EFR3s are palmitoylated plasma membrane proteins that control responsiveness to G-protein-coupled receptors

Journal of Cell Science

Volumn 128, Issue 1, 2015, Pages 118-128

  Bojjireddy, Naveen ^a   Guzman Hernandez, Maria Luisa ^a   Reinhard, Nathalie Renée ^b   Jovic, Marko ^a   Balla, Tamas ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Angiotensin II; EFR3; GPCR; Phosphoinositide; PI 4 kinase; Receptor desensitization

Indexed keywords

CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITIDE; PROTEIN EFR3; UNCLASSIFIED DRUG; AGTR1 PROTEIN, HUMAN; ANGIOTENSIN 1 RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; ISOPRENALINE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTROLLED STUDY; HUMAN; HUMAN CELL; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; LIPOYLATION; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SECOND MESSENGER;

EUKARYOTA; MAMMALIA;

ADRENERGIC BETA-AGONISTS; CYCLIC AMP; HEK293 CELLS; HUMANS; ISOPROTERENOL; LIPOYLATION; PHOSPHORYLATION; RECEPTOR, ANGIOTENSIN, TYPE 1; SECOND MESSENGER SYSTEMS;

EID: 84921694782     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.157495     Document Type: Article

References (34)

1. Adjobo-Hermans, M. J., Goedhart, J., van Weeren, L., Nijmeijer, S., Manders, E. M., Offermanns, S. and Gadella, T. W., Jr (2011). Real-time visualization of heterotrimeric G protein Gq activation in living cells. BMC Biol. 9, 32.
2. Audhya, A. and Emr, S. D. (2002). Stt4 PI 4-kinase localizes to the plasmamembrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2, 593-605.
3. Baird, D., Stefan, C., Audhya, A., Weys, S. and Emr, S. D. (2008). Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3. J. Cell Biol. 183, 1061-1074.
4. Balla, A., Tuymetova, G., Tsiomenko, A., Várnai, P. and Balla, T. (2005). A plasma membrane pool of phosphatidylinositol 4-phosphate is generated by phosphatidylinositol 4-kinase type-III alpha: studies with the PH domains of the oxysterol binding protein and FAPP1. Mol. Biol. Cell 16, 1282-1295.
5. Balla, A., Kim, Y. J., Varnai, P., Szentpetery, Z., Knight, Z., Shokat, K. M. and Balla, T. (2008). Maintenance of hormone-sensitive phosphoinositide pools in the plasma membrane requires phosphatidylinositol 4-kinase IIIalpha. Mol. Biol. Cell 19, 711-721.
6. Barak, L. S., Ferguson, S. S., Zhang, J. and Caron, M. G. (1997). A betaarrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J. Biol. Chem. 272, 27497-27500.
7. Berridge, M. J. (1984). Inositol trisphosphate and diacylglycerol as second messengers. Biochem. J. 220, 345-360.
8. Bojjireddy, N., Botyanszki, J., Hammond, G., Creech, D., Peterson, R., Kemp, D. C., Snead, M., Brown, R., Morrison, A., Wilson, S. et al. (2014). Pharmacological and genetic targeting of pPI4KA reveals its important role in maintaining plasma membrane PtdIns4p and PtdIns(4,5)p2 levels. J. Biol. Chem. 289, 6120-6132.
9. Goedhart, J., van Weeren, L., Adjobo-Hermans, M. J., Elzenaar, I., Hink, M. A. and Gadella, T. W., Jr (2011). Quantitative co-expression of proteins at the single cell level-application to a multimeric FRET sensor. PLoS ONE 6, e27321.
10. Huang, F. D., Matthies, H. J., Speese, S. D., Smith, M. A. and Broadie, K. (2004). Rolling blackout, a newly identified PIP2-DAG pathway lipase required for Drosophila phototransduction. Nat. Neurosci. 7, 1070-1078.
11. Hunyady, L., Bor, M., Balla, T. and Catt, K. J. (1994). Identification of a cytoplasmic Ser-Thr-Leu motif that determines agonist-induced internalization of the AT1 angiotensin receptor. J. Biol. Chem. 269, 31378-31382.
12. Hunyady, L., Baukal, A. J., Gaborik, Z., Olivares-Reyes, J. A., Bor, M., Szaszak, M., Lodge, R., Catt, K. J. and Balla, T. (2002). Differential PI 3-kinase dependence of early and late phases of recycling of the internalized AT1 angiotensin receptor. J. Cell Biol. 157, 1211-1222.
13. Iyer, V., Tran, T. M., Foster, E., Dai, W., Clark, R. B. and Knoll, B. J. (2006). Differential phosphorylation and dephosphorylation of beta2-adrenoceptor sites Ser262 and Ser355,356. Br. J. Pharmacol. 147, 249-259.
14. Klarenbeek, J. and Jalink, K. (2014). Detecting cAMP with an EPAC-based FRET sensor in single living cells. Methods Mol. Biol. 1071, 49-58.
