Phosphorylation dependence and stoichiometry of the complex formed by tyrosine hydroxylase and 14-3-3γ

Molecular and Cellular Proteomics

Volumn 13, Issue 8, 2014, Pages 2017-2030

  Kleppe, Rune ^a,b,c   Rosati, Sara ^d,e   Jorge Finnigan, Ana ^a   Alvira, Sara ^f   Ghorbani, Sadaf ^a   Haavik, Jan ^a,b,c   Valpuesta, José María ^f   Heck, Albert J R ^d,e   Martinez, Aurora ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b KG Jebsen Centre for Research on Neuropsychiatric Disorders   (Norway)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d UTRECHT UNIVERSITY   (Netherlands)

^e Netherlands Proteomics Center   (Netherlands)

^f CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN 14 3 3; PROTEIN 14 3 3 GAMMA; TETRAMER; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; SERINE;

ARTICLE; ELECTRON MICROSCOPY; ENZYME KINETICS; ENZYME PHOSPHORYLATION; ENZYME PURIFICATION; PRIORITY JOURNAL; STOICHIOMETRY; BINDING SITE; CHEMISTRY; HUMAN; KINETICS; MASS SPECTROMETRY; METABOLISM; PHOSPHORYLATION; PROCEDURES; PROTEIN MULTIMERIZATION; SURFACE PLASMON RESONANCE;

14-3-3 PROTEINS; BINDING SITES; HUMANS; KINETICS; MASS SPECTROMETRY; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; SERINE; SURFACE PLASMON RESONANCE; TYROSINE 3-MONOOXYGENASE;

EID: 84905265912     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.035709     Document Type: Article

References (63)

