Cyclic GMP-dependent stimulation of serotonin transport does not involve direct transporter phosphorylation by cGMP-dependent protein kinase

Journal of Biological Chemistry

Volumn 287, Issue 43, 2012, Pages 36051-36058

  Wong, Albert ^a   Zhang, Yuan Wei ^a   Jeschke, Grace R ^a   Turk, Benjamin E ^a   Rudnick, Gary ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 ,4-METHYLENEDIOXYMETHAMPHETAMINE; ATP ANALOGS; CULTURED CELL; GUANYLYL CYCLASE; IN-VITRO; KINASE CASCADE; MODEL PEPTIDES; NITRIC-OXIDE SYNTHASE; P38 MITOGEN-ACTIVATED PROTEIN KINASE; PEPTIDE LIBRARY; PHOSPHORYLATION SITES; PROTEIN KINASE; PROTEIN SUBSTRATE; RADIOLABEL; SEROTONIN TRANSPORTERS; SIGNALING PATHWAYS; VASODILATOR-STIMULATED PHOSPHOPROTEINS; WILD TYPES;

CYTOLOGY; NITRIC OXIDE; PEPTIDES; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ENZYMES;

6 N BENZYLADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE I ALPHA; MITOGEN ACTIVATED PROTEIN KINASE P38; SEROTONIN; SEROTONIN TRANSPORTER; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

AMINE TRANSPORT; ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME SPECIFICITY; IN VITRO STUDY; PEPTIDE LIBRARY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AMINO ACID SUBSTITUTION; BIOLOGICAL TRANSPORT, ACTIVE; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE I; HEK293 CELLS; HUMANS; MUTATION, MISSENSE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84867799491     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.394726     Document Type: Article

References (33)

