The solution structure of the regulatory domain of tyrosine hydroxylase

Journal of Molecular Biology

Volumn 426, Issue 7, 2014, Pages 1483-1497

  Zhang, Shengnan ^a   Huang, Tao ^a   Ilangovan, Udayar ^a   Hinck, Andrew P ^a   Fitzpatrick, Paul F ^a  

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

Author keywords

ACT domain; NMR spectroscopy; regulation; solution structure; tyrosine hydroxylase

Indexed keywords

CATECHOLAMINE; DIMER; HOMODIMER; MONOMER; PHENYLALANINE 4 MONOOXYGENASE; SERINE; TYROSINE 3 MONOOXYGENASE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME STRUCTURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; STRUCTURE ANALYSIS; ANIMAL EXPERIMENT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NUCLEAR OVERHAUSER EFFECT; PROTEIN EXPRESSION; PROTEIN QUATERNARY STRUCTURE;

RATTUS;

ACT DOMAIN; NMR SPECTROSCOPY; REGULATION; SOLUTION STRUCTURE; TYROSINE HYDROXYLASE;

MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; TYROSINE 3-MONOOXYGENASE;

EID: 84895920698     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.12.015     Document Type: Article

References (86)

1. F. Rao, K. Zhang, L. Zhang, B. Rana, J. Wessel, and M. Fung et al. Human tyrosine hydroxylase natural allelic variation: influence on autonomic function and hypertension Cell Mol Neurobiol 30 2010 1391 1394
2. G.F. Hoffmann, B. Assmann, C. Brautigam, C. Dionisi-Vici, M. Haussler, and J.B. de Klerk et al. Tyrosine hydroxylase deficiency causes progressive encephalopathy and dopa-nonresponsive dystonia Ann Neurol 54 2003 S56 S65
3. B. Ludecke, B. Dworniczak, and K. Bartholome A point mutation in the tyrosine hydroxylase gene associated with Segawa's syndrome Hum Genet 95 1995 123 125
4. P.F. Fitzpatrick Tetrahydropterin-dependent amino acid hydroxylases Ann Rev Biochem 68 1999 355 381
5. D.L. Lohse, and P.F. Fitzpatrick Identification of the intersubunit binding region in rat tyrosine hydroxylase Biochem Biophys Res Commun 197 1993 1543 1548
6. S.C. Daubner, D.L. Lohse, and P.F. Fitzpatrick Expression and characterization of catalytic and regulatory domains of rat tyrosine hydroxylase Protein Sci 2 1993 1452 1460
7. K.E. Goodwill, C. Sabatier, C. Marks, R. Raag, P.F. Fitzpatrick, and R.C. Stevens Crystal structure of tyrosine hydroxylase at 2.3 Å and its implications for inherited neurodegenerative diseases Nat Struct Biol 4 1997 578 585
8. B. Kobe, I.G. Jennings, C.M. House, B.J. Michell, K.E. Goodwill, and B.D. Santarsiero et al. Structural basis of autoregulation of phenylalanine hydroxylase Nat Struct Biol 6 1999 442 448
9. L. Wang, H. Erlandsen, J. Haavik, P.M. Knappskog, and R.C. Stevens Three-dimensional structure of human tryptophan hydroxylase and its implications for the biosynthesis of the neurotransmitters serotonin and melatonin Biochemistry 41 2002 12569 12574
10. P.F. Fitzpatrick Mechanism of aromatic amino acid hydroxylation Biochemistry 42 2003 14083 14091
11. T. Xia, D.W. Gray, and R. Shiman Regulation of rat liver phenylalanine hydroxylase. III. Control of catalysis by (6R)-tetrahydrobiopterin and phenylalanine J Biol Chem 269 1994 24657 24665
12. P.F. Fitzpatrick Allosteric regulation of phenylalanine hydroxylase Arch Biochem Biophys 519 2012 194 201
13. J.W. Haycock Phosphorylation of tyrosine hydroxylase in situ at serine 8, 19, 31, and 40 J Biol Chem 265 1990 11682 11691
14. S.C. Daubner, T. Le, and S. Wang Tyrosine hydroxylase and regulation of dopamine synthesis Arch Biochem Biophys 508 2011 1 12
15. A.J. Ramsey, and P.F. Fitzpatrick Effects of phosphorylation of serine 40 of tyrosine hydroxylase on binding of catecholamines: evidence for a novel regulatory mechanism Biochemistry 37 1998 8980 8986
