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First published online February 2, 2004
doi: 10.1242/10.1242/dev.00959

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The AHR-1 aryl hydrocarbon receptor and its co-factor the AHA-1 aryl hydrocarbon receptor nuclear translocator specify GABAergic neuron cell fate in C. elegans

Xun Huang^1,*, Jo Anne Powell-Coffman² and Yishi Jin^1,

¹ Department of Molecular, Cellular and Developmental Biology, Sinsheimer Laboratories, Howard Hughes Medical Institute, University of California, Santa Cruz, CA 95064, USA
² Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IA 50011-3260, USA

View larger version (59K): [in a new window]   Fig. 1. GABAergic RME neurons. (A) The cell lineage and morphology of RME cells. X, dying cells. (B) Punc-25GFP expression. For wild type (labeled as juIs76) and ju145, two focal planes are shown, one on RMED/V, the other on RMEL. Schematic illustrations are shown on the right. Asterisks denote the position of the processes from the RMED and RMEV neurons; arrowheads point to the ectopic process from RMEL in ju145. (C). Anti-GABA staining reveals defects in ahr-1 identical to those shown in B. Two focal planes are shown, one on RMED/V, the other on RMEL. Arrow points to the ectopic process from RMEL in ju145. Scale bar: 50 µm.

View larger version (22K): [in a new window]   Fig. 2. ju145 is a mutation in C41G7.5/AHR-1. (A,B) The genetic map position and transformation rescue of ahr-1(ju145). The rescuing activities are shown as number of rescued line/total number of lines. ND, not determined. (C) AHR-1 domain structure and the molecular lesion of ju145. HLH, helix-loop-helix; PAS, domain in Per, ARNT and Sim. The PAS domain can be further divided to PAS A and PAS B subdomains.

View larger version (58K): [in a new window]   Fig. 3. ju145 affects RMEL/R cell fate. (A,B) RMEL/R form fewer synapses (arrows) in ju145 animals compared with wild type; enlarged views are shown below with arrows. (C-H) ju145 mutation affects cell-specific marker expressions in RMEL/R neurons. Arrows point to the position of RMEL neurons. (C,D) Pglr-1GFP is expressed in RMEL/R neurons in wild type (C) but not in ju145 (D) animals. (E,F) Plim-6rGFP is expressed in RMEL/R neurons in wild type (E) but not ju145 (F) animals. (G,H) Punc-47sGFP is expressed in RMEL/R neurons in wild type (G) but not ju145 animals. (I) Pavr-15GFP expression in RMED/V cells (arrows) in wild-type animals. (J-L) Pavr-15GFP is ectopically expressed in RMEL/R cells (arrows in K and L) in ju145 animals; arrows in J indicate RMED/V cells. Scale bar: 20 µm.

View larger version (52K): [in a new window]   Fig. 4. AHR-1 is expressed in RMEL/R cells. (A) Nomarski picture of the head of an animal, with an enlarged view shown in B. (C) Fluorescence image of Pahr-1GFP expression. Overlay is shown D. Arrows indicate the RMEL neurons. Pahr-1GFP is also brightly expressed in a pair of sensory neurons (arrowhead), likely to be ASKL/R. Scale bar: in A,C,D, 50 µm; in B, 20 µm.

View larger version (63K): [in a new window]   Fig. 5. Ectopic AHR-1 expression in RMED/V cells can transform them into RMEL/R-like cells. (A) juIs76 wild-type animals. (B) Ectopic AHR-1 expression (juEx467) in RMED/V cells inhibits the growth of dorsal and ventral processes. Schematic illustrations are shown on the right. Arrowheads in A and B indicate the processes from REMD/V neurons. (C-F) Ectopic AHR-1 expression in RMED/V cells promotes Plim-6GFP expression. (C) Plim-6rGFP expression in a wild-type animal. Arrowhead indicates the RMEL neuron. (D-F) juEx467 animals. Three focal planes are shown for Plim-6rGFP expression in all four RME cells (arrowheads). Scale bar: 50 µm.

View larger version (92K): [in a new window]   Fig. 6. aha-1 but not daf-21 is required for AHR-1 function in RMEL/R cells. (A-D) Punc-25GFP expression in different mutants. Left and middle panels show two focal planes focused on RMED/V and RMEL neurons, respectively. Right panel shows the schematic illustration. Asterisk indicates process from RMED/V neurons; arrowheads, the ectopic processes from RMEL neurons. An aha-1 mutant has the same RMEL phenotype (arrowheads) as an ahr-1 mutant (B,C). In a daf-21 mutant, RMEL and RMER neurons are normal (D). (EH) Mutations in aha-1 but not in daf-21 suppress the effect of ectopic ahr-1 expression in juEx467. Two focal planes are shown in G and H. Arrowheads in E and F indicate the processes from RMED/V neurons, and in H indicate the ectopic process from RMEL in aha-1 mutants. Asterisk in G indicates the processes from RMED/V neurons. Scale bar: 50 µm.

View larger version (60K): [in a new window]   Fig. 7. ahr-1, ceh-10 and lim-4 function independently of each other in RME neurons. (A) Expression of a functional AHR-1::GFP (iaIs2) is unaltered in ceh-10 and lim-4 mutants. Arrows indicate RMEL in the three panels. Not all AHR-1 expressing neurons are in focus. (B) Double mutants of ahr-1, ceh-10 or lim-4 show additive phenotypes. Genotypes are shown above the panels. The top panels show RMEL/R neurons and the bottom panels show RMED/V neurons. Asterisks indicate the ectopic nerve process of RMEL/R; arrows indicate RMEV; solid arrowhead indicates RMED in ahr-1, lim-4 double mutants; empty triangles show the presumed RMED position; and the fluorescence spots are from the distal ends of RMEV. More than 100 animals were observed for each genotype.