Novel human D-amino acid oxidase inhibitors stabilize an active-site lid-open conformation

Bioscience Reports

Volumn 34, Issue 4, 2014, Pages 487-499

  Terry Lorenzo, Ryan T ^a   Chun, Lawrence E ^b   Brown, Scott P ^a   Heffernan, Michele L R ^a   Fang, Q Kevin ^a   Orsini, Michael A ^a   Pollegioni, Loredano ^c   Hardy, Larry W ^a   Spear, Kerry L ^a   Large, Thomas H ^a  

^a DAINIPPON SUMITOMO PHARMA CO LTD   (Japan)

^b Emerald BioSystems   (United States)

^c UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

Crystallography; DAAO; DAO; Drug discovery; NMDA receptor; Schizophrenia

Indexed keywords

CARRIER PROTEIN; DEXTRO AMINO ACID OXIDASE; ENZYME INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SERINE;

ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYME ACTIVE SITE; HUMAN; METABOLISM; SCHIZOPHRENIA;

CARRIER PROTEINS; CATALYTIC DOMAIN; D-AMINO-ACID OXIDASE; ENZYME INHIBITORS; HUMANS; RECEPTORS, N-METHYL-D-ASPARTATE; SCHIZOPHRENIA; SERINE;

EID: 84906830915     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20140071     Document Type: Article

References (45)

