Gap junctions in C. elegans: Their roles in behavior and development

Abstract

The nematode Caenorhabditis elegans utilizes gap junctions in different fashions in virtually all of its cells. This model animal has a surprisingly large number of innexin genes within its genome, and many nematode cell types can express multiple innexins at once, leading to the formation of diverse junction types and enough redundancy to limit the effect of single gene knockdowns on animal development or behavioral phenotypes. Here, we review the general properties of these junctions, their expression patterns, and their known roles in tissue development and in the animal's connectome. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 587-596, 2017.

Keywords: heteromeric; heterotypic; innexin; nematode.

Figure 1

Models of gap junction composition for C. elegans. (A) Classification of gap junction channels according to their subunit composition as homomeric, heterotypic, or heteromeric (after Koval et al., 2014). Rather little is yet known about which combinations of innexin subunits are capable of associating within a hemichannel (in one membrane) or of docking across the membrane with a partner in the opposing membrane. (B) Model of the homomeric innexin channel in C. elegans intestine (after Oshima et al., 2016). (C) Models of possible innexin heteromeric channels in bodywall muscle, assuming six subunits per hemichannel, utilizing two innexins in one subtype and four other innexins in a second subtype (after Liu et al, 2013). (D) Models of possible innexin heteromeric channels in distal gonad, assuming eight subunits per hemichannel (after Starich et al, 2014). At present, we do not know the number of subunits per channel, and the possible arrangements shown here are among many possibilities. [Color figure can be viewed at wileyonlinelibrary.com.]

Figure 2

Innexin expression pattern in the pharynx (Reproduced with permission from Altun et al, Developmental Dynamics, 2009, 238, 1936–1950). Expression patterns for innexin genes are mapped versus the pharyngeal muscle segments, pm1 to pm8, illustrating which are highly expressed (dark bars) or weekly expressed (lighter bars) in the adult hermaphrodite. While many muscles express similar sets of innexins, each segment of pm muscles tends to express a different combination than its nearest neighbors. Within a segment, pharyngeal muscles lie in cell pairs which are often syncytial to their nearest neighbor, and form gap junctions to nearby marginal cells (not shown). Between segments, each muscle cell forms gap junctions to the muscles in the neighboring segment. Arcade cells, purple; pharyngeal epithelium (pe) and pm muscles (1–8), green; valve cells, brown; and intestine, pink. [Color figure can be viewed at wileyonlinelibrary.com.]