Chapter 28
Invertebrate AHR Homologs: Ancestral Functions in Sensory Systems
Jo Anne Powell-Coffman,
Hongtao Qin,
Jo Anne Powell-Coffman
Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IO, USA
Search for more papers by this authorHongtao Qin
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
Search for more papers by this authorJo Anne Powell-Coffman,
Hongtao Qin,
Jo Anne Powell-Coffman
Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, IO, USA
Search for more papers by this authorHongtao Qin
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
Search for more papers by this authorBook Editor(s):Raimo Pohjanvirta,
Raimo Pohjanvirta
Department of Food Hygiene and Environmental Health, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
Search for more papers by this authorSummary
This chapter contains sections titled:
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Introduction
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Caenorhabditis Elegans AHR-1
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Drosophila Melanogaster Spineless
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Concluding Remarks
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References
REFERENCES
- Burbach, K. M., Poland, A., and Bradfield, C. A. (1992). Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor. Proceedings of the National Academy of Sciences of the United States of America, 89, 8185–8189.
- Pirkle, J. L., Wolfe, W. H., Patterson, D. G., Needham, L. L., Michalek, J. E., Miner, J. C., Peterson, M. R., and Phillips, D. L. (1989). Estimates of the half-life of 2,3,7,8-tetrachlorodibenzo-p-dioxin in Vietnam veterans of Operation Ranch Hand. Journal of Toxicology and Environmental Health, 27, 165–171.
- White, S. S. and Birnbaum, L. S. (2009). An overview of the effects of dioxins and dioxin-like compounds on vertebrates, as documented in human and ecological epidemiology. Journal of Environmental Science and Health, Part C, 27, 197–211.
- Gu, Y. Z., Hogenesch, J. B., and Bradfield, C. A. (2000). The PAS superfamily: sensors of environmental and developmental signals. Annual Review of Pharmacology and Toxicology, 40, 519–561.
- Denison, M. S., Fisher, J. M., and Whitlock, J. P. (1989). Protein–DNA interactions at recognition sites for the dioxin– Ah receptor complex. Journal of Biological Chemistry, 264, 16478–16482.
- Henry, E. C., Rucci, G., and Gasiewicz, T. A. (1994). Purification to homogeneity of the heteromeric DNA-binding form of the aryl hydrocarbon receptor from rat liver. Molecular Pharmacology, 46, 1022–1027.
- Hoffman, E. C., Reyes, H., Chu, F. F., Sander, F., Conley, L. H., Brooks, B. A., and Hankinson, O. (1991). Cloning of a factor required for activity of the Ah (dioxin) receptor. Science, 252, 954–958.
- Yao, E. F. and Denison, M. S. (1992). DNA sequence determinants for binding of transformed Ah receptor to a dioxin-responsive enhancer. Biochemistry, 31, 5060–5067.
- Bacsi, S. G., Reisz-Porszasz, S., and Hankinson, O. (1995). Orientation of the heterodimeric aryl hydrocarbon (dioxin) receptor complex on its asymmetric DNA recognition sequence. Molecular Pharmacology, 47, 432–438.
- Swanson, H. I., Chan, W. K., and Bradfield, C. A. (1995). DNA binding specificities and pairing rules of the Ah receptor, ARNT, and SIM proteins. Journal of Biological Chemistry, 270, 26292–26302.
- Ma, Q. and Whitlock, J. P. (1997). A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Journal of Biological Chemistry, 272, 8878–8884.
- Carver, L. A. and Bradfield, C. A. (1997). Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. Journal of Biological Chemistry, 272, 11452–11456.
- Meyer, B. K., Pray-Grant, M. G., Vanden Heuvel, J. P., and Perdew, G. H. (1998). Hepatitis B virus X-associated protein 2 is a subunit of the unliganded aryl hydrocarbon receptor core complex and exhibits transcriptional enhancer activity. Molecular and Cellular Biology, 18, 978–988.
