The Aryl Hydrocarbon Receptor and Its Ligands Inhibit Myofibroblast Formation and Activation: Implications for Thyroid Eye Disease

American Journal of Pathology

Volumn 186, Issue 12, 2016, Pages 3189-3202

  Woeller, Collynn F ^a   Roztocil, Elisa ^a   Hammond, Christine L ^a   Feldon, Steven E ^a   Phipps, Richard P ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (1'H INDOLE 3' CARBONYL)THIAZOLE 4 CARBOXYLIC ACID METHYL ESTER; 6 FORMYLINDOLO[3,2 B]CARBAZOLE; AGENTS ACTING ON THE EYE; ALPHA SMOOTH MUSCLE ACTIN; AROMATIC HYDROCARBON RECEPTOR; ASCORBIC ACID; BETA TUBULIN; CALPONIN; COLLAGEN; CYTOCHROME P450 1B1; GLYCOGEN SYNTHASE KINASE 3BETA; HYPOXIA INDUCIBLE FACTOR 1BETA; MESSENGER RNA; PROLINE; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG; WNT PROTEIN; LIGAND;

ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENDOCRINE OPHTHALMOPATHY; ENZYME PHOSPHORYLATION; FIBROBLAST; HEK293 CELL LINE; HUMAN; HUMAN CELL; MYOFIBROBLAST; ORBIT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; RNA EXTRACTION; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; CELL CULTURE; GENE SILENCING; GENETICS; GRAVES DISEASE; IMMUNOLOGY; METABOLISM; ORBIT DISEASE; PATHOPHYSIOLOGY; THYROID GLAND; WNT SIGNALING;

CELLS, CULTURED; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; GRAVES DISEASE; HUMANS; LIGANDS; MYOFIBROBLASTS; ORBITAL DISEASES; RECEPTORS, ARYL HYDROCARBON; RNA, SMALL INTERFERING; THYROID GLAND; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY;

EID: 84995972701     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2016.08.017     Document Type: Article

References (52)