16. L.R.M. Bevilaqua, M.E. Graham, P.R. Dunkley, E.I. von Nagy-Felsobuki, and P.W. Dickson Phosphorylation of Ser19 alters the conformation of tyrosine hydroxylase to increase the rate of phosphorylation of Ser40 J Biol Chem 276 2001 40411 40416
17. K. Toska, R. Kleppe, C.G. Armstrong, N.A. Morrice, P. Cohen, and J. Haavik Regulation of tyrosine hydroxylase by stress-activated protein kinases J Neurochem 83 2002 775 783
18. S. Wang, M. Lasagna, S.C. Daubner, G.D. Reinhart, and P.F. Fitzpatrick Fluorescence spectroscopy as a probe of the effect of phosphorylation at Ser40 of tyrosine hydroxylase on the conformation of its regulatory domain Biochemistry 50 2011 2364 2370
19. S. Wang, G.R. Sura, L.J. Dangott, and P.F. Fitzpatrick Identification by hydrogen/deuterium exchange of structural changes in tyrosine hydroxylase associated with regulation Biochemistry 48 2009 4972 4979
20. R.I. McCulloch, and P.F. Fitzpatrick Limited proteolysis of tyrosine hydroxylase identifies residues 33-50 as conformationally sensitive to phosphorylation state and dopamine binding Arch Biochem Biophys 367 1999 143 145
21. A.J. Ramsey, and P.F. Fitzpatrick Effects of phosphorylation on binding of catecholamines to tyrosine hydroxylase: specificity and thermodynamics Biochemistry 39 2000 773 778
22. J.P. Loria, M. Rance, and A.G. Palmer Transverse-relaxation-optimized (TROSY) gradient-enhanced triple-resonance NMR spectroscopy J Magn Reson 141 1999 180 184
23. M. Salzmann, G. Wider, K. Pervushin, H. Senn, and K. Wuthrich TROSY-type triple-resonance experiments for sequential NMR assignments of large proteins J Am Chem Soc 121 1999 844 848
24. H.R. Eghbalnia, L. Wang, A. Bahrami, A. Assadi, and J.L. Markley Protein energetic conformational analysis from NMR chemical shifts (PECAN) and its use in determining secondary structural elements J Biomol NMR 32 2005 71 81
25. 2H-labeled proteins: application to a 37-kDa Trp repressor-DNA complex J Am Chem Soc 116 1994 6464 6465
26. 13C enriched proteins J Biomol NMR 1 1991 99 104
27. M. Wittekind, and L. Mueller HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins J Magn Reson B 101 1993 201 205
28. 15N-enriched proteins J Biomol NMR 3 1993 185 204
29. 13C magnetization J Magn Reson B 101 1993 114 119
30. 2O samples of proteins J Magn Reson B 101 1993 333 337
31. 2O J Magn Reson B 102 1993 317 321
32. C. Zwahlen, P. Legault, S.J.F. Vincent, J. Greenblatt, R. Konrat, and L.E. Kay Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage λ N-peptide/boxB RNA complex J Am Chem Soc 119 1997 6711 6721
33. 2 symmetry J Am Chem Soc 119 1997 5958 5959
34. D. Ivanov, J.R. Stone, J.L. Maki, T. Collins, and G. Wagner Mammalian SCAN domain dimer is a domain-swapped homolog of the HIV capsid C-terminal domain Mol Cell 17 2005 137 143
35. J.P. Linge, S.I. O'Donoghue, and M. Nilges Automated assignment of ambiguous nuclear Overhauser effects with ARIA Methods Enzymol 339 2001 71 90
36. G. Cornilescu, F. Delaglio, and A. Bax Protein backbone angle restraints from searching a database for chemical shift and sequence homology J Biomol NMR 13 1999 289 302
37. M. Ottiger, F. Delaglio, and A. Bax Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra J Magn Reson 131 1998 373 378
38. A. Bax, G. Kontaxis, and N. Tjandra Dipolar couplings in macromolecular structure determination Methods Enzymol 339 2001 127 174
39. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J Biomol NMR 8 1996 477 486
40. 15N NMR relaxation J Am Chem Soc 117 1995 12562 12566
41. A.M. Mandel, M. Akke, and A.G. Palmer Backbone dynamics of Escherichia coli ribonuclease Hi - correlations with structure and function in an active enzyme J Mol Biol 246 1995 144 163
42. A. Ota, S. Yoshida, and T. Nagatsu Deletion mutagenesis of human tyrosine hydroxylase type 1 regulatory domain Biochem Biophys Res Commun 213 1995 1099 1106