- Petrulis, J. R., Kusnadi, A., Ramadoss, P., Hollingshead, B., and Perdew, G. H. (2003). The hsp90 co-chaperone XAP2 alters importin beta recognition of the bipartite nuclear localization signal of the Ah receptor and represses transcriptional activity. Journal of Biological Chemistry, 278, 2677–2685.
- Lin, B. C., Nguyen, L. P., Walisser, J. A., and Bradfield, C. A. (2008). A hypomorphic allele of aryl hydrocarbon receptor-associated protein-9 produces a phenocopy of the AHR-null mouse. Molecular Pharmacology, 74, 1367–1371.
- Nguyen, L. P. and Bradfield, C. A. (2008). The search for endogenous activators of the aryl hydrocarbon receptor. Chemical Research in Toxicology, 21, 102–116.
- Furness, S. G. and Whelan, F. (2009). The pleiotropy of dioxin toxicity: xenobiotic misappropriation of the aryl hydrocarbon receptor's alternative physiological roles. Pharmacology and Therapeutics, 124, 336–353.
- Whitlock, J. P., Jr., (1987). The regulation of gene expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Pharmacological Reviews, 39, 147–161.
- Nebert, D. W., Dalton, T. P., Okey, A. B., and Gonzalez, F. J. (2004). Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. Journal of Biological Chemistry, 279, 23847–23850.
- Puga, A., Maier, A., and Medvedovic, M. (2000). The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochemical Pharmacology, 60, 1129–1142.
- Fletcher, N., Wahlstrom, D., Lundberg, R., Nilsson, C. B., Nilsson, K. C., Stockling, K., Hellmold, H., and Håkansson, H. (2005). 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) alters the mRNA expression of critical genes associated with cholesterol metabolism, bile acid biosynthesis, and bile transport in rat liver: a microarray study. Toxicology and Applied Pharmacology, 207, 1–24.
- Hayes, K. R., Zastrow, G. M., Nukaya, M., Pande, K., Glover, E., Maufort, J. P., Liss, A. L., Liu, Y., Moran, S. M., Vollrath, A. L., and Bradfield, C. A. (2007). Hepatic transcriptional networks induced by exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chemical Research in Toxicology, 20, 1573–1581.
- Flaveny, C. A., Murray, I. A., and Perdew, G. H. (2010). Differential gene regulation by the human and mouse aryl hydrocarbon receptor. Toxicological Sciences, 114, 217–225.
- Lahvis, G. P., Lindell, S. L., Thomas, R. S., McCuskey, R. S., Murphy, C., Glover, E., Bentz, M., Southard, J., and Bradfield, C. A. (2000). Portosystemic shunting and persistent fetal vascular structures in aryl hydrocarbon receptor-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 97, 10442–10447.
- Lahvis, G. P., Pyzalski, R. W., Glover, E., Pitot, H. C., McElwee, M. K., and Bradfield, C. A. (2005). The aryl hydrocarbon receptor is required for developmental closure of the ductus venosus in the neonatal mouse. Molecular Pharmacology, 67, 714–720.
- 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.
- Schmidt, J. V., Su, 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. Proceedings of the National Academy of Sciences of the United States of America, 93, 6731–6736.
- McMillan, B. J. and Bradfield, C. A. (2007). The aryl hydrocarbon receptor sans xenobiotics: endogenous function in genetic model systems. Molecular Pharmacology, 72, 487–498.
- Hahn, M. E. (2002). Aryl hydrocarbon receptors: diversity and evolution. Chemico-Biological Interactions, 141, 131–160.
- 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 soft-shell clam, Mya arenaria: evidence that invertebrate AHR homologues lack 2,3,7,8-tetrachlorodibenzo-p-dioxin and beta-naphthoflavone binding. Gene, 278, 223–234.
- 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 & Development, 12, 1290–1303.
