Skip to main content

Advertisement

Log in

The role of protein–protein interactions in the intracellular traffic of the potassium channels TASK-1 and TASK-3

  • Invited Review
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

The intracellular transport of membrane proteins is controlled by trafficking signals: Short peptide motifs that mediate the contact with COPI, COPII or various clathrin-associated coat proteins. In addition, many membrane proteins interact with accessory proteins that are involved in the sorting of these proteins to different intracellular compartments. In the K2P channels, TASK-1 and TASK-3, the influence of protein–protein interactions on sorting decisions has been studied in some detail. Both TASK paralogues interact with the adaptor protein 14-3-3; TASK-1 interacts, in addition, with the adaptor protein p11 (S100A10) and the endosomal SNARE protein syntaxin-8. The role of these interacting proteins in controlling the intracellular traffic of the channels and the underlying molecular mechanisms are summarised in this review. In the case of 14-3-3, the interacting protein masks a retention signal in the C-terminus of the channel; in the case of p11, the interacting protein carries a retention signal that localises the channel to the endoplasmic reticulum; and in the case of syntaxin-8, the interacting protein carries an endocytosis signal that complements an endocytosis signal of the channel. These examples illustrate some of the mechanisms by which interacting proteins may determine the itinerary of a membrane protein within a cell and suggest that the intracellular traffic of membrane proteins may be adapted to the specific functions of that protein by multiple protein–protein interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Anders C, Higuchi Y, Koschinsky K, Bartel M, Schumacher B, Thiel P, Nitta H, Preisig-Müller R, Schlichthorl G, Renigunta V, Ohkanda J, Daut J, Kato N, Ottmann C (2013) A semisynthetic fusicoccane stabilizes a protein-protein interaction and enhances the expression of K+ channels at the cell surface. Chem Biol 20:583–593

    CAS  PubMed  Google Scholar 

  2. Arakel EC, Brandenburg S, Uchida K, Zhang H, Lin YW, Kohl T, Schrul B, Sulkin MS, Efimov IR, Nichols CG, Lehnart SE, Schwappach B (2014) Tuning the electrical properties of the heart by differential trafficking of KATP ion channel complexes. J Cell Sci 127:2106–2119

    PubMed Central  CAS  PubMed  Google Scholar 

  3. Arango-Lievano M, Schwarz JT, Vernov M, Wilkinson MB, Bradbury K, Feliz A, Marongiu R, Gelfand Y, Warner-Schmidt J, Nestler EJ, Greengard P, Russo SJ, Kaplitt MG (2014) Cell-type specific expression of p11 controls cocaine reward. Biol Psychiatry 76:794–801

    CAS  PubMed  Google Scholar 

  4. Ashmole I, Goodwin PA, Stanfield PR (2001) TASK-5, a novel member of the tandem pore K+ channel family. Pflugers Arch 442:828–833

    CAS  PubMed  Google Scholar 

  5. Bayliss DA, Barrett PQ (2008) Emerging roles for two-pore-domain potassium channels and their potential therapeutic impact. Trends Pharmacol Sci

  6. Behnia R, Munro S (2005) Organelle identity and the signposts for membrane traffic. Nature 438:597–604

    CAS  PubMed  Google Scholar 

  7. Bi X, Corpina RA, Goldberg J (2002) Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419:271–277

    CAS  PubMed  Google Scholar 

  8. Bichet D, Blin S, Feliciangeli S, Chatelain FC, Bobak N, Lesage F (2014) Silent but not dumb: how cellular trafficking and pore gating modulate expression of TWIK1 and THIK2. Pflugers Arch

  9. Bickford LC, Mossessova E, Goldberg J (2004) A structural view of the COPII vesicle coat. Curr Opin Struct Biol 14:147–153

    CAS  PubMed  Google Scholar 

  10. Bilan F, Nacfer M, Fresquet F, Norez C, Melin P, Martin-Berge A, Costa de Beauregard MA, Becq F, Kitzis A, Thoreau V (2008) Endosomal SNARE proteins regulate CFTR activity and trafficking in epithelial cells. Exp Cell Res 314:2199–2211

    CAS  PubMed  Google Scholar 

  11. Bilan F, Thoreau V, Nacfer M, Derand R, Norez C, Cantereau A, Garcia M, Becq F, Kitzis A (2004) Syntaxin 8 impairs trafficking of cystic fibrosis transmembrane conductance regulator (CFTR) and inhibits its channel activity. J Cell Sci 117:1923–1935

