An Evolutionarily Conserved Role for the Aryl Hydrocarbon Receptor in the Regulation of Movement

PLoS Genetics

Volumn 10, Issue 9, 2014, Pages

  Williams, Evan G ^a   Mouchiroud, Laurent ^a   Frochaux, Michael ^a   Pandey, Ashutosh ^b   Andreux, Pénélope A ^a   Deplancke, Bart ^a   Auwerx, Johan ^a  

^a EPFL   (Switzerland)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; RESVERATROL;

AHR GENE; ALLELE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENETIC CONSERVATION; GENETIC IDENTIFICATION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; LIPID DIET; MALE; MOUSE; MOVEMENT (PHYSIOLOGY); NONHUMAN; PHYLOGENY; QUANTITATIVE TRAIT LOCUS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; WAKEFULNESS; AMINO ACID SEQUENCE; ANIMAL; GENETIC ASSOCIATION; GENETICS; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOTOR ACTIVITY; NUCLEOTIDE SEQUENCE; PHENOTYPE; QUANTITATIVE TRAIT;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; FEMALE; GENETIC ASSOCIATION STUDIES; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; MOTOR ACTIVITY; PHENOTYPE; PHYLOGENY; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; RECEPTORS, ARYL HYDROCARBON; SEQUENCE ALIGNMENT;

EID: 84907587780     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004673     Document Type: Article

References (43)