- Powell-Coffman, J. A., Bradfield, C. A., and Wood, W. B. (1998). Caenorhabditis elegans orthologs of the aryl hydro-carbon receptor and its heterodimerization partner the aryl hydrocarbon receptor nuclear translocator. Proceedings of the National Academy of Sciences of the United States of America, 95, 2844–2849.
- 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.
- Sulston, J. E., Schierenberg, E., White, J. G., and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology, 100, 64–119.
- White, J. G., Southgate, E., Thomson, J. N., and Brenner, S. (1986). The structure of the nervous system in the nematode C. elegans. Philosophical Transactions of the Royal Society B, 314, 1–340.
- Hall, D. H. and Altun, Z. F. (2008). C. elegans Atlas. Cold Spring Harbor Laboratory Press, New York.
- Bell, D. R. and Poland, A. (2000). Binding of aryl hydrocarbon receptor (AhR) to AhR-interacting protein. The role of hsp90. Journal of Biological Chemistry, 275, 36407–36414.
- Carver, L. A., Jackiw, V., and Bradfield, C. A. (1994). The 90-kDa heat shock protein is essential for Ah receptor signaling in a yeast expression system. Journal of Biological Chemistry, 269, 30109–30112.
- Qin, H. and Powell-Coffman, J. A. (2004). The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Developmental Biology, 270, 64–75.
- 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. Proceedings of the National Academy of Sciences of the United States of America, 98, 7916–7921.
- Huang, X., Powell-Coffman, J. A., and Jin, Y. (2004). 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, 131, 819–828.
- Qin, H., Zhai, Z., and Powell-Coffman, J. A. (2006). The Caenorhabditis elegans AHR-1 transcription complex controls expression of soluble guanylate cyclase genes in the URX neurons and regulates aggregation behavior. Developmental Biology, 298, 606–615.
- de Bono, M. and Bargmann, C. I. (1998). Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell, 94, 679–689.
- Gray, J. M., Karow, D. S., Lu, H., Chang, A. J., Chang, J. S., Ellis, R. E., Marletta, M. A., and Bargmann, C. I. (2004). Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature, 430, 317–322.
- Cheung, B. H., Arellano-Carbajal, F., Rybicki, I., and de Bono, M. (2004). Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior. Current Biology, 14, 1105–1111.
- Styer, K. L., Singh, V., Macosko, E., Steele, S. E., Bargmann, C. I., and Aballay, A. (2008). Innate immunity in Caenorhabditis elegans is regulated by neurons expressing NPR-1/GPCR. Science, 322, 460–464.
- Reddy, K. C., Andersen, E. C., Kruglyak, L., and Kim, D. H. (2009). A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science, 323, 382–384.
- Cheung, B. H., Cohen, M., Rogers, C., Albayram, O., and de Bono, M. (2005). Experience-dependent modulation of C. elegans behavior by ambient oxygen. Current Biology, 15, 905–917.
- Rogers, C., Persson, A., Cheung, B., and de Bono, M. (2006). Behavioral motifs and neural pathways coordinating O2 responses and aggregation in C. elegans. Current Biology, 16, 649–659.
- Chang, A. J., Chronis, N., Karow, D. S., Marletta, M. A., and Bargmann, C. I. (2006). A distributed chemosensory circuit for oxygen preference in C. elegans. PLoS Biology, 4, e274.
- Zimmer, M., Gray, J. M., Pokala, N., Chang, A. J., Karow, D. S., Marletta, M. A., Hudson, M. L., Morton, D. B., Chronis, N., and Bargmann, C. I. (2009). Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron, 61, 865–879.
- Coates, J. C. and de Bono, M. (2002). Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature, 419, 925–929.
- de Bono, M., Tobin, D. M., Davis, M. W., Avery, L., and Bargmann, C. I. (2002). Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature, 419, 899–903.