    CAS  PubMed  Google Scholar 

  12. Boudanova E, Navaroli DM, Stevens Z, Melikian HE (2008) Dopamine transporter endocytic determinants: Carboxy terminal residues critical for basal and PKC-stimulated internalization. Mol Cell Neurosci 39:211–217

    PubMed Central  CAS  PubMed  Google Scholar 

  13. Brohawn SG, Campbell EB, MacKinnon R (2013) Domain-swapped chain connectivity and gated membrane access in a Fab-mediated crystal of the human TRAAK K+ channel. Proc Natl Acad Sci U S A 110:2129–2134

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Brohawn SG, del Marmol J, MacKinnon R (2012) Crystal structure of the human K2P TRAAK, a lipid- and mechano-sensitive K+ ion channel. Science 335:436–441

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Calhoun JD, Isom LL (2014) The role of non-pore-forming beta subunits in physiology and pathophysiology of voltage-gated sodium channels. Handb Exp Pharmacol 221:51–89

    PubMed  Google Scholar 

  16. Chen PC, Bruederle CE, Gaisano HY, Shyng SL (2011) Syntaxin 1A regulates surface expression of beta-cell ATP-sensitive potassium channels. Am J Physiol Cell Physiol 300:C506–C516

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37–44

    CAS  PubMed  Google Scholar 

  18. Cui YL, Holt AG, Lomax CA, Altschuler RA (2007) Deafness associated changes in two-pore domain potassium channels in the rat inferior colliculus. Neuroscience 149:421–433

    PubMed Central  CAS  PubMed  Google Scholar 

  19. de Boer AH, van Kleeff PJ, Gao J (2013) Plant 14-3-3 proteins as spiders in a web of phosphorylation. Protoplasma 250:425–440

    CAS  PubMed  Google Scholar 

  20. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657

    PubMed  Google Scholar 

  21. Dolphin AC (2009) Calcium channel diversity: Multiple roles of calcium channel subunits. Curr Opin Neurobiol 19:237–244

    CAS  PubMed  Google Scholar 

  22. Duprat F, Lesage F, Fink M, Reyes R, Heurteaux C, Lazdunski M (1997) TASK, a human background K+ channel to sense external pH variations near physiological pH. EMBO J 16:5464–5471

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Ellis RJ (2013) Assembly chaperones: a perspective. Philos Trans R Soc Lond B Biol Sci 368:20110398

    PubMed Central  PubMed  Google Scholar 

  24. Ellis RJ (2006) Molecular chaperones: Assisting assembly in addition to folding. Trends Biochem Sci 31:395–401

    CAS  PubMed  Google Scholar 

  25. Enyedi P, Czirjak G (2010) Molecular background of leak K+ currents: Two-pore domain potassium channels. Physiol Rev 90:559–605

    CAS  PubMed  Google Scholar 

  26. Feinshreiber L, Chikvashvili D, Michaelevski I, Lotan I (2009) Syntaxin modulates Kv1.1 through dual action on channel surface expression and conductance. Biochemistry 48:4109–4114

    CAS  PubMed  Google Scholar 

  27. Feng J, Cai X, Zhao J, Yan Z (2001) Serotonin receptors modulate GABA(A) receptor channels through activation of anchored protein kinase C in prefrontal cortical neurons. J Neurosci 21:6502–6511

    CAS  PubMed  Google Scholar 

  28. Fu H, Subramanian RR, Masters SC (2000) 14-3-3 proteins: Structure, function, and regulation. Annu Rev Pharmacol Toxicol 40:617–647

    CAS  PubMed  Google Scholar 

  29. Gabriel L, Lvov A, Orthodoxou D, Rittenhouse AR, Kobertz WR, Melikian HE (2012) The acid-sensitive, anesthetic-activated potassium leak channel, KCNK3, is regulated by 14-3-3beta-dependent, protein kinase C (PKC)-mediated endocytic trafficking. J Biol Chem 287:32354–32366

    PubMed Central  CAS  PubMed  Google Scholar 

  30. Gardino AK, Yaffe MB (2011) 14-3-3 proteins as signaling integration points for cell cycle control and apoptosis. Semin Cell Dev Biol 22:688–695

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Girard C, Tinel N, Terrenoire C, Romey G, Lazdunski M, Borsotto M (2002) p11, an annexin II subunit, an auxiliary protein associated with the background K+ channel, TASK-1. EMBO J 21:4439–4448

