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The Journal of Neuroscience, January 16, 2008, 28(3):757-765; doi:10.1523/JNEUROSCI.3825-07.2008

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Cellular/Molecular
Cumulative Activation of Voltage-Dependent KVS-1 Potassium Channels

Patricio Rojas,¹ Jonathan Garst-Orozco,¹ Beravan Baban,¹ Jose Antonio de Santiago-Castillo,³ Manuel Covarrubias,³ and Lawrence Salkoff^1,2

Departments of ¹Anatomy and Neurobiology and ²Genetics, Washington University School of Medicine, St. Louis, Missouri 63110, and ³Department of Pathology, Anatomy, and Cell Biology, Jefferson Medical College of Thomas Jefferson University, Philadelphia, Pennsylvania 19107

Correspondence should be addressed to Lawrence Salkoff, Department of Anatomy and Neurobiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO, 63110. Email: salkoffl{at}pcg.wustl.edu

In this study, we reveal the existence of a novel use-dependent phenomenon in potassium channels, which we refer to as cumulative activation (CA). CA consists of an increase in current amplitude in response to repetitive depolarizing step pulses to the same potential. CA persists for up to 20 s and is similar to a phenomenon called "voltage-dependent facilitation" observed in some calcium channels. The KVS-1 K⁺ channel, which exhibits CA, is a rapidly activating and inactivating voltage-dependent potassium channel expressed in chemosensory and other neurons of Caenorhabditis elegans. It is unusual in being most closely related to the Shab (Kv2) family of potassium channels, which typically behave like delayed rectifier K⁺ channels in other species. The magnitude of CA depends on the frequency, voltage, and duration of the depolarizing step pulse. CA also radically changes the activation and inactivation kinetics of the channel, suggesting that the channel may undergo a physical modification in a use-dependent manner; thus, a model that closely simulates the behavior of the channel postulates the existence of two populations of channels, unmodified and modified. Use-dependent changes in the behavior of potassium channels, such as CA observed in KVS-1, could be involved in functional mechanisms of cellular plasticity such as synaptic depression that represent the cellular basis of learning and memory.

Key words: potassium channels; facilitation; inactivation; use dependency; plasticity; physiology

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Received Aug. 21, 2007; revised Nov. 29, 2007; accepted Dec. 1, 2007.

Correspondence should be addressed to Lawrence Salkoff, Department of Anatomy and Neurobiology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO, 63110. Email: salkoffl{at}pcg.wustl.edu

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