1. Pollegioni, L. and Sacchi, S. (2010) Metabolism of the neuromodulator D-serine. Cell. Mol. Life Sci. 67, 2387-2404 CrossRef PubMed
2. Sacchi, S., Caldinelli, L., Cappelletti, P., Pollegioni, L. and Molla, G. (2012) Structure-function relationships in human D-amino acid oxidase. Amino Acids 43, 1833-1850 CrossRef PubMed
3. Konno, R., Sasaki, M., Asakura, S., Fukui, K., Enami, J. and Niwa, A. (1997) D-amino-acid oxidase is not present in the mouse liver. Biochim. Biophys. Acta 1335, 173-181 CrossRef PubMed (Pubitemid 27174518)
4. Konno, R., Niwa, A. and Yasumura, Y. (1990) Intestinal bacterial origin of D-alanine in urine of mutant mice lacking D-amino-acid oxidase. Biochem. J. 268, 263-265 PubMed (Pubitemid 20193960)
5. Hashimoto, A., Nishikawa, T., Hayashi, T., Fujii, N., Harada, K., Oka, T. and Takahashi, K. (1992) The presence of free D-serine in rat brain. FEBS Lett. 296, 33-36 CrossRef PubMed
6. Hashimoto, A., Oka, T. and Nishikawa, T. (1995) Extracellular concentration of endogenous free D-serine in the rat brain as revealed by in vivo microdialysis. Neuroscience 66, 635-643 CrossRef PubMed
7. Panatier, A., Theodosis, D. T., Mothet, J. P., Touquet, B., Pollegioni, L., Poulain, D. A. and Oliet, S. H. (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775-784 CrossRef PubMed
8. Henneberger, C., Papouin, T., Oliet, S. H. and Rusakov, D. A. (2010) Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236 CrossRef PubMed
9. Papouin, T., Ladepeche, L., Ruel, J., Sacchi, S., Labasque, M., Hanini, M., Groc, L., Pollegioni, L., Mothet, J. P. and Oliet, S. H. (2012) Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633-646 CrossRef PubMed
10. Zhou, Q. and Sheng, M. (2013) NMDA receptors in nervous system diseases. Neuropharmacology 74, 69-75 CrossRef PubMed
11. Wolosker, H. (2011) Serine racemase and the serine shuttle between neurons and astrocytes. Biochim. Biophys. Acta 1814, 1558-1566 CrossRef PubMed
12. Verrall, L., Burnet, P. W., Betts, J. F. and Harrison, P. J. (2010) The neurobiology of D-amino acid oxidase and its involvement in schizophrenia. Mol. Psychiatry 15, 122-137 CrossRef PubMed
13. Hopkins, S. C., Heffernan, M. L., Saraswat, L. D., Bowen, C. A., Melnick, L., Hardy, L. W., Orsini, M. A., Allen, M. S., Koch, P., Spear, K. L. et al. (2013) Structural, kinetic, and pharmacodynamic mechanisms of D-amino acid oxidase inhibition by small molecules. J. Med. Chem. 56, 3710-3724 CrossRef PubMed
14. Strick, C. A., Li, C., Scott, L., Harvey, B., Hajos, M., Steyn, S. J., Piotrowski, M. A., James, L. C., Downs, J. T., Rago, B. et al. (2011) Modulation of NMDA receptor function by inhibition of D-amino acid oxidase in rodent brain. Neuropharmacology 61, 1001-1015 CrossRef PubMed
15. Maekawa, M., Watanabe, M., Yamaguchi, S., Konno, R. and Hori, Y. (2005) Spatial learning and long-term potentiation of mutant mice lacking D-amino-acid oxidase. Neurosci. Res. 53, 34-38 CrossRef PubMed (Pubitemid 41073725)
16. Almond, S. L., Fradley, R. L., Armstrong, E. J., Heavens, R. B., Rutter, A. R., Newman, R. J., Chiu, C. S., Konno, R., Hutson, P. H. and Brandon, N. J. (2006) Behavioral and biochemical characterization of a mutant mouse strain lacking D-amino acid oxidase activity and its implications for schizophrenia. Mol. Cell Neurosci. 32, 324-334 CrossRef PubMed (Pubitemid 44163228)
17. Basu, A. C., Tsai, G. E., Ma, C. L., Ehmsen, J. T., Mustafa, A. K., Han, L., Jiang, Z. I., Benneyworth, M. A., Froimowitz, M. P., Lange, N. et al. (2009) Targeted disruption of serine racemase affects glutamatergic neurotransmission and behavior. Mol. Psychiatry 14, 719-727 CrossRef PubMed
18. Balu, D. T., Li, Y., Puhl, M. D., Benneyworth, M. A., Basu, A. C., Takagi, S., Bolshakov, V. Y. and Coyle, J. T. (2013) Multiple risk pathways for schizophrenia converge in serine racemase knockout mice, a mouse model of NMDA receptor hypofunction. Proc. Natl. Acad. Sci. U. S. A. 110, E2400-E2409 CrossRef PubMed
19. Kantrowitz, J. T. and Javitt, D. C. (2010) N-methyl-d-aspartate (NMDA) receptor dysfunction or dysregulation: the final common pathway on the road to schizophrenia? Brain Res. Bull. 83, 108-121 CrossRef PubMed
20. Lisman, J. E., Coyle, J. T., Green, R. W., Javitt, D. C., Benes, F. M., Heckers, S. and Grace, A. A. (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci. 31, 234-242 CrossRef PubMed
21. Ferraris, D., Duvall, B., Ko, Y. S., Thomas, A. G., Rojas, C., Majer, P., Hashimoto, K. and Tsukamoto, T. (2008) Synthesis and biological evaluation of D-amino acid oxidase inhibitors. J. Med. Chem. 51, 3357-3359 CrossRef PubMed (Pubitemid 351874993)
22. Duplantier, A. J., Becker, S. L., Bohanon, M. J., Borzilleri, K. A., Chrunyk, B. A., Downs, J. T., Hu, L. Y., El-Kattan, A., James, L. C., Liu, S. et al. (2009) Discovery, SAR, and pharmacokinetics of a novel 3-hydroxyquinolin- 2(1H)-one series of potent D-amino acid oxidase (DAAO) inhibitors. J. Med. Chem. 52, 3576-3585 CrossRef PubMed
23. Hopkins, S. C., Zhao, F. Y., Bowen, C. A., Fang, X., Wei, H., Heffernan, M. L., Spear, K. L., Spanswick, D. C., Varney, M. A. and Large, T. H. (2013) Pharmacodynamic effects of a D-amino acid oxidase inhibitor indicate a spinal site of action in rat models of neuropathic pain. J. Pharmacol. Exp. Therap. 345, 502-511 CrossRef
