FARAH - Fundamental and Applied Research for Animals and Health - ULiège GIGA‐R - Giga‐Research - ULiège
Disciplines :
Food science
Author, co-author :
Doan, Thi-Que ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
Connolly, L.
Igout, Ahmed ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Muller, Marc ✱; Université de Liège - ULiège > Département des sciences de la vie > I3-Laboratory for Organogenesis and Regeneration
Scippo, Marie-Louise ✱; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Analyse des denrées alimentaires
✱ These authors have contributed equally to this work.
Language :
English
Title :
In vitro differential responses of rat and human aryl hydrocarbon receptor to two distinct ligands and to different polyphenols
Publication date :
2020
Journal title :
Environmental Pollution
ISSN :
0013-9327
Publisher :
Applied Science Publishers, United Kingdom
Volume :
265
Pages :
114966
Peer reviewed :
Peer Reviewed verified by ORBi
European Projects :
H2020 - 722634 - PROTECTED - PROTECTion against Endocrine Disruptors; Detection, mixtures, health effects, risk assessment and communication.
Choi, E.J., Kim, T., Daidzein modulates induction of hepatic CYP1A1, 1B1, and AhR by 7,12-dimethylbenz[a]anthracene in mice. Arch Pharm. Res. (Seoul) 31 (2008), 1115–1119, 10.1007/s12272-001-1277-3.
Choi, H., Chun, Y.S., Shin, Y.J., Ye, S.K., Kim, M.S., Park, J.W., Curcumin attenuates cytochrome P450 induction in response to 2,3,7,8-tetrachlorodibenzo-p-dioxin by ROS-dependently degrading AhR and ARNT. Canc. Sci. 99 (2008), 2518–2524, 10.1111/j.1349-7006.2008.00984.x.
Choi, S.H., Nishikawa, M., Sakoda, A., Sakai, Y., Feasibility of a simple double-layered coculture system incorporating metabolic processes of the intestine and liver tissue: application to the analysis of benzo[a]pyrene toxicity. Toxicol. Vitro 18 (2004), 393–402, 10.1016/j.tiv.2003.09.010.
Denison, M.S., Soshilov, A.A., He, G., Degroot, D.E., Zhao, B., Exactly the same but different: promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol. Sci. 124 (2011), 1–22, 10.1093/toxsci/kfr218.
Dere, E., Lee, A.W., Burgoon, L.D., Zacharewski, T.R., Differences in TCDD-elicited gene expression profiles in human HepG2, mouse Hepa1c1c7 and rat H4IIE hepatoma cells. BMC Genom., 12, 2011, 193, 10.1186/1471-2164-12-193.
Doan, T., Berntsen, H., Zimmer, K., Verhaegen, S., Ropstad, E., Connolly, L., Igout, A., Muller, M., Scippo, M., A realistic mixture of Persistent Organic Pollutants (POPs) inhibits the transactivation activity of the Aryl hydrocarbon Receptor (AhR) in vitro. Environ. Pollut., 254, 2019, 113098, 10.1016/j.envpol.2019.113098.
Duarte, J.H., Di Meglio, P., Hirota, K., Ahlfors, H., Stockinger, B., Differential influences of the aryl hydrocarbon receptor on Th17 mediated responses in vitro and in vivo. PloS One, 8, 2013, e79819, 10.1371/journal.pone.0079819.
Farmahin, R., Crump, D., Kennedy, S.W., Sensitivity of avian species to the aryl hydrocarbon receptor ligand 6-formylindolo [3,2-b] carbazole (FICZ). Chem. Biol. Interact. 221 (2014), 61–69, 10.1016/j.cbi.2014.07.009.
Fritsche, E., Schafer, C., Calles, C., Bernsmann, T., Bernshausen, T., Wurm, M., Hubenthal, U., Cline, J.E., Hajimiragha, H., Schroeder, P., Klotz, L.O., Rannug, A., Furst, P., Hanenberg, H., Abel, J., Krutmann, J., Lightning up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc. Natl. Acad. Sci. Unit. States Am. 104 (2007), 8851–8856, 10.1073/pnas.0701764104.