1. 1 Kuriyan, A.E., Woeller, C.F., O'Loughlin, C.W., Phipps, R.P., Feldon, S.E., Orbital fibroblasts from thyroid eye disease patients differ in proliferative and adipogenic responses depending on disease subtype. Invest Ophthalmol Vis Sci 54 (2013), 7370–7377.
2. 2 Kuriyan, A.E., Phipps, R.P., Feldon, S.E., The eye and thyroid disease. Curr Opin Ophthalmol 19 (2008), 499–506.
3. 3 Burch, H.B., Cooper, D.S., Management of graves disease: a review. JAMA 314 (2015), 2544–2554.
4. 4 Bahn, R.S., Graves' ophthalmopathy. N Engl J Med 362 (2010), 726–738.
5. 5 Lehmann, G.M., Feldon, S.E., Smith, T.J., Phipps, R.P., Immune mechanisms in thyroid eye disease. Thyroid 18 (2008), 959–965.
6. 6 Hinz, B., Phan, S.H., Thannickal, V.J., Galli, A., Bochaton-Piallat, M.L., Gabbiani, G., The myofibroblast: one function, multiple origins. Am J Pathol 170 (2007), 1807–1816.
7. 7 Hinz, B., Phan, S.H., Thannickal, V.J., Prunotto, M., Desmouliere, A., Varga, J., De Wever, O., Mareel, M., Gabbiani, G., Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 180 (2012), 1340–1355.
8. 8 Smith, R.S., Smith, T.J., Blieden, T.M., Phipps, R.P., Fibroblasts as sentinel cells. Synthesis of chemokines and regulation of inflammation. Am J Pathol 151 (1997), 317–322.
9. 9 Micallef, L., Vedrenne, N., Billet, F., Coulomb, B., Darby, I.A., Desmouliere, A., The myofibroblast, multiple origins for major roles in normal and pathological tissue repair. Fibrogenesis Tissue Repair, 5, 2012, S5.
10. 10 Woeller, C.F., O'Loughlin, C.W., Roztocil, E., Feldon, S.E., Phipps, R.P., Salinomycin and other polyether ionophores are a new class of antiscarring agent. J Biol Chem 290 (2015), 3563–3575.
11. 11 Baglole, C.J., Maggirwar, S.B., Gasiewicz, T.A., Thatcher, T.H., Phipps, R.P., Sime, P.J., The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-kappaB family member RelB. J Biol Chem 283 (2008), 28944–28957.
12. 12 Stevens, E.A., Mezrich, J.D., Bradfield, C.A., The aryl hydrocarbon receptor: a perspective on potential roles in the immune system. Immunology 127 (2009), 299–311.
13. 13 Puga, A., Ma, C., Marlowe, J.L., The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem Pharmacol 77 (2009), 713–722.
14. 14 Carvajal-Gonzalez, J.M., Roman, A.C., Cerezo-Guisado, M.I., Rico-Leo, E.M., Martin-Partido, G., Fernandez-Salguero, P.M., Loss of dioxin-receptor expression accelerates wound healing in vivo by a mechanism involving TGFbeta. J Cell Sci 122 (2009), 1823–1833.
15. 15 Hogenesch, J.B., Chan, W.K., Jackiw, V.H., Brown, R.C., Gu, Y.Z., Pray-Grant, M., Perdew, G.H., Bradfield, C.A., Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J Biol Chem 272 (1997), 8581–8593.
16. 16 Hao, N., Whitelaw, M.L., The emerging roles of AhR in physiology and immunity. Biochem Pharmacol 86 (2013), 561–570.
17. 17 Milbrath, M.O., Wenger, Y., Chang, C.W., Emond, C., Garabrant, D., Gillespie, B.W., Jolliet, O., Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a function of age, body fat, smoking status, and breast-feeding. Environ Health Perspect 117 (2009), 417–425.
18. 18 Nguyen, N.T., Nakahama, T., Le, D.H., Van Son, L., Chu, H.H., Kishimoto, T., Aryl hydrocarbon receptor and kynurenine: recent advances in autoimmune disease research. Front Immunol, 5, 2014, 551.
19. 19 Lowe, M.M., Mold, J.E., Kanwar, B., Huang, Y., Louie, A., Pollastri, M.P., Wang, C., Patel, G., Franks, D.G., Schlezinger, J., Sherr, D.H., Silverstone, A.E., Hahn, M.E., McCune, J.M., Identification of cinnabarinic acid as a novel endogenous aryl hydrocarbon receptor ligand that drives IL-22 production. PLoS One, 9, 2014, e87877.
