Chapter 27
Structural and Functional Diversification of AHRs during Metazoan Evolution
Mark E. Hahn,
Sibel I. Karchner,
Mark E. Hahn
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Search for more papers by this authorSibel I. Karchner
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Search for more papers by this authorMark E. Hahn,
Sibel I. Karchner,
Mark E. Hahn
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Search for more papers by this authorSibel I. Karchner
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, 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:
-
Origins and Evolution of the AHR in (Eu)Metazoans
-
AHR Diversity in Vertebrates and other Chordates
-
Evolution of AHR Ligand Binding and other Functional Properties
-
Evolution of AHR Roles in Development and Physiology
-
Conclusions
-
Acknowledgments
-
References
REFERENCES
- Poland, A., Glover, E., and Kende, A. S. (1976). Stereospecific, high-affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol. Journal of Biological Chemistry, 251, 4936–4946.
- Okey, A. B. (2007). An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology – XI. Toxicological Sciences, 98, 5–38.
- Poland, A. and Kende, A. (1975). 2,3,7,8-Tetrachlorodibenzo-p-dioxin: environmental contaminant and molecular probe. Federation Proceedings, 35, 2404–2411.
- Nebert, D. W. and Karp, C. L. (2008). Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. Journal of Biological Chemistry, 283, 36061–36065.
- McMillan, B. J. and Bradfield, C. A. (2007). The aryl hydro-carbon receptor sans xenobiotics: endogenous function in genetic model systems. Molecular Pharmacology, 72, 487–498.
- Peterson, K. J., Lyons, J. B., Nowak, K. S., Takacs, C. M., Wargo, M. J., and McPeek, M. A. (2004). Estimating meta-zoan divergence times with a molecular clock. Proceedings of the National Academy of Sciences of the United States of America, 101, 6536–6541.
- Peterson, K. J. and Butterfield, N. J. (2005). Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proceedings of the National Academy of Sciences of the United States of America, 102, 9547–9552.
- Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., Jurka, J., Genikhovich, G., Grigoriev, I. V., Lucas, S. M., Steele, R. E., Finnerty, J. R., Technau, U., Martindale, M. Q., and Rokhsar, D. S. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science, 317, 86–94.
- Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., Signorovitch, A. Y., Moreno, M. A., Kamm, K., Grimwood, J., Schmutz, J., Shapiro, H., Grigoriev, I. V., Buss, L. W., Schierwater, B., Dellaporta, S. L., and Rokhsar, D. S. (2008). The Trichoplax genome and the nature of placozoans. Nature, 454, 955–960.
- Simionato, E., Ledent, V., Richards, G., Thomas-Chollier, M., Kerner, P., Coornaert, D., Degnan, B. M., and Vervoort, M. (2007). Origin and diversification of the basic helix–loop–helix gene family in metazoans: insights from comparative genomics. BMC Evolutionary Biology, 7, 33.
- Sebe-Pedros, A., de Mendoza, A., Lang, B. F., Degnan, B. M., and Ruiz-Trillo, I. (2011). Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Molecular Biology and Evolution, 28, 1241–1254.
- 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.
- 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.
- 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.
- 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. Proceedings of the National Academy of Sciences of the United States of America, 94, 13743–13748.
- 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.
- 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.
- Qin, H. and Powell-Coffman, J. A. (2004). The Caenorhabditis elegans aryl hydrocarbon receptor, AHR-1, regulates neuronal development. Developmental Biology, 270, 64–75.
- 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.
- Hahn, M. E. (2002). Aryl hydrocarbon receptors: diversity and evolution. Chemico-Biological Interactions, 141, 131–160.
- Hoegg, S. and Meyer, A. (2005). Hox clusters as models for vertebrate genome evolution. Trends in Genetics, 21, 421–424.
- Blomme, T., Vandepoele, K., De Bodt, S., Simillion, C., Maere, S., and Van de Peer, Y. (2006). The gain and loss of genes during 600 million years of vertebrate evolution. Genome Biology, 7, R43.
- Dehal, P. and Boore, J. L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biology, 3, e314.
- Fitch, W. M. (1970). Distinguishing homologous from analogous proteins. Systematic Zoology, 19, 99–113.
- Meyer, A. and Mindell, D. P. (2001). Homology evolving. Trends in Ecology and Evolution, 16, 434–440.
- Hahn, M. E., Karchner, S. I., Evans, B. R., Franks, D. G., Merson, R. R., and Lapseritis, J. M. (2006). Unexpected diversity of aryl hydrocarbon receptors in non-mammalian vertebrates: insights from comparative genomics. Journal of Experimental Zoology, 305A, 693–706.
- 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.
- Ema, M., Sogawa, K., Watanabe, N., Chujoh, Y., Matsushita, N., Gotoh, O., Funae, Y., and Fujii-Kuriyama, Y. (1992). cDNA cloning and structure of mouse putative Ah receptor. Biochemical and Biophysical Research Communications, 184, 246–253.
- Schmidt, J. V., Carver, L. A., and Bradfield, C. A. (1993). Molecular characterization of the murine Ahr gene. Organization, promoter analysis, and chromosomal assignment. Journal of Biological Chemistry, 268, 22203–22209.
- Hahn, M. E. and Karchner, S. I. (1995). Evolutionary conservation of the vertebrate Ah (dioxin) receptor: amplification and sequencing of the PAS domain of a teleost Ah receptor cDNA. Biochemical Journal, 310, 383–387.
- Karchner, S. I., Powell, W. H., and Hahn, M. E. (1999). Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus. Evidence for a novel subfamily of ligand-binding basic helix–loop–helix–Per–ARNT–Sim (bHLH–PAS) factors. Journal of Biological Chemistry, 274, 33814–33824.
- Mimura, J., Ema, M., Sogawa, K., and Fujii-Kuriyama, Y. (1999). Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes & Development, 13, 20–25.
- Nagase, T., Ishikawa, K., Kikuno, R., Hirosawa, M., Nomura, N., and Ohara, O. (1999). Prediction of the coding sequences of unidentified human genes. XV. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Research, 6, 337–345.