43. S.C. Daubner, and M.M. Piper Deletion mutants of tyrosine hydroxylase identify a region critical for heparin binding Protein Sci 4 1995 538 541
44. I. Alieva, N. Mustafayeva, and N. Gojayev Conformation analysis of the N-terminal sequence Met1-Val60 of the tyrosine hydroxylase J Mol Struct 785 2006 76 84
45. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, and E.C. Meng et al. UCSF Chimera - a visualization system for exploratory research and analysis J Comput Chem 25 2004 1605 1612
46. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, and H. McWilliam et al. Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
47. J. Li, U. Ilangovan, S.C. Daubner, A.P. Hinck, and P.F. Fitzpatrick Direct evidence for a phenylalanine site in the regulatory domain of phenylalanine hydroxylase Arch Biochem Biophys 505 2011 250 255
48. G.A. Grant The ACT domain: a small molecule binding domain and its role as a common regulatory element J Biol Chem 281 2006 33825 33829
49. D.M. Chipman, and B. Shaanan The ACT domain family Curr Opin Struct Biol 11 2001 694 700
50. L. Aravind, and E.V. Koonin Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches J Mol Biol 287 1999 1023 1040
51. R.D. Finn, J. Mistry, J. Tate, P. Coggill, A. Heger, and J.E. Pollington et al. The Pfam protein families database Nucleic Acids Res 38 2010 D211 D222
52. N. Sträter, G. Schnappauf, G. Braus, and W.N. Lipscomb Mechanisms of catalysis and allosteric regulation of yeast chorismate mutase from crystal structures Structure 5 1997 1437 1452
53. R. Al-Rabiee, Y. Zhang, and G.A. Grant The mechanism of velocity modulated allosteric regulation in d-3-phosphoglycerate dehydrogenase: site-directed mutagenesis of effector binding site residues J Biol Chem 271 1996 23235 23238
54. max-type cooperative enzyme phosphoglycerate dehydrogenase Nat Struct Biol 2 1995 69 76
55. C. Mas-Droux, G. Curien, M. Robert-Genthon, M. Laurencin, J.-L. Ferrer, and R. Dumas A novel organization of ACT domains in allosteric enzymes revealed by the crystal structure of Arabidopsis aspartate kinase Plant Cell 18 2006 1681 1692
56. P.M. Leonard, S.H.J. Smits, S.E. Sedelnikova, A.B. Brinkman, W.M. de Vos, and J. van der Oost et al. Crystal structure of the Lrp-like transcriptional regulator from the archaeon Pyrococcus furiosus EMBO J 20 2001 990 997
57. Y. Devedjiev, Y. Surendranath, U. Derewenda, A. Gabrys, D.R. Cooper, and R.-G. Zhang et al. The structure and ligand binding properties of the B. subtilis YkoF gene product, a member of a novel family of thiamin/HMP-binding proteins J Mol Biol 343 2004 395 406
58. A. Kaplun, M. Vyazmensky, Y. Zherdev, I. Belenky, A. Slutzker, and S. Mendel et al. Structure of the regulatory subunit of acetohydroxyacid synthase isozyme III from Escherichia coli J Mol Biol 357 2006 951 963
59. E.K. Jaffe, L. Stith, S.H. Lawrence, M. Andrake, and R.L. Dunbrack A new model for allosteric regulation of phenylalanine hydroxylase: implications for disease and therapeutics Arch Biochem Biophys 530 2013 73 82
60. S.C. Daubner, A. Avila, J.O. Bailey, D. Barrera, J.Y. Bermudez, and D.H. Giles et al. Mutagenesis of a specificity-determining residue in tyrosine hydroxylase establishes that the enzyme is a robust phenylalanine hydroxylase but a fragile tyrosine hydroxylase Biochemistry 52 2013 1446 1455
61. T. Solstad, A.J. Stokka, O.A. Andersen, and T. Flatmark Studies on the regulatory properties of the pterin cofactor and dopamine bound at the active site of human phenylalanine hydroxylase Eur J Biochem 270 2003 981 990
62. H. Erlandsen, M.G. Patch, A. Gamez, M. Straub, and R.C. Stevens Structural studies on phenylalanine hydroxylase and implications toward understanding and treating phenylketonuria Pediatrics 112 2003 1557 1565
