Induction of stable ER-plasma-membrane junctions by Kv2.1 potassium channels

Journal of Cell Science

Volumn 128, Issue 11, 2015, Pages 2096-2105

  Fox, Philip D ^a   Haberkorn, Christopher J ^a   Akin, Elizabeth J ^a   Seel, Peter J ^b   Krapf, Diego ^b   Tamkun, Michael M ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b Department of Mechanical Engineering   (United States)

Author keywords

Ion channels; Membrane contact sites; Sub surface cisterns

Indexed keywords

CALCIUM CHANNEL; GLUTAMIC ACID; POTASSIUM CHANNEL KV2.1; SHAB POTASSIUM CHANNEL; UNCLASSIFIED DRUG; CALCIUM; KCNB1 PROTEIN, HUMAN; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DENSITY; CELL MEMBRANE POTENTIAL; CELL MEMBRANE TRANSPORT; CELL SURFACE; EMBRYO; ENDOPLASMIC RETICULUM MEMBRANE; ENDOPLASMIC RETICULUM PLASMA MEMBRANE JUNCTION; HEK293 CELL LINE; HIPPOCAMPAL NEURONAL CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; HIPPOCAMPUS; HUMAN; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

MAMMALIA;

CALCIUM; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; GLUTAMIC ACID; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; NEURONS; PROTEIN TRANSPORT; SHAB POTASSIUM CHANNELS; SIGNAL TRANSDUCTION;

EID: 84930794073     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.166009     Document Type: Article

References (47)

