Scavenging of 14-3-3 proteins reveals their involvement in the cell-surface transport of ATP-sensitive K+ channels

Journal of Cell Science

Volumn 119, Issue 20, 2006, Pages 4353-4363

  Heusser, Katja ^a   Yuan, Hebao ^a   Neagoe, Ioana ^a   Tarasov, Andrei I ^b   Ashcroft, Frances M ^b   Schwappach, Blanche ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

14 3 3 proteins; ABC proteins; ER localization signals; Inward rectifier potassium channels; Membrane protrein assembly; Quality control

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; ARGININE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; PROTEIN 14 3 3;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SURFACE; CELL TRANSPORT; ENDOPLASMIC RETICULUM; FEMALE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

14-3-3 PROTEINS; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; ARGININE; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OOCYTES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; XENOPUS;

EID: 33751176024     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03196     Document Type: Article

References (37)

1. Aguilar-Bryan, L. and Bryan, J. (1999). Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr Rev. 20, 101-135.
2. Anderson, H. A. and Roche, P. A. (1998). Phosphorylation regulates the delivery of MHC class II invariant chain complexes to antigen processing compartments. J. Immunol. 160, 4850-4858.
3. Antcliff, J. F., Haider, S., Proks, P., Sansom, M. S. and Ashcroft, F. M. (2005). Functional analysis of a structural model of the ATP-binding site of the KATP channel Kir6.2 subunit. EMBO J. 24, 229-239.
4. Asfari, M., Janjic, D., Meda, P., Li, G., Halban, P. A. and Wollheim, C. B. (1992). Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130, 167-178.
5. Coblitz, B., Shikano, S., Wu, M., Gabelli, S. B., Cockrell, L. M., Spieker, M., Hanyu, Y., Fu, H., Amzel, L. M. and Li, M. (2005). C-terminal recognition by 14-3-3 proteins for surface expression of membrane receptors. J. Biol. Chem. 280, 36263-36272.
6. Collins, A., Chuang, H., Jan, Y. N. and Jan, L. Y. (1997). Scanning mutagenesis of the putative transmembrane segments of Kir2.1, an inward rectifier potassium channel. Proc. Natl. Acad. Sci. USA 94, 5456-5460.
7. Dedio, J., Jahnen-Dechent, W., Bachmann, M. and Muller-Esterl, W. (1998). The multiligand-binding protein gC1qR, putative C1q receptor, is a mitochondrial protein. J. Immunol. 160, 3534-3542.
8. Geng, X., Li, L., Watkins, S., Robbins, P. D. and Drain, P. (2003). The insulin secretory granule is the major site of K(ATP) channels of the endocrine pancreas. Diabetes 52, 767-776.
9. Giles, N., Forrest, A. and Gabrielli, B. (2003). 14-3-3 acts as an intramolecular bridge to regulate cdc25B localization and activity. J. Biol. Chem. 278, 28580-28587.
10. Harbury, P. B., Zhang, T., Kim, P. S. and Alber, T. (1993). A switch between two-,three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262, 1401-1407.
11. Jadot M., Hofmann, M. W., Graf, R., Quader, H. and Martoglio, B. (1995). Protein insertion into the endoplasmic reticulum of permeabilized cells. FEBS Lett. 371, 145-148.
12. Kuwana, T., Peterson, P. A. and Karlsson, L. (1998). Exit of major histocompatibility complex class II-invariant chain p35 complexes from the endoplasmic reticulum is modulated by phosphorylation. Proc. Natl. Acad Sci. USA 95, 1056-1061.
13. Liman, E. R, Tytgat, J. and Hess, P. (1992). Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9, 861-871.
14. Liu, X., Constantinescu, S. N., Sun, Y., Bogan, J. S., Hirsch, D., Weinberg, R. A. and Lodish, H. F. (2000). Generation of mammalian cells stably expressing multiple genes at predetermined levels. Anal. Biochem. 280, 20-28.
15. Michelsen, K., Mrowiec, T., Duderstadt, K. E., Frey, S., Minor, D. L., Mayer, M. P. and Schwappach, B. (2006). A multimeric membrane protein reveals 14-3-3 isoform specificity in forward transport in yeast. Traffic 7, 903-916.
16. Mikhailov, M. V., Campbell, J. D., de Wet, H., Shimomura, K., Zadek, B., Collins, R. F., Sansom, M. S., Ford, R. C. and Ashcroft, F. M. (2005). 3-D structural and functional characterization of the purified KATP channel complex Kir6.2-SUR1. EMBO J. 24, 4166-4175.
