ATP binding to human serine racemase is cooperative and modulated by glycine

FEBS Journal

Volumn 280, Issue 22, 2013, Pages 5853-5863

  Marchetti, Marialaura ^a   Bruno, Stefano ^a   Campanini, Barbara ^a   Peracchi, Alessio ^a   Mai, Nicole ^a   Mozzarelli, Andrea ^a,b  

^a UNIVERSITY OF PARMA   (Italy)

^b NATIONAL INSTITUTE OF BIOSTRUCTURES AND BIOSYSTEMS   (Italy)

Author keywords

allostery; ATP; cooperativity; d serine; enzyme regulation; fluorescence; neuropathologies; NMDA receptor; PLP; serine racemase

Indexed keywords

ADENOSINE TRIPHOSPHATE; DEXTRO SERINE; GLYCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RACEMASE; SERINE RACEMASE; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; DISSOCIATION CONSTANT; ENZYME ACTIVE SITE; PRIORITY JOURNAL; PROTEIN STABILITY; RACEMIZATION;

ALLOSTERY; ATP; COOPERATIVITY; D-SERINE; ENZYME REGULATION; FLUORESCENCE; NEUROPATHOLOGIES; NMDA RECEPTOR; PLP; SERINE RACEMASE;

ADENOSINE TRIPHOSPHATE; ALLOSTERIC SITE; CATALYTIC DOMAIN; ENZYME STABILITY; GLYCINE; HUMANS; KINETICS; LIGANDS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION; RACEMASES AND EPIMERASES; RECEPTORS, N-METHYL-D-ASPARTATE; SERINE; SPECTROMETRY, FLUORESCENCE; STEREOISOMERISM;

EID: 84886598971     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12510     Document Type: Article

References (67)

