Tyrosine hydroxylase binds tetrahydrobiopterin cofactor with negative cooperativity, as shown by kinetic analyses and surface plasmon resonance detection

European Journal of Biochemistry

Volumn 262, Issue 3, 1999, Pages 840-849

  Flatmark, Torgeir ^b   Almås, Bjørg ^c   Knappskog, Per M ^c   Berge, Sissel V ^c   Svebak, Randi M ^c   Chehin, Rosana ^a   Muga, Arturo ^a   Martínez, Aurora ^c  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b UNIVERSITY OF BERGEN   (Norway)

^c NONE

Author keywords

Conformational change; Negative cooperativity; Surface plasmon resonance; Tetrahydrobiopterin; Tyrosine hydroxylase

Indexed keywords

(6) LEVO ERYTHRO 5,6,7,8 TETRAHYDROBIOPTERIN; 3 METHYL 5,6,7,8 TETRAHYDROPTERIN; 6 METHYLTETRAHYDROPTERIN; CATECHOLAMINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; LEVO ERYTHRO DIHYDROBIOPTERIN; SERINE; TETRAHYDROBIOPTERIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CATECHOLAMINE SYNTHESIS; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STABILITY; EQUILIBRIUM CONSTANT; HALF LIFE TIME; KINETICS; LIGAND BINDING; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REACTION ANALYSIS; SURFACE PLASMON RESONANCE;

ANIMALS; APOENZYMES; BIOPTERIN; CATTLE; ENZYME STABILITY; HUMANS; KINETICS; LIGANDS; MICE; PROTEIN BINDING; PROTEIN CONFORMATION; PTERINS; RATS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; SURFACE PLASMON RESONANCE; TEMPERATURE; TYROSINE 3-MONOOXYGENASE;

EID: 0001623810     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00445.x     Document Type: Article

References (48)