    PubMed Central  CAS  PubMed  Google Scholar 

  32. Gong W, Zhou D, Ren Y, Wang Y, Zuo Z, Shen Y, Xiao F, Zhu Q, Hong A, Zhou X, Gao X, Li T (2008) PepCyber:P ∼ PEP: a database of human protein protein interactions mediated by phosphoprotein-binding domains. Nucleic Acids Res 36:D679–D683

    PubMed Central  CAS  PubMed  Google Scholar 

  33. Gonzalez C, Baez-Nieto D, Valencia I, Oyarzun I, Rojas P, Naranjo D, Latorre R (2012) K+ channels: Function-structural overview. Compr Physiol 2:2087–2149

    PubMed  Google Scholar 

  34. Gross SR, Sin CG, Barraclough R, Rudland PS (2014) Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell Mol Life Sci 71:1551–1579

    CAS  PubMed  Google Scholar 

  35. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85–100

    CAS  PubMed  Google Scholar 

  36. Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–579

    CAS  PubMed  Google Scholar 

  37. Hartl FU, Bracher A, Hayer-Hartl M (2011) Molecular chaperones in protein folding and proteostasis. Nature 475:324–332

    CAS  PubMed  Google Scholar 

  38. Holton KL, Loder MK, Melikian HE (2005) Nonclassical, distinct endocytic signals dictate constitutive and PKC-regulated neurotransmitter transporter internalization. Nat Neurosci 8:881–888

    PubMed Central  CAS  PubMed  Google Scholar 

  39. Hu K, Huang CS, Jan YN, Jan LY (2003) ATP-sensitive potassium channel traffic regulation by adenosine and protein kinase C. Neuron 38:417–432

    CAS  PubMed  Google Scholar 

  40. Hutt DM, Balch WE (2013) Expanding proteostasis by membrane trafficking networks. Cold Spring Harb Perspect Med 3:1–21

    PubMed  Google Scholar 

  41. Jahn R, Scheller RH (2006) SNAREs—Engines for membrane fusion. Nat Rev Mol Cell Biol 7:631–643

    CAS  PubMed  Google Scholar 

  42. Kanda VA, Purtell K, Abbott GW (2011) Protein kinase C downregulates IKs by stimulating KCNQ1-KCNE1 potassium channel endocytosis. Heart Rhythm 8:1641–1647

    PubMed Central  PubMed  Google Scholar 

  43. Karschin C, Wischmeyer E, Preisig-Müller R, Rajan S, Derst C, Grzeschik KH, Daut J, Karschin A (2001) Expression pattern in brain of TASK-1, TASK-3, and a tandem pore domain K+ channel subunit, TASK-5, associated with the central auditory nervous system. Mol Cell Neurosci 18:632–648

    CAS  PubMed  Google Scholar 

  44. Kim D, Gnatenco C (2001) TASK-5, a new member of the tandem-pore K+ channel family. Biochem Biophys Res Commun 284:923–930

    CAS  PubMed  Google Scholar 

  45. Kim Y, Bang H, Kim D (2000) TASK-3, a new member of the tandem pore K+ channel family. J Biol Chem 275:9340–9347

    CAS  PubMed  Google Scholar 

  46. Lesage F, Barhanin J (2011) Molecular physiology of pH-sensitive background K2P channels. Physiology (Bethesda) 26:424–437

    CAS  Google Scholar 

  47. Leung YM, Kang Y, Gao X, Xia F, Xie H, Sheu L, Tsuk S, Lotan I, Tsushima RG, Gaisano HY (2003) Syntaxin 1A binds to the cytoplasmic C terminus of Kv2.1 to regulate channel gating and trafficking. J Biol Chem 278:17532–17538

    CAS  PubMed  Google Scholar 

  48. Li X, Garrity AG, Xu H (2013) Regulation of membrane trafficking by signalling on endosomal and lysosomal membranes. J Physiol 591:4389–4401

    PubMed Central  CAS  PubMed  Google Scholar 

  49. Liu D, Bienkowska J, Petosa C, Collier RJ, Fu H, Liddington R (1995) Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376:191–194

    CAS  PubMed  Google Scholar 

  50. Ma D, Jan LY (2002) ER transport signals and trafficking of potassium channels and receptors. Curr Opin Neurobiol 12:287–292