20. 20 Goodale, B.C., La Du, J., Tilton, S.C., Sullivan, C.M., Bisson, W.H., Waters, K.M., Tanguay, R.L., Ligand-Specific Transcriptional Mechanisms Underlie Aryl Hydrocarbon Receptor-Mediated Developmental Toxicity of Oxygenated PAHs. Toxicol Sci 147 (2015), 397–411.
21. 21 Wheeler, J.L., Martin, K.C., Resseguie, E., Lawrence, B.P., Differential consequences of two distinct AhR ligands on innate and adaptive immune responses to influenza A virus. Toxicol Sci 137 (2014), 324–334.
22. 22 Lehmann, G.M., Woeller, C.F., Pollock, S.J., O'Loughlin, C.W., Gupta, S., Feldon, S.E., Phipps, R.P., Novel anti-adipogenic activity produced by human fibroblasts. Am J Physiol Cell Physiol 299 (2010), C672–C681.
23. 23 Veeman, M.T., Slusarski, D.C., Kaykas, A., Louie, S.H., Moon, R.T., Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr Biol 13 (2003), 680–685.
24. 24 Volotinen, M., Maenpaa, J., Kankuri, E., Oksala, O., Pelkonen, O., Nakajima, M., Yokoi, T., Hakkola, J., Expression of cytochrome P450 (CYP) enzymes in human nonpigmented ciliary epithelial cells: induction of CYP1B1 expression by TCDD. Invest Ophthalmol Vis Sci 50 (2009), 3099–3105.
25. 25 Nguyen, L.P., Bradfield, C.A., The search for endogenous activators of the aryl hydrocarbon receptor. Chem Res Toxicol 21 (2008), 102–116.
26. 26 Ma, Q., Baldwin, K.T., 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced degradation of aryl hydrocarbon receptor (AhR) by the ubiquitin-proteasome pathway: role of the transcription activaton and DNA binding of AhR. J Biol Chem 275 (2000), 8432–8438.
27. 27 Murad, S., Grove, D., Lindberg, K.A., Reynolds, G., Sivarajah, A., Pinnell, S.R., Regulation of collagen synthesis by ascorbic acid. Proc Natl Acad Sci U S A 78 (1981), 2879–2882.
28. 28 Bellon, G., Monboisse, J.C., Randoux, A., Borel, J.P., Effects of preformed proline and proline amino acid precursors (including glutamine) on collagen synthesis in human fibroblast cultures. Biochim Biophys Acta 930 (1987), 39–47.
29. 29 Piersma, B., Bank, R.A., Boersema, M., Signaling in fibrosis: TGF-beta, WNT, and YAP/TAZ converge. Front Med (Lausanne), 2, 2015, 59.
30. 30 Jeon, K.I., Kulkarni, A., Woeller, C.F., Phipps, R.P., Sime, P.J., Hindman, H.B., Huxlin, K.R., Inhibitory effects of PPARgamma ligands on TGF-beta1-induced corneal myofibroblast transformation. Am J Pathol 184 (2014), 1429–1445.
31. 31 Sun, Z., Wang, C., Shi, C., Sun, F., Xu, X., Qian, W., Nie, S., Han, X., Activated Wnt signaling induces myofibroblast differentiation of mesenchymal stem cells, contributing to pulmonary fibrosis. Int J Mol Med 33 (2014), 1097–1109.
32. 32 Zhou, B., Liu, Y., Kahn, M., Ann, D.K., Han, A., Wang, H., Nguyen, C., Flodby, P., Zhong, Q., Krishnaveni, M.S., Liebler, J.M., Minoo, P., Crandall, E.D., Borok, Z., Interactions between beta-catenin and transforming growth factor-beta signaling pathways mediate epithelial-mesenchymal transition and are dependent on the transcriptional co-activator cAMP-response element-binding protein (CREB)-binding protein (CBP). J Biol Chem 287 (2012), 7026–7038.
33. 33 Woeller, C.F., O'Loughlin, C.W., Pollock, S.J., Thatcher, T.H., Feldon, S.E., Phipps, R.P., Thy1 (CD90) controls adipogenesis by regulating activity of the Src family kinase, Fyn. FASEB J 29 (2015), 920–931.
34. 34 Douglas, R.S., Gupta, S., The pathophysiology of thyroid eye disease: implications for immunotherapy. Curr Opin Ophthalmol 22 (2011), 385–390.
35. 35 Esser, C., Rannug, A., The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology. Pharmacol Rev 67 (2015), 259–279.
36. 36 Singh, K.P., Casado, F.L., Opanashuk, L.A., Gasiewicz, T.A., The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem Pharmacol 77 (2009), 577–587.
