Divergent Ah Receptor Ligand Selectivity during Hominin Evolution

Molecular Biology and Evolution

Volumn 33, Issue 10, 2016, Pages 2648-2658

  Hubbard, Troy D ^a   Murray, Iain A ^a   Bisson, William H ^b   Sullivan, Alexis P ^a   Sebastian, Aswathy ^a   Perry, George H ^a   Jablonski, Nina G ^a   Perdew, Gary H ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Ah receptor; AHR; benzo(a)pyrene; Denisovan; Neandertal

Indexed keywords

ALANINE; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; INDICAN; INDOLE; POLYCYCLIC AROMATIC HYDROCARBON; VALINE; AHR PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYP1A1 PROTEIN, HUMAN; CYP1B1 PROTEIN, HUMAN; DNA; LIGAND;

AMINO ACID ANALYSIS; ARTICLE; CHLOROCEBUS SABAEUS; COOKING; DNA BINDING; ENVIRONMENTAL EXPOSURE; EXOME; FIRE; FIRST PASS EFFECT; HOMO NEANDERTHALENSIS; HUMAN; LIGAND BINDING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SEQUENCE ANALYSIS; SMOKE; ANIMAL; EVOLUTION; GENETICS; HOMINID; METABOLISM;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BENZO(A)PYRENE; BIOLOGICAL EVOLUTION; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1B1; DNA; EVOLUTION, MOLECULAR; HOMINIDAE; HUMANS; LIGANDS; NEANDERTHALS; POLYCYCLIC AROMATIC HYDROCARBONS; RECEPTORS, ARYL HYDROCARBON;

EID: 84993660326     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msw143     Document Type: Article

References (57)

