Structural features of the regulatory ACT domain of phenylalanine hydroxylase

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Carluccio, Carla ^a,b,c   Fraternali, Franca ^c   Salvatore, Francesco ^a,d   Fornili, Arianna ^c   Zagari, Adriana ^a  

^a CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d IRCCS SDN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PHENYLALANINE 4 MONOOXYGENASE;

AMINO ACID SEQUENCE; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; HYDROGEN BOND; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN CONFORMATION; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHENYLALANINE HYDROXYLASE; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84893820955     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079482     Document Type: Article

References (60)

1. Kaufman S (1993) The phenylalanine hydroxylating system. Adv Enzymol 70: 77-264.
2. Hufton S, Jennings I, Cotton R (1995) Structure and function of the aromatic amino acid hydroxylases. Biochem J 311: 353-366.
3. Erlandsen H, Stevens RC (1999) The structural basis of phenylketonuria. Mol Genet Metab 68: 103-125. (Pubitemid 29501084)
4. Okano Y, Wang T, Eisensmith RC, Longhi R, Riva E, et al. (1991) Phenylketonuria missense mutations in the Mediterranean. Genomics 9: 96-103.
5. Svensson E, Iselius L, Hagenfeldt L (1994) Severity of mutation in the phenylalanine hydroxylase gene influences phenylalanine metabolism in phenylketonuria and hyperphenylalaninaemia heterozygotes. J Inherit Metab Dis 17: 215-222. (Pubitemid 24182919)
6. Blau N, van Spronsen FJ, Levy HL (2010) Phenylketonuria. Lancet 376: 1417-1427.
7. Erlandsen H, Stevens RC (2001) A structural hypothesis for BH4 responsiveness in patients with mild forms of hyperphenylalaninaemia and phenylketonuria. J Inherit Metab Dis 24: 213-230. (Pubitemid 32479416)
8. Cerreto M, Mehdawy B, Ombrone D, Nisticò R, Ruoppolo M, et al. (2012) Reversal of Metabolic and Neurological Symptoms of Phenylketonuric Mice Treated with a PAH Containing Helper-Dependent Adenoviral Vector. Current Gene Therapy 12: 48-56.
9. Daniele A, Cardillo G, Pennino C, Carbone MT, Scognamiglio D, et al. (2008) Five human phenylalanine hydroxylase proteins identified in mild hyperphenylalaninemia patients are disease-causing variants. Biochim Biophys Acta 1782: 378-384.
10. Daniele A, Scala I, Cardillo G, Pennino C, Ungaro C, et al. (2009) Functional and structural characterization of novel mutations and genotype-phenotype correlation in 51 phenylalanine hydroxylase deficient families from Southern Italy. FEBS J 276: 2048-2059.
11. Cerreto M, Cavaliere P, Carluccio C, Amato F, Zagari A, et al. (2011) Natural phenylalanine hydroxylase variants that confer a mild phenotype affect the enzyme's conformational stability and oligomerization equilibrium. Biochim Biophys Acta 1812: 1435-1445.
12. Knappskog PM, Flatmark T, Aarden JM, Haavik J, 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.
13. Gersting S, Kemter K, Staudigl M, Messing D, Danecka M, et al. (2008) Loss of function in phenylketonuria is caused by impaired molecular motions and conformational instability. Am J Hum Genet 83: 5-17.
14. Eiken HG, Knappskog PM, Apold J, Flatmark T (1996) PKU mutation G46S is associated with increased aggregation and degradation of the phenylalanine hydroxylase enzyme. Hum Mutat 7: 228-238. (Pubitemid 26116058)
15. Kobe B, Jennings IG, House CM, Michell BJ, Goodwill KE, et al. (1999) Structural basis of autoregulation of phenylalanine hydroxylase. Nat Struct Biol 6: 442-448. (Pubitemid 29218013)
16. Aravind L, Koonin EV (1999) Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. J Mol Biol 287: 1023-1040. (Pubitemid 29188885)