1. Antonucci, D. E., Lim, S. T., Vassanelli, S. and Trimmer, J. S. (2001). Dynamic localization and clustering of dendritic Kv2.1 voltage-dependent potassium channels in developing hippocampal neurons. Neuroscience 108, 69-81.
2. Baver, S. B. and O'Connell, K. M. (2012). The C-terminus of neuronal Kv2.1 channels is required for channel localization and targeting but not for NMDA-receptor-mediated regulation of channel function. Neuroscience 217, 56-66.
3. Cardona, A., Saalfeld, S., Schindelin, J., Arganda-Carreras, I., Preibisch, S., Longair, M., Tomancak, P., Hartenstein, V. and Douglas, R. J. (2012). TrakEM2 software for neural circuit reconstruction. PLoS ONE 7, e38011.
4. Carrasco, S. and Meyer, T. (2011). STIM proteins and the endoplasmic reticulumplasma membrane junctions. Annu. Rev. Biochem. 80, 973-1000.
5. Carter, B. C., Shubeita, G. T. and Gross, S. P. (2005). Tracking single particles: a user-friendly quantitative evaluation. Phys. Biol. 2, 60-72.
6. Deutsch, E., Weigel, A. V., Akin, E. J., Fox, P., Hansen, G., Haberkorn, C. J., Loftus, R., Krapf, D. and Tamkun, M. M. (2012). Kv2.1 cell surface clusters are insertion platforms for ion channel delivery to the plasma membrane. Mol. Biol. Cell 23, 2917-2929.
7. Du, J., Tao-Cheng, J. H., Zerfas, P. and McBain, C. J. (1998). The K+ channel, Kv2.1, is apposed to astrocytic processes and is associated with inhibitory postsynaptic membranes in hippocampal and cortical principal neurons and inhibitory interneurons. Neuroscience 84, 37-48.
8. English, A. R. and Voeltz, G. K. (2013). Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb. Perspect. Biol. 5, a013227.
9. English, A. R., Zurek, N. and Voeltz, G. K. (2009). Peripheral ER structure and function. Curr. Opin. Cell Biol. 21, 596-602.
10. Fox, P. D., Haberkorn, C. J., Weigel, A. V., Higgins, J. L., Akin, E. J., Kennedy, M. J., Krapf, D. and Tamkun, M. M. (2013a). Plasma membrane domains enriched in cortical endoplasmic reticulum function as membrane protein trafficking hubs. Mol. Biol. Cell 24, 2703-2713.
11. Fox, P. D., Loftus, R. J. and Tamkun, M. M. (2013b). Regulation of Kv2.1 K(+) conductance by cell surface channel density. J. Neurosci. 33, 1259-1270.
12. Franzini-Armstrong, C. and Jorgensen, A. O. (1994). Structure and development of E-C coupling units in skeletal muscle. Annu. Rev. Physiol. 56, 509-534.
13. Giordano, F., Saheki, Y., Idevall-Hagren, O., Colombo, S. F., Pirruccello, M., Milosevic, I., Gracheva, E. O., Bagriantsev, S. N., Borgese, N. and De Camilli, P. (2013). PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153, 1494-1509.
14. Helle, S. C., Kanfer, G., Kolar, K., Lang, A., Michel, A. H. and Kornmann, B. (2013). Organization and function of membrane contact sites. Biochim. Biophys. Acta 1833, 2526-2541.
15. Hogan, P. G., Lewis, R. S. and Rao, A. (2010). Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28, 491-533.
16. Kaczmarek, L. K. (2006). Non-conducting functions of voltage-gated ion channels. Nat. Rev. Neurosci. 7, 761-771.
17. Kaufmann, W. A., Ferraguti, F., Fukazawa, Y., Kasugai, Y., Shigemoto, R., Laake, P., Sexton, J. A., Ruth, P., Wietzorrek, G., Knaus, H. G. et al. (2009). Large-conductance calcium-activated potassium channels in purkinje cell plasma membranes are clustered at sites of hypolemmal microdomains. J. Comp. Neurol. 515, 215-230.
18. King, A. N., Manning, C. F. and Trimmer, J. S. (2014). A unique ion channel clustering domain on the axon initial segment of mammalian neurons. J. Comp. Neuro. 522, 2594-2608.
19. Leung, Y. M., Kang, Y., Gao, X., Xia, F., Xie, H., Sheu, L., Tsuk, S., Lotan, I., Tsushima, R. G. and Gaisano, H. Y. (2003). Syntaxin 1A binds to the cytoplasmic C terminus of Kv2.1 to regulate channel gating and trafficking. J. Biol. Chem. 278, 17532-17538.
20. Lim, S. T., Antonucci, D. E., Scannevin, R. H. and Trimmer, J. S. (2000). A novel targeting signal for proximal clustering of the Kv2.1 K+ channel in hippocampal neurons. Neuron 25, 385-397.
21. Mandikian, D., Bocksteins, E., Parajuli, L. K., Bishop, H. I., Cerda, O., Shigemoto, R. and Trimmer, J. S. (2014). Cell type-specific spatial and functional coupling between mammalian brain Kv2.1 K channels and ryanodine receptors. J. Comp. Neurol. 522, 3555-3574.
22. McCord, M. C., Kullmann, P. H., He, K., Hartnett, K. A., Horn, J. P., Lotan, I. and Aizenman, E. (2014). Syntaxin-binding domain of Kv2.1 is essential for the expression of apoptotic K+ currents. J. Physiol. 592, 3511-3521.