1. Grima, B., Lamouroux, A., Boni, C., Julien, J. F., Javoy-Agid, F., and Mallet, J. (1987) A single human gene encoding multiple tyrosine hydroxylases with different predicted functional characteristics. Nature 326, 707-711 (Pubitemid 17059792)
2. Kaneda, N., Kobayashi, K., Ichinose, H., Kishi, F., Nakazawa, A., Kurosawa, Y., Fujita, K., and Nagatsu, T. (1987) Isolation of a novel cDNA clone for human tyrosine hydroxylase: alternative RNA splicing produces four kinds of mRNA from a single gene. Biochem. Biophys. Res. Commun. 146, 971-975 (Pubitemid 17153287)
3. Nagatsu, T. (1995) Tyrosine hydroxylase: human isoforms, structure and regulation in physiology and pathology. Essays Biochem. 30, 15-35
4. Cartier, E. A., Parra, L. A., Baust, T. B., Quiroz, M., Salazar, G., Faundez, V., Egana, L., and Torres, G. E. (2010) A biochemical and functional protein complex involving dopamine synthesis and transport into synaptic vesicles. J. Biol. Chem. 285, 1957-1966
5. Daubner, S. C., Le, T., and Wang, S. (2011) Tyrosine hydroxylase and regulation of dopamine synthesis. Arch. Biochem. Biophys. 508, 1-12
6. Chen, X., Xu, L., Radcliffe, P., Sun, B., and Tank, A. W. (2008) Activation of tyrosine hydroxylase mRNA translation by cAMP in midbrain dopaminergic neurons. Mol. Pharmacol. 73, 1816-1828 (Pubitemid 351724369)
7. Lewis, E. J., Harrington, C. A., and Chikaraishi, D. M. (1987) Transcriptional regulation of the tyrosine hydroxylase gene by glucocorticoid and cyclic AMP. Proc. Natl. Acad. Sci. U.S.A. 84, 3550-3554 (Pubitemid 17088318)
8. Andersson, K. K., Cox, D. D., Que, L., Jr., Flatmark, T., and 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 (Pubitemid 19016320)
9. Haycock, J. W., Bennett, W. F., George, R. J., and Waymire, J. C. (1982) Multiple site phosphorylation of tyrosine hydroxylase. Differential regulation in situ by a 8-bromo-cAMP and acetylcholine. J. Biol. Chem. 257, 13699-13703 (Pubitemid 13187132)
10. Ichimura, T., Isobe, T., Okuyama, T., Takahashi, N., Araki, K., Kuwano, R., and Takahashi, Y. (1988) Molecular cloning of cDNA coding for brainspecific 14-3-3 protein, a protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. Proc. Natl. Acad. Sci. U.S.A. 85, 7084-7088
11. Nagatsu, T., and Ichinose, H. (1999) Regulation of pteridine-requiring enzymes by the cofactor tetrahydrobiopterin. Mol. Neurobiol. 19, 79-96 (Pubitemid 29174242)
12. Salvatore, M. F., and Pruett, B. S. (2012) Dichotomy of tyrosine hydroxylase and dopamine regulation between somatodendritic and terminal field areas of nigrostriatal and mesoaccumbens pathways. PLoS One 7, e29867
13. Daubner, S. C., Le, T., and Wang, S. (2011) Tyrosine hydroxylase and regulation of dopamine synthesis. Arch. Biochem. Biophys. 508, 1-12
14. 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, 1025-1043 (Pubitemid 39587442)
15. 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
16. Andersson, K. K., Vassort, C., Brennan, B. A., Que, L., Jr., Haavik, J., Flatmark, T., Gros, F., and Thibault, J. (1992) Purification and characterization of the blue-green rat phaeochromocytoma (PC12) tyrosine hydroxylase with a dopamine-Fe(III) complex. Reversal of the endogenous feedback inhibition by phosphorylation of serine-40. Biochem. J. 284 (Pt 3), 687-695
17. Sutherland, C., Alterio, J., Campbell, D. G., Le Bourdelles, B., Mallet, J., Haavik, J., and Cohen, P. (1993) Phosphorylation and activation of human tyrosine hydroxylase in vitro by mitogen-activated protein (MAP) kinase and MAP-kinase-activated kinases 1 and 2. Eur. J. Biochem. 217, 715-722 (Pubitemid 23311985)
18. 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 (Pubitemid 39099979)
19. Almas, 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
20. Toska, K., Kleppe, R., Armstrong, C. G., Morrice, N. A., Cohen, P., and Haavik, J. (2002) Regulation of tyrosine hydroxylase by stress-activated protein kinases. J. Neurochem. 83, 775-783 (Pubitemid 35316027)
21. Haycock, J. W., Lew, J. Y., Garcia-Espana, A., Lee, K. Y., Harada, K., Meller, E., and Goldstein, M. (1998) Role of serine-19 phosphorylation in regulating tyrosine hydroxylase studied with site- and phosphospecific antibodies and site-directed mutagenesis. J. Neurochem. 71, 1670-1675 (Pubitemid 28443040)
22. Bevilaqua, L. R., Graham, M. E., Dunkley, P. R., von Nagy-Felsobuki, E. I., and Dickson, P. W. (2001) Phosphorylation of Ser(19) alters the conformation of tyrosine hydroxylase to increase the rate of phosphorylation of Ser(40). J. Biol. Chem. 276, 40411-40416