17. Mrowiec, T. and Schwappach, B. (2006). 14-3-3 proteins in membrane protein transport. Biol. Chem. 387,1227-1236.
18. Muta, T., Kang, D., Kitajima, S., Fujiwara, T. and Hamasaki, N. (1997). p32 protein, a splicing factor 2-associated protein, is localized in mitochondrial matrix and is functionally important in maintaining oxidative phosphorylation. J. Biol. Chem. 272, 24363-24370.
19. O'Kelly, L., Butler, M. H., Zilberberg, N. and Goldstein, S. A. (2002). Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111, 577-588.
20. Petosa, C., Masters, S. C., Bankston, L. A., Pohl, J., Wang, B., Fu, H. and Liddington, R. C. (1998). 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J. Biol. Chem. 273, 16305-16310.
21. Pouli, A. E., Emmanouilidou, E., Zhao, C., Wasmeier, C., Hutton, J. C. and Rutter, G. A. (1998). Secretory-granule dynamics visualized in vivo with a phogrin-green fluorescent protein chimaera. Biochem. J. 333, 193-199.
22. Proks, P., Antcliff, J. F., Lippiat, J., Gloyn, A. L., Hattersley, A. T. and Ashcroft, F. M. (2004). Molecular basis of Kir6.2 mutations associated with neonatal diabetes for neonatal diabetes plus neurological features. Proc. Natl. Acad. Sci. USA 101, 17539-17544.
23. Rajan, S., Preisig-Muller, R., Wischmeyer, E., Nehring, R., Hanley, P. J., Renigunta, V., Musset, B., Schlichthori, G., Derst, C., Karschin, A. et al. (2002). Interaction with 14-3-3 proteins promotes functional expression of the potassium channels TASK-I and TASK-3. J. Physiol. 545, 13-26.
24. Shikano, S. and Li, M. (2003). Membrane receptor trafficking: evidence of proximal and distal zones conferred by two independent endoplasmic reticulum localization signals. Proc. Natl. Acad. Sci. USA 100, 5783-5788.
25. Shikano, S., Coblitz, B., Sun, H. and Li, M. (2005). Genetic isolation of transport signals directing cell surface expression. Nat. Cell Biol. 7, 985-992.
26. Shikano, S., Coblitz, B., Wu, M. and Li, M. (2006). 14-3-3 proteins: regulation of endoplasmic reticulum localization and surface expression of membrane proteins. Trends Cell Biol. 16, 370-375.
27. Shyng, S. and Nichols, C. G. (1997). Octameric stoichiometry of the KATP channel complex. J. Gen. Physiol. 110, 655-664.
28. Trube G., Rorsman, P. and Ohno-Shosaku, T. (1986). Opposite effects of tolbutamide and diazoxide on the ATP-dependent K+ channel in mouse pancreatic beta-cells. Pflugers Arch. 407, 493-499.
29. Tucker, S. J., Bond, C. T., Herson, P., Pessia, M. and Adelman, J. P. (1996). Inhibitory interactions between two inward rectifier K+ channel subunits mediated by the transmembrane domains. J. Biol. Chem. 271, 5866-5870.
30. Tucker, S. J., Gribble, F. M., Zhao, C., Trapp, S. and Ashcroft, F. M. (1997). Truncation of Kir6.2 produces ATP-sensifive K+ channels in the absence of the sulphonylurea receptor. Nature 387, 179-183.
31. Varadi, A., Grant A., McCormack, M., Nicolson, T., Magistri, M., Mitchell, K. J., Halestrap, A. P., Yuan, H., Schwappach, B. and Rutter, G. A. (2006). Intracellular ATP-sensifive K+ channels in mouse pancreatic beta cells: against a role in organelle cation homeostasis. Diabetologia 49, 1567-1577.
32. Wang, B., Yang, H., Liu, Y. C., Jelinek, T., Zhang, L., Ruoslahti, E. and Fu, H. (1999). Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 38, 12499-12504.
33. Wasmeier, C. and Hutton, J. C. (1996). Molecular cloning of phogrin, a protein-tyrosine phosphatase homologue localized to insulin secretory granule membranes. J. Biol. Chem. 271, 18161-18170.
34. Wurtele, M., Jelich-Ottmann, C., Wittinghofer, A. and Oecking, C. (2003). Structural view of a fungal toxin acting on a 14-3-3 regulatory complex. EMBO J. 22, 987-994.
35. Yaffe, M. B., Rittinger, K., Volinia, S., Caron, P. R., Aitken, A., Leffers, H., Gamblin, S. J., Smerdon, S. J, and Cantley, L. C. (1997). The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961-971.
36. Yuan, H., Michelsen, K. and Schwappach, B. (2003). 14-3-3 dimers probe the assembly status of multimeric membrane proteins. Curr. Biol. 13, 638-646.
37. Zerangue, N., Schwappach, B., Jan, Y. N. and Jan, L. Y. (1999). A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22, 537-549.