoamine oxidase of brain. J Pharmacol Exp Ther 1973; 187: 365-71.
13. Hall DWR, Logan BW, Parsons GH. Further studies on the inhibition of monoamine oxidase by M and B 9302 (clorgyline)-I: substrate specificity in various mammalian species. Biochem Pharmacol 1969; 18: 1447-54.
14. Chiba K, Trevor A, Castagnoli N. Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine oxidase. Biochem Biophys Res Commun 1984; 120: 574-8.
15. Cesura AM, Pletscher A. The new generation of monoamine oxidase inhibitors. Prog Drug Res 1992; 38: 171-297.
16. Youdim MBH, Edmondson D, Tipton KF. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 2006; 7: 295-309.
17. Ma J, Yoshimura M, Yamashita E, Nakagawa A, Ito A, Tsukihara T. Structure of rat monoamine oxidase A and its specific recognitions for substrates and inhibitors. J Mol Biol 2004; 338: 103-14.
18. Binda C, Newton-Vinson P, Hubalek F, Edmondson D.E., Mattevi A. Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders. Nat Struct Biol 2002; 9: 22-6.
19. Upadhyay AK, Borbat PP, Wang J, Freed JH, Edmondson D.E. Determination of the Oligomeric States of Human and Rat Monoamine Oxidases in the Outer Mitochondrial Membrane and Octyl b-d-Glucopyranoside Micelles Using Pulsed Dipolar Electron Spin Resonance Spectroscopy. Biochemistry 2008; 47: 1554-66.
20. De Colibus L, Li M, Binda C, Lustig A, Edmondson D.E., Mattevi A. Three-dimensional structure of human monoamine oxidase A (MAO A): relation to the structures of rat M.A.O A and human M.A.O B. Proc Natl Acad Sci USA 2005; 102: 12684-9.
21. Rebrin I, Geha RM, Chen K, Shih JC. Effects of carboxylterminal truncations on the activity and solubility of human monoamine oxidase B. J Biol Chem 2001; 276: 29499-506.
22. Binda C, Li M, Hubalek F, Restelli N, Edmondson D, Mattevi A. Insights into the mode of inhibition of human mitochondrial monoamine oxidase B from high-resolution crystal structures. Proc Natl Acad Sci USA 2003; 100: 9750-5.
23. Nandigama RK, Miller J.R., Edmondson D. Loss of serotonin oxidation as a component of the altered substrate specificity in the Y444F mutant of recombinant human liver M.A.O A. Biochemistry 2001; 40: 14839-46.
24. Li M, Binda C, Mattevi A, Edmondson D.E. Functional role of the aromatic cage in human monoamine oxidase B: structures and catalytic properties of Tyr435 mutant proteins. Biochemistry 2006; 45: 4775-84.
25. Geha RM, Chen K, Wouters J, Ooms F, Shih JC. Analysis of conserved active site residues in monoamine oxidase A and B and their three-dimensional molecular modeling. J Biol Chem 2002; 277: 17209-16.
26. Alieva I, Mustafayeva N, Gojayev N. Conformation analysis of the N-terminal sequence Met1-Val60 of the tyrosine hydroxylase. J Mol Struct 2006; 785: 76-84.
27. Binda C, Wang J, Li M, Hubalek F, Mattevi A, Edmondson D.E. Structural and mechanistic studies of arylalkylhydrazine inhibition of human monoamine oxidases A and B. Biochemistry 2008; 47: 5616-25.
28. Edmondson D.E., Binda C, Mattevi A. Structural insights into the mechanism of amine oxidation by monoamine oxidases A and B. Arch Biochem Biophys 2007; 464: 269-76.
29. Hubaek F, Binda C, Khalil A, Li M, Mattevi A, Castagnoli N, Edmondson D.E. Demonstration of isoleucine 199 as a structural determinant for the selective inhibition of human monoamine oxidase B by specific reversible inhibitors. J Biol Chem 2005; 280: 15761-6.
30. Son S-Y, Ma J, Kondou Y, Yoshimura M, Yamashita E, Tsukihara T. Structure of human monoamine oxidase A at 2.2-Aresolution: the control of opening the entry for substrates/ inhibitors. Proc Natl Acad Sci USA 2008; 105: 5739-44.
31. Miller J.R., Edmondson D.E. Structure-activity relationships in the oxidation of para-substituted benzylamine analogues by recombinant human liver monoamine oxidase A. Biochemistry 1999; 38: 13670-83.
32. Dunn RV, Marshall KR, Munro AW, Scrutton NS. The pH dependence of kinetic isotope effects in monoamine oxidase A indicates stabilization of the neutral amine in the enzymesubstrate complex. FEBS J 2008; 275: 3850-8.