17. Grant GA (2006) The ACT domain: a small molecule binding domain and its role as a common regulatory element. Jurnal of biological chemistry 281: 33825-33829.
18. Fitzpatrick PF (2000) The aromatic amino acid hydroxylases. Adv Enzymol Relat Areas Mol Biol 74: 235-294.
19. Gersting SW, Staudigl M, Truger MS, Messing DD, Danecka MK, et al. (2010) Activation of phenylalanine hydroxylase induces positive cooperativity toward the natural cofactor. J Biol Chem 285: 30686-30697.
20. Thorolfsson M, Ibarra-Molero B, Fojan P, Petersen SB, Sanchez-Ruiz JM, et al. (2002) L-phenylalanine binding and domain organization in human phenylalanine hydroxylase: a differential scanning calorimetry study. Biochemistry 41: 7573-7585. (Pubitemid 34627784)
21. Thorolfsson M, Teigen K, Martinez A (2003) Activation of phenylalanine hydroxylase: effect of substitutions at Arg68 and Cys237. Biochemistry 42: 3419-3428. (Pubitemid 36368635)
22. Liberles JS, Thorolfsson M, Martinez A (2005) Allosteric machanism in ACT domain containing enzymes involved in amino acid metabolism. Amino Acid 28: 1-12. (Pubitemid 40385388)
23. Liberles JS, Martinez A (2009) Searching distant homologs of the regulatory ACT domain in phenylalanine hydroxylase. Amino Acid 36: 235-249.
24. Shiman R, Gray DW, Pater A (1979) A simple purification of phenylalanine hydroxylase by substrate-induced hydrophobic chromatography. Biol Chem 254: 11300-11306.
25. Li J, Ilangovan U, Daubner SC, Hinck AP, Fitzpatrick PF (2011) Direct evidence for a phenylalanine site in the regulatory domain of phenylalanine hydroxylase. Archives of Biochemistry and Biophysics 505: 250-255.
26. Gjetting T, Petersen M, Guldberg P, Guttler 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. (Pubitemid 32510611)
27. Tan K, Li H, Zhang R, Gu M, Clancy ST, et al. (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.
28. Gjetting T, Petersen M, Guldberg P, Guttler F (2001) In vitro expression of 34 naturally occurring mutant variants of phenylalanine hydroxylase: correlation with metabolic phenotypes and susceptibility toward protein aggregation. Mol Genet Metab 72: 132-143. (Pubitemid 34171453)
29. Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234: 779-815. (Pubitemid 24007801)
30. Lehtonen J, Still D, Rantanen V, Ekholm J, Björklund D, et al. (2004) BODIL: a molecular modeling environment for structure-function analysis and drug design. J Comput Aided Mol Des 18: 401-419. (Pubitemid 40069138)
31. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718. (Pubitemid 43076182)
32. van Gunsteren WF, Billeter SR, Eising AA, Hünenberger PH, Krüger P, et al. (1996) Biomolecular Simulation: The GROMOS96 manual and userguide. Hochschuleverlag AG an der ETH Zürich, Zürich, Switzerland.
33. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J (1981) Interaction models for water in relation to protein hydration. In Intermolecular Forces (Pullman, B, ed): 331-342.
34. Hess B, Bekker H, Berendsen H, Fraaije J (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472. (Pubitemid 127637344)
35. Miyamoto S, Kollman PA (1992) Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13: 952-962.
36. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
37. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. J Chem Phys 103: 8577-8593.
38. Humphrey W, Dalke A, Schulten K (1996) VMD - Visual Molecular Dynamics. Journal of Molecular Graphics 14: 33-38.
39. Schrödinger L (2009) The PyMOL Molecular Graphics System, Version 1.2r0.
40. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
41. Eisenhaber F, Lijnzaad P, Argos P, Sander C, Scharf M (1995) The double cube lattice method: efficient approaches to numerical integrations of surface area and volume and to dot surface contouring of molecular assemblies. J Comput Chem 16: 273-284.