1. Wolosker H, (2007) NMDA receptor regulation by d -serine: new findings and perspectives. Mol Neurobiol 36, 152-164.
2. Martineau M, Baux G, &, Mothet JP, (2006) d -serine signalling in the brain: friend and foe. Trends Neurosci 29, 481-491.
3. Boehning D, &, Snyder SH, (2003) Novel neural modulators. Annu Rev Neurosci 26, 105-131.
4. Wolosker H, Dumin E, Balan L, &, Foltyn VN, (2008) d -amino acids in the brain: d -serine in neurotransmission and neurodegeneration. FEBS J 275, 3514-3526.
5. Johnson JW, &, Ascher P, (1987) Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
6. Papouin T, Ladepeche L, Ruel J, Sacchi S, Labasque M, Hanini M, Groc L, Pollegioni L, Mothet JP, &, Oliet SH, (2012) Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633-646.
7. Henneberger C, Bard L, King C, Jennings A, &, Rusakov DA, (2013) NMDA receptor activation: two targets for two co-agonists. Neurochem Res 38, 1156-1162.
8. Rosenberg D, Artoul S, Segal AC, Kolodney G, Radzishevsky I, Dikopoltsev E, Foltyn VN, Inoue R, Mori H, Billard JM, et al,. (2013) Neuronal d -serine and glycine release via the Asc-1 transporter regulates NMDA receptor-dependent synaptic activity. J Neurosci 33, 3533-3544.
9. Kessler M, Terramani T, Lynch G, &, Baudry M, (1989) A glycine site associated with N-methyl- d -aspartic acid receptors: characterization and identification of a new class of antagonists. J Neurochem 52, 1319-1328.
10. Passera E, Campanini B, Rossi F, Casazza V, Rizzi M, Pellicciari R, &, Mozzarelli A, (2011) Human kynurenine aminotransferase II-reactivity with substrates and inhibitors. FEBS J 278, 1882-1900.
11. Labrie V, Wong AH, &, Roder JC, (2012) Contributions of the d -serine pathway to schizophrenia. Neuropharmacology 62, 1484-1503.
12. Ma TM, Abazyan S, Abazyan B, Nomura J, Yang C, Seshadri S, Sawa A, Snyder SH, &, Pletnikov MV, (2013) Pathogenic disruption of DISC1-serine racemase binding elicits schizophrenia-like behavior via d -serine depletion. Mol Psychiatry 18, 557-567.
13. Mustafa AK, Ahmad AS, Zeynalov E, Gazi SK, Sikka G, Ehmsen JT, Barrow RK, Coyle JT, Snyder SH, &, Dore S, (2010) Serine racemase deletion protects against cerebral ischemia and excitotoxicity. J Neurosci 30, 1413-1416.
14. Campanini B, Spyrakis F, Peracchi A, &, Mozzarelli A, (2013) Serine racemase: a key player in neuron activity and in neuropathologies. Front Biosci 18, 1112-1128.
15. Wolosker H, Blackshaw S, &, Snyder SH, (1999) Serine racemase: a glial enzyme synthesizing d -serine to regulate glutamate-N-methyl- d -aspartate neurotransmission. Proc Natl Acad Sci USA 96, 13409-13414.
16. Ding X, Ma N, Nagahama M, Yamada K, &, Semba R, (2011) Localization of d -serine and serine racemase in neurons and neuroglias in mouse brain. Neurol Sci 32, 263-267.
17. Benneyworth MA, Li Y, Basu AC, Bolshakov VY, &, Coyle JT, (2012) Cell selective conditional null mutations of serine racemase demonstrate a predominate localization in cortical glutamatergic neurons. Cell Mol Neurobiol 32, 613-624.
18. Ito T, Maekawa M, Hayashi S, Goto M, Hemmi H, &, Yoshimura T, (2013) Catalytic mechanism of serine racemase from Dictyostelium discoideum. Amino Acids 44, 1073-1084.
19. De Miranda J, Panizzutti R, Foltyn VN, &, Wolosker H, (2002) Cofactors of serine racemase that physiologically stimulate the synthesis of the N-methyl- d -aspartate (NMDA) receptor coagonist d -serine. Proc Natl Acad Sci USA 99, 14542-14547.
20. Foltyn VN, Bendikov I, De Miranda J, Panizzutti R, Dumin E, Shleper M, Li P, Toney MD, Kartvelishvily E, &, Wolosker H, (2005) Serine racemase modulates intracellular d-serine levels through an α, β-elimination activity. J Biol Chem 280, 1754-1763.
21. Yoshimura T, &, Goto M, (2008) d -amino acids in the brain: structure and function of pyridoxal phosphate-dependent amino acid racemases. FEBS J 275, 3527-3537.
22. Hoffman HE, Jiraskova J, Ingr M, Zvelebil M, &, Konvalinka J, (2009) Recombinant human serine racemase: enzymologic characterization and comparison with its mouse ortholog. Protein Expr Purif 63, 62-67.
