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

Development

Volumn 131, Issue 4, 2004, Pages 819-828

  Huang, Xun ^a,c   Powell Coffman, Jo Anne ^b   Jin, Yishi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ARNT (AHA 1); Aryl hydrocarbon receptor (AHR 1); C. elegans; Cell fate; GABA; HSP90; Neuron

Indexed keywords

4 AMINOBUTYRIC ACID; AROMATIC HYDROCARBON RECEPTOR; CAENORHABDITIS ELEGANS PROTEIN; HEAT SHOCK PROTEIN 90; HYPOXIA INDUCIBLE FACTOR 1BETA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL FATE; CELL SPECIFICITY; CELL TRANSFORMATION; CELL TYPE; CONTROLLED STUDY; GABAERGIC SYSTEM; HEAD MOVEMENT; MOTONEURON; NERVE CELL DIFFERENTIATION; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; GAMMA-AMINOBUTYRIC ACID; GENES, REPORTER; HOMEODOMAIN PROTEINS; HSP90 HEAT-SHOCK PROTEINS; MUTATION; NEURONS; RECEPTORS, ARYL HYDROCARBON; RECOMBINANT FUSION PROTEINS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; MAMMALIA;

EID: 1342263523     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00959     Document Type: Article

References (52)

1. Aurelio, O., Boulin, T. and Hobert, O. (2003). Identification of spatial and temporal cues that regulate postembryonic expression of axon maintenance factors in the C. elegans ventral nerve cord. Development 130, 599-610.
2. Bell, D. R. and Poland, A. (2000). Binding of aryl hydrocarbon receptor (AhR) to AhR-interacting protein. The role of hsp90. J. Biol. Chem. 275, 36407-36414.
3. Bianchi, L., Miller, D. M., III and George, A. L. (2001). Expression of a CIC chloride channel in Caenorhabditis elegans gamma-aminobutyric acidergic neurons. Neurosci. Lett. 299, 177-180.
4. Birnby, D. A., Link, E. M., Vowels, J. J., Tian, H., Colacurcio, P. L. and Thomas, J. H. (2000). A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155, 85-104.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Butler, R. A., Kelley, M. L., Powell, W. H., Hahn, M. E. and Van Beneden, R. J. (2001). An aryl hydrocarbon receptor (AHR) homologue from the softshell clam, Mya arenaria: evidence that invertebrate AHR homologues lack 2,3,7,8-tetrachlorodibenzo-p-dioxin and beta-naphthoflavone binding. Gene 278, 223-234.
7. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
8. Crews, S. T. and Fan, C. M. (1999). Remembrance of things PAS: regulation of development by bHLH-PAS proteins. Curr. Opin. Genet. Dev. 9, 580-587.
9. Dent, J. A., Davis, M. W. and Avery, L. (1997). avr-15 encodes a chloride channel subunit that mediates inhibitory glutamatergic neurotransmission and ivermectin sensitivity in Caenorhabditis elegans. EMBO J. 16, 5867-5879.
10. Dong, W., Teraoka, H., Kondo, S. and Hiraga, T. (2001). 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin induces apoptosis in the dorsal midbrain of zebrafish embryos by activation of arylhydrocarbon receptor. Neurosci. Lett. 303, 169-172.
11. Duncan, D. M., Burgess, E. A. and Duncan, I. (1998). Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor. Genes Dev. 12, 1290-1303.
12. Eastman, C., Horvitz, H. R. and Jin, Y. (1999). Coordinated transcriptional regulation of the unc-25 glutamic acid decarboxylase and the unc-47 GABA vesicular transporter by the Caenorhabditis elegans UNC-30 homeodomain protein. J. Neurosci. 19, 6225-6234.
13. Emmons, R. B., Duncan, D., Estes, P. A., Kiefel, P., Mosher, J. T., Sonnenfeld, M., Ward, M. P., Duncan, I. and Crews, S. T. (1999). The spineless-aristapedia and tango bHLH-PAS proteins interact to control antennal and tarsal development in Drosophila. Development 126, 3937-3945.
14. Fernandez-Salguero, P., Pineau, T., Hilbert, D. M., McPhail, T., Lee, S. S., Kimura, S., Nebert, D. W., Rudikoff, S., Ward, J. M. and Gonzalez, F. J. (1995). Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268, 722-726.
15. Forrester, W. C., Perens, E., Zallen, J. A. and Garriga, G. (1998). Identification of Caenorhabditis elegans genes required for neuronal differentiation and migration. Genetics 148, 151-165.
16. Gonzalez, F. J. and Fernandez-Salguero, P. (1998). The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab. Dispos. 26, 1194-1198.
17. Hahn, M. (2002). Aryl hydrocarbon receptors: diversity and evolution (1). Chem. Biol. Interact. 141, 131-160.
18. Hahn, M. E., Karchner, S. I., Shapiro, M. A. and Perera, S. A. (1997). Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. USA 94, 13743-13748.
19. Hart, A. C., Sims, S. and Kaplan, J. M. (1995). Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378, 82-85.
20. Hays, L. E., Carpenter, C. D. and Petersen, S. L. (2002). Evidence that GABAergic neurons in the preoptic area of the rat brain are targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin during development. Environ. Health Perspect. 110 Suppl. 3, 369-376.
21. Hobert, O., Tessmar, K. and Ruvkun, G. (1999). The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particuiar GABAergic neurons. Development 126, 1547-1562.
22. Horvitz, H. R., Brenner, S., Hodgkin, J. and Herman, R. K. (1979). A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol. Gen. Genet. 175, 129-133.