- Baba, T., Mimura, J., Gradin, K., Kuroiwa, A., Watanabe, T., Matsuda, Y., Inazawa, J., Sogawa, K., and Fujii-Kuriyama, Y. (2001). Structure and expression of the Ah receptor repressor gene. Journal of Biological Chemistry, 276, 33101–33110.
- Korkalainen, M., Tuomisto, J., and Pohjanvirta, R. (2004). Primary structure and inducibility by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) of aryl hydrocarbon receptor repressor in a TCDD-sensitive and a TCDD-resistant rat strain. Biochemical and Biophysical Research Communications, 315, 123–131.
- Karchner, S. I., Franks, D. G., Powell, W. H., and Hahn, M. E. (2002). Regulatory interactions among three members of the vertebrate aryl hydrocarbon receptor family: AHR repressor, AHR1, and AHR2. Journal of Biological Chemistry, 277, 6949–6959.
- Sodergren, E., Weinstock, G. M., Davidson, E. H., Cameron, R. A., Gibbs, R. A., Angerer, R. C., Angerer, L. M., Arnone, M. I., Burgess, D. R., Burke, R. D., Coffman, J. A., Dean, M., Elphick, M. R., Ettensohn, C. A., Foltz, K. R., Hamdoun, A., Hynes, R. O., Klein, W. H., Marzluff, W., McClay, D. R., Morris, R. L., Mushegian, A., Rast, J. P., Smith, L. C., Thorndyke, M. C., Vacquier, V. D., Wessel, G. M., Wray, G., Zhang, L., Elsik, C. G., Ermolaeva, O., Hlavina, W., Hofmann, G., Kitts, P., Landrum, M. J., Mackey, A. J., Maglott, D., Panopoulou, G., Poustka, A. J., Pruitt, K., Sapojnikov, V., Song, X., Souvorov, A., Solovyev, V., Wei, Z., Whittaker, C. A., Worley, K., Durbin, K. J., Shen, Y., Fedrigo, O., Garfield, D., Haygood, R., Primus, A., Satija, R., Severson, T., Gonzalez-Garay, M. L., Jackson, A. R., Milosavljevic, A., Tong, M., Killian, C. E., Livingston, B. T., Wilt, F. H., Adams, N., Belle, R., Carbonneau, S., Cheung, R., Cormier, P., Cosson, B., Croce, J., Fernandez-Guerra, A., Geneviere, A. M., Goel, M., Kelkar, H., Morales, J., Mulner-Lorillon, O., Robertson, A. J., Goldstone, J. V., Cole, B., Epel, D., Gold, B., Hahn, M. E., Howard-Ashby, M., Scally, M., Stegeman, J. J., Allgood, E. L., Cool, J., Judkins, K. M., McCafferty, S. S., Musante, A. M., Obar, R. A., Rawson, A. P., Rossetti, B. J., Gibbons, I. R., Hoffman, M. P., Leone, A., Istrail, S., Materna, S. C., Samanta, M. P., Stolc, V., Tongprasit, W., Tu, Q., Bergeron, K. F., Brandhorst, B. P., Whittle, J., Berney, K., Bottjer, D. J., Calestani, C., Peterson, K., Chow, E., Yuan, Q. A., Elhaik, E., Graur, D., Reese, J. T., Bosdet, I., Heesun, S., Marra, M. A., Schein, J., Anderson, M. K., Brockton, V., Buckley, K. M., Cohen, A. H., Fugmann, S. D., Hibino, T., Loza-Coll, M., Majeske, A. J., Messier, C., Nair, S. V., Pancer, Z., Terwilliger, D. P., Agca, C., Arboleda, E., Chen, N., Churcher, A. M., Hallbook, F., Humphrey, G. W., Idris, M. M., Kiyama, T., Liang, S., Mellott, D., Mu, X., Murray, G., Olinski, R. P., Raible, F., Rowe, M., Taylor, J. S., TessmarRaible, K., Wang, D., Wilson, K. H., Yaguchi, S., Gaasterland, T., Galindo, B. E., Gunaratne, H. J., Juliano, C., Kinukawa, M., Moy, G. W., Neill, A. T., Nomura, M., Raisch, M., Reade, A., Roux, M. M., Song, J. L., Su, Y. H., Townley, I. K., Voronina, E., Wong, J. L., Amore, G., Branno, M., Brown, E. R., Cavalieri, V., Duboc, V., Duloquin, L., Flytzanis, C., Gache, C., Lapraz, F., Lepage, T., Locascio, A., Martinez, P., Matassi, G., Matranga, V., Range, R., Rizzo, F., Rottinger, E., Beane, W., Bradham, C., Byrum, C., Glenn, T., Hussain, S., Manning, F. G., Miranda, E., Thomason, R., Walton, K., Wikramanayke, A., Wu, S. Y., Xu, R., Brown, C. T., Chen, L., Gray, R. F., Lee, P. Y., Nam, J., Oliveri, P., Smith, J., Muzny, D., Bell, S., Chacko, J., Cree, A., Curry, S., Davis, C., Dinh, H., Dugan-Rocha, S., Fowler, J., Gill, R., Hamilton, C., Hernandez, J., Hines, S., Hume, J., Jackson, L., Jolivet, A., Kovar, C., Lee, S., Lewis, L., Miner, G., Morgan, M., Nazareth, L. V., Okwuonu, G., Parker, D., Pu, L. L., Thorn, R., and Wright, R. (2006). The genome of the sea urchin Strongylocentrotus purpuratus. Science, 314, 941–952.
- Goldstone, J. V., Hamdoun, A., Cole, B. J., Howard-Ashby, M., Nebert, D. W., Scally, M., Dean, M., Epel, D., Hahn, M. E., and Stegeman, J. J. (2006). The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Developmental Biology, 300, 366–384.
