Correlations in Ion Channel mRNA in Rhythmically Active Neurons

Background To what extent do identified neurons from different animals vary in their expression of ion channel genes? In neurons of the same type, is ion channel expression highly variable and/or is there any relationship between ion channel expression that is conserved? Methodology/Principal Findings To address these questions we measured ion channel mRNA in large cells (LCs) of the crab cardiac ganglion. We cloned a calcium channel, caco, and a potassium channel, shaker. Using single-cell quantitative PCR, we measured levels of mRNA for these and 6 other different ion channels in cardiac ganglion LCs. Across the population of LCs we measured 3–9 fold ranges of mRNA levels, and we found correlations in the expression of many pairs of conductances Conclusions/Significance In previous measurements from the crab stomatogastric ganglion (STG), ion channel expression was variable, but many pairs of channels had correlated expression. However, each STG cell type had a unique combination of ion channel correlations. Our findings from the crab cardiac ganglion are similar, but the correlations in the LCs are different from those in STG neurons, supporting the idea that such correlations could be markers of cell identity or activity.

[1]  D. Hartline,et al.  Impulse identification and axon mapping of the nine neurons in the cardiac ganglion of the lobster Homarus americanus. , 1967, The Journal of experimental biology.

[2]  E. Mayeri,et al.  Functional Organization of the Cardiac Ganglion of the Lobster, Homarus americanus , 1973, The Journal of general physiology.

[3]  Chun-Fang Wu,et al.  Drosophila cacophony Channels: A Major Mediator of Neuronal Ca2+ Currents and a Trigger for K+ Channel Homeostatic Regulation , 2007, The Journal of Neuroscience.

[4]  R. Harris-Warrick,et al.  Alternative Splicing in the Pore-Forming Region of shakerPotassium Channels , 1997, The Journal of Neuroscience.

[5]  G. Turrigiano.  Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same , 1999, Trends in Neurosciences.

[6]  E. Marder,et al.  Variable channel expression in identified single and electrically coupled neurons in different animals , 2006, Nature Neuroscience.

[7]  B. Bean,et al.  Robustness of Burst Firing in Dissociated Purkinje Neurons with Acute or Long-Term Reductions in Sodium Conductance , 2005, The Journal of Neuroscience.

[8]  E. Marder,et al.  Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  E. Marder,et al.  Activity-dependent regulation of conductances in model neurons. , 1993, Science.

[10]  Eve Marder,et al.  Structure and visualization of high-dimensional conductance spaces. , 2006, Journal of neurophysiology.

[11]  K Tazaki,et al.  Characterization of Ca current underlying burst formation in lobster cardiac ganglion motorneurons. , 1990, Journal of neurophysiology.

[12]  E. Marder,et al.  Mass spectrometric characterization and physiological actions of GAHKNYLRFamide, a novel FMRFamide‐like peptide from crabs of the genus Cancer , 2006, Journal of neurochemistry.

[13]  S. Lammel,et al.  Unique Properties of Mesoprefrontal Neurons within a Dual Mesocorticolimbic Dopamine System , 2008, Neuron.

[14]  K Tazaki,et al.  Spontaneous electrical activity and interaction of large and small cells in cardiac ganglion of the crab, Portunus sanguinolentus. , 1979, Journal of neurophysiology.

[15]  E. Marder,et al.  Similar network activity from disparate circuit parameters , 2004, Nature Neuroscience.

[16]  Eve Marder,et al.  Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. , 2003, Journal of neurophysiology.

[17]  D. Hartline.  Integrative Neurophysiology of the Lobster Cardiac Ganglion , 1979 .

[18]  E. Marder,et al.  Multiple modulators act on the cardiac ganglion of the crab, Cancer borealis , 2007, Journal of Experimental Biology.

[19]  I. Cooke,et al.  Reliable, Responsive Pacemaking and Pattern Generation With Minimal Cell Numbers: the Crustacean Cardiac Ganglion , 2002, The Biological Bulletin.

[20]  K. Tazaki,et al.  Ionic bases of slow, depolarizing responses of cardiac ganglion neurons in the crab, Portunus sanguinolentus. , 1979, Journal of neurophysiology.

[21]  E. Marder,et al.  Activity-Dependent Regulation of Potassium Currents in an Identified Neuron of the Stomatogastric Ganglion of the Crab Cancer borealis , 1999, The Journal of Neuroscience.

[22]  E. Marder,et al.  Activity-dependent changes in the intrinsic properties of cultured neurons. , 1994, Science.

[23]  Ronald L Calabrese,et al.  Endogenous and half-center bursting in morphologically inspired models of leech heart interneurons. , 2006, Journal of neurophysiology.

[24]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[25]  K Tazaki,et al.  Neuronal mechanisms underlying rhythmic bursts in crustacean cardiac ganglia. , 1983, Symposia of the Society for Experimental Biology.

[26]  K. Tazaki,et al.  Isolation and characterization of slow, depolarizing responses of cardiac ganglion neurons in the crab, Portunus sanguinolentus. , 1979, Journal of neurophysiology.

[27]  Erik De Schutter,et al.  Complex Parameter Landscape for a Complex Neuron Model , 2006, PLoS Comput. Biol..

[28]  Bruce R. Johnson,et al.  Activity-Independent Homeostasis in Rhythmically Active Neurons , 2003, Neuron.

[29]  Nicholas C. Spitzer,et al.  New dimensions of neuronal plasticity , 1999, Nature Neuroscience.

[30]  E. Marder,et al.  How Multiple Conductances Determine Electrophysiological Properties in a Multicompartment Model , 2009, The Journal of Neuroscience.

[31]  Allan R. Willms,et al.  Quantitative Single-Cell-Reverse Transcription-PCR Demonstrates That A-Current Magnitude Varies as a Linear Function ofshal Gene Expression in Identified Stomatogastric Neurons , 1997, The Journal of Neuroscience.

[32]  Niraj S. Desai,et al.  Plasticity in the intrinsic excitability of cortical pyramidal neurons , 1999, Nature Neuroscience.

[33]  B. Liss,et al.  Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription , 2001, The EMBO journal.

[34]  Expression of Panulirus shaker potassium channel splice variants. , 1998, Receptors & channels.

[35]  E. Marder,et al.  Failure of averaging in the construction of a conductance-based neuron model. , 2002, Journal of neurophysiology.

[36]  Jeffrey C. Hall,et al.  A Drosophila Calcium Channel α1 Subunit Gene Maps to a Genetic Locus Associated with Behavioral and Visual Defects , 1996, The Journal of Neuroscience.

[37]  K. Tazaki,et al.  Currents under voltage clamp of burst-forming neurons of the cardiac ganglion of the lobster (Homarus americanus). , 1986, Journal of neurophysiology.

[38]  John Guckenheimer,et al.  Activity-independent coregulation of IA and Ih in rhythmically active neurons. , 2005, Journal of neurophysiology.

[39]  E. Marder,et al.  Variability, compensation and homeostasis in neuron and network function , 2006, Nature Reviews Neuroscience.

[40]  D. Maynard.  ACTIVITY IN A CRUSTACEAN GANGLION. II. PATTERN AND INTERACTION IN BURST FORMATION , 1955 .

[41]  J. Littleton,et al.  Presynaptic N-type Calcium Channels Regulate Synaptic Growth* , 2003, Journal of Biological Chemistry.

[42]  Jean-Marc Goaillard,et al.  Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression , 2007, Proceedings of the National Academy of Sciences.