1. 1. Kaufman, S. (1995) Tyrosine hydroxylase. Adv. Enzymol. 70, 103-220.
2. 2. Kappock, T.J. & Caradonna, J.P. (1996) Pterin-dependent amino acid hydroxylases. Chem. Rev. 96, 2659-2756.
3. 3. Fitzpatrick, P.F. (1991) Steady state kinetic mechanism of rat tyrosine hydroxylase. Biochemistry 30, 3658-3662.
4. 4. Haavik, J., Thomas, G. & Cohen, P. (1997) Activation of tyrosine hydroxylase by phosphorylation. A comparison of different protein kinases and phosphorylation sites. In Chemistry and Biology of Pteridines and Folates 1997 (Pfleiderer, W. & Rokos, H., eds). pp. 509-514. Blackwell Science, Berlin.
5. 5. Le Bourdelles, B., Horellou, P., Le Caer, J.-P., Denefle, P., Latta, M., Haavik, J., Guibert, B., Mayaux, J.-F. & Mallet, J. (1991) Phosphorylation of tyrosine hydroxylase isoforms 1 and 2: an additional phosphorylated residue in isoform 2, generated through alternative splicing. J. Biol. Chem. 266, 17124-17130.
6. 6. Goodwill, K.E., Sabatier, C., Marks, C., Raag, R., Fitzpatrick, P.F. & 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. 7. Goodwill, K.E., Sabatier, C. & Stevens, R.C. (1998) Crystal structure of tyrosine hydroxylase with bound cofactor analogue and iron at 2.3 Å resolution: self-hydroxylation of Phe300 and the pterin-binding site. Biochemistry 37, 13437-13445.
8. 8. Martínez, A., Abeygunawardana, C., Haavik, J., Flatmark, T. & Mildvan, A.S. (1993) Conformation and interaction of phenylalanine with the divalent cation at the active site of human recombinant tyrosine hydroxylase as determined by proton NMR. Biochemistry 32, 6381-6390.
9. 9. Martínez A., Vageli, O., Pfleiderer, W. & Flatmark, T. (1998) Proton NMR studies on the conformation of pterin cofactor bound at the active site of recombinant human tyrosine hydroxylase. Pteridines 9, 44-52.
10. 10. Minami, M., Takahashi, T., Maruyama, W., Takahashi, A., Nagatsu, T. & Naoi, M. (1992) Allosteric effect of tetrahydrobiopterin cofactors on tyrosine hydroxylase activity. Life Sci. 50, 15-20.
11. 11. Maruyama, W. & Naoi, M. (1994) Inhibition of tyrosine hydroxylase by a dopamine neurotoxin, 1-methyl-4-phenylpyridinium ion: depletion of allostery to the biopterin cofactor. Life Sci. 55, 207-212.
12. 12. Nasrin, S., Ichinose, H., Hidaka, H. & Nagatsu, T. (1994) Recombinant human tyrosine hydroxylase types 1-4 show regulatory kinetic properties for the natural (6R)-tetrahydrobiopterin cofactor. J. Biochem. 116, 393-398.
13. 13. Knappskog, P.M., Flatmark, T., Mallet, J., Lüdecke, B. & Bartholomé, K. (1995) Recessively inherited L-DOPA-responsive dystonia caused by a point mutation (Q381K) in the tyrosine hydroxylase gene. Hum. Mol. Gen. 4, 1209-1212.
14. 14. Knappskog, P.M., Eiken, H.G., Martínez, A., Bruland, O., Apold, J. & Flatmark, T. (1996) PKU mutation (D143G) associated with an apparent high residual enzyme activity: expression of a kinetic variant form of phenylalanine hydroxylase in three different systems. Hum. Mut. 8 (1996), 236-246.
15. 15. Martínez, A., Knappskog, P.M., Olafsdottir, S., Døskeland, A.P., Eiken, H.G., Svebak, R.M., Bozzini, M.L., Apold, J. & Flatmark, T. (1995) Expression of recombinant human phenylalanine hydroxylase as fusion protein in E. coli circumvents proteolytic degradation by host cell proteases. Isolation and characterization of the wild-type enzyme. Biochem. J. 306, 589-597.
16. 16. Martínez, A., Haavik, J., Flatmark, T., Arrondo, J.L. & Muga, A. (1996) Conformational properties and stability of tyrosine hydroxylase studied by infrared spectroscopy. Effect of iron/catecholamine binding and phosphorylation. J. Biol. Chem. 271, 19737-19742.
17. 17. Haavik, J., Andersson, K.K., Petersson, L. & Flatmark, T. (1988) Soluble tyrosine hydroxylase from bovine adrenal medulla: large-scale purification and physicochemical properties. Biochim. Biophys. Acta 953, 142-156.
18. 3H]-tyrosine by charchoal. Life Sci. 39, 2185-2189.
19. 19. Haavik, J. & Flatmark, T. (1980) Rapid and sensitive assay of tyrosine 3-monooxygenase activity by high-performance liquid chromatography using the native fluorescence of DOPA. J. Chromatogr. 198, 511-515.
20. 20. Davis, M.D. & Kaufman, S. (1991) Studies on the partially uncoupled oxidation of tetrahydropterins by phenylalanine hydroxylase. Neurochem. Res. 16, 813-819.
21. 21. Knack, I. & Röhm, K.H. (1981) Microcomputers in enzymology. A versatile basic computer program for analyzing kinetic data. Hoppe-Syeler Z. Physiol. Chem. 362, 1119-1130.
22. 22. Arrondo, J.L., Castresana, J., Valpuesta, J.M. & Goñi, F.M. (1994) Structure and thermal denaturation of crystalline and noncrystalline cytochrome oxidase as studied by infrared spectroscopy. Biochemistry 33, 11650-11655.
23. 23. Almås, B., Le Bourdelles, B., Flatmark, T., Mallet, J. & Haavik, J. (1992) Regulation of recombinant human tyrosine hydroxylase isozymes by catecholamine binding and phosphorylation. Structure/ activity studies and mechanistic implications. Eur. J. Biochem. 209, 249-255.