33. Nandigama RK, Edmondson D.E. Structure-activity relations in the oxidation of phenethylamine analogues by recombinant human liver monoamine oxidase A. Biochemistry 2000; 39: 15258-65.
34. Pretorius A, Ogunrombi MO, TerreBlanche G, Castagnoli Jr N, Bergh JJ, Petzer JP. Deuterium isotope effects for the oxidation of 1-methyl-3-phenyl-3-pyrrolinyl analogues by monoamine oxidase B. Biorg Med Chem 2008; 16: 8813-7.
35. Silverman RB. Effect of a-methylation on inactivation of monoamine oxidase by N-cyclopropylbenzylamine. Biochemistry 1984; 23: 5206-13.
36. Silverman RB, Zieske PA. Mechanism of inactivation of monoamine oxidase by 1-phenylcyclopropylamine. Biochemistry 1985; 24: 2128-38.
37. Silverman RB, Hoffman SJ. Mechanism of inactivation of mitochondrial monoamine oxidase by N-cyclopropyl-N-arylalkyl amines. J Am Chem Soc 1980; 102: 884-6.
38. Yue KT, Bhattacharyya AK, Zhelyaskov VR, Edmondson D.E. Resonance Raman Spectroscopic Evidence for an Anionic Flavin Semiquinone in Bovine Liver Monoamine Oxidase. Arch Biochem Biophys 1993; 300: 178-85.
39. DeRose VJ, Woo JCG, Hawe WP, Hoffman BM, Silverman RB, Yelekci K. Observation of a flavin semiquinone in the resting state of monoamine oxidase B by electron paramagnetic resonance and electron nuclear double resonance spectroscopy. Biochemistry 1996; 35: 11085-91.
40. Sablin SO, Ramsay RR. Substrates but not inhibitors alter the redox potentials of monoamine oxidases. Antioxid Redox Signal 2001; 3: 723-9.
41. Rigby SE, Hynson RM, Ramsay RR, Munro AW, Scrutton NS. A stable tyrosyl radical in monoamine oxidase A. J Biol Chem 2005; 280: 4627-31.
42. Royo M, Fitzpatrick PF. Mechanistic studies of mouse polyamine oxidase with N1, N12-bisethylspermine as a substrate. Biochemistry 2005; 44: 7079-84.
43. Jaffe HH. Theoretical Considerations Concerning Hammetts Equation. IV. Calculation of r-Values. J Chem Phys 1953; 21: 415-9.
44. Peters FB, Johnson HW, Jr. Ionization constants of substituted 2-aminoacetanilides and benzylamines. Transmission of electronic effects through amide links. J Org Chem 1975; 40: 1517-9.
45. Eberlein G, Bruice TC. The chemistry of a 1,5-diblocked flavin. Proton and electron transfer steps in the reaction of dihydroflavins with oxygen. J Am Chem Soc 1983; 105: 6685-97.
46. Massey V. Activation of molecular oxygen by flavins and flavoproteins. J Biol Chem 1994; 269: 22459-62.
47. Roth JP, Klinman JP. Catalysis of electron transfer during the activation of O2 by the flavoprotein glucose oxidase. Proc Natl Acad Sci USA 2003; 100: 62-7.
48. Jorns MS, Chen Z-W, Mathews FS. Structural Characterization of Mutations at the Oxygen Activation Site in Monomeric Sarcosine Oxidase. Biochemistry 2010; 49: 3631-9.
49. Zhao G, Bruckner RC, Jorns MS. Identification of the oxygen activation site in monomeric sarcosine oxidase: role of Lys265 in catalysis. Biochemistry 2008; 47: 9124-35.
50. Tabor CW, Tabor H. Polyamines. Ann Rev Biochem 1984; 53: 749-90.
51. Hu RH, Pegg AE. Rapid induction of apoptosis by deregulated uptake of polyamine analogues. Biochem J 1997; 328: 307-16.
52. Casero RA, Woster PM. Recent advances in the development of polyamine analogues as antitumor agents. J Med Chem 2009; 52: 4551-73.
53. Porter CW. Effect of polyamine analogues and inhibition of polyamine oxidase on spermidine/spermine N1-acetyltransferase activity and cell proliferation. Anticancer Res 1986; 6: 525-42.
54. Marton LJ, Pegg AE. Polyamines as targets for therapeutic intervention. Ann Rev Pharmacol Toxicol 1995; 35: 55-91.
55. Holtta E. Oxidation of spermidine and spermine in rat liver: purification and properties of polyamine oxidase. Biochemistry 1977; 16: 91-100.