23. Huang, X., Cheng, H. J., Tessier-Lavigne, M. and Jin, Y. (2002). MAX-1, a novel PH/MyTH4/FERM domain cytoplasmic protein implicated in netrin-mediated axon repulsion. Neuron 34, 563-576.
24. Jiang, H., Guo, R. and Powell-Coffman, J. A. (2001). The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc. Natl. Acad. Sci. USA 98, 7916-7921.
25. Jin, Y., Hoskins, R. and Horvitz, H. R. (1994). Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 372, 780-783.
26. Jin, Y., Jorgensen, E., Hartwieg, E. and Horvitz, H. R. (1999). The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19, 539-548.
27. Kobayashi, A., Numayama-Tsuruta, K., Sogawa, K. and Fujii-Kuriyama, Y. (1997). CBP/p300 functions as a possible transcriptional coactivator of Ah receptor nuclear translocator (Arnt). J. Biochem. 122, 703-710.
28. Kozak, K. R., Abbott, B. and Hankinson, O. (1997). ARNT-deficient mice and placental differentiation. Dev. Biol. 191, 297-305.
29. Kumar, M. B. and Perdew, G. H. (1999). Nuclear receptor coactivator SRC-1 interacts with the Q-rich subdomain of the AhR and modulates its transactivation potential. Gene Expr. 8, 273-286.
30. Matikainen, T., Perez, G. I., Jurisicova, A., Pru, J. K., Schlezinger, J. J., Ryu, H. Y., Laine, J., Sakai, T., Korsmeyer, S. J., Casper, R. F. et al. (2001). Aromatic hydrocarbon receptor-driven Bax gene expression is required for premature ovarian failure caused by biohazardous environmental chemicals. Nat. Genet. 28, 355-360.
31. McIntire, S. L., Garriga, G., White, J., Jacobson, D., and Horvitz, H. R. (1992). Genes necessary for directed axonal elongation or fasciculation in C. elegans. Neuron 8, 307-322.
32. McIntire, S. L., Jorgensen, E., Kaplan, J. and Horvitz, H. R. (1993). The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337-341.
33. McIntire, S. L., Reimer, R. J., Schuske, K., Edwards, R. H. and Jorgensen, E. M. (1997). Identification and characterization of the vesicular GABA transporter. Nature 389, 870-876.
34. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
35. Nguyen, T. A., Hoivik, D., Lee, J. E. and Safe, S. (1999). Interactions of nuclear receptor coactivator/corepressor proteins with the aryl hydrocarbon receptor complex. Arch. Biochem. Biophys. 367, 250-257.
36. Petrulis, J. and Perdew, G. (2002). The role of chaperone proteins in the aryl hydrocarbon receptor core complex. Chem. Biol. Interact. 141, 25-40.
37. Poland, A., Clover, E., Kende, A. S., DeCamp, M. and Giandomenico, C. M. (1976). 3,4,3′,4′-Tetrachloro azoxybenzene and azobenzene: potent inducers of aryl hydrocarbon hydroxylase. Science 194, 627-630.
38. Pongratz, I., Mason, G. G. and Poellinger, L. (1992). Dual roles of the 90-kDa heat shock protein hsp90 in modulating functional activities of the dioxin receptor. Evidence that the dioxin receptor functionally belongs to a subclass of nuclear receptors which require hsp90 both for ligand binding activity and repression of intrinsic DNA binding activity. J. Biol. Chem. 267, 13728-13734.
39. Powell-Coffman, J. A., Bradfield, C. A. and Wood, W. B. (1998). Caenorhabditis elegans orthologs of the aryl hydrocarbon receptor and its heterodimerization partner the aryl hydrocarbon receptor nuclear translocator. Proc. Natl. Acad. Sci. USA 95, 2844-2849.
40. Probst, M. R., Reisz-Porszasz, S., Agbunag, R. V., Ong, M. S. and Hankinson, O. (1993). Role of the aryl hydrocarbon receptor nuclear translocator protein in aryl hydrocarbon (dioxin) receptor action. Mol. Pharmacol. 44, 511-518.
41. Reyes, H., Reisz-Porszasz, S. and Hankinson, O. (1992). Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256, 1193-1195.
42. Sagasti, A., Hobert, O., Troemel, E. R., Ruvkun, G. and Bargmann, C. I. (1999). Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. Genes Dev. 13, 1794-1806.
43. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Schmidt, J. V. and Bradfield, C. A. (1996). Ah receptor signaling pathways. Annu. Rev. Cell Dev. Biol. 12, 55-89.
45. Schmidt, J. V., So, G. H., Reddy, J. K., Simon, M. C. and Bradfield, C. A. (1996). Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc. Natl. Acad. Sci. USA 93, 6731-6736.
46. Shimizu, Y., Nakatsuru, Y., Ichinose, M., Takahashi, Y., Kume, H., Mimura, J., Fujii-Kuriyama, Y. and Ishikawa, T. (2000). Benzo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. USA 97, 779-782.
47. Sulston, J. E. and Hodgkin J. (1988). Methods. In The Nematode Caenorhabditis elegans (ed. W. B. Wood), pp. 587-606. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Sulston, J. E., Schierenberg, E., White, J. G. and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
49. Tohkin, M., Fukuhara, M., Elizondo, G., Tomita, S. and Gonzalez, F. J. (2000). Aryl hydrocarbon receptor is required for p300-mediated induction of DNA synthesis by adenovirus E1A. Mol. Pharmacol. 58, 845-851.
50. Ward, M. P., Mosher, J. T. and Crews, S. T. (1998). Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis. Development 125, 1599-1608.
51. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1-340.
52. Zhen, M. and Jin, Y. (1999). The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401, 371-375.