23. Pollegioni L, &, Sacchi S, (2010) Metabolism of the neuromodulator d -serine. Cell Mol Life Sci 67, 2387-2404.
24. Sacchi S, Caldinelli L, Cappelletti P, Pollegioni L, &, Molla G, (2012) Structure-function relationships in human d -amino acid oxidase. Amino Acids 43, 1833-1850.
25. Wolosker H, (2011) Serine racemase and the serine shuttle between neurons and astrocytes. Biochim Biophys Acta 1814, 1558-1566.
26. Jiraskova-Vanickova J, Ettrich R, Vorlova B, Hoffman HE, Lepsik M, Jansa P, &, Konvalinka J, (2011) Inhibition of human serine racemase, an emerging target for medicinal chemistry. Curr Drug Targets 12, 1037-1055.
27. Foltyn VN, Zehl M, Dikopoltsev E, Jensen ON, &, Wolosker H, (2010) Phosphorylation of mouse serine racemase regulates d -serine synthesis. FEBS Lett 584, 2937-2941.
28. Wolosker H, &, Mori H, (2012) Serine racemase: an unconventional enzyme for an unconventional transmitter. Amino Acids 43, 1895-1904.
29. Neidle A, &, Dunlop DS, (2002) Allosteric regulation of mouse brain serine racemase. Neurochem Res 27, 1719-1724.
30. Mustafa AK, Kumar M, Selvakumar B, Ho GP, Ehmsen JT, Barrow RK, Amzel LM, &, Snyder SH, (2007) Nitric oxide S-nitrosylates serine racemase, mediating feedback inhibition of d -serine formation. Proc Natl Acad Sci USA 104, 2950-2955.
31. + ATPase in mammalian astrocytes. Glia 21, 35-45.
32. + channels. J Physiol 544, 429-445.
33. Goto M, Yamauchi T, Kamiya N, Miyahara I, Yoshimura T, Mihara H, Kurihara T, Hirotsu K, &, Esaki N, (2009) Crystal structure of a homolog of mammalian serine racemase from Schizosaccharomyces pombe. J Biol Chem 284, 25944-25952.
34. Peracchi A, &, Mozzarelli A, (2011) Exploring and exploiting allostery: models, evolution, and drug targeting. Biochim Biophys Acta 1814, 922-933.
35. Eaton WA, Henry ER, Hofrichter J, Bettati S, Viappiani C, &, Mozzarelli A, (2007) Evolution of allosteric models for hemoglobin. IUBMB Life 59, 586-599.
36. Changeux JP, (2012) Allostery and the Monod-Wyman-Changeux model after 50 years. Annu Rev Biophys 41, 103-133.
37. Nussinov R, &, Tsai CJ, (2013) Allostery in disease and in drug discovery. Cell 153, 293-305.
38. Cui Q, &, Karplus M, (2008) Allostery and cooperativity revisited. Protein Sci 17, 1295-1307.
39. Spyrakis F, Felici P, Bayden AS, Salsi E, Miggiano R, Kellogg GE, Cozzini P, Cook PF, Mozzarelli A, &, Campanini B, (2013) Fine tuning of the active site modulates specificity in the interaction of O-acetylserine sulfhydrylase isozymes with serine acetyltransferase. Biochim Biophys Acta 1834, 169-181.
40. Salsi E, Campanini B, Bettati S, Raboni S, Roderick SL, Cook PF, &, Mozzarelli A, (2010) A two-step process controls the formation of the bienzyme cysteine synthase complex. J Biol Chem 285, 12813-12822.
41. Salsi E, Bayden AS, Spyrakis F, Amadasi A, Campanini B, Bettati S, Dodatko T, Cozzini P, Kellogg GE, Cook PF, et al,. (2010) Design of O-acetylserine sulfhydrylase inhibitors by mimicking nature. J Med Chem 53, 345-356.
42. Matsui T, Sekiguchi M, Hashimoto A, Tomita U, Nishikawa T, &, Wada K, (1995) Functional comparison of d -serine and glycine in rodents: the effect on cloned NMDA receptors and the extracellular concentration. J Neurochem 65, 454-458.
43. Horio M, Kohno M, Fujita Y, Ishima T, Inoue R, Mori H, &, Hashimoto K, (2011) Levels of d -serine in the brain and peripheral organs of serine racemase (Srr) knock-out mice. Neurochem Int 59, 853-859.
44. 1H-MRS at 3 T: application in brain tumors. Magn Reson Med 66, 609-618.
45. Monod J, Wyman J, &, Changeaux JP, (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12, 88-118.
46. Ellerby LM, Nishida CR, Nishida F, Yamanaka SA, Dunn B, Valentine JS, &, Zink JI, (1992) Encapsulation of proteins in transparent porous silicate glasses prepared by the sol-gel method. Science 255, 1113-1115.
