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The Journal of Neuroscience, September 20, 2006, 26(38):9609-9618; doi:10.1523/JNEUROSCI.1825-06.2006

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Cellular/Molecular
Kv2.1 Potassium Channels Are Retained within Dynamic Cell Surface Microdomains That Are Defined by a Perimeter Fence

Kristen M. S. O'Connell,¹ Annah S. Rolig,¹ Jennifer D. Whitesell,¹ and Michael M. Tamkun^1,2

Departments of ¹Biomedical Sciences and ²Biochemistry and Molecular Biology, Colorado State University, Ft. Collins, Colorado 80523

Correspondence should be addressed to Dr. Michael M. Tamkun, Department of Biomedical Sciences, Colorado State University, Ft. Collins, CO 80523-1617. Email: tamkunmm{at}lamar.colostate.edu

Ion channel localization to specific cell surface regions is essential for proper neuronal function. The Kv2.1 K⁺ channel forms large clusters on the plasma membrane of hippocampal neurons and transfected human embryonic kidney (HEK) cells. Using live cell imaging, we address mechanisms underlying this Kv2.1 clustering in both HEK cells and cultured hippocampal neurons. The Kv2.1-containing surface clusters have properties unlike those expected for a scaffolding protein bound channel. After channel is delivered to the plasma membrane via intracellular transport vesicles, it remains localized at the insertion site. Fluorescence recovery after photobleaching (FRAP) and quantum dot tracking experiments indicate that channel within the surface cluster is mobile (FRAP, = 14.1 ± 1.5 and 11.5 ± 6.1 s in HEK cells and neurons, respectively). The cluster perimeter is not static, because after fusion of adjacent clusters, green fluorescent protein (GFP)–Kv2.1 completely exchanged between the two domains within 60 s. Treatment of hippocampal neurons expressing GFP-Kv2.1 with 5 µM latrunculin A resulted in a significant increase in average cluster size from 0.89 ± 0.16 µm² to 12.15 ± 1.4 µm² with a concomitant decrease in cluster number. Additionally, Kv2.1 was no longer restricted to the cell body, suggesting a role for cortical actin in both cluster maintenance and localization. Thus, Kv2.1 surface domains likely trap mobile Kv2.1 channels within a well defined, but fluid, perimeter rather than being tightly bound to a scaffolding protein-containing complex. Channel moves directly into these clusters via trafficking vesicles. Such domains allow for efficient trafficking to the cell surface while sequestering channel with signaling proteins.

Key words: Kv channel; restricted diffusion; membrane insertion; quantum dot tracking; fluorescence microscopy; hippocampal neurons

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Received April 29, 2006; revised July 21, 2006; accepted Aug. 8, 2006.

Correspondence should be addressed to Dr. Michael M. Tamkun, Department of Biomedical Sciences, Colorado State University, Ft. Collins, CO 80523-1617. Email: tamkunmm{at}lamar.colostate.edu

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