The Amino Acid Specificity for Activation of Phenylalanine Hydroxylase Matches the Specificity for Stabilization of Regulatory Domain Dimers

Biochemistry

Volumn 54, Issue 33, 2015, Pages 5167-5174

  Zhang, Shengnan ^a   Hinck, Andrew P ^a   Fitzpatrick, Paul F ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; DIMERIZATION; ENZYMES; MAGNETIC DOMAINS; MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ALLOSTERIC ACTIVATION; ANALYTICAL ULTRACENTRIFUGATION; D-PHENYLALANINE; ENZYME SUPPORTS; L-ISOLEUCINE; L-PHENYLALANINE; PHENYLALANINE HYDROXYLASE; REGULATORY DOMAIN;

AMINO ACIDS;

4 AMINOPHENYLALANINE; AMINO ACID; DEXTRO PHENYLALANINE; DIMER; HYDROCINNAMIC ACID; ISOLEUCINE; LEUCINE; METHIONINE; NORLEUCINE; PHENYLALANINE; PHENYLALANINE 4 MONOOXYGENASE; PROPANOL; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; DIMERIZATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; ULTRACENTRIFUGATION; ALLOSTERISM; ANIMAL; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYME SPECIFICITY; ENZYME STABILITY; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RAT;

ALLOSTERIC REGULATION; ANIMALS; ENZYME ACTIVATION; ENZYME STABILITY; PHENYLALANINE; PHENYLALANINE HYDROXYLASE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RATS; SUBSTRATE SPECIFICITY;

EID: 84939617405     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00616     Document Type: Article

References (42)