47. Shibayama N, &, Saigo S, (2001) Direct observation of two distinct affinity conformations in the T state human deoxyhemoglobin. FEBS Lett 492, 50-53.
48. Bettati S, &, Mozzarelli A, (1997) T state hemoglobin binds oxygen noncooperatively with allosteric effects of protons, inositol hexaphosphate, and chloride. J Biol Chem 272, 32050-32055.
49. Bruno S, Bonaccio M, Bettati S, Rivetti C, Viappiani C, Abbruzzetti S, &, Mozzarelli A, (2001) High and low oxygen affinity conformations of T state hemoglobin. Protein Sci 10, 2401-2407.
50. Ronda L, Bruno S, Viappiani C, Abbruzzetti S, Mozzarelli A, Lowe KC, &, Bettati S, (2006) Circular dichroism spectroscopy of tertiary and quaternary conformations of human hemoglobin entrapped in wet silica gels. Protein Sci 15, 1961-1967.
51. Abbruzzetti S, Viappiani C, Bruno S, Bettati S, Bonaccio M, &, Mozzarelli A, (2001) Functional characterization of heme proteins encapsulated in wet nanoporous silica gels. J Nanosci Nanotechnol 1, 407-415.
52. Ronda L, Bruno S, Faggiano S, Bettati S, &, Mozzarelli A, (2008) Oxygen binding to heme proteins in solution, encapsulated in silica gels, and in the crystalline state. Methods Enzymol 437, 311-328.
53. Viappiani C, Bettati S, Bruno S, Ronda L, Abbruzzetti S, Mozzarelli A, &, Eaton WA, (2004) New insights into allosteric mechanisms from trapping unstable protein conformations in silica gels. Proc Natl Acad Sci USA 101, 14414-14419.
54. Samuni U, Dantsker D, Juszczak LJ, Bettati S, Ronda L, Mozzarelli A, &, Friedman JM, (2004) Spectroscopic and functional characterization of T state hemoglobin conformations encapsulated in silica gels. Biochemistry 43, 13674-13682.
55. West JM, &, Kantrowitz ER, (2003) Trapping specific quaternary states of the allosteric enzyme aspartate transcarbamoylase in silica matrix sol-gels. J Am Chem Soc 125, 9924-9925.
56. 2 complex. FEBS Lett 579, 2197-2202.
57. Chirico G, Cannone F, Beretta S, Diaspro A, Campanini B, Bettati S, Ruotolo R, &, Mozzarelli A, (2002) Dynamics of green fluorescent protein mutant2 in solution, on spin-coated glasses, and encapsulated in wet silica gels. Protein Sci 11, 1152-1161.
58. Campanini B, Bologna S, Cannone F, Chirico G, Mozzarelli A, &, Bettati S, (2005) Unfolding of Green Fluorescent Protein mut2 in wet nanoporous silica gels. Protein Sci 14, 1125-1133.
59. Conti P, Tamborini L, Pinto A, Blondel A, Minoprio P, Mozzarelli A, &, De Micheli C, (2011) Drug discovery targeting amino acid racemases. Chem Rev 111, 6919-6946.
60. Amadasi A, Bertoldi M, Contestabile R, Bettati S, Cellini B, di Salvo ML, Borri-Voltattorni C, Bossa F, &, Mozzarelli A, (2007) Pyridoxal 5′-phosphate enzymes as targets for therapeutic agents. Curr Med Chem 14, 1291-1324.
61. Billard JM, (2013) Serine racemase as a prime target for age-related memory deficits. Eur J Neurosci 37, 1931-1938.
62. Dixon SM, Li P, Liu R, Wolosker H, Lam KS, Kurth MJ, &, Toney MD, (2006) Slow-binding human serine racemase inhibitors from high-throughput screening of combinatorial libraries. J Med Chem 49, 2388-2397.
63. de Marco A, Vigh L, Diamant S, &, Goloubinoff P, (2005) Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid- or benzyl alcohol-overexpressed molecular chaperones. Cell Stress Chaperones 10, 329-339.
64. Molla G, Piubelli L, Volonte F, &, Pilone MS, (2012) Enzymatic detection of d -amino acids. Methods Mol Biol 794, 273-289.
65. Campanini B, Speroni F, Salsi E, Cook PF, Roderick SL, Huang B, Bettati S, &, Mozzarelli A, (2005) Interaction of serine acetyltransferase with O-acetylserine sulfhydrylase active site: evidence from fluorescence spectroscopy. Protein Sci 14, 2115-2124.
66. Copeland RA, (2000) Enzymes: A Practical Introduction to Structure, Mechanism, and Data Analysis. Wiley-VCH Inc, New York, USA.
67. Smith MA, Mack V, Ebneth A, Moraes I, Felicetti B, Wood M, Schonfeld D, Mather O, Cesura A, &, Barker J, (2010) The structure of mammalian serine racemase: evidence for conformational changes upon inhibitor binding. J Biol Chem 285, 12873-12881.