- Sonnenfeld, M., Ward, M., Nystrom, G., Mosher, J., Stahl, S., and Crews, S. (1997). The Drosophila tango gene encodes a bHLH–PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development, 124, 4571–4582.
- Kudo, K., Takeuchi, T., Murakami, Y., Ebina, M., and Kikuchi, H. (2009). Characterization of the region of the aryl hydrocarbon receptor required for ligand dependency of transactivation using chimeric receptor between Drosophila and Mus musculus. Biochimica et Biophysica Acta, 1789, 477–486.
- Kozu, S., Tajiri, R., Tsuji, T., Michiue, T., Saigo, K., and Kojima, T. (2006). Temporal regulation of late expression of Bar homeobox genes during Drosophila leg development by Spineless, a homolog of the mammalian dioxin receptor. Developmental Biology, 294, 497–508.
- 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.
- Kim, M. D., Jan, L. Y., and Jan, Y. N. (2006). The bHLH–PAS protein Spineless is necessary for the diversification of dendrite morphology of Drosophila dendritic arborization neurons. Genes & Development, 20, 2806–2819.
- Wernet, M. F., Mazzoni, E. O., Celik, A., Duncan, D. M., Duncan, I., and Desplan, C. (2006). Stochastic spineless expression creates the retinal mosaic for colour vision. Nature, 440, 174–180.
-
Bridges, C. B. and Morgan, T. H. (1923) The third-chromosome group of mutant characters of Drosophila melanogaster. Publication No. 327, Carnegie Institute of Washington, Washington, DC.
10.5962/bhl.title.24013 Google Scholar
- Struhl, G. (1982). Spineless-aristapedia: a homeotic gene that does not control the development of specific compartments in Drosophila. Genetics, 102, 737–749.
- Shippy, T. D., Yeager, S. J., and Denell, R. E. (2009). The Tribolium spineless ortholog specifies both larval and adult antennal identity. Development Genes and Evolution, 219, 45–51.
- Toegel, J. P., Wimmer, E. A., and Prpic, N. M. (2009). Loss of spineless function transforms the Tribolium antenna into a thoracic leg with pretarsal, tibiotarsal, and femoral identity. Development Genes and Evolution, 219, 53–58.
- Angelini, D. R., Kikuchi, M., and Jockusch, E. L. (2009). Genetic patterning in the adult capitate antenna of the beetle Tribolium castaneum. Developmental Biology, 327, 240–251.
- Feiler, R., Bjornson, R., Kirschfeld, K., Mismer, D., Rubin, G. M., Smith, D. P., Socolich, M., and Zuker, C. S. (1992). Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. Journal of Neuroscience, 12, 3862–3868.
- Papatsenko, D., Sheng, G., and Desplan, C. (1997). A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development, 124, 1665–1673.
- Chou, W. H., Hall, K. J., Wilson, D. B., Wideman, C. L., Townson, S. M., Chadwell, L. V., and Britt, S. G. (1996). Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells. Neuron, 17, 1101–1115.
- Grueber, W. B., Jan, L. Y., and Jan, Y. N. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development, 129, 2867–2878.
- Taylor, B. L. and Zhulin, I. B. (1999). PAS domains: internal sensors of oxygen, redox potential, and light. Microbiology and Molecular Biology Reviews, 63, 479–506.
- Kaasik, K. and Lee, C. C. (2004). Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature, 430, 467–471.
- Dioum, E. M., Rutter, J., Tuckerman, J. R., Gonzalez, G., Gilles-Gonzalez, M. A., and McKnight, S. L. (2002). NPAS2: a gas-responsive transcription factor. Science, 298, 2385–2387.
- Scheuermann, T. H., Tomchick, D. R., Machius, M., Guo, Y., Bruick, R. K., and Gardner, K. H. (2009). Artificial ligand binding within the HIF2alpha PAS-B domain of the HIF2 transcription factor. Proceedings of the National Academy of Sciences of the United States of America, 106, 450–455.