- Freeman, R. M., Jr., Wu, M., Cordonnier-Pratt, M. M., Pratt, L. H., Gruber, C. E., Smith, M., Lander, E. S., Stange-Thomann, N., Lowe, C. J., Gerhart, J., and Kirschner, M. (2008). cDNA sequences for transcription factors and signaling proteins of the hemichordate Saccoglossus kowalevskii: efficacy of the expressed sequence tag (EST) approach for evolutionary and developmental studies of a new organism. Biological Bulletin, 214, 284–302.
- Lowe, C. J. (2008). Molecular genetic insights into deuterostome evolution from the direct-developing hemichordate Saccoglossus kowalevskii. Philosophical Transactions of the Royal Society B, 363, 1569–1578.
- Dehal, P., Satou, Y., Campbell, R. K., Chapman, J., Degnan, B., De Tomaso, A., Davidson, B., Di Gregorio, A., Gelpke, M., Goodstein, D. M., Harafuji, N., Hastings, K. E., Ho, I., Hotta, K., Huang, W., Kawashima, T., Lemaire, P., Martinez, D., Meinertzhagen, I. A., Necula, S., Nonaka, M., Putnam, N., Rash, S., Saiga, H., Satake, M., Terry, A., Yamada, L., Wang, H. G., Awazu, S., Azumi, K., Boore, J., Branno, M., Chin-Bow, S., DeSantis, R., Doyle, S., Francino, P., Keys, D. N., Haga, S., Hayashi, H., Hino, K., Imai, K. S., Inaba, K., Kano, S., Kobayashi, K., Kobayashi, M., Lee, B. I., Makabe, K. W., Manohar, C., Matassi, G., Medina, M., Mochizuki, Y., Mount, S., Morishita, T., Miura, S., Nakayama, A., Nishizaka, S., Nomoto, H., Ohta, F., Oishi, K., Rigoutsos, I., Sano, M., Sasaki, A., Sasakura, Y., Shoguchi, E., Shin-i, T., Spagnuolo, A., Stainier, D., Suzuki, M. M., Tassy, O., Takatori, N., Tokuoka, M., Yagi, K., Yoshizaki, F., Wada, S., Zhang, C., Hyatt, P. D., Larimer, F., Detter, C., Doggett, N., Glavina, T., Hawkins, T., Richardson, P., Lucas, S., Kohara, Y., Levine, M., Satoh, N., and Rokhsar, D. S. (2002). The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science, 298, 2157–2167.
- Putnam, N. H., Butts, T., Ferrier, D. E., Furlong, R. F., Hellsten, U., Kawashima, T., Robinson-Rechavi, M., Shoguchi, E., Terry, A., Yu, J. K., Benito-Gutierrez, E. L., Dubchak, I., Garcia-Fernandez, J., Gibson-Brown, J. J., Grigoriev, I. V., Horton, A. C., de Jong, P. J., Jurka, J., Kapitonov, V. V., Kohara, Y., Kuroki, Y., Lindquist, E., Lucas, S., Osoegawa, K., Pennacchio, L. A., Salamov, A. A., Satou, Y., Sauka-Spengler, T., Schmutz, J., Shin, I. T., Toyoda, A., Bronner-Fraser, M., Fujiyama, A., Holland, L. Z., Holland, P. W., Satoh, N., and Rokhsar, D. S. (2008). The amphioxus genome and the evolution of the chordate karyotype. Nature, 453, 1064–1071.
- Kuraku, S. (2010). Palaeophylogenomics of the vertebrate ancestor—impact of hidden paralogy on hagfish and lamprey gene phylogeny. Integrative and Comparative Biology, 50, 124–129.
- Hahn, M. E., Poland, A., Glover, E., and Stegeman, J. J. (1994). Photoaffinity labeling of the Ah receptor: phylogenetic survey of diverse vertebrate and invertebrate species. Archives of Biochemistry and Biophysics, 310, 218–228.
- Hahn, M. E., Woodin, B. R., Stegeman, J. J., and Tillitt, D. E. (1998). Aryl hydrocarbon receptor function in early vertebrates: inducibility of cytochrome P4501A in agnathan and elasmobranch fish. Comparative Biochemistry and Physiology, 120C, 67–75.
- Hahn, M. E., Sakai, J. A., Greninger, D., Franks, D. G., Merson, R. R., and Karchner, S. I. (2004). Structural and functional characterization of the aryl hydrocarbon receptor in an early diverging vertebrate, the lamprey Petromyzon marinus. Marine Environmental Research, 58, 137–138.
- Venkatesh, B., Kirkness, E. F., Loh, Y. H., Halpern, A. L., Lee, A. P., Johnson, J., Dandona, N., Viswanathan, L. D., Tay, A., Venter, J. C., Strausberg, R. L., and Brenner, S. (2007). Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biology, 5, e101.
- Betka, M., Welenc, A., Franks, D. G., Hahn, M. E., and Callard, G. V. (2000). Characterization of two aryl hydrocarbon receptor (AhR) mRNA forms in Squalus acanthias and stage-specific expression during spermatogenesis. Bulletin of the Mount Desert Island Biological Laboratory, 39, 110–112.
- Merson, R. R., Hersey, S. P., Zalobowski, T. W., Albanese, A. R., Franks, D. G., and Hahn, M. E. (2009). Aryl hydro-carbon receptors (AHR) of sharks: structural and functional divergence among AHR paralogs. Toxicological Sciences (The Toxicologist Supplement), 108, 15 (Abstract #81).
- Merson, R. R., Mattingly, C. J., and Planchart, A. J. (2009). Tandem duplication of aryl hydrocarbon receptor (AHR) genes in the genome of the spiny dogfish shark (Squalus acanthias). Bulletin of the Mount Desert Island Biological Laboratory, 48, 43–44.
- Hansson, M. C., Wittzell, H., Persson, K., and von Schantz, T. (2003). Characterization of two distinct aryl hydrocarbon receptor (AhR2) genes in Atlantic salmon (Salmo salar) and evidence for multiple AhR2 gene lineages in salmonid fish. Gene, 303, 197–206.