1. Fitzpatrick, P. F. (1999) Tetrahydropterin-dependent amino acid hydroxylases Annu. Rev. Biochem. 68, 355-381 10.1146/annurev.biochem.68.1.355
2. Kobe, B., Jennings, I. G., House, C. M., Michell, B. J., Goodwill, K. E., Santarsiero, B. D., Stevens, R. C., Cotton, R. G. H., and Kemp, B. E. (1999) Structural basis of autoregulation of phenylalanine hydroxylase Nat. Struct. Biol. 6, 442-448 10.1038/8247
3. Goodwill, K. E., Sabatier, C., Marks, C., Raag, R., Fitzpatrick, P. F., and Stevens, R. C. (1997) Crystal structure of tyrosine hydroxylase at 2.3 Å and its implications for inherited neurodegenerative diseases Nat. Struct. Biol. 4, 578-585 10.1038/nsb0797-578
4. Wang, L., Erlandsen, H., Haavik, J., Knappskog, P. M., and Stevens, R. C. (2002) Three-dimensional structure of human tryptophan hydroxylase and its implications for the biosynthesis of the neurotransmitters serotonin and melatonin Biochemistry 41, 12569-12574 10.1021/bi026561f
5. Fitzpatrick, P. F. (2003) Mechanism of aromatic amino acid hydroxylation Biochemistry 42, 14083-14091 10.1021/bi035656u
6. Zhang, S., Huang, T., Ilangovan, U., Hinck, A. P., and Fitzpatrick, P. F. (2014) The solution structure of the regulatory domain of tyrosine hydroxylase J. Mol. Biol. 426, 1483-1497 10.1016/j.jmb.2013.12.015
7. Grant, G. A. (2006) The ACT domain: a small molecule binding domain and its role as a common regulatory element J. Biol. Chem. 281, 33825-33829 10.1074/jbc.R600024200
8. Xia, T., Gray, D. W., and Shiman, R. (1994) Regulation of rat liver phenylalanine hydroxylase. III. Control of catalysis by (6R)-tetrahydrobiopterin and phenylalanine J. Biol. Chem. 269, 24657-24665
9. Fitzpatrick, P. F. (2012) Allosteric regulation of phenylalanine hydroxylase Arch. Biochem. Biophys. 519, 194-201 10.1016/j.abb.2011.09.012
10. Haycock, J. W. (1990) Phosphorylation of tyrosine hydroxylase in situ at serine 8, 19, 31, and 40 J. Biol. Chem. 265, 11682-11691
11. Daubner, S. C., Le, T., and Wang, S. (2011) Tyrosine hydroxylase and regulation of dopamine synthesis Arch. Biochem. Biophys. 508, 1-12 10.1016/j.abb.2010.12.017
12. Flydal, M. I. and Martlnez, A. (2013) Phenylalanine hydroxylase: Function, structure, and regulation IUBMB Life 65, 341-349 10.1002/iub.1150
13. Knappskog, P. M., Flatmark, T., Aarden, J. M., Haavik, J., and Martinez, A. (1996) 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, 813-821 10.1111/j.1432-1033.1996.0813r.x
14. Shiman, R., Jones, S. H., and Gray, D. W. (1990) Mechanism of phenylalanine regulation of phenylalanine hydroxylase J. Biol. Chem. 265, 11633-11642
15. Phillips, R. S., Parniak, M. A., and Kaufman, S. (1984) Spectroscopic investigation of ligand interaction with hepatic phenylalanine hydroxylase: Evidence for a conformational change associated with activation Biochemistry 23, 3836-3842 10.1021/bi00312a007
16. Kowlessur, D., Yang, X.-J., and Kaufman, S. (1995) Further studies of the role of Ser-16 in the regulation of the activity of phenylalanine hydroxylase Proc. Natl. Acad. Sci. U. S. A. 92, 4743-4747 10.1073/pnas.92.11.4743
17. Døskeland, A. P., Martinez, A., Knappskog, P. M., and Flatmark, T. (1996) Phosphorylation of recombinant human phenylalanine hydroxylase: Effect on catalytic activity, substrate activation and protection against non-specific cleavage of the fusion protein by restriction protease Biochem. J. 313, 409-414 10.1042/bj3130409
18. Shiman, R., Mortimore, G. E., Schworer, C. M., and Gray, D. W. (1982) Regulation of phenylalanine hydroxylase activity by phenylalanine in vivo, in vitro, and in perfused rat liver J. Biol. Chem. 257, 11213-11216
19. Jennings, I. G., Teh, T., and Kobe, B. (2001) Essential role of the N-terminal autoregulatory sequence in the regulation of phenylalanine hydroxylase FEBS Lett. 488, 196-200 10.1016/S0014-5793(00)02426-1
20. Thorolfsson, M., Ibarra-Molero, B., Fojan, P., Petersen, S. B., Sanchez-Ruiz, J. M., and Martinez, A. (2002) L-Phenylalanine binding and domain organization in human phenylalanine hydroxylase: a differential scanning calorimetry study Biochemistry 41, 7573-7585 10.1021/bi0160720
21. Flydal, M. I., Mohn, T. C., Pey, A. L., Siltberg-Liberles, J., Teigen, K., and Martinez, A. (2010) Superstoichiometric binding of L-Phe to phenylalanine hydroxylase from Caenorhabditis elegans: evolutionary implications Amino Acids 39, 1463-1475 10.1007/s00726-010-0611-6