23. Misonou, H., Mohapatra, D. P., Park, E. W., Leung, V., Zhen, D., Misonou, K., Anderson, A. E. and Trimmer, J. S. (2004). Regulation of ion channel localization and phosphorylation by neuronal activity. Nat. Neurosci. 7, 711-718.
24. Misonou, H., Mohapatra, D. P., Menegola, M. and Trimmer, J. S. (2005). Calciumand metabolic state-dependent modulation of the voltage-dependent Kv2.1 channel regulates neuronal excitability in response to ischemia. J. Neurosci. 25, 11184-11193.
25. Misonou, H., Thompson, S. M. and Cai, X. (2008). Dynamic regulation of the Kv2.1 voltage-gated potassium channel during brain ischemia through neuroglial interaction. J. Neurosci. 28, 8529-8538.
26. Mohapatra, D. P. and Trimmer, J. S. (2006). The Kv2.1 C terminus can autonomously transfer Kv2.1-like phosphorylation-dependent localization, voltage-dependent gating, and muscarinic modulation to diverse Kv channels. J. Neurosci. 26, 685-695.
27. Muennich, E. A. L. and Fyffe, R. E.W. (2004). Focal aggregation of voltage-gated, Kv2.1 subunit-containing, potassium channels at synaptic sites in rat spinal motoneurones. J. Physiol. 554, 673-685.
28. Mulholland, P. J., Carpenter-Hyland, E. P., Hearing, M. C., Becker, H. C., Woodward, J. J. and Chandler, L. J. (2008). Glutamate transporters regulate extrasynaptic NMDA receptor modulation of Kv2.1 potassium channels. J. Neurosci. 28, 8801-8809.
29. Nagy, J. I., Yamamoto, T. and Jordan, L. M. (1993). Evidence for the cholinergic nature of C-terminals associated with subsurface cisterns in alpha-motoneurons of rat. Synapse 15, 17-32.
30. O'Connell, K. M. and Tamkun, M. M. (2005). Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains. J. Cell Sci. 118, 2155-2166.
31. O'Connell, K. M., Rolig, A. S., Whitesell, J. D. and Tamkun, M. M. (2006). Kv2.1 potassium channels are retained within dynamic cell surface microdomains that are defined by a perimeter fence. J. Neurosci. 26, 9609-9618.
32. O'Connell, K. M. S., Whitesell, J. D. and Tamkun, M. M. (2008). Localization and mobility of the delayed-rectifer K+ channel Kv2.1 in adult cardiomyocytes. Am. J. Physiol. 294, H229-H237.
33. O'Connell, K. M., Loftus, R. and Tamkun, M. M. (2010). Localization-dependent activity of the Kv2.1 delayed-rectifier K+ channel. Proc. Natl. Acad. Sci. USA 107, 12351-12356.
34. Orci, L., Ravazzola, M., Le Coadic, M., Shen, W. W., Demaurex, N. and Cosson, P. (2009). From the cover: STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 106, 19358-19362.
35. Park, C. Y., Shcheglovitov, A. and Dolmetsch, R. (2010). The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 330, 101-105.
36. Porter, K. R. and Palade, G. E. (1957). Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol. 3, 269-300.
37. Press, W. H., Teukolsky, S. A., Vetterling, W. T. and Flannery, B. P. (2007). Numerical Recipes: The Art of Scientific Computing, 3rd edn. Cambridge, MA: Cambridge University Press.
38. Prinz, W. A. (2014). Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205, 759-769.
39. Raffel, M., Willert, C. E., Wereley, S. T. and J., Kompenhans (2007). Particle Image Velocimetry: A Practical Guide. Berlin; Heidelberg: Springer.
40. Rosenbluth, J. (1962). Subsurface cisterns and their relationship to the neuronal plasma membrane. J. Cell Biol. 13, 405-421.
41. Sarmiere, P. D., Weigle, C. M. and Tamkun, M. M. (2008). The Kv2.1 K+ channel targets to the axon initial segment of hippocampal and cortical neurons in culture and in situ. BMC Neurosci. 9, 112.
42. Schauder, C. M., Wu, X., Saheki, Y., Narayanaswamy, P., Torta, F., Wenk, M. R., De Camilli, P. and Reinisch, K. M. (2014). Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510, 552-555.
43. Schneider, C. A., Rasband, W. S. and Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
44. Tamkun, M. M., O'connell, K. M. and Rolig, A. S. (2007). A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels. J. Cell Sci. 120, 2413-2423.
45. Thielicke, W. and Stamhuis, E. J. (2014). PIVlab - Time-Resolved Digital Particle Image Velocimetry Tool for MATLAB.
46. Wang, Y., Deng, X., Mancarella, S., Hendron, E., Eguchi, S., Soboloff, J., Tang, X. D. and Gill, D. L. (2010). The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330, 105-109.
47. Weigel, A. V., Simon, B., Tamkun, M. M. and Krapf, D. (2011). Ergodic and nonergodic processes coexist in the plasma membrane as observed by single-molecule tracking. Proc. Natl. Acad. Sci. USA 108, 6438-6443.