    CAS  PubMed  Google Scholar 

  51. Ma D, Taneja TK, Hagen BM, Kim BY, Ortega B, Lederer WJ, Welling PA (2011) Golgi export of the Kir2.1 channel is driven by a trafficking signal located within its tertiary structure. Cell 145:1102–1115

    PubMed Central  CAS  PubMed  Google Scholar 

  52. Ma D, Zerangue N, Lin YF, Collins A, Yu M, Jan YN, Jan LY (2001) Role of ER export signals in controlling surface potassium channel numbers. Science 291:316–319

    CAS  PubMed  Google Scholar 

  53. Ma D, Zerangue N, Raab-Graham K, Fried SR, Jan YN, Jan LY (2002) Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron 33:715–729

    CAS  PubMed  Google Scholar 

  54. Malkus P, Jiang F, Schekman R (2002) Concentrative sorting of secretory cargo proteins into COPII-coated vesicles. J Cell Biol 159:915–921

    PubMed Central  CAS  PubMed  Google Scholar 

  55. Malsam J, Kreye S, Söllner TH (2008) Membrane fusion: SNAREs and regulation. Cell Mol Life Sci 65:2814–2832

    CAS  PubMed  Google Scholar 

  56. Mancias JD, Goldberg J (2008) Structural basis of cargo membrane protein discrimination by the human COPII coat machinery. EMBO J 27:2918–2928

    PubMed Central  CAS  PubMed  Google Scholar 

  57. Mancias JD, Goldberg J (2007) The transport signal on Sec22 for packaging into COPII-coated vesicles is a conformational epitope. Mol Cell 26:403–414

    CAS  PubMed  Google Scholar 

  58. Mant A, Elliott D, Eyers PA, O’Kelly IM (2011) Protein kinase A is central for forward transport of two-pore domain potassium channels K2P3.1 and K2P9.1. J Biol Chem 286:14110–14119

    PubMed Central  CAS  PubMed  Google Scholar 

  59. Marenholz I, Heizmann CW, Fritz G (2004) S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun 322:1111–1122

    CAS  PubMed  Google Scholar 

  60. Maritzen T, Koo SJ, Haucke V (2012) Turning CALM into excitement: AP180 and CALM in endocytosis and disease. Biol Cell 104:588–602

    CAS  PubMed  Google Scholar 

  61. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12:517–533

    CAS  PubMed  Google Scholar 

  62. McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K, Paumet F, Sollner TH, Rothman JE (2000) Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407:153–159

    CAS  PubMed  Google Scholar 

  63. Mikosch M, Hurst AC, Hertel B, Homann U (2006) Diacidic motif is required for efficient transport of the K+ channel KAT1 to the plasma membrane. Plant Physiol 142:923–930

    PubMed Central  CAS  PubMed  Google Scholar 

  64. Mikosch M, Kaberich K, Homann U (2009) ER export of KAT1 is correlated to the number of acidic residues within a triacidic motif. Traffic 10:1481–1487

    CAS  PubMed  Google Scholar 

  65. Millar JA, Barratt L, Southan AP, Page KM, Fyffe RE, Robertson B, Mathie A (2000) A functional role for the two-pore domain potassium channel TASK-1 in cerebellar granule neurons. Proc Natl Acad Sci U S A 97:3614–3618

    PubMed Central  CAS  PubMed  Google Scholar 

  66. Miller AN, Long SB (2012) Crystal structure of the human two-pore domain potassium channel K2P1. Science 335:432–436

    CAS  PubMed  Google Scholar 

  67. Miller E, Antonny B, Hamamoto S, Schekman R (2002) Cargo selection into COPII vesicles is driven by the Sec24p subunit. Embo J 21:6105–6113

    PubMed Central  CAS  PubMed  Google Scholar 

  68. Miller EA, Beilharz TH, Malkus PN, Lee MC, Hamamoto S, Orci L, Schekman R (2003) Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:497–509

    CAS  PubMed  Google Scholar 

  69. Milroy LG, Brunsveld L, Ottmann C (2013) Stabilization and inhibition of protein-protein interactions: the 14-3-3 case study. ACS Chem Biol 8:27–35

    CAS  PubMed  Google Scholar 

  70. Milroy LG, Grossmann TN, Hennig S, Brunsveld L, Ottmann C (2014) Modulators of protein-protein interactions. Chem Rev 114:4695–4748