- Hansson, M. C., Wittzell, H., Persson, K., and von Schantz, T. (2004). Unprecedented genomic diversity of AhR1 and AhR2 genes in Atlantic salmon (Salmo salar L.). Aquatic Toxicology, 68, 219–232.
- Roy, N. K. and Wirgin, I. (1997). Characterization of the aromatic hydrocarbon receptor gene and its expression in Atlantic tomcod. Archives of Biochemistry and Biophysics, 344, 373–386.
- Tanguay, R. L., Abnet, C. C., Heideman, W., and Peterson, R. E. (1999). Cloning and characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor. Biochimica et Biophysica Acta, 1444, 35–48.
- Andreasen, E. A., Hahn, M. E., Heideman, W., Peterson, R. E., and Tanguay, R. L. (2002). The zebrafish (Danio rerio) aryl hydrocarbon receptor type 1 (zfAHR1) is a novel vertebrate receptor. Molecular Pharmacology, 62, 234–249.
- Karchner, S. I., Franks, D. G., and Hahn, M. E. (2005). AHR1B, a new functional aryl hydrocarbon receptor in zebra-fish: tandem arrangement of ahr1b and ahr2 genes. Biochemical Journal, 392, 153–161.
- Kawamura, T. and Yamashita, I. (2002). Aryl hydrocarbon receptor is required for prevention of blood clotting and for the development of vasculature and bone in the embryos of medaka fish, Oryzias latipes. Zoological Science, 19, 309–319.
- Hanno, K., Oda, S., and Mitani, H. (2010). Effects of dioxin isomers on induction of AhRs and CYP1A1 in early developmental stage embryos of medaka (Oryzias latipes). Chemo-sphere, 78, 830–839.
- Karchner, S. I. and Hahn, M. E. (2004). Pufferfish (Fugu rubripes) aryl hydrocarbon receptors: unusually high diversity in a compact genome. Marine Environmental Research, 58, 139–140.
- Jung, R. E. and Walker, M. K. (1997). Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on development of anuran amphibians. Environmental Toxicology and Chemistry, 16, 230–240.
- Beatty, P. W., Holscher, M. A., and Neal, R. A. (1976). Toxicity of 2,3,7,8-tetrachloridibenzo-p-dioxin in larval and adult forms of Rana catesbeiana. Bulletin of Environmental Contamination and Toxicology, 16, 578–581.
- Laub, L. B., Jones, B. D., and Powell, W. H. (2009). Responsiveness of a Xenopus laevis cell line to the aryl hydrocarbon receptor ligands 6-formylindolo[3,2-b]carbazole (FICZ) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Chemico-Biological Interactions, 183, 202–211.
- Jonsson, M. E., Berg, C., Goldstone, J. V., and Stegeman, J. J. (2011). New CYP1 genes in the frog Xenopus (Silurana) tropicalis: induction patterns and effects of AHR agonists during development. Toxicology and Applied Pharmacology, 250, 170–183.
- Ohi, H., Fujita, Y., Miyao, M., Saguchi, K., Murayama, N., and Higuchi, S. (2003). Molecular cloning and expression analysis of the aryl hydrocarbon receptor of Xenopus laevis. Biochemical and Biophysical Communications, 307, 595–599.
- Lavine, J. A., Rowatt, A. J., Klimova, T., Whitington, A. J., Dengler, E., Beck, C., and Powell, W. H. (2005). Aryl hydro-carbon receptors in the frog Xenopus laevis: two AhR1 paralogs exhibit low affinity for 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicological Sciences, 88, 60–72.
- Zimmermann, A. L., King, E. A., Dengler, E., Scogin, S. R., and Powell, W. H. (2008). An aryl hydrocarbon receptor repressor from Xenopus laevis: function, expression, and role in dioxin responsiveness during frog development. Toxico-logical Sciences, 104, 124–134.
- Barley, A. J., Spinks, P. Q., Thomson, R. C., and Shaffer, H. B. (2010). Fourteen nuclear genes provide phylogenetic resolution for difficult nodes in the turtle tree of life. Molecular Phylogenetics and Evolution, 55, 1189–1194.
- Marquez, E. C. (2010). Cloning of cDNAs for estrogen receptor alpha, aromatase, and aryl hydrocarbon receptors and environmental effects on gene expression in the painted turtle (Chrysemys picta) and the red-eared slider (Pseudemys scripta). Ph.D. thesis, Boston University, Boston, MA.
- Poland, A. and Glover, E. (1973). Chlorinated dibenzo-p-dioxins: potent inducers of delta-aminolevulinic acid synthetase and aryl hydrocarbon hydroxylase. II. A study of the structure–activity relationship. Molecular Pharmacology, 9, 736–747.
- Poland, A., and Glover, E. (1973). 2,3,7,8-Tetrachlorodibenzo-p-dioxin: potent inducer of δ-aminolevulinic acid synthetase. Science, 179, 476–477.
- Poland, A. and Glover, E. (1977). Chlorinated biphenyl induction of aryl hydrocarbon hydroxylase activity: a study of the structure–activity relationship. Molecular Pharmacology, 13, 924–938.
- Giesy, J. P., Ludwig, J. P., and Tillitt, D. E. (1994). Deformities in birds of the Great Lakes region: assigning causality. Environmental Science and Technology, 28, 128A–135A.
- Karchner, S. I., Kennedy, S. W., Trudeau, S., and Hahn, M. E. (2000). Towards a molecular understanding of species differences in dioxin sensitivity: initial characterization of Ah receptor cDNAs in birds and an amphibian. Marine Environmental Research, 50, 51–56.
- Karchner, S. I., Franks, D. G., Kennedy, S. W., and Hahn, M. E. (2006). The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. Proceedings of the National Academy of Sciences of the United States of America, 103, 6252–6257.
- Yasui, T., Kim, E. Y., Iwata, H., and Tanabe, S. (2004). Identification of aryl hydrocarbon receptor 2 in aquatic birds;cDNA cloning of AHR1 and AHR2 and characteristics of their amino acid sequences. Marine Environmental Research, 58, 113–118.
