Divergence in enzyme regulation between Caenorhabditis elegans and human tyrosine hydroxylase, the key enzyme in the synthesis of dopamine

Biochemical Journal

Volumn 434, Issue 1, 2011, Pages 133-141

  Calvo, Ana C ^a   Pey, Angel L ^b   Miranda Vizuete, Antonio ^c,d   Døskeland, Anne P ^a   Martinez, Aurora ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF GRANADA   (Spain)

^c Universidad Pablo de Olavide   (Spain)

^d HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

Caenorhabditis elegans; Dopamine; Nervous system; Phosphorylation; Tyrosine hydroxylase

Indexed keywords

CAT 2 PROTEIN; COMPLEMENTARY DNA; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE; HELMINTH PROTEIN; TYROSINE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; DOPAMINE METABOLISM; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CLONING, MOLECULAR; DOPAMINE; GENETIC VARIATION; HUMANS; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; PHENYLALANINE; PHOSPHORYLATION; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TRYPTOPHAN; TYROSINE; TYROSINE 3-MONOOXYGENASE;

CAENORHABDITIS ELEGANS; EUKARYOTA; MAMMALIA;

EID: 79251567350     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101561     Document Type: Article

References (50)

1. Teigen, K., McKinney, J. A., Haavik, J. and Martinez, A. (2007) Selectivity and affinity determinants for ligand binding to the aromatic amino acid hydroxylases. Curr. Med. Chem. 14, 455-467
2. Fitzpatrick, P. F. (2000) The aromatic amino acid hydroxylases. Adv. Enzymol. Relat. Areas Mol. Biol. 74, 235-294
3. Flatmark, T. and Stevens, R. C. (1999) Structural insight into the aromatic amino acid hydroxylases and their disease-related mutant forms. Chem. Rev. 99, 2137-2160
4. Leiros, H. K., Pey, A. L., Innselset, M., Moe, E., Leiros, I., Steen, I. H. and Martinez, A. (2007) Structure of phenylalanine hydroxylase from Colwellia psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability. J. Biol. Chem. 282, 21973-21986
5. Erlandsen, H., Kim, J. Y., Patch, M. G., Han, A., Volner, A., Abu-Omar, M. M. and Stevens, R. C. (2002) Structural comparison of bacterial and human iron-dependent phenylalanine hydroxylases: similar fold, different stability and reaction rates. J. Mol. Biol. 320, 645-661
6. Chen, Y. C., Priyadarshini, M. and Panula, P. (2009) Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem. Cell Biol. 132, 375-381
7. Nagatsu, T. (1995) Tyrosine hydroxylase: human isoforms, structure and regulation in physiology and pathology. Essays Biochem. 30, 15-35
8. Dumas, S., Le Hir, H., Bodeau-Pean, S., Hirsch, E., Thermes, C. and Mallet, J. (1996) New species of human tyrosine hydroxylase mRNA are produced in variable amounts in adrenal medulla and are overexpressed in progressive supranuclear palsy. J. Neurochem. 67, 19-25
9. Ohye, T., Ichinose, H., Yoshizawa, T., Kanazawa, I. and Nagatsu, T. (2001) A new splicing variant for human tyrosine hydroxylase in the adrenal medulla. Neurosci. Lett. 312, 157-60
10. Nishii, K., Matsushita, N., Sawada, H., Sano, H., Noda, Y., Mamiya, T., Nabeshima, T., Nagatsu, I., Hata, T., Kiuchi, K. et al. (1998) Motor and learning dysfunction during postnatal development in mice defective in dopamine neuronal transmission. J. Neurosci. Res. 54, 450-464
11. Kobayashi, K. (2001) Role of catecholamine signaling in brain and nervous system functions: new insights from mouse molecular genetic study. J. Invest. Dermatol. Symp. Proc. 6, 115-121