Froyen, E.B., Steinberg, F.M., Genistein decreases basal hepatic cytochrome P450 1A1 protein expression and activity in Swiss Webster mice. Nutr. Res. 36 (2016), 430–439, 10.1016/j.nutres.2016.01.001.
Fujii-Kuriyama, Y., Kawajiri, K., Molecular mechanisms of the physiological functions of the aryl hydrocarbon (dioxin) receptor, a multifunctional regulator that senses and responds to environmental stimuli. Proc. Japan Acad. Ser. B Phys. Biol. Sci. 86 (2010), 40–53, 10.2183/pjab.86.40.
Garrison, P.M., Tullis, K., Aarts, J.M.M.J.G., Brouwer, A., Giesy, J.P., Denison, M.S., Species-specific recombinant cell lines as bioassay systems for the detection of 2,3,7,8-tetrachlorodibenzo- p -dioxin-like chemicals. Toxicol. Sci. 30 (1996), 194–203, 10.1093/toxsci/30.2.194.
Jönsson, M.E., Franks, D.G., Woodin, B.R., Jenny, M.J., Garrick, R.A., Behrendt, L., Hahn, M.E., Stegeman, J.J., The tryptophan photoproduct 6-formylindolo[3,2-b]carbazole (FICZ) binds multiple AHRs and induces multiple CYP1 genes via AHR2 in zebrafish. Chem. Biol. Interact. 181 (2009), 447–454, 10.1016/j.cbi.2009.07.003.
Karunaweera, N., Raju, R., Gyengesi, E., Munch, G., Plant polyphenols as inhibitors of nf-Кb induced cytokine production—a potential anti-inflammatory treatment for alzheimer's disease?. Front. Mol. Neurosci. 8 (2015), 1–5, 10.3389/fnmol.2015.00024.
Kawajiri, K., Fujii-KuriYama, Y., The aryl hydrocarbon receptor: a multifunctional chemical sensor for host defense and homeostatic maintenance. Exp. Anim. 66 (2016), 75–89, 10.1538/expanim.16-0092.
Kim, I.S., Hwang, J.H., Hirano, M., Iwata, H., Kim, E.Y., In vitro and in silico evaluation of transactivation potencies of avian AHR1 and AHR2 by endogenous ligands: implications for the physiological role of avian AHR2. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 187 (2016), 1–9, 10.1016/j.cbpc.2016.03.011.
Laub, L., Jones, B., Powell, W., 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). Chem. Biol. Interact. 183 (2010), 202–211, 10.1038/jid.2014.371.
Lee, J.E., Safe, S., Involvement of a post-transcriptional mechanism in the inhibition of CYP1A1 expression by resveratrol in breast cancer cells. Biochem. Pharmacol. 62 (2001), 1113–1124, 10.1016/S0006-2952(01)00763-8.
Middleton, E., Kandaswami, C., Theoharides, T.C., The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 52 (2000), 673–751.
Moriguchi, T., Motohashi, H., Hosoya, T., Nakajima, O., Takahashi, S., Ohsako, S., Aoki, Y., Nishimura, N., Tohyama, C., Fujii-Kuriyama, Y., Yamamoto, M., Distinct response to dioxin in an arylhydrocarbon receptor (AHR)-humanized mouse. Proc. Natl. Acad. Sci. Unit. States Am. 100 (2003), 5652–5657, 10.1073/pnas.1037886100.
Mullen, W., Edwards, C.A., Crozier, A., Absorption, excretion and metabolite profiling of methyl-, glucuronyl-, glucosyl- and sulpho-conjugates of quercetin in human plasma and urine after ingestion of onions. Br. J. Nutr., 96, 2006, 107, 10.1079/bjn20061809.
Niestroy, J., Barbara, A., Herbst, K., Rode, S., van Liempt, M., Roos, P.H., Single and concerted effects of benzo[a]pyrene and flavonoids on the AhR and Nrf2-pathway in the human colon carcinoma cell line Caco-2. Toxicol. Vitro 25 (2011), 671–683, 10.1016/j.tiv.2011.01.008.
