The evolution of information transfer in excitable cells
I study the electrophysiology of Cnidarian medusae to try to understand the structure, properties and functions of ion channels in systems derived from an early stage in the evolution of nerves. A considerable advantage arises from the ability to make direct links between molecular events in excitable cells and an animal’s different behavioural strategies.
In the jellyfish Aglantha digitale motor axons conduct two separate kinds of action potential based on multiple K+ channel phenotypes, mammalian-like Na+, and T-type Ca2+ channels.
Each action potential is linked to a specific form of swimming (see video recording below). George Mackie (University of Victoria) & I find that during the course of evolution the increased bandwidth provided by dual impulse propagation has permitted the reorganization of communication pathways responsible for defense and feeding (Mackie, Marx & Meech, 2003; Meech, 2004).
Aglantha has both nervous and non-nervous (epithelial) communication pathways that interact during feeding and swimming. We have compared the ion channels responsible for propagating action potentials in epithelia with those in nerve axons. We use a loose, macro-patch recording configuration and find that differences in the strength of muscle contraction during swimmming arise from differences in the rate of rise of synaptic potentials in the muscle epithelium (Meech & Mackie, 2006).
A long-term interest is in how ion channels and ion pumps interact at the intracellular membrane surface. My experiments on Aplysia neurones in Felix Strumwasser's laboratory in 1969 provided the first direct experimental evidence for the activation of a K+ conductance by intracellular Ca2+. More recently Ian Spreadbury, Corne Kros & I, have examined the role of these Ca2+ activated K+ currents in cochlea outer hair cells (Spreadbury, Kros & Meech, 2004).
K+ channels gated by internal Na+ are also widely distributed in different animal tissues. Xiao-wei Nui & I have found that activation of these KNa channels in guinea-pig ventricular myocytes is competitively inhibited by internal K+ (Niu & Meech, 2000).
Discovered in snail neurones in collaboration with Roger Thomas, voltage-gated proton pathways are now known to be present in a wide variety of cells. In human neutrophils efflux of H+ through a voltage-gated proton pathway compensates for the intracellular acidification associated with the production of super oxide. Work with Lydia Henderson has revealed that gp91phox is the proton pathway in these cells (Henderson & Meech, 2002).
Recent research has focussed on the structural similarities between ion channels and ion pumps. An emerging theme is that transport proteins have a modular structure with components that are shared with conductive pathways such as ion channels. A recent finding that the removal of one such ‘module’ from the chloride/bicarbonate transporter (AE1) can transform it into a conductive pathway suggests that conductive pores and membrane transporters are part of a continuum of ion carrying mechanisms (Parker, Tanner, Boron & Meech, 2005).
Video recordings of two forms of swimming in the jellyfish Aglantha digitale: LEFT a fast swim in response to stimulus from a glass probe and RIGHT a sequence of two spontaneous slow swims