12. Kumer, S. C. and Vrana, K. E. (1996) Intricate regulation of tyrosine hydroxylase activity and gene expression. J. Neurochem. 67, 443-462
13. Sura, G. R., Daubner, S. C. and Fitzpatrick, P. F. (2004) Effects of phosphorylation by protein kinase A on binding of catecholamines to the human tyrosine hydroxylase isoforms. J. Neurochem. 90, 970-978
14. Ramsey, A. J. and Fitzpatrick, P. F. (1998) Effects of phosphorylation of serine 40 of tyrosine hydroxylase on binding of catecholamines: evidence for a novel regulatory mechanism. Biochemistry 37, 8980-8986
15. Dunkley, P. R., Bobrovskaya, L., Graham, M. E., von Nagy-Felsobuki, E. I. and Dickson, P. W. (2004) Tyrosine hydroxylase phosphorylation: regulation and consequences. J. Neurochem. 91, 1025-43
16. Halskau, Jr, O., Ying, M., Baumann, A., Kleppe, R., Rodriguez-Larrea, D., Almas, B., Haavik, J. and Martinez, A. (2009) Three-way interaction between 14-3-3 proteins, the N-terminal region of tyrosine hydroxylase, and negatively charged membranes. J. Biol. Chem. 284, 32758-32769
17. Haycock, J. W. and Wakade, A. R. (1992) Activation and multiple-site phosphorylation of tyrosine hydroxylase in perfused rat adrenal glands. J. Neurochem. 58, 57-64
18. Vie, A., Cigna, M., Toci, R. and Birman, S. (1999) Differential regulation of Drosophila tyrosine hydroxylase isoforms by dopamine binding and cAMP-dependent phosphorylation. J. Biol. Chem. 274, 16788-16795
19. Gorman, M. J., An, C. and Kanost, M. R. (2007) Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochem. Mol. Biol. 37, 1327-1337
20. Gaskell, E. A., Smith, J. E., Pinney, J. W., Westhead, D. R. and McConkey, G. A. (2009) A unique dual activity amino acid hydroxylase in Toxoplasma gondii. PLoS ONE 4, e4801
21. Lints, R. and Emmons, S. W. (1999) Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFβ family signaling pathway and a Hox gene. Development 126, 5819-5831
22. Sulston, J., Dew, M. and Brenner, S. (1975) Dopaminergic neurons in the nematode Caenorhabditis elegans. J. Comp. Neurol. 163, 215-226
23. Nass, R. and Blakely, R. D. (2003) The Caenorhabditis elegans dopaminergic system: opportunities for insights into dopamine transport and neurodegeneration. Annu. Rev. Pharmacol. Toxicol. 43, 521-544
24. Sawin, E. R., Ranganathan, R. and Horvitz, H. R. (2000) C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26, 619-631
25. Sanyal, S., Wintle, R. F., Kindt, K. S., Nuttley, W. M., Arvan, R., Fitzmaurice, P., Bigras, E., Merz, D. C., Hebert, T. E., van der Kooy, D. et al. (2004) Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J. 23, 473-482
26. Kindt, K. S., Quast, K. B., Giles, A. C., De, S., Hendrey, D., Nicastro, I., Rankin, C. H. and Schafer, W. R. (2007) Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron 55, 662-676
27. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94
28. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
29. Haavik, J., Le Bourdelles, B., Martínez, A., Flatmark, T. and Mallet, J. (1991) Recombinant human tyrosine hydroxylase isozymes: reconstitution with iron and inhibitory effect of other metal ions. Eur. J. Biochem. 199, 371-378
30. 3H]-tyrosine by charcoal. Life Sci. 39, 2185-2189
31. Calvo, A. C., Pey, A. L., Ying, M., Loer, C. M. and Martinez, A. (2008) Anabolic function of phenylalanine hydroxylase in Caenorhabditis elegans. FASEB J. 22, 3046-3058
32. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V. and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860
33. Birkeland, E., Nygaard, G., Oveland, E., Mjaavatten, O., Ljones, M., Doskeland, S. O., Krakstad, C. and Selheim, F. (2009) Epac-induced alterations in the proteome of human SH-SY5Y nueroblastoma cells. J. Proteomics Bioinform. 2, 244-254
34. Graber, J. H., Salisbury, J., Hutchins, L. N. and Blumenthal, T. (2007) C. elegans sequences that control trans-splicing and operon pre-mRNA processing. RNA 13, 1409-1426
35. Flatmark, T., Alm̊as, B., Knappskog, P. M., Berge, S. V., Svebak, R. M., Chehin, R., Muga, A. and Martínez, A. (1999) Tyrosine hydroxylase binds tetrahydrobiopterin cofactor with negative cooperativity, as shown by kinetic analyses and surface plasmon resonance detection. Eur. J. Biochem. 262, 840-849
36. Nakashima, A., Mori, K., Suzuki, T., Kurita, H., Otani, M., Nagatsu, T. and Ota, A. (1999) Dopamine inhibition of human tyrosine hydroxylase type 1 is controlled by the specific portion in the N-terminus of the enzyme. J. Neurochem. 72, 2145-2153
37. Fukami, M. H., Haavik, J. and Flatmark, T. (1990) Phenylalanine as substrate for tyrosine hydroxylase in bovine adrenal chromaffin cells. Biochem. J. 268, 525-528
38. Mann, M., Ong, S. E., Gronborg, M., Steen, H., Jensen, O. N. and Pandey, A. (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol. 20, 261-268 (Pubitemid 34451062)
39. Haavik, J., Martínez, A. and Flatmark, T. (1990) pH-dependent release of catecholamines from tyrosine hydroxylase and the effect of phosphorylation of Ser-40. FEBS Lett. 262, 363-365
40. Kaufman, S. (1995) Tyrosine hydroxylase. Adv. Enzymol. Relat. Areas Mol. Biol. 70, 103-220
41. Quinsey, N. S., Luong, A. Q. and Dickson, P. W. (1998) Mutational analysis of substrate inhibition in tyrosine hydroxylase. J. Neurochem. 71, 2132-2138
42. Neckameyer, W. S., Holt, B. and Paradowski, T. J. (2005) Biochemical conservation of recombinant Drosophila tyrosine hydroxylase with its mammalian cognates. Biochem. Genet. 43, 425-443
43. Alm̊as, B., Le Bourdelles, B., Flatmark, T., Mallet, J. and 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
44. Bowling, K. M., Huang, Z., Xu, D., Ferdousy, F., Funderburk, C. D., Karnik, N., Neckameyer, W. and O'Donnell, J. M. (2008) Direct binding of GTP cyclohydrolase and tyrosine hydroxylase: regulatory interactions between key enzymes in dopamine biosynthesis. J. Biol. Chem. 283, 31449-31459
45. Aitken, A. (2006) 14-3-3 proteins: a historic overview. Semin. Cancer Biol. 16, 162-172
46. Kleppe, R., Toska, K. and Haavik, J. (2001) Interaction of phosphorylated tyrosine hydroxylase with 14-3-3 proteins: evidence for a phosphoserine 40-dependent association. J. Neurochem. 77, 1097-1107
47. Wang, Y., Oh, S. W., Deplancke, B., Luo, J., Walhout, A. J. and Tissenbaum, H. A. (2006) C. elegans 14-3-3 proteins regulate life span and interact with SIR-2. 1 and DAF-16/FOXO. Mech. Ageing Dev. 127, 741-747
48. Hills, T., Brockie, P. J. and Maricq, A. V. (2004) Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J. Neurosci. 24, 1217-1225
49. Haavik, J., Blau, N. and Thony, B. (2008) Mutations in human monoamine-related neurotransmitter pathway genes. Hum. Mutat. 29, 891-902
50. Zhou, Q. Y., Quaife, C. J. and Palmiter, R. D. (1995) Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374, 640-643