- Yasui, T., Kim, E. Y., Iwata, H., Franks, D. G., Karchner, S. I., Hahn, M. E., and Tanabe, S. (2007). Functional characterization and evolutionary history of two aryl hydrocarbon receptor isoforms (AhR1 and AhR2) from avian species. Toxicological Sciences, 99, 101–117.
- Walker, M. K., Heid, S. E., Smith, S. M., and Swanson, H. I. (2000). Molecular characterization and developmental expression of the aryl hydrocarbon receptor from the chick embryo. Comparative Biochemistry and Physiology, 126C, 305–319.
- Head, J. A., Hahn, M. E., and Kennedy, S. W. (2008). Key amino acids in the aryl hydrocarbon receptor predict dioxin sensitivity in avian species. Environmental Science & Technology, 42, 7535–7541.
- Fernandez-Salguero, P., Hilbert, D. M., Rudikoff, S., Ward, J. M., and Gonzalez, F. J. (1996). Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicology and Applied Pharmacology, 140, 173–179.
- Mimura, J., Yamashita, K., Nakamura, K., Morita, M., Takagi, T., Nakao, K., Ema, M., Sogawa, K., Yasuda, M., Katsuki, M., and Fujii-Kuriyama, Y. (1997). Loss of teratogenic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor. Genes to Cells, 2, 645–654.
- Schmidt, J. V., Su, G. H.-T., 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.
- 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.
- Robles, R., Morita, Y., Mann, K. K., Perez, G. I., Yang, S., Matikainen, T., Sherr, D. H., and Tilly, J. L. (2000). The aryl hydrocarbon receptor, a basic helix–loop–helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. Endocrinology, 141, 450–453.
- Benedict, J. C., Lin, T. M., Loeffler, I. K., Peterson, R. E., and Flaws, J. A. (2000). Physiological role of the aryl hydrocarbon receptor in mouse ovary development. Toxicological Sciences, 56, 382–388.
- Warren, W. C., Hillier, L. W., Marshall Graves, J. A., Birney, E., Ponting, C. P., Grutzner, F., Belov, K., Miller, W., Clarke, L., Chinwalla, A. T., Yang, S. P., Heger, A., Locke, D. P., Miethke, P., Waters, P. D., Veyrunes, F., Fulton, L., Fulton, B., Graves, T., Wallis, J., Puente, X. S., Lopez-Otin, C., Ordonez, G. R., Eichler, E. E., Chen, L., Cheng, Z., Deakin, J. E., Alsop, A., Thompson, K., Kirby, P., Papenfuss, A. T., Wakefield, M. J., Olender, T., Lancet, D., Huttley, G. A., Smit, A. F., Pask, A., Temple-Smith, P., Batzer, M. A., Walker, J. A., Konkel, M. K., Harris, R. S., Whittington, C. M., Wong, E. S., Gemmell, N. J., Buschiazzo, E., Vargas Jentzsch, I. M., Merkel, A., Schmitz, J., Zemann, A., Churakov, G., Kriegs, J. O., Brosius, J., Murchison, E. P., Sachidanandam, R., Smith, C., Hannon, G. J., Tsend-Ayush, E., McMillan, D., Attenborough, R., Rens, W., Ferguson-Smith, M., Lefevre, C. M., Sharp, J. A., Nicholas, K. R., Ray, D. A., Kube, M., Reinhardt, R., Pringle, T. H., Taylor, J., Jones, R. C., Nixon, B., Dacheux, J. L., Niwa, H., Sekita, Y., Huang, X., Stark, A., Kheradpour, P., Kellis, M., Flicek, P., Chen, Y., Webber, C., Hardison, R., Nelson, J., Hallsworth-Pepin, K., Delehaunty, K., Markovic, C., Minx, P., Feng, Y., Kremitzki, C., Mitreva, M., Glasscock, J., Wylie, T., Wohldmann, P., Thiru, P., Nhan, M. N., Pohl, C. S., Smith, S. M., Hou, S., Nefedov, M., de Jong, P. J., Renfree, M. B., Mardis, E. R., and Wilson, R. K. (2008). Genome analysis of the platypus reveals unique signatures of evolution. Nature, 453, 175–183.
- Mikkelsen, T. S., Wakefield, M. J., Aken, B., Amemiya, C. T., Chang, J. L., Duke, S., Garber, M., Gentles, A. J., Goodstadt, L., Heger, A., Jurka, J., Kamal, M., Mauceli, E., Searle, S. M., Sharpe, T., Baker, M. L., Batzer, M. A., Benos, P. V., Belov, K., Clamp, M., Cook, A., Cuff, J., Das, R., Davidow, L., Deakin, J. E., Fazzari, M. J., Glass, J. L., Grabherr, M., Greally, J. M., Gu, W., Hore, T. A., Huttley, G. A., Kleber, M., Jirtle, R. L., Koina, E., Lee, J. T., Mahony, S., Marra, M. A., Miller, R. D., Nicholls, R. D., Oda, M., Papenfuss, A. T., Parra, Z. E., Pollock, D. D., Ray, D. A., Schein, J. E., Speed, T. P., Thompson, K., VandeBerg, J. L., Wade, C. M., Walker, J. A., Waters, P. D., Webber, C., Weidman, J. R., Xie, X., Zody, M. C., Graves, J. A., Ponting, C. P., Breen, M., Samollow, P. B., Lander, E. S., and Lindblad-Toh, K. (2007). Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature, 447, 167–177.
- Kuraku, S., Meyer, A., and Kuratani, S. (2009). Timing of genome duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after? Molecular Biology and Evolution, 26, 47–59.
- Sundstrom, G., Larsson, T. A., and Larhammar, D. (2008). Phylogenetic and chromosomal analyses of multiple gene families syntenic with vertebrate Hox clusters. BMC Evolutionary Biology, 8, 254.