56. Wu T, Yankovskaya V, McIntire WS. Cloning, sequencing, and heterologous expression of the murine peroxisomal flavoprotein, N1-acetylated polyamine oxidase. J Biol Chem 2003; 278: 20514-25.
57. Federico R, Ercolini L, Laurenzi M, Angelini R. Oxidation of acetylpolyamines by maize polyamine oxidase. Phytochemistry 1996; 43: 339-41.
58. Kim BG. Polyamine metabolism in Acanthamoeba: polyamine content and synthesis of ornithine, putrescine, and diaminopropane. J Protozoology 1987; 34: 728-84.
59. Wang Y, Murray-Stewart T, Devereux W, Hacker A, Frydman B, Woster PM, Casero RA, Jr. Properties of purified recombinant human polyamine oxidase, PAOh1/SMO. Biochem Biophys Res Commun 2003; 304: 605-11.
60. Cervelli M, Polticelli F, Federico R, Mariottini P. Heterologous expression and characterization of mouse spermine oxidase. J Biol Chem 2003; 278: 5271-6.
61. Wang Y, Devereux W, Woster PM, Stewart TM, Hacker A, Casero RA, Jr. Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure. Cancer Res 2001; 61: 5370-3.
62. Pledgie A, Huang Y, Hacker A, Zhang Z, Woster PM, Davidson NE, Casero RA, Jr. Spermine oxidase SMO(PAOh1), not N1-acetylpolyamine oxidase PAO, is the primary source of cytotoxic H2O2 in polyamine analogue-treated human breast cancer cell lines. J Biol Chem 2005; 280: 39843-51.
63. Ha HC, Woster PM, Yager JD, Casero RA, Jr. The role of polyamine catabolism in polyamine analogue-induced programmed cell death. Proc Natl Acad Sci USA 1997; 94: 11557-62.
64. Babbar N, Casero RA, Jr. Tumor necrosis factor-a increases reactive oxygen species by inducing spermine oxidase in human lung epithelial cells: a potential mechanism for inflammation-induced carcinogenesis. Cancer Res 2006; 66: 11125-30.
65. Tavladoraki P, Schininá ME, Cecconi F, Di Agostino S, Manera F, Rea G, Mariottini P, Federico R, Angelini R. Maize polyamine oxidase: primary structure from protein and cDNA sequencing. FEBS Lett 1998; 426: 62-6.
66. Binda C, Coda A, Angelini R, Federico R, Ascenzi P, Mattevi A. A 30 Along U-shaped catalytic tunnel in the crystal structure of polyamine oxidase. Structure 1999; 7: 265-76.
67. Binda C, Angelini R, Federico R, Ascenzi P, Mattevi A. Structural bases for inhibitor binding and catalysis in polyamine oxidase. Biochemistry 2001; 40: 2766-76.
68. Landry J, Sternglanz R. Yeast Fms1 is a FAD-utilizing polyamine oxidase. Biochem Biophys Res Commun 2003; 303: 771-6.
69. Huang Q, Liu Q, Hao Q. Crystal structures of Fms1 and its complex with spermine reveal substrate specificity. J Mol Biol 2005; 348: 951-9.
70. Bianchi M, Polticelli F, Ascenzi P, Botta M, Federico R, Mariottini P, Cona A. Inhibition of polyamine and spermine oxidases by polyamine analogues. FEBS J 2006; 273: 1115-23.
71. Adachi MS, Torres JM, Fitzpatrick PF. Mechanistic studies of the yeast polyamine oxidase Fms1: kinetic mechanism, substrate specificity, and pH dependence. Biochemistry 2010; 49: 10440-8.
72. Adachi MS, Juarez PR, Fitzpatrick PF. Mechanistic studies of human spermine oxidase: kinetic mechanism and pH effects. Biochemistry 2010; 49: 386-92.
73. Henderson Pozzi M, Gawandi V, Fitzpatrick PF. pH dependence of a mammalian polyamine oxidase: insights into substrate specificity and the role of lysine 315. Biochemistry 2009; 48: 1508-16.
74. Henderson Pozzi M, Gawandi V, Fitzpatrick PF. Mechanistic studies of para-substituted N, N9-dibenzyl-1,4-diaminobutanes as substrates for a mammalian polyamine oxidase. Biochemistry 2009; 48: 12305-13.
75. Polticelli F, Basran J, Faso C, Cona A, Minervini G, Angelini R, Federico R, Scrutton NS, Tavladoraki P. Lys300 plays a major role in the catalytic mechanism of maize polyamine oxidase. Biochemistry 2005; 44: 16108-20.