Nishiumi, S., Yoshida, K. ichi, Ashida, H., Curcumin suppresses the transformation of an aryl hydrocarbon receptor through its phosphorylation. Arch. Biochem. Biophys. 466 (2007), 267–273, 10.1016/j.abb.2007.08.007.
O'Brien, P.J., High-content analysis in toxicology: screening substances for human toxicity potential, elucidating subcellular mechanisms and in vivo use as translational safety biomarkers. Basic Clin. Pharmacol. Toxicol. 115 (2014), 4–17, 10.1111/bcpt.12227.
OECD. Test No. 455: Performance-Based Test Guideline for Stably Transfected Transactivation in Vitro Assays to Detect Estrogen Receptor Agonists and Antagonists. 2016, 10.1787/20745788.
Perdew, G.H., Hollingshead, B.D., DiNatale, B.C., Morales, J.L., Labrecque, M.P., Takhar, M.K., Tam, K.J., Beischlag, T.V., Estrogen receptor expression is required for low-dose resveratrol-mediated repression of aryl hydrocarbon receptor activity. J. Pharmacol. Exp. Therapeut. 335 (2010), 273–283, 10.1124/jpet.110.170654.
Poland, A., Palen, D., Glover, E., Analysis of the four alleles of the murine aryl hydrocarbon receptor. Mol. Pharmacol. 46 (1994), 915–921.
Puga, A., Ma, C., Marlowe, J.L., The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem. Pharmacol. 77 (2009), 713–722, 10.1016/j.bcp.2008.08.031.
Quideau, S., Deffieux, D., Douat-Casassus, C., Pouységu, L., Plant polyphenols: chemical properties, biological activities, and synthesis. Angew. Chem. Int. Ed. 50 (2011), 586–621, 10.1002/anie.201000044.
Rannug, A., Rannug, U., The tryptophan derivative 6-formylindolo[3,2-b]carbazole, FICZ, a dynamic mediator of endogenous aryl hydrocarbon receptor signaling, balances cell growth and differentiation. Crit. Rev. Toxicol. 48 (2018), 555–574, 10.1080/10408444.2018.1493086.
Rannug, A., Rannug, U., Rosenkranz, H., Winqvist, L., Westerholm, R., Agurell, E., Grafstrom, A., Certain photooxidized derivatives of tryptophan bind with very high affinity to the Ah receptor and are likely to be endogenous signal substances. J. Biol. Chem. 262 (1987), 15–427.
Romero-Pérez, A.I., Ibern-Gómez, M., Lamuela-Raventós, R.M., De La Torre-Boronat, M.C., Piceid, the major resveratrol derivative in grape juices. J. Agric. Food Chem. 47 (1999), 1533–1536, 10.1021/jf981024g.
Safe, S., Wormke, M., Inhibitory aryl hydrocarbon receptor-estrogen receptor α cross-talk and mechanisms of action. Chem. Res. Toxicol. 16 (2003), 807–816, 10.1021/tx034036r.
Scippo, M.L., Eppe, G., De Pauw, E., Maghuin-Rogister, G., DR-CALUX® screening of food samples: evaluation of the quantitative approach to measure dioxin, furans and dioxin-like PCBs. Talanta 63 (2004), 1193–1202, 10.1016/j.talanta.2004.05.037.
Sharan, K., Mishra, J.S., Swarnkar, G., Siddiqui, J.A., Khan, K., Kumari, R., Rawat, P., Maurya, R., Sanyal, S., Chattopadhyay, N., A novel quercetin analogue from a medicinal plant promotes peak bone mass achievement and bone healing after injury and exerts an anabolic effect on osteoporotic bone: the role of aryl hydrocarbon receptor as a mediator of osteogenic action. J. Bone Miner. Res. 26 (2011), 2096–2111, 10.1002/jbmr.434.
Smirnova, A., Wincent, E., Vikström Bergander, L., Alsberg, T., Bergman, J., Rannug, A., Rannug, U., Evidence for new light-independent pathways for generation of the endogenous aryl hydrocarbon receptor agonist FICZ. Chem. Res. Toxicol. 29 (2016), 75–86, 10.1021/acs.chemrestox.5b00416.