15. Korzeniowski, M. K., Popovic, M. A., Szentpetery, Z., Varnai, P., Stojilkovic, S. S. and Balla, T. (2009). Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J. Biol. Chem. 284, 21027-21035.
16. Linder, M. E., Kleuss, C. and Mumby, S. M. (1995). Palmitoylation of G-protein alpha subunits. Methods Enzymol. 250, 314-330.
17. Luttrell, L. M. and Lefkowitz, R. J. (2002). The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J. Cell Sci. 115, 455-465.
18. Montini, E., Rugarli, E. I., Van de Vosse, E., Andolfi, G., Mariani, M., Puca, A. A., Consalez, G. G., den Dunnen, J. T., Ballabio, A. and Franco, B. (1997). A novel human serine-threonine phosphatase related to the Drosophila retinal degeneration C (rdgC) gene is selectively expressed in sensory neurons of neural crest origin. Hum. Mol. Genet. 6, 1137-1145.
19. Moore, C. A., Milano, S. K. and Benovic, J. L. (2007). Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol. 69, 451-482.
20. Nakanishi, S., Catt, K. J. and Balla, T. (1995). A wortmannin-sensitive phosphatidylinositol 4-kinase that regulates hormone-sensitive pools of inositolphospholipids. Proc. Natl. Acad. Sci. USA 92, 5317-5321.
21. Nakatsu, F., Baskin, J. M., Chung, J., Tanner, L. B., Shui, G., Lee, S. Y., Pirruccello, M., Hao, M., Ingolia, N. T., Wenk, M. R. et al. (2012). PtdIns4P synthesis by PI4KIIIa at the plasma membrane and its impact on plasma membrane identity. J. Cell Biol. 199, 1003-1016.
22. Olivares-Reyes, J. A., Smith, R. D., Hunyady, L., Shah, B. H. and Catt, K. J. (2001). Agonist-induced signaling, desensitization, and internalization of a phosphorylation-deficient AT1A angiotensin receptor. J. Biol. Chem. 276, 37761-37768.
23. Ramulu, P., Kennedy, M., Xiong, W. H., Williams, J., Cowan, M., Blesh, D., Yau, K. W., Hurley, J. B. and Nathans, J. (2001). Normal light response, photoreceptor integrity, and rhodopsin dephosphorylation in mice lacking both protein phosphatases with EF hands (PPEF-1 and PPEF-2). Mol. Cell. Biol. 21, 8605-8614.
24. Reiter, E., Ahn, S., Shukla, A. K. and Lefkowitz, R. J. (2012). Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52, 179-197.
25. Sherman, P. M., Sun, H., Macke, J. P., Williams, J., Smallwood, P. M. and Nathans, J. (1997). Identification and characterization of a conserved family of protein serine/threonine phosphatases homologous to Drosophila retinal degeneration C. Proc. Natl. Acad. Sci. USA 94, 11639-11644.
26. Steele, F. R., Washburn, T., Rieger, R. and O'Tousa, J. E. (1992). Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase. Cell 69, 669-676.
27. Szentpetery, Z., Balla, A., Kim, Y. J., Lemmon, M. A. and Balla, T. (2009). Live cell imaging with protein domains capable of recognizing phosphatidylinositol 4,5-bisphosphate; a comparative study. BMC Cell Biol. 10, 67.
28. Vasudevan, N. T., Mohan, M. L., Goswami, S. K. and Naga Prasad, S. V. (2011). Regulation of b-adrenergic receptor function: an emphasis on receptor resensitization. Cell Cycle 10, 3684-3691.
29. Vijayakrishnan, N., Woodruff, E. A., III and Broadie, K. (2009). Rolling blackout is required for bulk endocytosis in non-neuronal cells and neuronal synapses. J. Cell Sci. 122, 114-125.
30. Vijayakrishnan, N., Phillips, S. E. and Broadie, K. (2010). Drosophila rolling blackout displays lipase domain-dependent and-independent endocytic functions downstream of dynamin. Traffic 11, 1567-1578.
31. Vinós, J., Jalink, K., Hardy, R. W., Britt, S. G. and Zuker, C. S. (1997). A G protein-coupled receptor phosphatase required for rhodopsin function. Science 277, 687-690.
32. Wei, H., Ahn, S., Shenoy, S. K., Karnik, S. S., Hunyady, L., Luttrell, L. M. and Lefkowitz, R. J. (2003). Independent beta-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc. Natl. Acad. Sci. USA 100, 10782-10787.
33. Yang, S. D., Fong, Y. L., Benovic, J. L., Sibley, D. R., Caron, M. G. and Lefkowitz, R. J. (1988). Dephosphorylation of the beta 2-adrenergic receptor and rhodopsin by latent phosphatase 2. J. Biol. Chem. 263, 8856-8858.
34. Yu, S. S., Lefkowitz, R. J. and Hausdorff, W. P. (1993). Beta-adrenergic receptor sequestration. A potential mechanism of receptor resensitization. J. Biol. Chem. 268, 337-341.