Academic journal article Genetics

Genes Required for Osmoregulation and Apical Secretion in Caenorhabditis Elegans

Academic journal article Genetics

Genes Required for Osmoregulation and Apical Secretion in Caenorhabditis Elegans

Article excerpt

ABSTRACT

Few studies have investigated whether or not there is an interdependence between osmoregulation and vesicular trafficking. We previously showed that in Caenorhabditis elegans che-14 mutations affect osmoregulation, cuticle secretion, and sensory organ development. We report the identification of seven lethal mutations displaying che-14-like phenotypes, which define four new genes, rdy-1-rdy-4 (rod-like larval lethality and dye-filling defective). rdy-1, rdy-2, and rdy-4 mutations affect excretory canal function and cuticle formation. Moreover, rdy-1 and rdy-2 mutations reduce the amount of matrix material normally secreted by sheath cells in the amphid channel. In contrast, rdy-3 mutants have short cystic excretory canals, suggesting that it acts in a different process. rdy-1 encodes the vacuolar H^sup +^-ATPase a-subunit VHA-5, whereas rdy-2 encodes a new tetraspan protein. We suggest that RDY-1/VHA-5 acts upstream of RDY-2 and CHE-14 in some tissues, since it is required for their delivery to the epidermal, but not the amphid sheath, apical plasma membrane. Hence, the RDY-1/VHA-5 trafficking function appears essential in some cells and its proton pump function essential in others. Finally, we show that RDY-1/VHA-5 distribution changes prior to molting in parallel with that of actin microfilaments and propose a model for molting whereby actin provides a spatial cue for secretion.

THE ability to control solute and water balance during osmotic challenge is essential for cellular life (YANCEY et al. 1982). Most cellular functions, in particular vesicle trafficking, depend on the specific balance of inorganic ions in the cytosol and the lumen. For instance, loss of the yeast endosomal Na1/H+ exchanger Nhx1 alters cytoplasmic and luminal pH, with profound consequences on the endocytic trafficking pathway (BRETT et al. 2005). In Caenorhabditis elegans, disruption of the epidermal chloride channel gene clh-1 results in a significantly wider body and an abnormal structure of cuticular specializations called alae, which are secreted by the epidermis (PETALCORIN et al. 1999). Conversely, many animals and plants respond to the need to modify their internal ion balance by regulating the trafficking of certain ion transporters, channels, and exchangers. For instance, vasopressin triggers the fusion of subapical vesicles containing the aquaporin-2 membrane water channel with the apical plasma membrane of kidney-collecting-duct principal cells to mediate water excretion (NIELSEN et al. 1993, 1995). Although vesicle trafficking and osmoregulation seem interwoven, whether or not there is a genetic basis for their interdependence is largely unclear.

An obvious approach to addressing this problem is to find mutations that would affect both osmoregulation and trafficking. In contrast to Saccharomyces cerevisiae for which a wealth of information on the genetic control of osmoregulation (HOHMANN 2002) or trafficking (SCHEKMAN and NOVICK 2004) is available, less is known about multicellular organisms. The nematode C. elegans provides many powerful experimental advantages for defining evolutionarily conserved genes, pathways, and mechanisms that give rise to diverse physiological processes (JORGENSEN and MANGO 2002). In particular, C. elegans has helped define genes that contribute to osmotic homeostasis (KAITNA et al. 2002; SOLOMON et al. 2004; LAMITINA and STRANGE 2005) and trafficking (NURRISH 2002).

We previously found that the C. elegans protein CHE-14 is important for both osmoregulation and apical trafficking (MICHAUX et al. 2000). A proportion of che-14 larvae dies with an appearance of rods that are filled with fluid, which resemble larvae observed after laser ablation of the kidney-like excretory cell (NELSON and RIDDLE 1984). In addition, transmission electron microscopy (TEM) reveals that che-14 mutants accumulate large vesicles in support cells of the amphid sensory organs and dark material at the apical surface of the epidermis, while the cuticle normally secreted apically is much thinner than normal (MICHAUX et al. …

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