76. Henderson Pozzi M, Fitzpatrick PF. A lysine conserved in the monoamine oxidase family is involved in oxidation of the reduced flavin in mouse polyamine oxidase. Arch Biochem Biophys 2010; 498: 83-8.
77. Pawelek PD, Cheah J, Coulombe R, Macheroux P, Ghisla S, Vrielink A. The structure of L-amino acid oxidase reveals the substrate trajectory into an enantiomerically conserved active site. EMBO J 2000; 19: 4204-15.
78. Moustafa IM, Foster S, Lyubimov AY, Vrielink A. Crystal structure of LAAO from Calloselasma rhodostoma with an Lphenylalanine substrate: insights into structure and mechanism. J Mol Biol 2006; 364: 991-1002.
79. Faust A, Niefind K, Hummel W, Schomburg D. The structure of a bacterial L-amino acid oxidase from Rhodococcus opacus gives new evidence for the hydride mechanism for dehydrogenation. J Mol Biol 2007; 367: 234-48.
80. Curti B, Ronchi S, Simonetta MP. D-and L-amino acid oxidases. In: Müler F, editor. Chemistry and Biochemistry of flavoenzymes, Vol. III. Boca Raton: CRC Press, 1991: 69-94.
81. Fitzpatrick PF. Substrate dehydrogenation by flavoproteins. Acc Chem Res 2001; 34: 299-307.
82. Fitzpatrick PF. Carbanion versus hydride transfer mechanisms in flavoprotein-catalyzed dehydrogenations. Bioorg Chem 2004; 32: 125-39.
83. Magie AR, Wilson EE, Kosuge T. Indoleacetamide as an intermediate in the synthesis of indoleacetic acid in Pseudomonas savastanoi. Science 1963; 141: 1281-82.
84. Thomashow MF, Hugly S, Buchholz WG, Thomashow LS. Molecular basis for the auxin-independent phenotype of crown gall tumor tissues. Science 1986; 231: 616-8.
85. Sobrado P, Fitzpatrick PF. Analysis of the roles of amino acid residues in the flavoprotein tryptophan 2-monooxygenase modified by 2-oxo-3-pentynoate: characterization of His338, Cys339, and Cys511 mutant enzymes. Arch Biochem Biophys 2002; 402: 24-30.
86. Sobrado P, Fitzpatrick P. Analysis of the role of the active site residue Arg98 in the flavoprotein tryptophan 2-monooxygenase, a member of the L-amino oxidase family. Biochemistry 2003; 42: 13826-32.
87. Sobrado P, Fitzpatrick PF. Identification of Tyr413 as an active site residue in the flavoprotein tryptophan 2-monooxygenase and analysis of its contribution to catalysis. Biochemistry 2003; 42: 13833-8.
88. Emanuele JJ Jr., Fitzpatrick PF. Mechanistic studies of the flavoprotein tryptophan 2-monooxygenase. 1. Kinetic mechanism. Biochemistry 1995; 34: 3710-5.
89. Emanuele JJ Jr., Fitzpatrick PF. Mechanistic studies of the flavoprotein tryptophan 2-monooxygenase. 2. pH and kinetic isotope effects. Biochemistry 1995; 34: 3716-23.
90. Ralph EC, Anderson M.A., Cleland WW, Fitzpatrick PF. Mechanistic studies of the flavoenzyme tryptophan 2-monooxygenase: deuterium and 15N kinetic isotope effects on alanine oxidation by an L-amino acid oxidase. Biochemistry 2006; 45: 15844-52.
91. Ralph EC, Hirschi JS, Anderson M.A., Cleland WW, Singleton D.A., Fitzpatrick PF. Insights into the mechanism of flavoprotein-catalyzed amine oxidation from nitrogen isotope effects on the reaction of N-methyltryptophan oxidase. Biochemistry 2007; 46: 7655-64.
92. Shi Y, Lan F, Matson C, Mulligan P, Whetstine J.R., Cole PA, Casero RA. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004; 119: 941-53.
93. Forneris F, Binda C, Vanoni M.A., Mattevi A, Battaglioli E. Histone demethylation catalysed by LSD1 is a flavin-dependent oxidative process. FEBS Lett 2005; 579: 2203-7.
94. Huang J, Sengupta R, Espejo AB, Lee MG, Dorsey JA, Richter M, Opravil S, Shiekhattar R, Bedford MT, Jenuwein T, Berger SL. p53 is regulated by the lysine demethylase LSD1. Nature 2007; 449: 105-8.