- Hahn, M. E., Merson, R. R., and Karchner, S. I. (2005). Xenobiotic receptors in fishes: structural and functional diversity and evolutionary insights. In Biochemistry and Molecular Biology of Fishes. Vol. 6 Environmental Toxicology ( T. W. Moon and T. P. Mommsen, Eds). Elsevier, The Netherlands.
- Amores, A., Force, A., Yan, Y.-L., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Prince, V., Wang, Y.-L., Westerfield, M., Ekker, M., and Postlethwait, J. H. (1998). Zebrafish hox clusters and vertebrate genome evolution. Science, 282, 1711–1714.
- Meyer, A. and Van de Peer, Y. (2005). From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays, 27, 937–945.
- Postlethwait, J., Amores, A., Cresko, W., Singer, A., and Yan, Y. L. (2004). Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends in Genetics, 20, 481–490.
- Vandepoele, K., De Vos, W., Taylor, J. S., Meyer, A., and Van de Peer, Y. (2004). Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 101, 1638–1643.
- Christoffels, A., Koh, E. G., Chia, J. M., Brenner, S., Aparicio, S., and Venkatesh, B. (2004). Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Molecular Biology and Evolution, 21, 1146–1151.
- Postlethwait, J. H. (2007). The zebrafish genome in context: ohnologs gone missing. Journal of Experimental Zoology, Part B, 308, 563–577.
- Postlethwait, J. H. (2006). The zebrafish genome: a review and msx gene case study. In Vertebrate Genomes, Vol. 2 Karger, Basel.
- Poland, A., Palen, D., and Glover, E. (1994). Analysis of the four alleles of the murine aryl hydrocarbon receptor. Molecular Pharmacology, 46, 915–921.
- Thomas, R. S., Penn, S. G., Holden, K., Bradfield, C. A., and Rank, D. R. (2002). Sequence variation and phylogenetic history of the mouse Ahr gene. Pharmacogenetics, 12, 151–163.
- Pohjanvirta, R., Wong, J. M. Y., Li, W., Harper, P. A., Tuomisto, J., and Okey, A. B. (1998). Point mutation in intron sequence causes altered carboxyl-terminal structure in the aryl hydrocarbon receptor of the most 2,3,7,8-tetrachlorodibenzo-p-dioxin-resistant rat strain. Molecular Pharmacology, 54, 86–93.
- Harper, P. A., Wong, J. M. Y., Lam, M. S. M., and Okey, A. B. (2002). Polymorphisms in the human AH receptor. Chemico-Biological Interactions, 141, 161–187.
- Okey, A. B., Franc, M. A., Moffat, I. D., Tijet, N., Boutros, P. C., Korkalainen, M., Tuomisto, J., and Pohjanvirta, R. (2005). Toxicological implications of polymorphisms in receptors for xenobiotic chemicals: the case of the aryl hydrocarbon receptor. Toxicology and Applied Pharmacology, 207, 43–51.
- Hahn, M. E., Karchner, S. I., Franks, D. G., and Merson, R. R. (2004). Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus). Pharmacogenetics, 14, 131–143.
- Wirgin, I., Roy, N. K., Loftus, M., Chambers, R. C., Franks, D. G., and Hahn, M. E. (2011). Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science, 331, 1322–1325.
- Reitzel, A. M., Karchner, S. I., Franks, D. G., Evans, B. R., Nacci, D. E., Champlin, D., Vieira, V., and Hahn, M. E. (2011). Genetic diversity in aryl hydrocarbon receptor (AHR) loci in PCB-sensitive and PCB-resistant populations of Atlantic killifish (Fundulus heteroclitus). manuscript in preparation.
- Poland, A. and Glover, E. (1980). 2,3,7,8-Tetrachlorodibenzo-p-dioxin: segregation of toxicity with the Ah locus. Molecular Pharmacology, 17, 86–94.
- Okey, A. B., Vella, L. M., and Harper, P. A. (1989). Detection and characterization of a low affinity form of cytosolic Ah receptor in livers of mice nonresponsive to induction of cytochrome P1-450 by 3-methylcholanthrene. Molecular Pharmacology, 35, 823–830.
- Safe, S. (1990). Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). CRC Critical Reviews in Toxicology, 21, 51–88.
- Butler, R. B., Kelley, M. L., Powell, W. H., Hahn, M. E., and Van Beneden, R. J. (2001). An aryl hydrocarbon receptor homologue from the soft-shell clam, Mya arenaria: evidence that invertebrate AHR homologues lack TCDD and BNF binding. Gene, 278, 223–234.
- Céspedes, M. A., Galindo, M. I., and Couso, J. P. (2010). Dioxin toxicity in vivo results from an increase in the dioxin-independent transcriptional activity of the aryl hydrocarbon receptor. PLoS ONE, 5, e15382.
- 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.
- Ema, M., Ohe, N., Suzuki, M., Mimura, J., Sogawa, K., Ikawa, S., and Fujii-Kuriyama, Y. (1994). Dioxin binding activities of polymorphic forms of mouse and human aryl hydrocarbon receptors. Journal of Biological Chemistry, 269, 27337– 27343.
- Ramadoss, P. and Perdew, G. H. (2004). Use of 2-azido-3-[125I]iodo-7,8-dibromodibenzo-p-dioxin as a probe to determine the relative ligand affinity of human versus mouse aryl hydrocarbon receptor in cultured cells. Molecular Pharmacology, 66, 129–136.
- Pandini, A., Denison, M. S., Song, Y., Soshilov, A. A., and Bonati, L. (2007). Structural and functional characterization of the aryl hydrocarbon receptor ligand binding domain by homology modeling and mutational analysis. Biochemistry, 46, 696–708.
- Pandini, A., Soshilov, A. A., Song, Y., Zhao, J., Bonati, L., and Denison, M. S. (2009). Detection of the TCDD binding-fingerprint within the Ah receptor ligand binding domain by structurally driven mutagenesis and functional analysis. Biochemistry, 48, 5972–5983.