37. 37 Lehmann, G.M., Xi, X., Kulkarni, A.A., Olsen, K.C., Pollock, S.J., Baglole, C.J., Gupta, S., Casey, A.E., Huxlin, K.R., Sime, P.J., Feldon, S.E., Phipps, R.P., The aryl hydrocarbon receptor ligand ITE inhibits TGFbeta1-induced human myofibroblast differentiation. Am J Pathol 178 (2011), 1556–1567.
38. 38 McMillan, B.J., Bradfield, C.A., The aryl hydrocarbon receptor sans xenobiotics: endogenous function in genetic model systems. Mol Pharmacol 72 (2007), 487–498.
39. 39 Stan, M.N., Bahn, R.S., Risk factors for development or deterioration of Graves' ophthalmopathy. Thyroid 20 (2010), 777–783.
40. 40 Li, Y., Kilani, R.T., Rahmani-Neishaboor, E., Jalili, R.B., Ghahary, A., Kynurenine increases matrix metalloproteinase-1 and -3 expression in cultured dermal fibroblasts and improves scarring in vivo. J Invest Dermatol 134 (2014), 643–650.
41. 41 Hinz, B., Dugina, V., Ballestrem, C., Wehrle-Haller, B., Chaponnier, C., Alpha-smooth muscle actin is crucial for focal adhesion maturation in myofibroblasts. Mol Biol Cell 14 (2003), 2508–2519.
42. 42 Guo, Y., Xiao, L., Sun, L., Liu, F., Wnt/beta-catenin signaling: a promising new target for fibrosis diseases. Physiol Res 61 (2012), 337–346.
43. 43 Ezra, D.G., Krell, J., Rose, G.E., Bailly, M., Stebbing, J., Castellano, L., Transcriptome-level microarray expression profiling implicates IGF-1 and Wnt signalling dysregulation in the pathogenesis of thyroid-associated orbitopathy. J Clin Pathol 65 (2012), 608–613.
44. 44 Flaveny, C.A., Perdew, G.H., Transgenic humanized AHR mouse reveals differences between human and mouse AHR ligand selectivity. Mol Cell Pharmacol 1 (2009), 119–123.
45. 45 Flaveny, C.A., Murray, I.A., Perdew, G.H., Differential gene regulation by the human and mouse aryl hydrocarbon receptor. Toxicol Sci 114 (2010), 217–225.
46. 46 Corchero, J., Martin-Partido, G., Dallas, S.L., Fernandez-Salguero, P.M., Liver portal fibrosis in dioxin receptor-null mice that overexpress the latent transforming growth factor-beta-binding protein-1. Int J Exp Pathol 85 (2004), 295–302.
47. 47 Faust, D., Vondracek, J., Krcmar, P., Smerdova, L., Prochazkova, J., Hruba, E., Hulinkova, P., Kaina, B., Dietrich, C., Machala, M., AhR-mediated changes in global gene expression in rat liver progenitor cells. Arch Toxicol 87 (2013), 681–698.
48. 48 Diaz-Flores, L., Gutierrez, R., Lizartza, K., Gomez, M.G., Garcia Mdel, P., Saez, F.J., Diaz-Flores, L. Jr., Madrid, J.F., Behavior of in situ human native adipose tissue CD34+ stromal/progenitor cells during different stages of repair: tissue-resident CD34+ stromal cells as a source of myofibroblasts. Anat Rec 298 (2015), 917–930.
49. 49 Fernando, R., Atkins, S., Raychaudhuri, N., Lu, Y., Li, B., Douglas, R.S., Smith, T.J., Human fibrocytes coexpress thyroglobulin and thyrotropin receptor. Proc Natl Acad Sci U S A 109 (2012), 7427–7432.
50. 50 Smith, T.J., Padovani-Claudio, D.A., Lu, Y., Raychaudhuri, N., Fernando, R., Atkins, S., Gillespie, E.F., Gianoukakis, A.G., Miller, B.S., Gauger, P.G., Doherty, G.M., Douglas, R.S., Fibroblasts expressing the thyrotropin receptor overarch thyroid and orbit in Graves' disease. J Clin Endocrinol Metab 96 (2011), 3827–3837.
51. 51 Braun, J., Kurtz, A., Barutcu, N., Bodo, J., Thiel, A., Dong, J., Concerted regulation of CD34 and CD105 accompanies mesenchymal stromal cell derivation from human adventitial stromal cell. Stem Cells Dev 22 (2013), 815–827.
52. 52 Kerkvliet, N.I., Shepherd, D.M., Baecher-Steppan, L., T lymphocytes are direct, aryl hydrocarbon receptor (AhR)-dependent targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): AhR expression in both CD4+ and CD8+ T cells is necessary for full suppression of a cytotoxic T lymphocyte response by TCDD. Toxicol Appl Pharmacol 185 (2002), 146–152.