Sulfated signal from ASJ sensory neurons modulates stomatin-dependent coordination in Caenorhabditis elegans.
The neuronal stomatin-like proteins UNC-1 and UNC-24 play important roles in the nervous system of Caenorhabditis elegans. These neuronal stomatin-like proteins are putative chaperone proteins that can modify volatile anesthetic sensitivity and disrupt coordinated locomotion. A suppressor of unc-1 and unc-24, named ssu-1(fc73) (for suppressor of stomatin uncoordination), suppresses three phenotypes of neuronal stomatin-like protein deficiency as follows: volatile anesthetic sensitivity, uncoordinated locomotion, and a constitutive alternative developmental phenotype known as dauer. Here we provide the first phenotypic characterization of ssu-1, predicted to be the only C. elegans cytosolic alcohol sulfotransferase, a family of enzymes that catalyze a sulfate linkage with the alcohol group of small molecules for the purposes of detoxification or modification of signaling. In vitro enzyme analysis of bacterially expressed SSU-1 demonstrates sulfotransferase activity and thus confirms the function predicted by protein sequence similarities. Whereas unc-1 is expressed in the majority of neurons of C. elegans, expression of SSU-1 protein in only the two ASJ amphid interneurons is sufficient to restore the wild type phenotype. This work demonstrates that SSU-1 is a functional sulfotransferase that likely modifies endocrine signaling in C. elegans. The expression of SSU-1 in the ASJ neurons refines the understanding of the function of these cells and supports their classification as endocrine tissue. The relationship of unc-1, unc-24, and ssu-1 is the first association of neuronal stomatin-like proteins sharing regulatory roles with a sulfotransferase enzyme.
Carroll
Bryan T
BT
Department of Genetics, Case School of Medicine, Cleveland, Ohio 44106, USA.
Dubyak
George R
GR
Sedensky
Margaret M
MM
Morgan
Phil G
PG
D000483:Alleles; D000818:Animals; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D003600:Cytosol / Q000378:metabolism; D005786:Gene Expression Regulation; D008565:Membrane Proteins / Q000737:chemistry / Q000378:metabolism; D008954:Models, Biological; D008957:Models, Genetic; D009475:Neurons, Afferent / Q000378:metabolism*; D020033:Protein Isoforms; D015398:Signal Transduction; D013431:Sulfates / Q000378:metabolism; D015238:Sulfotransferases / Q000737:chemistry / Q000378:metabolism
D029742:Caenorhabditis elegans Proteins; D008565:Membrane Proteins; D020033:Protein Isoforms; D013431:Sulfates; C113701:Unc-1 protein, C elegans; C099877:Unc-24 protein, C elegans; D015238:Sulfotransferases; C515970:SSU-1 protein, C elegans; C028152:alcohol sulfotransferase