1. Kilic, F., Murphy, D. L., and Rudnick, G. (2003) A human serotonin transporter mutation causes constitutive activation of transport activity. Mol. Pharmacol. 64, 440-446 (Pubitemid 36910008)
2. Prasad, H. C., Zhu, C. B., McCauley, J. L., Samuvel, D. J., Ramamoorthy, S., Shelton, R. C., Hewlett, W. A., Sutcliffe, J. S., and Blakely, R. D. (2005) Human serotonin transporter variants display altered sensitivity to protein kinase G and p38 mitogen-activated protein kinase. Proc. Natl. Acad. Sci. U.S.A. 102, 11545-11550 (Pubitemid 41153856)
3. Miller, K. J., and Hoffman, B. J. (1994) Adenosine A3 receptors regulate serotonin transport via nitric oxide and cGMP. J. Biol. Chem. 269, 27351-27356
4. Ramamoorthy, S., Samuvel, D. J., Buck, E. R., Rudnick, G., and Jayanthi, L. D. (2007) Phosphorylation of threonine residue 276 is required for acute regulation of serotonin transporter by cyclic GMP. J. Biol. Chem. 282, 11639-11647 (Pubitemid 47100698)
5. Zhang, Y. W., Gesmonde, J., Ramamoorthy, S., and Rudnick, G. (2007) Serotonin transporter phosphorylation by cGMP-dependent protein kinase is altered by a mutation associated with obsessive compulsive disorder. J. Neurosci. 27, 10878-10886 (Pubitemid 47535855)
6. Zhang, Y. W., and Rudnick, G. (2011) Myristoylation of cGMP-dependent protein kinase dictates isoform specificity for serotonin transporter regulation. J. Biol. Chem. 286, 2461-2468
7. Steiner, J. A., Carneiro, A. M., Wright, J., Matthies, H. J., Prasad, H. C., Nicki, C. K., Dostmann, W. R., Buchanan, C. C., Corbin, J. D., Francis, S. H., and Blakely, R. D. (2009) cGMP-dependent protein kinase Iα associates with the antidepressant-sensitive serotonin transporter and dictates rapid modulation of serotonin uptake. Mol. Brain 2, 26
8. Zhu, C. B., Hewlett, W. A., Feoktistov, I., Biaggioni, I., and Blakely, R. D. (2004) Adenosine receptor, protein kinase G, and p38 mitogen-activated protein kinase-dependent up-regulation of serotonin transporters involves both transporter trafficking and activation. Mol. Pharmacol. 65, 1462-1474 (Pubitemid 38668304)
9. Zhu, C. B., Carneiro, A. M., Dostmann, W. R., Hewlett, W. A., and Blakely, R. D. (2005) p38 MAPK activation elevates serotonin transport activity via a trafficking-independent, protein phosphatase 2A-dependent process. J. Biol. Chem. 280, 15649-15658 (Pubitemid 40616683)
10. Mitchell, R. D., Glass, D. B., Wong, C. W., Angelos, K. L., and Walsh, D. A. (1995) Heat-stable inhibitor protein derived peptide substrate analogs: phosphorylation by cAMP-dependent and cGMP-dependent protein kinases. Biochemistry 34, 528-534
11. Tegge, W., Frank, R., Hofmann, F., and Dostmann, W. R. (1995) Determination of cyclic nucleotide-dependent protein kinase substrate specificity by the use of peptide libraries on cellulose paper. Biochemistry 34, 10569-10577
12. Goldsmith, E. J., Akella, R., Min, X., Zhou, T., and Humphreys, J. M. (2007) Substrate and docking interactions in serine/threonine protein kinases. Chem Rev 107, 5065-5081 (Pubitemid 350225869)
13. Bishop, A. C., Ubersax, J. A., Petsch, D. T., Matheos, D. P., Gray, N. S., Blethrow, J., Shimizu, E., Tsien, J. Z., Schultz, P. G., Rose, M. D., Wood, J. L., Morgan, D. O., and Shokat, K. M. (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401
14. Shah, K., Liu, Y., Deirmengian, C., and Shokat, K. M. (1997) Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc. Natl. Acad. Sci. U.S.A. 94, 3565-3570 (Pubitemid 27180412)
15. Boyle, S. N., and Koleske, A. J. (2007) Use of a chemical genetic technique to identify myosin IIb as a substrate of the Abl-related gene (Arg) tyrosine kinase. Biochemistry 46, 11614-11620 (Pubitemid 47585507)
16. Blethrow, J., Zhang, C., Shokat, K. M., and Weiss, E. L. (2004) Curr. Protoc. Mol. Biol. Chapter 18, Unit 18.11
17. Sheridan, D. L., Kong, Y., Parker, S. A., Dalby, K. N., and Turk, B. E. (2008) Substrate discrimination among mitogen-activated protein kinases through distinct docking sequence motifs. J. Biol. Chem. 283, 19511-19520
18. Mok, J., Kim, P. M., Lam, H. Y., Piccirillo, S., Zhou, X., Jeschke, G. R., Sheridan, D. L., Parker, S. A., Desai, V., Jwa, M., Cameroni, E., Niu, H., Good, M., Remenyi, A., Ma, J. L., Sheu, Y. J., Sassi, H. E., Sopko, R., Chan, C. S., De Virgilio, C., Hollingsworth, N. M., Lim, W. A., Stern, D. F., Stillman, B., Andrews, B. J., Gerstein, M. B., Snyder, M., and Turk, B. E. (2010) Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Sci. Signal. 3, ra12
19. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
20. Smolenski, A., Bachmann, C., Reinhard, K., Hönig-Liedl, P., Jarchau, T., Hoschuetzky, H., and Walter, U. (1998) Analysis and regulation of vasodilator- stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J. Biol. Chem. 273, 20029-20035 (Pubitemid 28377554)
21. Lohmann, S. M., and Walter, U. (2005) Tracking functions of cGMP-dependent protein kinases (cGK). Front Biosci. 10, 1313-1328
22. Samuvel, D. J., Jayanthi, L. D., Bhat, N. R., and Ramamoorthy, S. (2005) A role for p38 mitogen-activated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression. J. Neurosci. 25, 29-41 (Pubitemid 40110763)
23. Knight, Z. A., and Shokat, K. M. (2005) Features of selective kinase inhibitors. Chem. Biol. 12, 621-637 (Pubitemid 43142039)
24. Ubersax, J. A., Woodbury, E. L., Quang, P. N., Paraz, M., Blethrow, J. D., Shah, K., Shokat, K. M., and Morgan, D. O. (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425, 859-864 (Pubitemid 37351471)
25. Carlson, S. M., Chouinard, C. R., Labadorf, A., Lam, C. J., Schmelzle, K., Fraenkel, E., and White, F. M. (2011) Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3. Sci. Signal. 4, rs11
26. Banko, M. R., Allen, J. J., Schaffer, B. E., Wilker, E. W., Tsou, P., White, J. L., Villén, J., Wang, B., Kim, S. R., Sakamoto, K., Gygi, S. P., Cantley, L. C., Yaffe, M. B., Shokat, K. M., and Brunet, A. (2011) Chemical genetic screen for AMPKα2 substrates uncovers a network of proteins involved in mitosis. Mol. Cell 44, 878-892
27. Hornbeck, P. V., Chabra, I., Kornhauser, J. M., Skrzypek, E., and Zhang, B. (2004) PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4, 1551-1561 (Pubitemid 38738314)
28. Zhu, C. B., Lindler, K. M., Campbell, N. G., Sutcliffe, J. S., Hewlett, W. A., and Blakely, R. D. (2011) Colocalization and regulated physical association of presynaptic serotonin transporters with A adenosine receptors. Mol. Pharmacol. 80, 458-465
29. Chanrion, B., Mannoury la Cour, C., Bertaso, F., Lerner-Natoli, M., Freissmuth, M., Millan, M. J., Bockaert, J., and Marin, P. (2007) Physical interaction between the serotonin transporter and neuronal nitric oxide synthase underlies reciprocal modulation of their activity. Proc. Natl. Acad. Sci. U.S.A. 104, 8119-8124 (Pubitemid 47185885)
30. Bauman, A. L., Apparsundaram, S., Ramamoorthy, S., Wadzinski, B. E., Vaughan, R. A., and Blakely, R. D. (2000) Cocaine and antidepressantsensitive biogenic amine transporters exist in regulated complexes with protein phosphatase 2A. J. Neurosci. 20, 7571-7578
31. Ciccone, M. A., Timmons, M., Phillips, A., and Quick, M. W. (2008) Calcium/ calmodulin-dependent kinase II regulates the interaction between the serotonin transporter and syntaxin 1A. Neuropharmacology 55, 763-770
32. Miller, M. L., Jensen, L. J., Diella, F., Jørgensen, C., Tinti, M., Li, L., Hsiung, M., Parker, S. A., Bordeaux, J., Sicheritz-Ponten, T., Olhovsky, M., Pasculescu, A., Alexander, J., Knapp, S., Blom, N., Bork, P., Li, S., Cesareni, G., Pawson, T., Turk, B. E., Yaffe, M. B., Brunak, S., and Linding, R. (2008) Linear motif atlas for phosphorylation-dependent signaling. Sci. Signal. 1, ra2
33. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190 (Pubitemid 38811555)