Description

Recent studies have shown that accessory cells of mammalian touch receptors, such as the Merkel receptors, play an essential role in transducing touch (Pawson et al., 2009, Maricich et al., 2009, Maksimovic et al., 2014, Woo et al., 2014, Ikeda et al., 2014, Woo et al., 2015). Similarly, in C. elegans, we found that OLQ and IL glial socket cells are needed for responses to nose touch. More specifically, we reported that these glial cells express DEG/ENaC Na⁺ channel DELM-1 and DELM-2, which are needed specifically in glia for OLQ neuronal responses to touch and nose-touch avoidance behavior. We also showed that nose touch responses are restored by overexpression of the worm inward rectifier K⁺ channel IRK-2 in socket glia of delm-1 mutants (Han et al., 2013). These published results suggest that glial Na⁺ and K⁺ channels are needed for the function of the associated touch receptor neurons.

We next wondered whether it is the influx of cations or expression of DEG/ENaC Na⁺channels that is needed in glia for nose touch avoidance. To distinguish between these possibilities, we expressed the temperature-sensitive mosquito TRPA1, AgTRPA1, in socket glia of delm-1 mutants and assayed nose-touch avoidance (Kang et al., 2012). AgTRPA1 belongs to the TRP family of ion channels and is a Na⁺ and Ca²⁺ permeable channel (Kang et al., 2012). Furthermore, AgTRPA1 has the advantage that it is activated by temperature, which allows for a direct test of whether the influx of cations in glia is needed for nose touch response.

When we expressed AgTRPA1 in OLQ and IL socket glia of delm-1 mutants, we did not find any gross abnormalities of glial cells (Fig. 1 A and B). We previously published that knock-out of delm-1 does not alter glial morphology either (Han et al., 2013). When we assayed nose touch at 22˚C, when AgTRPA1 channel is closed, we found no rescue of the nose touch response (Fig. 1 C and D). On the contrary, when assayed at 28˚C, when AgTRPA1 is open, the transgenic animals expressing AgTRPA1 in OLQ and IL socket glia of delm-1 mutants, showed restoration of nose touch sensitivity (Fig. 1 C and E). These results support that movement of cations across the OLQ and IL socket glial plasma membrane is needed for nose touch response in C. elegans, suggesting that depolarization of the glial plasma membrane is what is required for nose touch avoidance behavior. Given that we published that overexpression of worm IRK-2 restores nose touch defects of delm-1 mutants, we propose that depolarization of the glial plasma membrane might be required for vectorial transport of K⁺ from the surrounding tissue to the microenvironment between glia and neurons to regulate neuronal output (Wang et al., 2008, Wang et al., 2012), as suggested by work in Pacinian corpuscles (Ilyinsky et al., 1976).