1. Andreux PA, Williams EG, Koutnikova H, Houtkooper RH, Champy MF, et al. (2012) Systems genetics of metabolism: the use of the BXD murine reference panel for multiscalar integration of traits. Cell 150: 1287–1299.
2. Wang X, Agarwala R, Capra J, Chen Z, Church D, et al. (2010) High-throughput sequencing of the DBA/2J mouse genome. BMC Bioinformatics 11: O7.
3. Koutnikova H, Laakso M, Lu L, Combe R, Paananen J, et al. (2009) Identification of the UBP1 locus as a critical blood pressure determinant using a combination of mouse and human genetics. PLoS Genet 5: e1000591.
4. Thomas RS, Penn SG, Holden K, Bradfield CA, Rank DR, (2002) Sequence variation and phylogenetic history of the mouse Ahr gene. Pharmacogenetics 12: 151–163.
5. Williams R, Lim JE, Harr B, Wing C, Walters R, et al. (2009) A common and unstable copy number variant is associated with differences in Glo1 expression and anxiety-like behavior. PLoS One 4: e4649.
6. Peters JM, Narotsky MG, Elizondo G, Fernandez-Salguero PM, Gonzalez FJ, et al. (1999) Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-null mice. Toxicol Sci 47: 86–92.
7. Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, et al. (2000) Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochemical Pharmacology 59: 65–85.
8. Mezrich JD, Fechner JH, Zhang XJ, Johnson BP, Burlingham WJ, et al. (2010) An Interaction between Kynurenine and the Aryl Hydrocarbon Receptor Can Generate Regulatory T Cells. Journal of Immunology 185: 3190–3198.
9. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, et al. (2011) An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 478: 197–203.
10. Rowlands JC, Gustafsson JA, (1997) Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 27: 109–134.
11. Ramadoss P, Marcus C, Perdew GH, (2005) Role of the aryl hydrocarbon receptor in drug metabolism. Expert Opin Drug Metab Toxicol 1: 9–21.
12. Alexander DL, Ganem LG, Fernandez-Salguero P, Gonzalez F, Jefcoate CR, (1998) Aryl-hydrocarbon receptor is an inhibitory regulator of lipid synthesis and of commitment to adipogenesis. J Cell Sci 111: 3311–3322.
13. Peter GF, Martin MV, McCormick WA, Nguyen LP, Glover E, et al. (2004) Aryl hydrocarbon receptor response to indigoids in vitro and in vivo. Arch Biochem Biophys 423: 309–316.
14. Leclerc S, Garnier M, Hoessel R, Marko D, Bibb JA, et al. (2001) Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J Biol Chem 276: 251–260.
15. Pelclova D, Urban P, Preiss J, Lukas E, Fenclova Z, et al. (2006) Adverse health effects in humans exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Rev Environ Health 21: 119–138.
16. Poland A, Palen D, Glover E, (1994) Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol Pharmacol 46: 915–921.
17. Sulem P, Gudbjartsson DF, Geller F, Prokopenko I, Feenstra B, et al. (2011) Sequence variants at CYP1A1-CYP1A2 and AHR associate with coffee consumption. Hum Mol Genet 20: 2071–2077.
18. Chang C, Smith DR, Prasad VS, Sidman CL, Nebert DW, et al. (1993) Ten nucleotide differences, five of which cause amino acid changes, are associated with the Ah receptor locus polymorphism of C57BL/6 and DBA/2 mice. Pharmacogenetics 3: 312–321.
19. Abiola O, Angel JM, Avner P, Bachmanov AA, Belknap JK, et al. (2003) The nature and identification of quantitative trait loci: a community's view. Nat Rev Genet 4: 911–916.
20. Wiltshire T, Pletcher MT, Batalov S, Barnes SW, Tarantino LM, et al. (2003) Genome-wide single-nucleotide polymorphism analysis defines haplotype patterns in mouse. Proc Natl Acad Sci U S A 100: 3380–3385.
21. Mozhui K, Lu L, Armstrong WE, Williams RW, (2012) Sex-specific modulation of gene expression networks in murine hypothalamus. Front Neurosci 6: 63.
22. McMillan BJ, Bradfield CA, (2007) The aryl hydrocarbon receptor sans xenobiotics: endogenous function in genetic model systems. Mol Pharmacol 72: 487–498.
23. Ema M, Ohe N, Suzuki M, Mimura J, Sogawa K, et al. (1994) Dioxin Binding Activities of Polymorphic Forms of Mouse and Human Arylhydrocarbon Receptors. J Biol Chem 269: 27337–27343.
24. Connor KT, Aylward LL, (2006) Human response to dioxin: aryl hydrocarbon receptor (AhR) molecular structure, function, and dose-response data for enzyme induction indicate an impaired human AhR. J Toxicol Environ Health B Crit Rev 9: 147–171.
25. Flaveny CA, Murray IA, Chiaro CR, Perdew GH, (2009) Ligand selectivity and gene regulation by the human aryl hydrocarbon receptor in transgenic mice. Mol Pharmacol 75: 1412–1420.
26. Gasiewicz TA, Rucci G, (1984) Cytosolic receptor for 2,3,7,8-tetrachlorodibenzo-p-dioxin. Evidence for a homologous nature among various mammalian species. Mol Pharmacol 26: 90–98.
27. Lesca P, Witkamp R, Maurel P, Galtier P, (1994) The pig as a model for studying AH receptor and other PAH-binding proteins in man. Biochem Biophys Res Commun 200: 475–481.
28. Flaveny CA, Perdew GH, (2009) Transgenic Humanized AHR Mouse Reveals Differences between Human and Mouse AHR Ligand Selectivity. Mol Cell Pharmacol 1: 119–123.
29. Duncan DM, Burgess EA, 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.
30. Huang X, Powell-Coffman JA, 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.
31. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, et al. (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268: 722–726.
32. Andreola F, Fernandez-Salguero PM, Chiantore MV, Petkovich MP, Gonzalez FJ, et al. (1997) Aryl hydrocarbon receptor knockout mice (AHR−/−) exhibit liver retinoid accumulation and reduced retinoic acid metabolism. Cancer Res 57: 2835–2838.
33. Kudo K, Takeuchi T, Murakami Y, Ebina M, 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. Biochim Biophys Acta 1789: 477–486.
34. Casper RF, Quesne M, Rogers IM, Shirota T, Jolivet A, et al. (1999) Resveratrol has antagonist activity on the aryl hydrocarbon receptor: Implications for prevention of dioxin toxicity. Molecular Pharmacology 56: 784–790.
35. Jeuken A, Keser BJG, Khan E, Brouwer A, Koeman J, et al. (2003) Activation of the Ah receptor by extracts of dietary herbal supplements, vegetables, and fruits. Journal of Agricultural and Food Chemistry 51: 5478–5487.
36. Matikainen T, Perez GI, Jurisicova A, Pru JK, Schlezinger JJ, 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.
37. Zhang J, Li X, Jevince AR, Guan L, Wang J, et al. (2013) Neuronal target identification requires AHA-1-mediated fine-tuning of Wnt signaling in C. elegans. PLoS Genet 9: e1003618.
38. Chang CY, Puga A, (1998) Constitutive activation of the aromatic hydrocarbon receptor. Mol Cell Biol 18: 525–535.
39. Cauchi S, Stucker I, Cenee S, Kremers P, Beaune P, et al. (2003) Structure and polymorphisms of human aryl hydrocarbon receptor repressor (AhRR) gene in a French population: relationship with CYP1A1 inducibility and lung cancer. Pharmacogenetics 13: 339–347.
40. Rowlands CJ, Staskal DF, Gollapudi B, Budinsky R, (2010) The human AHR: identification of single nucleotide polymorphisms from six ethnic populations. Pharmacogenet Genomics 20: 283–290.
41. Mandillo S, Tucci V, Holter SM, Meziane H, Banchaabouchi MA, et al. (2008) Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol Genomics 34: 243–255.
42. Ramot D, Johnson BE, Berry TL, JrCarnell L, Goodman MB, (2008) The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS One 3: e2208.
43. Wang JT, Williams RW, Manly KF, (2003) WebQTL - Web-based complex trait analysis. Neuroinformatics 1: 299–308.