42. Amadei A, Linssen AB, Berendsen HJ (1993) Essential dynamics of proteins. Proteins 17: 412-425. (Pubitemid 23358549)
43. Barrett CP, Hall BA, Noble ME (2004) Dynamite: a simple way to gain insight into protein motions. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1): 2280-2287.
44. van Aalten DM, Amadei A, Linssen AB, Eijsink VG, Vriend G, et al. (1995) The essential dynamics of thermolysin: confirmation of the hinge-bending motion and comparison of simulations in vacuum and water. Proteins 22: 45-54.
45. Ivetac A, McCammon JA (2009) Elucidating the inhibition mechanism of HIV-1 non-nucleoside reverse transcriptase inhibitors through multicopy molecular dynamics simulations. J Mol Biol 388: 644-658.
46. Shan J, Khelashvili G, Mondal S, Mehler EL, Weinstein H (2012) Liganddependent conformations and dynamics of the serotonin 5-HT(2A) receptor determine its activation and membrane-driven oligomerization properties. PLoS Comput Biol 8: e1002473.
47. Seeliger D, Haas J, de Groot BL (2007) Geometry-based sampling of conformational transitions in proteins. Structure 15: 1482-1492. (Pubitemid 350051928)
48. Jorgensen W, Tirado-Rives J (1988) The Opls Potential Functions for Proteins - Energy Minimizations for Crystals of Cyclic-Peptides and Crambin. J Am Chem Soc 110: 1657-1666.
49. Lounnas V, Pettitt BM, Phillips Jr GN (1994) A global model of the proteinsolvent interface. Biophys J 66: 601-614.
50. Lounnas V, Pettitt BM (1994) Distribution function implied dynamics versus residence times and correlations: solvation shells of myoglobin. Proteins 18: 148-160. (Pubitemid 24055077)
51. De Simone A, Dodson GG, Verma CS, Zagari A, Fraternali F (2005) Prion and water: tight and dynamical hydration sites have a key role in structural stability. Proc Natl Acad Sci USA 102: 7535-7540. (Pubitemid 40741006)
52. Fornili A, Autore F, Chakroun N, Martinez P, Fraternali F (2012) Protein-Water Interactions in MD Simulations: POPS/POPSCOMP Solvent Accessibility Analysis, Solvation Forces and Hydration Sites. Methods Mol Biol 819: 375-392.
53. Hub JS, de Groot BL (2009) Detection of functional modes in protein dynamics. PLoS Comput Biol 5: 1-13.
54. Li J, Dangott LJ, Fitzpatrick PF (2010) Regulation of phenylalanine hydroxylase: conformational changes upon phenylalanine binding detected by hydrogen/deuterium exchange and mass spectrometry. Biochemistry 49: 3327-3335.
55. Miranda FF, Teigen K, Thorolfsson M, Svebak RM, Knappskog PM, et al. (2002) Phosphorylation and mutations of Ser(16) in human phenylalanine hydroxylase. Kinetic and structural effects. J Biol Chem 277: 40937-40943. (Pubitemid 35215681)
56. Flatmark T, Stevens RC (1999) Structural insight into the aromatic amino acid hydroxylases and their disease-related mutant forms. Chem Rev 99: 2137-2160. (Pubitemid 129585182)
57. Schlick T (2009) Molecular dynamics-based approaches for enhanced sampling of long-time, large-scale conformational changes in biomolecules. F1000 Biol Rep 1: 51.
58. Erlandsen H, Pey AL, Gamez A, Perez B, Desviat LR, et al. (2004) Correction of kinetic and stability defects by tetrahydrobiopterin in phenylketonuria patients with certain phenylalanine hydroxylase mutations. Proc Natl Acad Sci U S A 101: 16903-16908. (Pubitemid 39601336)
59. Leandro J, Simonsen N, Saraste J, Leandro P, Flatmark T (2011) Phenylketonuria as a protein misfolding disease: The mutation pG46S in phenylalanine hydroxylase promotes self-association and fibril formation. Biochim Biophys Acta 1812: 106-120.
60. Pey A, Stricher F, Serrano L, Martinez A (2007) Predicted effects of missense mutations on native-state stability account for phenotypic outcome in phenylketonuria, a paradigm of misfolding diseases. Am J Hum Genet 81: 1006-1024. (Pubitemid 47580253)