- Farmahin, R., Wu, D., Bursian, S. J., Crump, D., Giesy, J. P., Hahn, M. E., Jones, S. P., Karchner, S. I., Mundy, L. J., Zwiernik, M. J., and Kennedy, S. W. (2010). The ligand binding domain—the key to the classification of avian sensitivity to dioxin-like compounds. Toxicology Letters, 196S, S116–S117.
- Wirgin, I. and Waldman, J. R. (2004). Resistance to contaminants in North American fish populations. Mutation Research, 552, 73–100.
- Hahn, M. E., Karchner, S. I., Franks, D. G., Evans, B. R., Nacci, D., Champlin, D., and Cohen, S. (2005). Mechanism of PCB- and dioxin-resistance in fish in the Hudson River Estuary: role of receptor polymorphisms. Final report, Hudson River Foundation, New York.
- Haarmann-Stemmann, T. and Abel, J. (2006). The arylhydro-carbon receptor repressor (AhRR): structure, expression, and function. Biological Chemistry, 387, 1195–1199.
- Hahn, M. E., Allan, L. L., and Sherr, D. H. (2009). Regulation of constitutive and inducible AHR signaling: complex interactions involving the AHR repressor. Biochemical Pharmacology, 77, 485–497.
- Evans, B. R., Karchner, S. I., Franks, D. G., and Hahn, M. E. (2005). Duplicate aryl hydrocarbon receptor repressor genes (ahrr1 and ahrr2) in the zebrafish Danio rerio: structure, function, evolution, and AHR-dependent regulation in vivo. Archives of Biochemistry and Biophysics, 441, 151–167.
- Lee, J. S., Kim, E. Y., Nomaru, K., and Iwata, H. (2011). Molecular and functional characterization of aryl hydrocarbon receptor repressor from the chicken (Gallus gallus): interspecies similarities and differences. Toxicological Sciences, 119, 319–334.
- Flaveny, C. A., Murray, I. A., Chiaro, C. R., and Perdew, G. H. (2009). Ligand selectivity and gene regulation by the human aryl hydrocarbon receptor in transgenic mice. Molecular Pharmacology, 75, 1412–1420.
- DiNatale, B. C., Murray, I. A., Schroeder, J. C., Flaveny, C. A., Lahoti, T. S., Laurenzana, E. M., Omiecinski, C. J., and Perdew, G. H. (2010). Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicological Sciences, 115, 89–97.
- Boitano, A. E., Wang, J., Romeo, R., Bouchez, L. C., Parker, A. E., Sutton, S. E., Walker, J. R., Flaveny, C. A., Perdew, G. H., Denison, M. S., Schultz, P. G., and Cooke, M. P. (2010). Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science, 329, 1345–1348.
- Henry, E. C. and Gasiewicz, T. A. (2008). Molecular determinants of species-specific agonist and antagonist activity of a substituted flavone towards the aryl hydrocarbon receptor. Archives of Biochemistry and Biophysics, 472, 77–88.
- Zhou, J. G., Henry, E. C., Palermo, C. M., Dertinger, S. D., and Gasiewicz, T. A. (2003). Species-specific transcriptional activity of synthetic flavonoids in guinea pig and mouse cells as a result of differential activation of the aryl hydrocarbon receptor to interact with dioxin-responsive elements. Molecular Pharmacology, 63, 915–924.
- Whelan, F., Hao, N., Furness, S. G., Whitelaw, M. L., and Chapman-Smith, A. (2010). Amino acid substitutions in the aryl hydrocarbon receptor ligand binding domain reveal YH439 as an atypical AhR activator. Molecular Pharmacology, 77, 1037–1046.
- Zhao, B., Degroot, D. E., Hayashi, A., He, G., and Denison, M. S. (2010). CH223191 is a ligand-selective antagonist of the Ah (dioxin) receptor. Toxicological Sciences, 117, 393–403.
- Zhang, S., Rowlands, C., and Safe, S. (2008). Ligand-dependent interactions of the Ah receptor with coactivators in a mammalian two-hybrid assay. Toxicology and Applied Pharmacology, 227, 196–206.
- Murray, I. A., Krishnegowda, G., DiNatale, B. C., Flaveny, C., Chiaro, C., Lin, J.M., Sharma, A.K., Amin, S., and Perdew, G.H. (2010). Development of a selective modulator of aryl hydrocarbon (Ah) receptor activity that exhibits anti-inflammatory properties. Chemical Research in Toxicology, 23, 955–966.
- Murray, I. A., Morales, J. L., Flaveny, C. A., Dinatale, B. C., Chiaro, C., Gowdahalli, K., Amin, S., and Perdew, G. H. (2010). Evidence for ligand-mediated selective modulation of aryl hydrocarbon receptor activity. Molecular Pharmacology, 77, 247–254.
- Gooch, J. W., Elskus, A. A., Kloepper-Sams, P. J., Hahn, M. E., and Stegeman, J. J. (1989). Effects of ortho and non-ortho substituted polychlorinated biphenyl congeners on the hepatic monooxygenase system in scup (Stenotomus chrysops). Toxicology and Applied Pharmacology, 98, 422–433.
- Walker, M. K. and Peterson, R. E. (1991). Potencies of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners, relative to 2,3,7,8-tetrachlorodibenzo-p-dioxin, for producing early life stage mortality in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 21, 219–238.
- Abnet, C. C., Tanguay, R. L., Heideman, W., and Peterson, R. E. (1999). Transactivation activity of human, zebrafish, and rainbow trout aryl hydrocarbon receptors expressed in COS-7 cells: greater insight into species differences in toxic potency of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners. Toxicology and Applied Pharmacology, 159, 41–51.
- Hestermann, E. V., Stegeman, J. J., and Hahn, M. E. (2000). Relative contributions of affinity and intrinsic efficacy to aryl hydrocarbon receptor ligand potency. Toxicology and Applied Pharmacology, 168, 160–172.