95. Zhu X, Wang J, Ju BG, Rosenfeld MG. Signaling and epigenetic regulation of pituitary development. Curr Opin Cell Biol 2007; 19: 605-11.
96. Su ST, Ying HY, Chiu YK, Lin FR, Chen MY, Lin KI. Involvement of histone demethylase LSD1 in Blimp-1-mediated gene repression during plasma cell differentiation. Mol Cell Biol 2009; 29: 1421-31.
97. Saleque S, Kim J, Rooke HM, Orkin SH. Epigenetic Regulation of Hematopoietic Differentiation by Gfi-1 and Gfi-1b Is Mediated by the Cofactors CoREST and LSD1. Mol Cell 2007; 27: 562-72.
98. Hakimi M-A, Bochar D.A., Chenoweth J, Lane WS, Mandel G, Shiekhattar R. A core-BRAF35 complex containing histone deacetylase mediates repression of neuronal-specific genes. Proc Natl Acad Sci USA 2002; 99: 7420-5.
99. Schulte JH, 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, Kirfel J. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy. Cancer Res 2009; 69: 2065-71.
100. Kahl P, Gullotti L, Heukamp LC, Wolf S, Friedrichs N, Vorreuther R, Solleder G, Bastian PJ, Ellinger J, Metzger E, Schule R, Buettner R. Androgen receptor coactivators lysinespecific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res 2006; 66: 11341-7.
101. Culhane JC, Szewczuk LM, Liu X, Da G, Marmorstein R, Cole PA. A mechanism-based inactivator for histone demethylase LSD1. J Am Chem Soc 2006; 128: 4536-7.
102. Szewczuk LM, Culhane JC, Yang M, Majumdar A, Yu H, Cole PA. Mechanistic analysis of a suicide inactivator of histone demethylase LSD1. Biochemistry 2007; 46: 6892-902.
103. Yang M, Gocke CB, Luo X, Borek D, Tomchick DR, Machius M, Otwinowski Z, Yu H. Structural basis for CoRESTdependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol Cell 2006; 23: 377-87.
104. Gooden DM, Schmidt DMZ, Pollock JA, Kabadi AM, McCafferty DG. Facile synthesis of substituted trans-2-arylcyclopropylamine inhibitors of the human histone demethylase LSD1 and monoamine oxidases A and B. Bioorg Med Chem Lett 2008; 18: 3047-51.
105. Schmidt DMZ, McCafferty DG. trans-2-Phenylcyclopropylamine is a mechanism-based inactivator of the histone demethylase LSD1. Biochemistry 2007; 46: 4408-16.
106. Lee MG, Wynder C, Schmidt DM, McCafferty DG, Shiekhattar R. Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications Chem Biol 2006; 13: 563-7.
107. Forneris F, Binda C, Adamo A, Battaglioli E, Mattevi A. Structural basis of LSD1-CoREST selectivity in histone H3 recognition. J Biol Chem 2007; 282: 20070-4.
108. Chen Y, Yang Y, Wang F, Wan K, Yamane K, Zhang Y, Lei M. Crystal structure of human histone lysine-specific demethylase 1 (LSD1). Proc Natl Acad Sci USA 2006; 103: 13956-61.
109. Da G, Lenkart J, Zhao K, Shiekhattar R, Cairns BR, Marmorstein R. Structure and function of the SWIRM domain, a conserved protein module found in chromatin regulatory complexes. Proc Natl Acad Sci USA 2006; 103: 2057-62.
110. Stavropoulos P, Blobel G, Hoelz A. Crystal structure and mechanism of human lysine-specific demethylase-1. Nat Struct Mol Biol 2006; 13: 626-32.
111. Metzger E, Wissmann M, Yin N, Muller JM, Schneider R, Peters AHFM, Gunther T, Buettner R, Schule R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005; 437: 436-9.
112. Mimasu S, Sengoku T, Fukuzawa S, Umehara T, Yokoyama S. Crystal structure of histone demethylase LSD1 and tranylcypromine at 2.25 A. Biochem Biophys Res Commun 2008; 366: 15-22.
113. Forneris F, Battaglioli E, Mattevi A, Binda C. New roles of flavoproteins in molecular cell biology: histone demethylase LSD1 and chromatin. FEBS J 2009; 276: 4304-12.
114. Gaweska H, Henderson Pozzi M, Schmidt DMZ, McCafferty DG, Fitzpatrick PF. Use of pH and kinetic isotope effects to establish chemistry as rate-limiting in oxidation of a peptide substrate by LSD1. Biochemistry 2009; 48: 5440-5.
115. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605-12.