23. Nakashima, A., Mori, K., Kaneko, Y. S., Hayashi, N., Nagatsu, T., and Ota, A. (2011) Phosphorylation of the N-terminal portion of tyrosine hydroxylase triggers proteasomal digestion of the enzyme. Biochem. Biophys. Res. Commun. 407, 343-347
24. Itagaki, C., Isobe, T., Taoka, M., Natsume, T., Nomura, N., Horigome, T., Omata, S., Ichinose, H., Nagatsu, T., Greene, L. A., and Ichimura, T. (1999) Stimulus-coupled interaction of tyrosine hydroxylase with 14-3-3 proteins. Biochemistry 38, 15673-15680 (Pubitemid 129503612)
25. Kleppe, R., Martinez, A., Doskeland, S. O., and Haavik, J. (2011) The 14-3-3 proteins in regulation of cellular metabolism. Semin. Cell Dev. Biol. 22, 713-719
26. Obsil, T., and Obsilova, V. (2011) Structural basis of 14-3-3 protein functions. Semin. Cell Dev. Biol. 22, 663-672
27. Aitken, A. (2011) Post-translational modification of 14-3-3 isoforms and regulation of cellular function. Semin. Cell Dev. Biol. 22, 673-680
28. Roth, D., Morgan, A., Martin, H., Jones, D., Martens, G. J., Aitken, A., and Burgoyne, R. D. (1994) Characterization of 14-3-3 proteins in adrenal chromaffin cells and demonstration of isoform-specific phospholipid binding. Biochem. J. 301, 305-310 (Pubitemid 24214715)
29. Martin, H., Rostas, J., Patel, Y., and Aitken, A. (1994) Subcellular localisation of 14-3-3 isoforms in rat brain using specific antibodies. J. Neurochem. 63, 2259-2265 (Pubitemid 24370003)
30. Halskau, 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
31. Bustad, H. J., Skjaerven, L., Ying, M., Halskau, O., Baumann, A., Rodriguez-Larrea, D., Costas, M., Underhaug, J., Sanchez-Ruiz, J. M., and Martinez, A. (2012) The peripheral binding of 14-3-3gamma to membranes involves isoform-specific histidine residues. PLoS ONE 7, e49671
32. Skjevik, A. A., Mileni, M., Baumann, A., Halskau, O., Teigen, K., Stevens, R. C., and Martinez, A. (2014) The N-terminal sequence of tyrosine hydroxylase is a conformationally versatile motif that binds 14-3-3 proteins and membranes. J. Mol. Biol. 426, 150-168
33. 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 (Pubitemid 32467064)
34. Obsilova, V., Nedbalkova, E., Silhan, J., Boura, E., Herman, P., Vecer, J., Sulc, M., Teisinger, J., Dyda, F., and Obsil, T. (2008) The 14-3-3 protein affects the conformation of the regulatory domain of human tyrosine hydroxylase. Biochemistry 47, 1768-1777 (Pubitemid 351231226)
35. Yaffe, M. B. (2002) How do 14-3-3 proteins work? Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57
36. Gardino, A. K., Smerdon, S. J., and Yaffe, M. B. (2006) Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the x-ray crystal structures of all human 14-3-3 isoforms. Semin. Cancer Biol. 16, 173-182 (Pubitemid 43796126)
37. Bobrovskaya, L., Dunkley, P. R., and Dickson, P. W. (2004) Phosphorylation of Ser19 increases both Ser40 phosphorylation and enzyme activity of tyrosine hydroxylase in intact cells. J. Neurochem. 90, 857-864 (Pubitemid 39099967)
38. Kostelecky, B., Saurin, A. T., Purkiss, A., Parker, P. J., and McDonald, N. Q. (2009) Recognition of an intra-chain tandem 14-3-3 binding site within PKCepsilon. EMBO Rep. 10, 983-989
39. Obsil, T., Ghirlando, R., Anderson, D. E., Hickman, A. B., and Dyda, F. (2003) Two 14-3-3 binding motifs are required for stable association of Forkhead transcription factor FOXO4 with 14-3-3 proteins and inhibition of DNA binding. Biochemistry 42, 15264-15272 (Pubitemid 38031725)
40. Molzan, M., and Ottmann, C. (2012) Synergistic binding of the phosphorylated S233- and S259-binding sites of C-RAF to one 14-3-3zeta dimer. J. Mol. Biol. 423, 486-495
41. Johnson, C., Crowther, S., Stafford, M. J., Campbell, D. G., Toth, R., and MacKintosh, C. (2010) Bioinformatic and experimental survey of 14-3-3- binding sites. Biochem. J. 427, 69-78
42. Sharon, M., and Robinson, C. V. (2007) The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 76, 167-193
43. Heck, A. J. (2008) Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 5, 927-933
44. Bogomolovas, J., Simon, B., Sattler, M., and Stier, G. (2009) Screening of fusion partners for high yield expression and purification of bioactive viscotoxins. Protein Expr. Purif. 64, 16-23
45. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41, 207-234
46. Kopperud, R., Christensen, A. E., Kjarland, E., Viste, K., Kleivdal, H., and Doskeland, S. O. (2002) Formation of inactive cAMP-saturated holoenzyme of cAMP-dependent protein kinase under physiological conditions. J. Biol. Chem. 277, 13443-13448 (Pubitemid 34967939)