- Kennedy, S. W., Lorenzen, A., Jones, S. P., Hahn, M. E., and Stegeman, J. J. (1996). Cytochrome P4501A induction in avian hepatocyte cultures: a promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicology and Applied Pharmacology, 141, 214–230.
- Herve, J. C., Crump, D. L., McLaren, K. K., Giesy, J. P., Zwiernik, M. J., Bursian, S. J., and Kennedy, S. W. (2010). 2,3,4,7,8-Pentachlorodibenzofuran is a more potent cyto-chrome P4501A inducer than 2,3,7,8-tetrachlorodibenzo-p-dioxin in herring gull hepatocyte cultures. Environmental Toxicology and Chemistry, 29, 2088–2095.
- Herve, J. C., Crump, D., Jones, S. P., Mundy, L. J., Giesy, J. P., Zwiernik, M. J., Bursian, S. J., Jones, P. D., Wiseman, S. B., Wan, Y., and Kennedy, S. W. (2010). Cytochrome P4501A induction by 2,3,7,8-tetrachlorodibenzo-p-dioxin and two chlorinated dibenzofurans in primary hepatocyte cultures of three avian species. Toxicological Sciences, 113, 380–391.
- Vezina, C. M., Lin, T. M., and Peterson, R. E. (2009). AHR signaling in prostate growth, morphogenesis, and disease. Biochemical Pharmacology, 77, 566–576.
- Singh, K. P., Casado, F. L., Opanashuk, L. A., and Gasiewicz, T. A. (2009). The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/ progenitor cell populations. Biochemical Pharmacology, 77, 577–587.
- Hernandez-Ochoa, I., Karman, B. N., and Flaws, J. A. (2009). The role of the aryl hydrocarbon receptor in the female reproductive system. Biochemical Pharmacology, 77, 547–559.
- Esser, C. (2009). The immune phenotype of AhR null mouse mutants: not a simple mirror of xenobiotic receptor over-activation. Biochemical Pharmacology, 77, 597–607.
- Stevens, E. A., Mezrich, J. D., and Bradfield, C. A. (2009). The aryl hydrocarbon receptor: a perspective on potential roles in the immune system. Immunology, 127, 299–311.
- McIntosh, B. E., Hogenesch, J. B., and Bradfield, C. A. (2010). Mammalian Per–Arnt–Sim proteins in environmental adaptation. Annual Reviews in Physiology, 72, 625–645.
- Brown, R. P., McDonnell, C. M., Berenbaum, M. R., and Schuler, M. A. (2005). Regulation of an insect cytochrome P450 monooxygenase gene (CYP6B1) by aryl hydrocarbon and xanthotoxin response cascades. Gene, 358, 39–52.
- Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y.-L., and Postlethwait, J. H. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151, 1531–1545.
- Lynch, M., and Force, A. (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics, 154, 459–473.
- Prasch, A. L., Teraoka, H., Carney, S. A., Dong, W., Hiraga, T., Stegeman, J. J., Heideman, W., and Peterson, R. E. (2003). Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxico-logical Sciences, 76, 138–150.
- Dong, W., Teraoka, H., Tsujimoto, Y., Stegeman, J. J., and Hiraga, T. (2004). Role of aryl hydrocarbon receptor in mesencephalic circulation failure and apoptosis in zebrafish embryos exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicological Sciences, 77, 109–116.
- Antkiewicz, D. S., Peterson, R. E., and Heideman, W. (2006). Blocking expression of AHR2 and ARNT1 in zebrafish larvae protects against cardiac toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicological Sciences, 94, 175–182.
- Billiard, S. M., Timme-Laragy, A. R., Wassenberg, D. M., Cockman, C., and Di Giulio, R. T. (2006). The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicological Sciences, 92, 526–536.
- Mathew, L. K., Andreasen, E. A., and Tanguay, R. L. (2006). Aryl hydrocarbon receptor activation inhibits regenerative growth. Molecular Pharmacology, 69, 257–265.
- Clark, B. W., Matson, C. W., Jung, D., and Di Giulio, R. T. (2010). AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquatic Toxicology, 99, 232–240.
- Jönsson, M. E., Jenny, M. J., Woodin, B. R., Hahn, M. E., and Stegeman, J. J. (2007). Role of AHR2 in the expression of novel cytochrome P450 1 family genes, cell cycle genes, and morphological defects in developing zebra fish exposed to 3,3′,4,4′,5-pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicological Sciences, 100, 180–193.
- Incardona, J. P., Day, H. L., Collier, T. K., and Scholz, N. L. (2006). Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism. Toxicology and Applied Pharmacology, 217, 308–321.
- Lee, J. S., Kim, E. Y., and Iwata, H. (2009). Dioxin activation of CYP1A5 promoter/enhancer regions from two avian species, common cormorant (Phalacrocorax carbo) and chicken (Gallus gallus): association with aryl hydrocarbon receptor 1 and 2 isoforms. Toxicology and Applied Pharmacology, 234, 1–13.
- Jenny, M. J., Karchner, S. I., Franks, D. G., Woodin, B. R., Stegeman, J. J., and Hahn, M. E. (2009). Distinct roles of two zebrafish AHR repressors (AHRRa and AHRRb) in embryonic development and regulating the response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicological Sciences, 110, 426–441.
- Doyon, Y., McCammon, J. M., Miller, J. C., Faraji, F., Ngo, C., Katibah, G. E., Amora, R., Hocking, T. D., Zhang, L., Rebar, E. J., Gregory, P. D., Urnov, F. D., and Amacher, S. L. (2008). Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nature Biotechnology, 26, 702–708.
- Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D., and Wolfe, S. A. (2008). Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nature Biotechnology, 26, 695–701.
- Foley, J. E., Yeh, J. R., Maeder, M. L., Reyon, D., Sander, J. D., Peterson, R. T., and Joung, J. K. (2009). Rapid mutation of endogenous zebrafish genes using zinc finger nucleases made by Oligomerized Pool ENgineering (OPEN). PLoS ONE, 4, e4348.
