Identification of the allosteric site for phenylalanine in rat phenylalanine hydroxylase

Journal of Biological Chemistry

Volumn 291, Issue 14, 2016, Pages 7418-7425

  Zhang, Shengnan ^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; DIMERS; ENZYMES; LOCATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS; RATS;

ALLOSTERIC ENZYMES; ALLOSTERIC SITE; INTACT PROTEINS; ISOTOPICALLY LABELED; PHENYLALANINE HYDROXYLASE; REGULATORY DOMAIN; SIDE BY SIDES; SITE-SPECIFIC;

AMINO ACIDS;

DIMER; PHENYLALANINE; PHENYLALANINE 4 MONOOXYGENASE;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR STABILITY; MUTAGENESIS; MUTATIONAL ANALYSIS; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROBABILITY; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; REGULATORY DOMAIN; STEADY STATE; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; ALLOSTERISM; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MISSENSE MUTATION; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

ALLOSTERIC REGULATION; AMINO ACID SUBSTITUTION; ANIMALS; CATALYTIC DOMAIN; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; PHENYLALANINE; PHENYLALANINE HYDROXYLASE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RATS;

EID: 84962829766     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.709998     Document Type: Article

References (36)

1. Eisensmith, R. C., and Woo, S. L. (1991) Phenylketonuria and the phenylalanine hydroxylase gene. Mol. Biol. Med. 8, 3-18
2. Fitzpatrick, P. F. (2012) Allosteric regulation of phenylalanine hydroxylase. Arch. Biochem. Biophys. 519, 194-201
3. Flydal, M. I., and Martinez, A. (2013) Phenylalanine hydroxylase: function, structure, and regulation. IUBMB Life 65, 341-349
4. 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 nonspecific cleavage of the fusion protein by restriction protease. Biochem. J. 313, 409-414
5. Kobe, B., Jennings, I. G., House, C. M., Michell, B. J., Goodwill, K. E., Santarsiero, B. D., Stevens, R. C., Cotton, R. G., and Kemp, B. E. (1999) Structural basis of autoregulation of phenylalanine hydroxylase. Nat. Struct. Biol. 6, 442-448
6. 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
7. 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
8. Fitzpatrick, P. F. (2003) Mechanism of aromatic amino acid hydroxylation. Biochemistry 42, 14083-14091
9. 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. 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
11. Daubner, S. C., Le, T., and Wang, S. (2011) Tyrosine hydroxylase and regulation of dopamine synthesis. Arch. Biochem. Biophys. 508, 1-12
12. 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
13. Li, J., Dangott, L. J., and Fitzpatrick, P. F. (2010) Regulation of phenylalanine hydroxylase: conformational changes upon phenylalanine binding detected by hydrogen/deuterium exchange and mass spectrometry. Biochemistry 49, 3327-3335
14. 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
15. Shiman, R., Gray, D. W., and Pater, A. (1979) A simple purification of phenylalanine hydroxylase by substrate-induced hydrophobic chromatography. J. Biol. Chem. 254, 11300-11306
16. 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 acti-vation in the control of enzymatic activity. J. Biol. Chem. 269, 24647-24656
17. Carluccio, C., Fraternali, F., Salvatore, F., Fornili, A., and Zagari, A. (2015) Towards the identification of the allosteric Phe-binding site in phenylalanine hydroxylase. J. Biomol. Struct. Dyn. 10.1080/07391102.2015.1052016
18. Jaffe, E. K., Stith, L., Lawrence, S. H., Andrake, M., and Dunbrack, R. L., Jr. (2013)Anew model for allosteric regulation of phenylalanine hydroxylase: Implications for disease and therapeutics. Arch. Biochem. Biophys. 530, 73-82
19. 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
20. Thórólfsson, M., Ibarra-Molero, B., Fojan, P., Petersen, S. B., Sanchez-Ruiz, J. M., and Martínez, A. (2002) L-Phenylalanine binding and domain organization in human phenylalanine hydroxylase: a differential scanning calorimetry study. Biochemistry 41, 7573-7585
21. Lang, E. J., Cross, P. J., Mittelstadt, 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
22. Ronau, J. A., Paul, L. N., Fuchs, J. E., Corn, I. R., Wagner, K. T., Liedl, K. R., Abu-Omar, M. M., and Das, C. (2013) An additional substrate binding site in a bacterial phenylalanine hydroxylase. Eur. Biophys. J. 42, 691-708
23. 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
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
25. Zhang, S., Hinck, A. P., and Fitzpatrick, P. F. (2015) The amino acid specificity for activation of phenylalanine hydroxylase matches the specificity for stabilization of regulatory domain dimers. Biochemistry 54, 5167-5174
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
27. Marley, J., Lu, M., and Bracken, C. (2001) A method for efficient isotopic labeling of recombinant proteins. J. Biomol. NMR 20, 71-75
28. Bax, A. (1994) Multidimensional nuclear magnetic resonance methods for protein studies. Curr. Opin. Struct. Biol. 4, 738-744
29. 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
30. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352
31. Gabrielson, J. P., Randolph, T. W., Kendrick, B. S., and Stoner, M. R. (2007) Sedimentation velocity analytical ultracentrifugation and SEDFIT/c(s): limits of quantitation for a monoclonal antibody system. Anal. Biochem. 361, 24-30
32. Eghbalnia, H. R., Wang, L., Bahrami, A., Assadi, A., and Markley, J. L. (2005) Protein energetic conformational analysis from NMR chemical shifts (PECAN) and its use in determining secondary structural elements. J. Biomol. NMR 32, 71-81
33. Schuller, D. J., Grant, G. A., and Banaszak, L. J. (1995) The allosteric ligand site in the Vmax-type cooperative enzyme phosphoglycerate dehydrogenase. Nat. Struct. Biol. 2, 69-76
34. Gjetting, T., Petersen, M., Guldberg, P., and Güttler, F. (2001) Missense mutations in the N-terminal domain of human phenylalanine hydroxylase interfere with binding of regulatory phenylalanine. Am. J. Hum. Genet. 68, 1353-1360
35. Tan, K., Li, H., Zhang, R., Gu, M., Clancy, S. T., and Joachimiak, A. (2008) Structures of open (R) and close (T) states of prephenate dehydratase (PDT)-implication of allosteric regulation by L-phenylalanine. J. Struct. Biol. 162, 94-107
36. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612