63. F. Fusetti, H. Erlandsen, T. Flatmark, and R.C. Stevens Structure of tetrametic human phenylalanine hydroxylase and its implications for phenylketonuria J Biol Chem 273 1998 16962 16967
64. D.B. Fisher, and S. Kaufman The stimulation of rat liver phenylalanine hydroxylase by lysolecithin and α-chymotrypsin J Biol Chem 248 1973 4345 4353
65. P.M. Knappskog, T. Flatmark, J.M. Aarden, J. Haavik, and A. Martinez Structure/function relationships in human phenylalanine hydroxylase. Effect of terminal deletions on the oligomerization, activation and cooperativity of substrate binding to the enzyme Eur J Biochem 242 1996 813 821
66. S.C. Daubner, P.J. Hillas, and P.F. Fitzpatrick Expression and characterization of the catalytic domain of human phenylalanine hydroxylase Arch Biochem Biophys 348 1997 295 302
67. J. Li, L.J. Dangott, and P.F. Fitzpatrick Regulation of phenylalanine hydroxylase: conformational changes upon phenylalanine binding detected by hydrogen/deuterium exchange and mass spectrometry Biochemistry 49 2010 3327 3335
68. S. Wang Identification of structural changes related to the regulation of tyrosine hydroxylase (PhD Thesis) 2010 Texas A&M University College Station
69. J. Cao, F. Shi, X. Liu, G. Huang, and M. Zhou Phylogenetic analysis and evolution of aromatic amino acid hydroxylase FEBS Lett 584 2010 4775 4782
70. J. Siltberg-Liberles, I.H. Steen, R.M. Svebak, and A. Martinez The phylogeny of the aromatic amino acid hydroxylases revisited by characterizing phenylalanine hydroxylase from Dictyostelium discoideum Gene 427 2008 86 92
71. J. Marley, M. Lu, and C. Bracken A method for efficient isotopic labeling of recombinant proteins J Biomol NMR 20 2001 71 75
72. D.A. Flockhart, and J.D. Corbin Preparation of the catalytic subunit of cAMP-dependent protein kinase P.J. Maranos, I.C. Campbell, R.M. Cohen, Brain Receptor Methodologies, Part A 1984 Academic Press New York 209 215
73. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on UNIX pipes J Biomol NMR 6 1995 277 293
74. B.A. Johnson Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol Biol 278 2004 313 352
75. L.E. Kay, M. Ikura, R. Tschudin, and A. Bax Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins J Magn Reson 89 1990 496 514
76. 13C-labelled proteins J Magn Reson 97 1992 213 217
77. G.W. Vuister, and A. Bax Measurement of four-bond HN-H alpha J-couplings in staphylococcal nuclease J Biomol NMR 4 1994 193 200
78. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve et al. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr Sect D Biol Crystallogr 54 1998 905 921
79. 2 values in proteins J Magn Reson 97 1992 359 375
80. 15N relaxation with monomer/dimer equilibration J Mol Biol 266 1997 173 194
81. D.I. Freedberg, R. Ishima, J. Jacob, Y.X. Wang, I. Kustanovich, and J.M. Louis et al. Rapid structural fluctuations of the free HIV protease flaps in solution: relationship to crystal structures and comparison with predictions of dynamics calculations Protein Sci 11 2002 221 232
82. 15N relaxation using inverse detected two-dimensional NMR-spectroscopy - the central helix is flexible Biochemistry 31 1992 5269 5278
83. V. Copie, Y. Tomita, S.K. Akiyama, S. Aota, K.M. Yamada, and R.M. Venable et al. Solution structure and dynamics of linked cell attachment modules of mouse fibronectin containing the RGD and synergy regions: comparison with the human fibronectin crystal structure J Mol Biol 277 1998 663 682
84. G. Lipari, and A. Szabo Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity J Am Chem Soc 104 1982 4546 4559
85. G.M. Clore, A. Szabo, A. Bax, L.E. Kay, P.C. Driscoll, and A.M. Gronenborn Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins J Am Chem Soc 112 1990 4989 4991
86. A. Fiser, R.K.G. Do, and A. Šali Modeling of loops in protein structures Protein Sci 9 2000 1753 1773