47. Kastner, B., Fischer, N., Golas, M. M., Sander, B., Dube, P., Boehringer, D., Hartmuth, K., Deckert, J., Hauer, F., Wolf, E., Uchtenhagen, H., Urlaub, H., Herzog, F., Peters, J. M., Poerschke, D., Luhrmann, R., and Stark, H. (2008) GraFix: sample preparation for single-particle electron cryomicroscopy. Nat. Methods 5, 53-55
48. de la Rosa-Trevin, J. M., Oton, J., Marabini, R., Zaldivar, A., Vargas, J., Carazo, J. M., and Sorzano, C. O. (2013) Xmipp 3.0: an improved software suite for image processing in electron microscopy. J. Struct. Biol. 184, 321-328
49. Scheres, S. H., Nunez-Ramirez, R., Sorzano, C. O., Carazo, J. M., and Marabini, R. (2008) Image processing for electron microscopy singleparticle analysis using XMIPP. Nat. Protoc. 3, 977-990 (Pubitemid 351818686)
50. Scheres, S. H., Valle, M., Nunez, R., Sorzano, C. O., Marabini, R., Herman, G. T., and Carazo, J. M. (2005) Maximum-likelihood multi-reference refinement for electron microscopy images. J. Mol. Biol. 348, 139-149 (Pubitemid 40461846)
51. Yang, X., Lee, W. H., Sobott, F., Papagrigoriou, E., Robinson, C. V., Grossmann, J. G., Sundstrom, M., Doyle, D. A., and Elkins, J. M. (2006) Structural basis for protein-protein interactions in the 14-3-3 protein family. Proc. Natl. Acad. Sci. U.S.A. 103, 17237-17242 (Pubitemid 44788953)
52. Benesch, J. L., Aquilina, J. A., Ruotolo, B. T., Sobott, F., and Robinson, C. V. (2006) Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies. Chem. Biol. 13, 597-605
53. van Duijn, E., Barbu, I. M., Barendregt, A., Jore, M. M., Wiedenheft, B., Lundgren, M., Westra, E. R., Brouns, S. J., Doudna, J. A., van der Oost, J., and Heck, A. J. (2012) Native tandem and ion mobility mass spectrometry highlight structural and modular similarities in clustered-regularly-interspaced shot-palindromic-repeats (CRISPR)-associated protein complexes from Escherichia coli and Pseudomonas aeruginosa. Mol. Cell. Proteomics 11, 1430-1441
54. Johnson, C., Tinti, M., Wood, N. T., Campbell, D. G., Toth, R., Dubois, F., Geraghty, K. M., Wong, B. H., Brown, L. J., Tyler, J., Gernez, A., Chen, S., Synowsky, S., and MacKintosh, C. (2011) Visualization and biochemical analyses of the emerging mammalian 14-3-3-phosphoproteome. Mol. Cell. Proteomics 10, M110.005751
55. Obsil, T., Ghirlando, R., Klein, D. C., Ganguly, S., and Dyda, F. (2001) Crystal structure of the 14-3-3zeta:serotonin N-acetyltransferase complex. A role for scaffolding in enzyme regulation. Cell 105, 257-267 (Pubitemid 32429515)
56. Rezabkova, L., Man, P., Novak, P., Herman, P., Vecer, J., Obsilova, V., and Obsil, T. (2011) Structural basis for the 14-3-3 protein-dependent inhibition of the regulator of G protein signaling 3 (RGS3) function. J. Biol. Chem. 286, 43527-43536
57. Rezabkova, L., Boura, E., Herman, P., Vecer, J., Bourova, L., Sulc, M., Svoboda, P., Obsilova, V., and Obsil, T. (2010) 14-3-3 protein interacts with and affects the structure of RGS domain of regulator of G protein signaling 3 (RGS3). J. Struct. Biol. 170, 451-461
58. Daubner, S. C., and Piper, M. M. (1995) Deletion mutants of tyrosine hydroxylase identify a region critical for heparin binding. Protein Sci. 4, 538-541
59. 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 A and its implications for inherited neurodegenerative diseases. Nat. Struct. Biol. 4, 578-585
60. 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
61. Lindgren, N., Xu, Z. Q., Lindskog, M., Herrera-Marschitz, M., Goiny, M., Haycock, J., Goldstein, M., Hokfelt, T., and Fisone, G. (2000) Regulation of tyrosine hydroxylase activity and phosphorylation at Ser(19) and Ser(40) via activation of glutamate NMDA receptors in rat striatum. J. Neurochem. 74, 2470-2477 (Pubitemid 30314223)
62. Lou, H., Montoya, S. E., Alerte, T. N., Wang, J., Wu, J., Peng, X., Hong, C. S., Friedrich, E. E., Mader, S. A., Pedersen, C. J., Marcus, B. S., McCormack, A. L., Di Monte, D. A., Daubner, S. C., and Perez, R. G. (2010) Serine 129 phosphorylation reduces the ability of alpha-synuclein to regulate tyrosine hydroxylase and protein phosphatase 2A in vitro and in vivo. J. Biol. Chem. 285, 17648-17661
63. Sachs, N. A., and Vaillancourt, R. R. (2004) Cyclin-dependent kinase 11p110 and casein kinase 2 (CK2) inhibit the interaction between tyrosine hydroxylase and 14-3-3. J. Neurochem. 88, 51-62 (Pubitemid 38030208)