    CAS  PubMed  Google Scholar 

  71. Mossessova E, Bickford LC, Goldberg J (2003) SNARE selectivity of the COPII coat. Cell 114:483–495

    CAS  PubMed  Google Scholar 

  72. Mu D, Chen L, Zhang X, See LH, Koch CM, Yen C, Tong JJ, Spiegel L, Nguyen KC, Servoss A, Peng Y, Pei L, Marks JR, Lowe S, Hoey T, Jan LY, McCombie WR, Wigler MH, Powers S (2003) Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene. Cancer Cell 3:297–302

    CAS  PubMed  Google Scholar 

  73. Musset B, Meuth SG, Liu GX, Derst C, Wegner S, Pape HC, Budde T, Preisig-Muller R, Daut J (2006) Effects of divalent cations and spermine on the K+ channel TASK-3 and on the outward current in thalamic neurons. J Physiol 572:639–657

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Nishimura N, Balch WE (1997) A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277:556–558

    CAS  PubMed  Google Scholar 

  75. O’Kelly I (2014) Endocytosis as a mode to regulate functional expression of two-pore domain potassium (K2P) channels. Pflügers Archiv European Journal of Physiology

  76. O’Kelly I, Butler MH, Zilberberg N, Goldstein SA (2002) Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111:577–588

    PubMed  Google Scholar 

  77. O’Kelly I, Goldstein SA (2008) Forward transport of K(2P)3.1: Mediation by 14-3-3 and COPI, modulation by p11. Traffic 9:72–78

    PubMed  Google Scholar 

  78. Obsil T (2011) 14–3–3 proteins–a family of universal scaffolds and regulators. Semin Cell Dev Biol 22:661–662

    PubMed  Google Scholar 

  79. Obsilova V, Kopecka M, Kosek D, Kacirova M, Kylarova S, Rezabkova L, Obsil T (2014) Mechanisms of the 14-3-3 protein function: Regulation of protein function through conformational modulation. Physiol Res 63(Suppl 1):S155–S164

    CAS  PubMed  Google Scholar 

  80. Otte S, Barlowe C (2004) Sorting signals can direct receptor-mediated export of soluble proteins into COPII vesicles. Nat Cell Biol 6:1189–1194

    CAS  PubMed  Google Scholar 

  81. Ottmann C (2013) Small-molecule modulators of 14-3-3 protein-protein interactions. Bioorg Med Chem 21:4058–4062

    CAS  PubMed  Google Scholar 

  82. Pei L, Wiser O, Slavin A, Mu D, Powers S, Jan LY, Hoey T (2003) Oncogenic potential of TASK3 (KCNK9) depends on K+ channel function. Proc Natl Acad Sci U S A 100:7803–7807

    PubMed Central  CAS  PubMed  Google Scholar 

  83. Pfeffer SR (2011) Entry at the trans-face of the Golgi. Cold Spring Harb Perspect Biol 3

  84. Pongs O, Schwarz JR (2010) Ancillary subunits associated with voltage-dependent K+ channels. Physiol Rev 90:755–796

    CAS  PubMed  Google Scholar 

  85. Pryor PR, Jackson L, Gray SR, Edeling MA, Thompson A, Sanderson CM, Evans PR, Owen DJ, Luzio JP (2008) Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the ArfGAP Hrb. Cell 134:817–827

    PubMed Central  CAS  PubMed  Google Scholar 

  86. Pucadyil TJ, Schmid SL (2009) Conserved functions of membrane active GTPases in coated vesicle formation. Science 325:1217–1220

    PubMed Central  CAS  PubMed  Google Scholar 

  87. Putzke C, Wemhöner K, Sachse FB, Rinné S, Schlichthörl G, Li XT, Jae L, Eckhardt I, Wischmeyer E, Wulf H, Preisig-Müller R, Daut J, Decher N (2007) The acid-sensitive potassium channel TASK-1 in rat cardiac muscle. Cardiovasc Res 75:59–68

    CAS  PubMed  Google Scholar 

  88. Rajan S, Preisig-Müller R, Wischmeyer E, Nehring R, Hanley PJ, Renigunta V, Musset B, Schlichthörl G, Derst C, Karschin A, Daut J (2002) Interaction with 14-3-3 proteins promotes functional expression of the potassium channels TASK-1 and TASK-3. J Physiol 545:13–26