Smith, K.J., Murray, I.A., Tanos, R., Tellew, J., Boitano, A.E., Bisson, W.H., Kolluri, S.K., Cooke, M.P., Perdew, G.H., Identification of a high-affinity ligand that exhibits complete aryl hydrocarbon receptor antagonism. J. Pharmacol. Exp. Therapeut. 338 (2011), 318–327, 10.1124/jpet.110.178392.
Stejskalova, L., Dvorak, Z., Pavek, P., Endogenous and exogenous ligands of aryl hydrocarbon receptor: current state of art. Curr. Drug Metabol. 12 (2011), 198–212, 10.2174/138920011795016818.
Stervbo, U., Vang, O., Bonnesen, C., A review of the content of the putative chemopreventive phytoalexin resveratrol in red wine. Food Chem. 101 (2007), 449–457, 10.1016/j.foodchem.2006.01.047.
Van der Heiden, E., Bechoux, N., Muller, M., Sergent, T., Schneider, Y.J., Larondelle, Y., Maghuin-Rogister, G., Scippo, M.L., Food flavonoid aryl hydrocarbon receptor-mediated agonistic/antagonistic/synergic activities in human and rat reporter gene assays. Anal. Chim. Acta 637 (2009), 337–345, 10.1016/j.aca.2008.09.054.
Wall, R.J., Fernandes, A., Rose, M., Bell, D.R., Mellor, I.R., Characterisation of chlorinated, brominated and mixed halogenated dioxins, furans and biphenyls as potent and as partial agonists of the Aryl hydrocarbon receptor. Environ. Int. 76 (2015), 49–56, 10.1016/j.envint.2014.12.002.
Wheeler, J.L.H., Martin, K.C., Resseguie, E., Paige Lawrence, B., Differential consequences of two distinct AhR ligands on innate and adaptive immune responses to influenza A virus. Toxicol. Sci. 137 (2014), 324–334, 10.1093/toxsci/kft255.
Willemsen, P., Scippo, M.L., Maghuin-Rogister, G., Martial, J.A., Muller, M., Enhancement of steroid receptor-mediated transcription for the development of highly responsive bioassays. Anal. Bioanal. Chem. 382 (2005), 894–905, 10.1007/s00216-005-3253-x.
Williamson, G., The role of polyphenols in modern nutrition. Nutr. Bull. 42 (2017), 226–235, 10.1111/nbu.12278.
Wincent, E., Amini, N., Luecke, S., Glatt, H., Bergman, J., Crescenzi, C., Rannug, A., Rannug, U., The suggested physiologic aryl hydrocarbon receptor activator and cytochrome P4501 substrate 6-formylindolo[3,2-b]carbazole is present in humans. J. Biol. Chem. 284 (2009), 2690–2696, 10.1074/jbc.M808321200.
Wincent, E., Kubota, A., Timme-Laragy, A., Jönsson, M.E., Hahn, M.E., Stegeman, J.J., Biological effects of 6-formylindolo[3,2-b]carbazole (FICZ) in vivo are enhanced by loss of CYP1A function in an Ahr2-dependent manner. Biochem. Pharmacol 110–111 (2016), 117–129, 10.1016/j.bcp.2016.04.012.
Wright, E.J., Pereira De Castro, K., Joshi, A.D., Elferink, C.J., Canonical and non-canonical aryl hydrocarbon receptor signaling pathways. Curr. Opin. Toxicol. 2 (2017), 87–92, 10.1016/j.cotox.2017.01.001.
Wu, Q., Needs, P.W., Lu, Y., Kroon, P.A., Ren, D., Yang, X., Different antitumor effects of quercetin, quercetin-3′-sulfate and quercetin-3-glucuronide in human breast cancer MCF-7 cells. Food Funct. 9 (2018), 1736–1746, 10.1039/C7FO01964E.
Xue, Z., Li, D., Yu, W., Zhang, Q., Hou, X., He, Y., Kou, X., Mechanisms and therapeutic prospects of polyphenols as aryl hydrocarbon receptor modulators. Food Funct. 8 (2017), 1414–1437, 10.1039/c6fo01810f.