22. Shiman, R. and Gray, D. W. (1980) Substrate activation of phenylalanine hydroxylase. A kinetic characterizaion J. Biol. Chem. 255, 4793-4800
23. Shiman, R., Xia, T., Hill, M. A., and Gray, D. W. (1994) Regulation of rat liver phenylalanine hydroxylase. II. Substrate binding and the role of activation in the control of enzymatic activity J. Biol. Chem. 269, 24647-24656
24. Zhang, S., Roberts, K. M., and Fitzpatrick, P. F. (2014) Phenylalanine binding is linked to dimerization of the regulatory domain of phenylalanine hydroxylase Biochemistry 53, 6625-6627 10.1021/bi501109s
25. Li, J., Ilangovan, U., Daubner, S. C., Hinck, A. P., and Fitzpatrick, P. F. (2011) Direct evidence for a phenylalanine site in the regulatory domain of phenylalanine hydroxylase Arch. Biochem. Biophys. 505, 250-255 10.1016/j.abb.2010.10.009
26. Roberts, K. M., Khan, C. A., Hinck, C. S., and Fitzpatrick, P. F. (2014) Activation of phenylalanine hydroxylase by phenylalanine does not require binding in the active site Biochemistry 53, 7846-7853 10.1021/bi501183x
27. Jaffe, E. K., Stith, L., Lawrence, S. H., Andrake, M., and Dunbrack, R. L., Jr (2013) A new model for allosteric regulation of phenylalanine hydroxylase: Implications for disease and therapeutics Arch. Biochem. Biophys. 530, 73-82 10.1016/j.abb.2012.12.017
28. Lang, E. J. M., Cross, P. J., Mittelstädt, G., Jameson, G. B., and Parker, E. J. (2014) Allosteric ACTion: the varied ACT domains regulating enzymes of amino-acid metabolism Curr. Opin. Struct. Biol. 29, 102-111 10.1016/j.sbi.2014.10.007
29. Marley, J., Lu, M., and Bracken, C. (2001) A method for efficient isotopic labeling of recombinant proteins J. Biomol. NMR 20, 71-75 10.1023/A:1011254402785
30. Daubner, S. C., Hillas, P. J., and Fitzpatrick, P. F. (1997) Characterization of chimeric pterin-dependent hydroxylases: Contributions of the regulatory domains of tyrosine and phenylalanine hydroxylase to substrate specificity Biochemistry 36, 11574-11582 10.1021/bi9711137
31. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293 10.1007/BF00197809
32. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278, 313-352 10.1385/1-59259-809-9:313
33. Demeler, B. (2005) UltraScan: A comprehensive data analysis software package for analytical ultracentrifugation experiments. In Modern Analytical Ultracentrifugation: Techniques and Methods (Scott, D. J., Harding, S. E., and Row, A. J., Eds.) pp 210-229, Royal Society of Chemistry, London.
34. Schuck, P. (2000) Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Biophys. J. 78, 1606-1619 10.1016/S0006-3495(00)76713-0
35. Kappock, T. J., Harkins, P. C., Friedenberg, S., and Caradonna, J. P. (1995) Spectroscopic and kinetic properties of unphosphorylated rat hepatic phenylalanine hydroxylase expressed in Escherichia coli. Comparison of resting and activated states J. Biol. Chem. 270, 30532-30544 10.1074/jbc.270.51.30532
36. Kaufman, S. and Mason, K. (1982) Specificity of amino acids as activators and substrates for phenylalanine hydroxylase J. Biol. Chem. 257, 14667-14678
37. Stegink, L. D., Filer, L. J., Brummel, M. C., Baker, G. L., Krause, W. L., Bell, E. F., and Ziegler, E. E. (1991) Plasma amino acid concentrations and amino acid ratios in normal adults and adults heterozygous for phenylketonuria ingesting a hamburger and milk shake meal Am. J. Clin. Nutr. 53, 670-675
38. Ryan, W. L. and Carver, M. J. (1966) Free amino acids of human foetal and adult liver Nature 212, 292-293 10.1038/212292a0
39. Williams, R. A., Mamotte, C. D. S., and Burnett, J. R. (2008) Phenylketonuria: An inborn error of phenylalanine metabolism Clin. Biochem. Rev. 29, 31-41
40. van Spronsen, F. J., de Groot, M. J., Hoeksma, M., Reijngoud, D. J., and van Rijn, M. (2010) Large neutral amino acids in the treatment of PKU: from theory to practice J. Inherited Metab. Dis. 33, 671-676 10.1007/s10545-010-9216-1
41. Pietz, J., Kreis, R., Rupp, A., Mayatepek, E., Rating, D., Boesch, C., and Bremer, H. J. (1999) Large neutral amino acids block phenylalanine transport into brain tissue in patients with phenylketonuria J. Clin. Invest. 103, 1169-1178 10.1172/JCI5017
42. Matalon, R., Michals-Matalon, K., Bhatia, G., Grechanina, E., Novikov, P., McDonald, J. D., Grady, J., Tyring, S. K., and Guttler, F. (2006) Large neutral amino acids in the treatment of phenylketonuria (PKU) J. Inherited Metab. Dis. 29, 732-738 10.1007/s10545-006-0395-8