    PubMed Central  CAS  PubMed  Google Scholar 

  89. Rajan S, Preisig-Müller, R., Wischmeyer, E., Nehring, R., Daut, J., Karschin, A. & Derst, C. (2002) A C-terminal pentapeptide motif interacting with 14-3-3 protein strongly enhances cell surface expression of TASK-1, a 2P domain K+ channel. Biophys J 82:201a-202a (abstract; January 2002)

  90. Rajan S, Wischmeyer E, Liu GX, Preisig-Müller R, Daut J, Karschin A, Derst C (2000) TASK-3, a novel tandem pore domain acid-sensitive K+ channel. an extracellular histidine as pH sensor. J Biol Chem 275:16650–16657

    CAS  PubMed  Google Scholar 

  91. Reinhardt HC, Yaffe MB (2013) Phospho-Ser/Thr-binding domains: Navigating the cell cycle and DNA damage response. Nat Rev Mol Cell Biol 14:563–580

    CAS  PubMed  Google Scholar 

  92. Renigunta V, Fischer T, Zuzarte M, Kling S, Zou X, Siebert K, Limberg MM, Rinne S, Decher N, Schlichthörl G, Daut J (2014) Cooperative endocytosis of the endosomal SNARE protein syntaxin-8 and the potassium channel TASK-1. Mol Biol Cell 25:1877–1891

    PubMed Central  CAS  PubMed  Google Scholar 

  93. Renigunta V, Yuan H, Zuzarte M, Rinné S, Koch A, Wischmeyer E, Schlichthörl G, Gao Y, Karschin A, Jacob R, Schwappach B, Daut J, Preisig-Müller R (2006) The retention factor p11 confers an endoplasmic reticulum-localization signal to the potassium channel TASK-1. Traffic 7:168–181

    CAS  PubMed  Google Scholar 

  94. Rescher U, Gerke V (2008) S100A10/p11: Family, friends and functions. Pflugers Arch 455:575–582

    CAS  PubMed  Google Scholar 

  95. Rety S, Sopkova J, Renouard M, Osterloh D, Gerke V, Tabaries S, Russo-Marie F, Lewit-Bentley A (1999) The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nat Struct Biol 6:89–95

    CAS  PubMed  Google Scholar 

  96. Rinné S, Renigunta V, Schlichthörl G, Zuzarte M, Bittner S, Meuth SG, Decher N, Daut J, Preisig-Müller R (2014) A splice variant of the two-pore domain potassium channel TREK-1 with only one pore domain reduces the surface expression of full-length TREK-1 channels. Pflugers Arch 466:1559–1570

    PubMed  Google Scholar 

  97. Schiekel J, Lindner M, Hetzel A, Wemhöner K, Renigunta V, Schlichthörl G, Decher N, Oliver D, Daut J (2013) The inhibition of the potassium channel TASK-1 in rat cardiac muscle by endothelin-1 is mediated by phospholipase C. Cardiovasc Res 97:97–105

    CAS  PubMed  Google Scholar 

  98. Schwappach B (2008) An overview of trafficking and assembly of neurotransmitter receptors and ion channels (Review). Mol Membr Biol 25:270–278

    CAS  PubMed  Google Scholar 

  99. Seet BT, Dikic I, Zhou MM, Pawson T (2006) Reading protein modifications with interaction domains. Nat Rev Mol Cell Biol 7:473–483

    CAS  PubMed  Google Scholar 

  100. Shikano S, Coblitz B, Sun H, Li M (2005) Genetic isolation of transport signals directing cell surface expression. Nat Cell Biol 7:985–992

    CAS  PubMed  Google Scholar 

  101. Smith AJ, Daut J, Schwappach B (2011) Membrane proteins as 14-3-3 clients in functional regulation and intracellular transport. Physiology (Bethesda) 26:181–191

    CAS  Google Scholar 

  102. Stauber T, Weinert S, Jentsch TJ (2012) Cell biology and physiology of CLC chloride channels and transporters. Compr Physiol 2:1701–1744

    PubMed  Google Scholar 

  103. Svenningsson P, Greengard P (2007) p11 (S100A10)—an inducible adaptor protein that modulates neuronal functions. Curr Opin Pharmacol 7:27–32

    CAS  PubMed  Google Scholar 

  104. Svenningsson P, Kim Y, Warner-Schmidt J, Oh YS, Greengard P (2013) p11 and its role in depression and therapeutic responses to antidepressants. Nat Rev Neurosci 14:673–680

    PubMed Central  CAS  PubMed  Google Scholar 

  105. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA (2001) Cns distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21:7491–7505

