Golgin-97 Targets Ectopically Expressed Inward Rectifying Potassium Channel, Kir2.1, to the -Golgi Network in COS-7 Cells

Overview

Journal Front Physiol

Date 2018 Aug 21

PMID 30123141

Citations 10

Authors

Tarvinder K Taneja

Donghui Ma

Bo Y Kim

Paul A Welling

Affiliations

Soon will be listed here.

Abstract

The inward rectifying potassium channel, Kir2.1, is selected as cargo at the -Golgi network (TGN) for export to the cell surface through a unique signal-dependent interaction with the AP1 clathrin-adaptor, but it is unknown how the channel is targeted at earlier stages in the secretory pathway for traffic to the TGN. Here we explore a mechanism. A systematic screen of Golgi tethers identified Golgin-97 as a Kir2.1 binding partner. protein-interaction studies revealed the interaction is direct, occurring between the GRIP domain of Golgin-97 and the cytoplasmic domain of Kir2.1. Imaging and interaction studies in COS-7 cells suggest that Golgi-97 binds to the channel en route through the Golgi. RNA interference-mediated knockdown of Golgin-97 prevented exit of Kir2.1 from the Golgi. These observations identify Golgin-97 as a Kir2.1 binding partner that is required for targeting the channel to the TGN. Based on our studies in COS-7 cells, we propose Golgi-97 facilitates formation of AP1-dependent export carriers for Kir2.1 by coupling anterograde delivery of Kir2.1 with retrograde recycling of AP-1 containing endosomes to the TGN.

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References

Lock J, Hammond L, Houghton F, Gleeson P, Stow J . E-cadherin transport from the trans-Golgi network in tubulovesicular carriers is selectively regulated by golgin-97. Traffic. 2005; 6(12):1142-56. DOI: 10.1111/j.1600-0854.2005.00349.x. View

Gillingham A, Munro S . Finding the Golgi: Golgin Coiled-Coil Proteins Show the Way. Trends Cell Biol. 2016; 26(6):399-408. DOI: 10.1016/j.tcb.2016.02.005. View

Lu L, Tai G, Hong W . Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-golgi network. Mol Biol Cell. 2004; 15(10):4426-43. PMC: 519138. DOI: 10.1091/mbc.e03-12-0872. View

Hase K, Nakatsu F, Ohmae M, Sugihara K, Shioda N, Takahashi D . AP-1B-mediated protein sorting regulates polarity and proliferation of intestinal epithelial cells in mice. Gastroenterology. 2013; 145(3):625-35. DOI: 10.1053/j.gastro.2013.05.013. View

Plaster N, Tawil R, Tristani-Firouzi M, Canun S, Bendahhou S, Tsunoda A . Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen's syndrome. Cell. 2001; 105(4):511-9. DOI: 10.1016/s0092-8674(01)00342-7. View

Wong M, Munro S . Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science. 2014; 346(6209):1256898. PMC: 4254398. DOI: 10.1126/science.1256898. View

Ma D, Taneja T, Hagen B, Kim B, Ortega B, Lederer W . Golgi export of the Kir2.1 channel is driven by a trafficking signal located within its tertiary structure. Cell. 2011; 145(7):1102-15. PMC: 3139129. DOI: 10.1016/j.cell.2011.06.007. View

Leonoudakis D, Conti L, Anderson S, Radeke C, McGuire L, Adams M . Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins. J Biol Chem. 2004; 279(21):22331-46. DOI: 10.1074/jbc.M400285200. View

Bundis F, Neagoe I, Schwappach B, Steinmeyer K . Involvement of Golgin-160 in cell surface transport of renal ROMK channel: co-expression of Golgin-160 increases ROMK currents. Cell Physiol Biochem. 2006; 17(1-2):1-12. DOI: 10.1159/000091454. View

10.

Shin J, Gillingham A, Begum F, Chadwick J, Munro S . TBC1D23 is a bridging factor for endosomal vesicle capture by golgins at the trans-Golgi. Nat Cell Biol. 2017; 19(12):1424-1432. PMC: 5712222. DOI: 10.1038/ncb3627. View

11.

Ward T, Polishchuk R, Caplan S, Hirschberg K, Lippincott-Schwartz J . Maintenance of Golgi structure and function depends on the integrity of ER export. J Cell Biol. 2001; 155(4):557-70. PMC: 2198855. DOI: 10.1083/jcb.200107045. View

12.

Han H, Rosenhouse-Dantsker A, Gnanasambandam R, Epshtein Y, Chen Z, Sachs F . Silencing of Kir2 channels by caveolin-1: cross-talk with cholesterol. J Physiol. 2014; 592(18):4025-38. PMC: 4198012. DOI: 10.1113/jphysiol.2014.273177. View

13.

Lieu Z, Lock J, Hammond L, La Gruta N, Stow J, Gleeson P . A trans-Golgi network golgin is required for the regulated secretion of TNF in activated macrophages in vivo. Proc Natl Acad Sci U S A. 2008; 105(9):3351-6. PMC: 2265200. DOI: 10.1073/pnas.0800137105. View

14.

Ma D, Zerangue N, Lin Y, Collins A, Yu M, Jan Y . Role of ER export signals in controlling surface potassium channel numbers. Science. 2001; 291(5502):316-9. DOI: 10.1126/science.291.5502.316. View

15.

Vaidyanathan R, Van Ert H, Haq K, Morotti S, Esch S, McCune E . Inward Rectifier Potassium Channels (Kir2.x) and Caveolin-3 Domain-Specific Interaction: Implications for Purkinje Cell-Dependent Ventricular Arrhythmias. Circ Arrhythm Electrophysiol. 2018; 11(1):e005800. PMC: 5771420. DOI: 10.1161/CIRCEP.117.005800. View

16.

Shin H, Kobayashi H, Kitamura M, Waguri S, Suganuma T, Uchiyama Y . Roles of ARFRP1 (ADP-ribosylation factor-related protein 1) in post-Golgi membrane trafficking. J Cell Sci. 2005; 118(Pt 17):4039-48. DOI: 10.1242/jcs.02524. View

17.

Ballester L, Benson D, Wong B, Law I, Mathews K, Vanoye C . Trafficking-competent and trafficking-defective KCNJ2 mutations in Andersen syndrome. Hum Mutat. 2006; 27(4):388. DOI: 10.1002/humu.9418. View

18.

Vaidyanathan R, Vega A, Song C, Zhou Q, Tan B, Tan B . The interaction of caveolin 3 protein with the potassium inward rectifier channel Kir2.1: physiology and pathology related to long qt syndrome 9 (LQT9). J Biol Chem. 2013; 288(24):17472-80. PMC: 3682547. DOI: 10.1074/jbc.M112.435370. View

19.

Wong M, Gillingham A, Munro S . The golgin coiled-coil proteins capture different types of transport carriers via distinct N-terminal motifs. BMC Biol. 2017; 15(1):3. PMC: 5267433. DOI: 10.1186/s12915-016-0345-3. View

20.

Derby M, Lieu Z, Brown D, Stow J, Goud B, Gleeson P . The trans-Golgi network golgin, GCC185, is required for endosome-to-Golgi transport and maintenance of Golgi structure. Traffic. 2007; 8(6):758-73. DOI: 10.1111/j.1600-0854.2007.00563.x. View