1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. 2010. A method and server for predicting damaging missense mutations. Nat Methods. 7:248-249
2. Available from: http://www.ncbi.nlm.nih.gov/variation/ tools/1000genomes/, https://genome.ucsc.edu/cgi-bin/hgGateway, last accessed July 2, 2016
3. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH. 2008. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr. 18:207-250
4. Bello SM, Franks DG, Stegeman JJ, HahnME. 2001. Acquired resistance to Ah receptor agonists in a population of Atlantic killifish (Fundulus heteroclitus) inhabiting a marine superfund site: in vivo and in vitro studies on the inducibility of xenobiotic metabolizing enzymes. Toxicol Sci. 60:77-91
5. Brown KS, Marean CW, Herries AIR, Jacobs Z, Tribolo C, Braun D, Roberts DL, Meyer MC, Bernatchez J. 2009. Fire as an engineering tool of early modern humans. Science 325:859-862
6. Bruhs A, Haarmann-Stemmann T, Frauenstein K, Krutmann J, Schwarz T, Schwarz A. 2015. Activation of the arylhydrocarbon receptor causes immunosuppression primarily by modulating dendritic cells. J Invest Dermatol. 135:435-444
7. Castellano S, Parra G, Sanchez-Quinto FA, Racimo F, Kuhlwilm M, Kircher M, Sawyer S, Fu Q, Heinze A, Nickel B, et al. 2014. Patterns of coding variation in the complete exomes of three Neandertals. Proc Natl Acad Sci U S A. 111:6666-6671
8. Chiaro CR, Morales JL, Prabhu KS, Perdew GH. 2008. Leukotriene A4 metabolites are endogenous ligands for the Ah receptor. Biochemistry 47:8445-8455
9. DiNatale BC,Murray IA, Schroeder JC, Flaveny CA, Lahoti TS, Laurenzana EM, Omiecinski CJ, Perdew GH. 2010. Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicol Sci. 115:89-97
10. DiNatale BC, Schroeder JC, Francey LJ, Kusnadi A, Perdew GH. 2010. Mechanistic insights into the events that lead to synergistic induction of interleukin 6 transcription upon activation of the aryl hydrocarbon receptor and inflammatory signaling. J Biol Chem. 285:24388-24397
11. EmaM,Ohe N, Suzuki M, Mimura J, Sogawa K, Ikawa S, Fujii-Kuriyama Y. 1994. Dioxin binding activities of polymorphic forms of mouse and human arylhydrocarbon receptors. J Biol Chem. 269:27337-27343
12. Endicott P, Ho SYW, Stringer C. 2010. Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins. J HumEvol. 59:87-95
13. Esakky P, Moley KH. 2016. Preventing germ cell death by inactivating aryl hydrocarbon receptor (AHR). Cell Death Dis. 7:e2116
14. Esser C, Rannug A. 2015. The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology. Pharmacol Rev 67:259-279
15. 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
16. Fonseca-Azevedo K, Herculano-Houzel S. 2012. Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution. Proc Natl Acad Sci U S A. 109:18571-18576
17. Fu Q, Li H, Moorjani P, Jay F, Slepchenko SM, Bondarev AA, Johnson PL, Aximu-Petri A, Prufer K, Filippo C, et al. 2014. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514:445-449
18. Gaitanis G, Magiatis P, Stathopoulou K, Bassukas ID, Alexopoulos EC, Velegraki A, Skaltsounis AL. 2008. AhR ligands, malassezin, and indolo[3,2-b]carbazole are selectively produced by Malassezia furfur strains isolated from seborrheic dermatitis. J Invest Dermatol. 128:1620-1625
19. Garrison E, Marth G. 2012. Haplotype-based variant detection from short read sequencing. Preprint arXiv 1207.3907v2 [q-bio.GN]
20. Gelboin HV. 1980. Benzo[alpha]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol Rev. 60:1107-1166
21. Gonzalez FJ, Fernandez-Salguero P. 1998. The aryl hydrocarbon receptor: studies using the AHR-null mice. Drug Metab Dispos. 26:1194-1198
22. Goren-Inbar N, Alperson N, Kislev ME, Simchoni O, Melamed Y, Ben-Nun A,Werker E. 2004. Evidence of hominin control of fire at Gesher Benot Ya'aqov, Israel. Science 304:725-727
23. Gowlett JAJ, Wrangham RW. 2013. Earliest fire in Africa: towards the convergence of archaeological evidence and the cooking hypothesis. Azania: Archaeol Res Afr. 48:5-30
24. Hallegouet B, Hinguant S, Gebhardt A, Monnier J-L. 1992. Le gisement Paleolithique inferieur de Menez-Dregan 1 (Plouhinec, Finistere) Premiers resultats des fouilles. Bull Soc Prehist Fr. 89:77-81
25. Hardy K, Radini A, Buckley S, Sarig R, Copeland L, Gopher A, Barkai R. 2016. Dental calculus reveals potential respiratory irritants and ingestion of essential plant-based nutrients at Lower Palaeolithic Qesem Cave Israel. Quaternary International. 398:129-135
26. Harper PA, Golas CL,Okey AB. 1988. Characterization of the Ah receptor and aryl hydrocarbon hydroxylase induction by 2,3,7,8-tetrachlorodibenzo-p-dioxin and benz(a)anthracene in the human A431 squamous cell carcinoma line. Cancer Res. 48:2388-2395
27. Hovers E, Ilani S, Bar-Yosef O, Vandermeersch B. 2003. An early case of color symbolism: ochre use by modern humans in Qafzeh Cave. Curr Anthropol. 44:491-522
28. Huang Z, Jiang Y, Yang Y, Shao J, Sun X, Chen J, Dong L, Zhang J. 2013. 3,3'-Diindolylmethane alleviates oxazolone-induced colitis through Th2/Th17 suppression and Treg induction. Mol Immunol. 53:335-344