    CAS  PubMed  Google Scholar 

  106. Veale EL, Rees KA, Mathie A, Trapp S (2010) Dominant negative effects of a non-conducting TREK1 splice variant expressed in brain. J Biol Chem 285:29295–29304

    PubMed Central  CAS  PubMed  Google Scholar 

  107. Venditti R, Wilson C, De Matteis MA (2014) Exiting the ER: what we know and what we don’t. Trends Cell Biol 24:9–18

    CAS  PubMed  Google Scholar 

  108. Wagner MJ, Stacey MM, Liu BA, Pawson T (2013) Molecular mechanisms of SH2- and PTB-domain-containing proteins in receptor tyrosine kinase signaling. Cold Spring Harb Perspect Biol 5:a008987

    PubMed  Google Scholar 

  109. Welling PA (2013) Regulation of potassium channel trafficking in the distal nephron. Curr Opin Nephrol Hypertens 22:559–565

    PubMed Central  CAS  PubMed  Google Scholar 

  110. Welling PA, Weisz OA (2010) Sorting it out in endosomes: an emerging concept in renal epithelial cell transport regulation. Physiology (Bethesda) 25:280–292

    CAS  Google Scholar 

  111. Wendeler MW, Paccaud JP, Hauri HP (2007) Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep 8:258–264

    PubMed Central  CAS  PubMed  Google Scholar 

  112. Wilke BU, Lindner M, Greifenberg L, Albus A, Kronimus Y, Bünemann M, Leitner MG, Oliver D (2014) Diacylglycerol mediates regulation of TASK potassium channels by Gq-coupled receptors. Nat Commun 5:5540

    CAS  PubMed  Google Scholar 

  113. Williams S, Bateman A, O’Kelly I (2013) Altered expression of two-pore domain potassium (K2P) channels in cancer. PLoS ONE 8:e74589

    PubMed Central  CAS  PubMed  Google Scholar 

  114. Xiao B, Smerdon SJ, Jones DH, Dodson GG, Soneji Y, Aitken A, Gamblin SJ (1995) Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376:188–191

    CAS  PubMed  Google Scholar 

  115. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, Cantley LC (1997) The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91:961–971

    CAS  PubMed  Google Scholar 

  116. Yu FH, Yarov-Yarovoy V, Gutman GA, Catterall WA (2005) Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol Rev 57:387–395

    CAS  PubMed  Google Scholar 

  117. Zerangue N, Schwappach B, Jan YN, Jan LY (1999) A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane KATP channels. Neuron 22:537–548

    CAS  PubMed  Google Scholar 

  118. Zhang J, Yan J (2014) Regulation of BK channels by auxiliary gamma subunits. Front Physiol 5:401

    PubMed Central  PubMed  Google Scholar 

  119. Zhang X, Dong C, Wu QJ, Balch WE, Wu G (2011) Di-acidic motifs in the membrane-distal C termini modulate the transport of angiotensin II receptors from the endoplasmic reticulum to the cell surface. J Biol Chem 286:20525–20535

    PubMed Central  CAS  PubMed  Google Scholar 

  120. Zuzarte M, Heusser K, Renigunta V, Schlichthörl G, Rinné S, Wischmeyer E, Daut J, Schwappach B, Preisig-Müller R (2009) Intracellular traffic of the K+ channels TASK-1 and TASK-3: role of N- and C-terminal sorting signals and interaction with 14-3-3 proteins. J Physiol 587:929–952

    PubMed Central  CAS  PubMed  Google Scholar 

  121. Zuzarte M, Rinné S, Schlichthörl G, Schubert A, Daut J, Preisig-Müller R (2007) A di-acidic sequence motif enhances the surface expression of the potassium channel TASK-3. Traffic 8:1093–1100

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Deutsche Forschungsgemeinschaft (FOR 1086, TP7 and TP9; SFB 593, TP4).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Vijay Renigunta or Jürgen Daut.

Additional information

Markus Kilisch and Olga Lytovchenko contributed equally.

This article is published as part of the special issue on K2P-channels.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kilisch, M., Lytovchenko, O., Schwappach, B. et al. The role of protein–protein interactions in the intracellular traffic of the potassium channels TASK-1 and TASK-3. Pflugers Arch - Eur J Physiol 467, 1105–1120 (2015). https://doi.org/10.1007/s00424-014-1672-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-014-1672-2

Keywords

Navigation