24. Zhao, W. J., Gao, Z. Y., Wei, H., Nie, H. Z., Zhao, Q., Zhou, X. J. and Wang, Y. X. (2010) Spinal D-amino acid oxidase contributes to neuropathic pain in rats. J. Pharmacol. Exp. Therap. 332, 248-254 CrossRef
25. Lu, J. M., Gong, N., Wang, Y. C. and Wang, Y. X. (2012) D-Amino acid oxidase-mediated increase in spinal hydrogen peroxide is mainly responsible for formalin-induced tonic pain. Br. J. Pharmacol. 165, 1941-1955 CrossRef PubMed
26. Sacchi, S., Rosini, E., Pollegioni, L. and Molla, G. (2013) D-amino acid oxidase inhibitors as a novel class of drugs for schizophrenia therapy. Curr. Pharm. Des. 19, 2499-2511 CrossRef PubMed
27. Sparey, T., Abeywickrema, P., Almond, S., Brandon, N., Byrne, N., Campbell, A., Hutson, P. H., Jacobson, M., Jones, B., Munshi, S. et al. (2008) The discovery of fused pyrrole carboxylic acids as novel, potent D-amino acid oxidase (DAO) inhibitors. Bioorg. Med. Chem. Lett. 18, 3386-3391 CrossRef PubMed (Pubitemid 351718313)
28. Todone, F., Vanoni, M. A., Mozzarelli, A., Bolognesi, M., Coda, A., Curti, B. and Mattevi, A. (1997) Active site plasticity in D-amino acid oxidase: a crystallographic analysis. Biochemistry 36, 5853-5860 CrossRef PubMed (Pubitemid 27214937)
29. Kawazoe, T., Tsuge, H., Imagawa, T., Aki, K., Kuramitsu, S. and Fukui, K. (2007) Structural basis of D-DOPA oxidation by D-amino acid oxidase: alternative pathway for dopamine biosynthesis. Biochem. Biophys. Res. Commun. 355, 385-391 CrossRef PubMed (Pubitemid 46282639)
30. Hondo, T., Warizaya, M., Niimi, T., Namatame, I., Yamaguchi, T., Nakanishi, K., Hamajima, T., Harada, K., Sakashita, H., Matsumoto, Y. et al. (2013) 4-Hydroxypyridazin-3(2H)-one derivatives as novel D-amino acid oxidase inhibitors. J. Med. Chem. 56, 3582-3592 CrossRef PubMed
31. Raje, M., Hin, N., Duvall, B., Ferraris, D. V., Berry, J. F., Thomas, A. G., Alt, J., Rojas, C., Slusher, B. S. and Tsukamoto, T. (2013) Synthesis of kojic acid derivatives as secondary binding site probes of D-amino acid oxidase. Bioorg. Med. Chem. Lett. 23, 3910-3913 CrossRef PubMed
32. Molla, G., Sacchi, S., Bernasconi, M., Pilone, M. S., Fukui, K. and Pollegioni, L. (2006) Characterization of human D-amino acid oxidase. FEBS Lett. 580, 2358-2364 CrossRef PubMed
33. Caldinelli, L., Molla, G., Sacchi, S., Pilone, M. S. and Pollegioni, L. (2009) Relevance of weak flavin binding in human D-amino acid oxidase. Protein Sci. 18, 801-810 PubMed
34. Yagi, K., Ozawa, T. and Nagatsu, T. (1960) Mechanism of inhibition of D-amino acid oxidase. IV. Inhibitory action of chlorpromazine. Biochim. Biophys. Acta 43, 310-317 CrossRef PubMed
35. Sacchi, S., Bernasconi, M., Martineau, M., Mothet, J. P., Ruzzene, M., Pilone, M. S., Pollegioni, L. and Molla, G. (2008) pLG72 modulates intracellular D-serine levels through its interaction with D-amino acid oxidase: effect on schizophrenia susceptibility. J. Biol. Chem. 283, 22244-22256 CrossRef PubMed
36. Brandish, P. E., Chiu, C. S., Schneeweis, J., Brandon, N. J., Leech, C. L., Kornienko, O., Scolnick, E. M., Strulovici, B. and Zheng, W. (2006) A cell-based ultra-high-throughput screening assay for identifying inhibitors of D-amino acid oxidase. J. Biomol. Screen 11, 481-487 CrossRef PubMed (Pubitemid 44222999)
37. Frattini, L. F., Piubelli, L., Sacchi, S., Molla, G. and Pollegioni, L. (2011) Is rat an appropriate animal model to study the involvement of D-serine catabolism in schizophrenia? Insights from characterization of D-amino acid oxidase. FEBS J. 278, 4362-4373 CrossRef PubMed
38. Copeland, R. A., Basavapathruni, A., Moyer, M. and Scott, M. P. (2011) Impact of enzyme concentration and residence time on apparent activity recovery in jump dilution analysis. Anal. Biochem. 416, 206-210 CrossRef PubMed
39. Kawazoe, T., Tsuge, H., Pilone, M. S. and Fukui, K. (2006) Crystal structure of human D-amino acid oxidase: context-dependent variability of the backbone conformation of the VAAGL hydrophobic stretch located at the Si-face of the flavin ring. Protein Sci. 15, 2708-2717 CrossRef PubMed (Pubitemid 44833752)
40. Berry, J. F., Ferraris, D. V., Duvall, B., Hin, N., Rais, R., Alt, J., Thomas, A. G., Rojas, C., Hashimoto, K., Slusher, B. S. and Tsukamoto, T. (2012) Synthesis and SAR of 1-hydroxy-1H-benzo[d]imidazole-2(3H)-ones as inhibitors of D-amino acid oxidase. ACS Med. Chem. Lett. 3, 839-843 CrossRef PubMed
41. Di, L., Rong, H. and Feng, B. (2013) Demystifying brain penetration in central nervous system drug discovery. Miniperspective. J. Med. Chem. 56, 2-12 CrossRef
42. Pollegioni, L., Caldinelli, L., Molla, G., Sacchi, S. and Pilone, M. S. (2004) Catalytic properties of D-amino acid oxidase in cephalosporin C bioconversion: a comparison between proteins from different sources. Biotechnol. Prog. 20, 467-473 CrossRef PubMed (Pubitemid 38459154)
43. Caligiuri, A., D'Arrigo, E., Rosini, E., Tessaro, D., Molla, G., Servi, S. and Pollegioni, L. (2006) Enzymatic conversion of unnatural amino acids by yeast D-amino acid oxidase. Adv. Synth. Catal. 348, 2183-2190 CrossRef (Pubitemid 44662646)
44. 2. Proc. Natl. Acad. Sci. U. S. A. 93, 7496-7501 CrossRef PubMed
45. Setoyama, C., Nishina, Y., Mizutani, H., Miyahara, I., Hirotsu, K., Kamiya, N., Shiga, K. and Miura, R. (2006) Engineering the substrate specificity of porcine kidney D-amino acid oxidase by mutagenesis of the 'active-site lid'. J. Biochem. 139, 873-879 CrossRef PubMed (Pubitemid 44014581)