29. Hubbard TD, Murray IA, Bisson WH, Lahoti TS, Gowda K, Amin SG, Patterson AD, Perdew GH. 2015. Adaptation of the human aryl hydrocarbon receptor to sense microbiota-derived indoles. Sci Rep. 5:12689
30. Kiss EA, Vonarbourg C, Kopfmann S, Hobeika E, Finke D, Esser C, Diefenbach A. 2011. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science 334:1561-1565
31. MacKenzie KM, Angevine DM. 1981. Infertility in mice exposed in utero to benzo(a)pyrene. Biol Reprod. 24:183-191
32. Matikainen T, Perez GI, Jurisicova A, Pru JK, Schlezinger JJ, Ryu HY, Laine J, Sakai T, Korsmeyer SJ, Casper RF, 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
33. Meyer M, Kircher M, Gansauge MT, Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Prufer K, de Filippo C, et al. 2012. A high-coverage genome sequence from an archaic Denisovan individual. Science 338:222-226
34. Monge G, Jimenez-Espejo FJ, García-Alix A, Martínez-Ruiz F, Mattielli N, Finlayson C,Ohkouchi N, Sánchez MC, de Castro JMB, Blasco R, et al. 2015. Earliest evidence of pollution by heavymetals in archaeological sites. Sci Rep. 5:14252
35. Parker CH, Keefe ER, Herzog NM, O'Connell JF, Hawkes K. 2016. The pyrophilic primate hypothesis. Evol Anthropol. 25:54-63
36. Perdew GH, Abbott B, Stanker LH. 1995. Production and characterization of monoclonal antibodies directed against the Ah receptor. Hybridoma 14:279-283
37. Perkins A, Phillips JL, Kerkvliet NI, Tanguay RL, Perdew GH, Kolluri SK, Bisson WH. 2014. A structural switch between agonist and antagonist bound conformations for a ligand-optimized model of the human aryl hydrocarbon receptor ligand binding domain. Biology (Basel) 3:645-669
38. Poland A, Glover E, Ebetino FH, Kende AS. 1986. Photoaffinity labeling of the Ah receptor. J Biol Chem. 261:6352-6365
39. Poland A, Palen D, Glover E. 1994. Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol Pharmacol. 46:915-921
40. Prufer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, de Filippo C, et al. 2014. The complete genome sequence of a Neanderthal from the Altai mountains. Nature 505:43-49
41. Ramadoss P, Perdew GH. 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. Mol Pharmacol. 66:129-136
42. Revel A, Raanani H, Younglai E, Xu J, Han R, Savouret JF, Casper RF. 2001. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm fromDNAdamage and apoptosis caused by benzo(a)pyrene. Reprod Toxicol. 15:479-486
43. Schroeder JC, Dinatale BC, Murray IA, Flaveny CA, Liu Q, Laurenzana EM, Lin JM, Strom SC, Omiecinski CJ, Amin S, et al. 2010. The uremic toxin 3-indoxyl sulfate is a potent endogenous agonist for the human aryl hydrocarbon receptor. Biochemistry 49:393-400
44. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 7:539
45. Smith KR, Samet JM, Romieu I, Bruce N. 2000. Indoor air pollution in developing countries and acute lower respiratory infections in children. Thorax 55:518-532
46. Swanson HI, Perdew GH. 1991. Detection of the Ah receptor in rainbow trout: use of 2-azido-3-[125I]iodo-7,8-dibromodibenzo-p-dioxin in cell culture. Toxicol Lett. 58:85-95
47. Tian J, Feng Y, Fu H, Xie HQ, Jiang JX, Zhao B. 2015. The aryl hydrocarbon receptor: a key bridging molecule of external and internal chemical signals. Environ Sci Technol. 49:9518-9531
48. Uno S, Dalton TP, Shertzer HG, Genter MB, Warshawsky D, Talaska G, NebertDW. 2001. Benzo[a]pyrene-induced toxicity: paradoxical protection in Cyp1a1(-/-) knockout mice having increased hepatic BaPDNA adduct levels. Biochem Biophys Res Commun. 289:1049-1056
49. Vattathil S, Akey JM. 2015. Small amounts of archaic admixture provide big insights into Human history. Cell 163:281-284
50. Weiss C, Kolluri SK, Kiefer F, GottlicherM. 1996. Complementation of Ah receptor deficiency in hepatoma cells: negative feedback regulation and cell cycle control by the Ah receptor. Exp Cell Res. 226:154-163
51. Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, Hahn ME. 2011. Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science 331:1322-1325
52. Wong JM, Harper PA,Meyer UA, Bock KW, Morike K, Lagueux J,Ayotte P, Tyndale RF, Sellers EM, Manchester DK, et al. 2001. Ethnic variability in the allelic distribution of human aryl hydrocarbon receptor codon 554 and assessment of variant receptor function in vitro. Pharmacogenetics 11:85-94
53. Wrangham R, Conklin-Brittain N. 2003. Cooking as a biological trait. Comp Biochem Physiol A Mol Integr Physiol. 136:35-46
54. Yang EJ, Stokes JV, Kummari E, Eells J, Kaplan BL. 2016. Immunomodulation by subchronic low dose 2,3,7,8-tetrachlorodibenzo-p-dioxin in experimental autoimmune encephalomyelitis in the absence of pertussis toxin. Toxicol Sci. 151(1):35-43
55. Yuan Z, Courtenay S, Wirgin I. 2006. Comparison of hepatic and extra hepatic induction of cytochrome P4501A by graded doses of aryl hydrocarbon receptor agonists in Atlantic tomcod from two populations. Aquat Toxicol. 76:306-320
56. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, Zecchi R, D'Angelo C, Massi-Benedetti C, Fallarino F, et al. 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372-385
57. Zelikoff JT, Chen LC, Cohen MD, Schlesinger RB. 2002. The toxicology of inhaled woodsmoke. J Toxicol Environ Health B Crit Rev. 5:269-282