24. 24. Henis, Y.I. & Levitzki, A. (1989) Mammalian glyceraldehyde-3-phosphate dehydrogenase and its use to elucidate molecular mechanisms of cooperativity. Allosteric Enzymes (Hervé, G., ed.), pp. 153-174. CRC Press, Inc., Boca Raton, Florida.
25. 25. Haavik, J., Le Bourdelles, B., Martinez, A., Flatmark, T. & Mallet, J. (1991). Recombinant tyrosine hydroxylase isozymes: reconstitution with iron and inhibitory effect of other metal ions. Eur. J. Biochem. 199, 371-378.
26. 26. Glaser, R.W. (1993) Antigen-antibody binding and mass transport by convection and diffusion to a surface: a two-dimensional computer model of binding and dissociation kinetics. Anal. Biochem. 213, 152-161.
27. 27. Andersson, K.K., Cox, D.D., Que, L. Jr, Flatmark, T. & Haavik, J. (1988) Resonance Raman studies on the blue-green colored bovine adrenal tyrosine 3-monooxygenase (tyrosine hydroxylase). Evidence that the feedback inhibitors adrenaline and noradrenaline are coordinated to iron. J. Biol. Chem. 263, 18621-18626.
28. 28. Michaud-Soret, I., Andersson, K.K., Que, L. Jr & Haavik, J. (1995) Resonance Raman studies of catecholate and phenolate complexes of recombinant human tyrosine hydroxylase. Biochemistry 34, 5504-5510.
29. 29. Erlandsen, H., Flatmark, T., Stevens, R.C. & Hough, E. (1998) Crystallographic analysis of the human phenylalanine hydroxylase catalytic domain with bound catechol inhibitors at 2.0 Å resolution. Biochemistry 37, 15638-15646.
30. 30. Alterio, J., Ravassard, P., Haavik, J., Le Caer, J.-P., Biguet, N.F., Waksman, G. & Mallet, J. (1998) Human tyrosine hydroxylase isoforms. Inhibition by excess tetrahydropterin and unusual behaviour of isoform 3 after cAMP-dependent protein kinase phosphorylation. J. Biol. Chem. 273, 10196-10201.
31. 31. Morgenroth, V.H. III, Hegstrand, L.R., Roth, R.H. & Greengard, P. (1975) Evidence for involvement of protein kinase in the activation by adenosine 3′,5′-monophosphate of brain tyrosine 3-monooxygenase. J. Biol. Chem. 250, 1946-1948.
32. 32. Neet, K.E. (1995) Cooperatively in enzyme function: equilibrium and kinetic aspects. Meth. Enzymol. 249, 519-567.
33. 33. Koshland, D.E. Jr, Nemethy, G. & Filmer, D. (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385.
34. 34. Haycock, J.W. (1993) Multiple signaling pathways in bovine chromaffin cells regulate tyrosine hydroxylase phosphorylation at Ser19, Ser31, and Ser40. Neurochem. Res. 18, 15-26.
35. 35. Kumer, S.C. & Vrana, K.E. (1996) Intricate regulation of tyrosine hydroxylase activity and gene expression. J. Neurochem. 67, 443-462.
36. 36. Shiman, R., Mortimore, G.E., Schworer, C.M. & 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.
37. 37. Guroff, G., Rhoads, C.A. & Abramowitz, A. (1967) A simple radioisotope assay for phenylalanine hydroxylase cofactor. Anal. Biochem. 21, 273-278.
38. 38. Fukushima, T. & Nixon, J.C. (1980) Analysis of reduced forms of biopterin in biological tissues and fluids. Anal. Biochem. 102, 176-188.
39. 39. Nagatsu, T., Yamaguchi, T., Kato, T., Sugimoto, T., Matsuura, S., Akino, M., Tsushima, S., Nakazawa, N. & Ogawa, H. (1981) Radio-immunoassay for biopterin in body fluids and tissues. Anal. Biochem. 110, 182-189.
40. 40. Miwa, S., Watanabe, Y. & Hayaishi, O. (1985) 6R-L-erythro-5,6,7,8-tetrahydrobiopterin as a regulator of dopamine and serotonin biosynthesis in the rat brain. Arch. Biochem. Biophys. 239, 234-241.
41. 41. Abou-Donia, M.M., Wilson, S.P., Zimmerman, T.P., Nichol, C.A. & Viveros, O.H. (1986) Regulation of guanosine triphosphate cyclohydrolase and tetrahydrobiopterin levels and the role of the cofactor in tyrosine hydroxylation in primary cultures of adrenomedullary chromaffin cells. J. Neurochem. 46, 1190-1199.
42. 42. Levine, R.A., Zoephel, G.P., Niederwieser, A. & Curtius, H.-C. (1987) Entrance of tetrahydropterin derivatives in brain after peripheral administration: effect on biogenic amine metabolism. J. Pharamcol. Exp. Ther. 242, 514-522.
43. 43. Brand, M.P., Hyland, K., Engle, T., Smith, I. & Heales, S.J. (1996) Neurochemical effects following peripheral administration of tetrahydropterin derivatives to the hph-I mouse. J. Neurochem. 66, 1150-1156.
44. 44. Musacchio, J.M., D'Angelo, G.L. & McQueen, C.A. (1971) Dihydropteridine reductase: Implication on the regulation of catecholamine biosynthesis. Proc. Natl Acad. Sci. USA 68, 2087-2091.
45. 45. Kettler, R., Bartholini, G. & Pletscher, A. (1974) In vivo enhancement of tyrosine hydroxylation in rat striatum by tetrahydrobiopterin. Nature 249, 476-478.
46. 46. Flatmark, T. & Knappskog, P.M. (1998) Mutations in the genes of the catecholamine biosynthetic enzymes and human diseases. In Adrenal Chromaffin Cell (Kanno, T., Nakazato, Y. & Kumakura, K., eds) pp. 233-242. Hokkaido University Press, Sapporo.
47. 47. Lentz, S.I. & Kapatos, G. (1996) Tetrahydrobiopterin biosynthesis in the rat brain: heterogeneity of GTP cyclohydrolase I mRNA expression in monoamine-containing neurons. Neurochem. Int. 28, 569-582.
48. 48. Hirayama, K. & Kapatos, G. (1998) Nigrostriatal dopamine neurons express low levels of GTP cyclohydrolase I protein. J. Neurochem. 70, 164-170.