Worm Breeder's Gazette 14(2): 90 (February 1, 1996)

These abstracts should not be cited in bibliographies. Material contained herein should be treated as personal communication and should be cited as such only with the consent of the author.

The Degenerin gene family is also expanding.....

Nektarios Tavernarakis, Jian Xue, Monica Driscoll

Department of Molecular Biology and Biochemistry Rutgers University New Brunswick NJ 08855

C. elegans mec-4, mec-10, deg-1 and unc-105 encode members of the
degenerin gene family that exhibit sequence similarity to subunits of
the vertebrate amiloride-sensitive epithelial Na+ channel. The
vertebrate Na+ channel includes at least three homologous subunits. The
channel expressed in the C. elegans touch receptor neurons, hypothesized
to be a mechanosensitive channel, includes at least two related
subunits, MEC-4 and MEC-10. Recently four additional family members,
housed in cosmids T28D9 (II), F58G6 (IV), R13A1 (IV), and E02H4 (X) have
been entered into the C. elegans database by the Genome Consortium. We
have begun characterization of these newly identified degenerin genes by
assaying the expression of lacZ fusions to the predicted open reading
frames. In addition, we fused their putative 5' regulatory regions to
the toxic mec-4(d), so that the cells in which the new family member is
expressed undergo degeneration. These ablation studies help both in
identification of the cells in which degenerinX is expressed and in
determination of potential mutant phenotypes (provided that degenerinX
is needed for cell function). Here we report on the two new family
members most similar to the touch receptor degenerins (60% and 66%
similarity to MEC-4 respectively), designated R13A1_4 and E02H4_1.

R13A1_4 is expressed in about 35 neurons that have cell bodies situated
primarily in the ventral cord and nerve ring. Staining is most intense
in L1 and L2 animals, although it is evident at late embryonic stages
and persists into adulthood. The neuronal processes of stained cells are
clearly detectable, which has facilitated identification of some of the
cells that express this potential degenerin family member. PDA, PDB, DD,
DB and posibly DA motorneurons express R13A1_4. We have not yet
unambiguously identified neurons whose cell bodies are situated in the
nerve ring, but it is interesting that included among the candidates are
the ASH, FLP and OLQ neurons that have been demonstrated by Kaplan and
colleagues to mediate nose touch. We are able to state with certainty
that the posterior touch receptor neurons do not express this fusion
gene. Animals harboring fusions of the toxic mec-4(d) to R13A1_4 are
severely uncoordinated. The most affected are nearly paralyzed; an often
seen phenotype is that animals are unable to back up and coil when
prodded with a pick. Transgenic animals also appear to be touch abnormal
and somewhat hypercontracted at the posterior part of the body. Some
mobile animals are insensitive to nose touch, (4 out of 50 mosaic
transformants examined). Given this data, we examined the genetic map to
identify candidate mutations in R13A1 which maps between genes deb-1 and
dif-1 on chromosome IV. One very interesting gene in the general region
(although not specifically mapped within the deb-1-dif-1 interval) is
unc-8. unc-8 has been proposed to encode a member of the degenerin gene
family by Shreffler, Wolinsky and colleagues because dominant
gain-of-function mutations cause swelling of ventral cord neurons, a
phenotype suppressed by mutations in mec-6 (which also suppress swelling
and death induced by toxic alleles of degenerin family members mec-4,
mec-10 and deg-1). The phenotype of some mosaics of the R13A1_4-mec-4(d)
ablation fusion line very closely resembles the phenotype of the
semi-dominant unc-8(n491) allele. Cosmid R13A1, however, does not
unambiguously rescue unc-8(n491) or unc-8(e49) (a weaker recessive
allele). Rescue by increased dosage of the wild type gene might not be
expected since unc-8 alleles are gain-of-function alleles and
overexpression of the gene might exacerbate the phenotype (unc-8
loss-of-function mutants exhibit no behavioral abnormalities). We
consider R13A1 a strong candidate for unc-8 or a gene whose product
could interact with unc-8.

E02H4_1 is expressed in about 15 neurons whose cell bodies are also
situated in the ventral cord and nerve ring. The cells that express this
degenerin-related gene appear to be a subset of those cells in which
R13A1_4 is expressed. When the E02H4_1 expressing cells were genetically
ablated using a mec-4(d) gene fusion, worms were moderately
uncoordinated but they retained the ability to back and did not coil.
Hypercontraction or touch abnormalities were not evident. E02H4 maps to
the middle of X, between genes col-9 and his-24. We are in the process
of characterizing mutants in the region to test whether they might
correspond to E02H4_1.

One theme that emerges is that members of the degenerin gene family are
expressed widely in the C. elegans nervous system. What are they all
doing? Possibly, Na+ channels made up of degenerin subunits are
generally involved in cell volume regulation or in maintenance of
osmotic balance that is critical to neuronal function. All might be
mechanically gated and some, such as those expressed in the touch
neurons, may play essential roles in the conversion of mechanical
stimuli to behavioral responses. Interestingly, it has been suggested
that A and B type motorneurons act as stretch receptors that help
propagate the sinusoidal body wave in response to contraction of body
wall muscles. Perhaps degenerins expressed in these motorneurons
function in this capacity.