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July 2017; 4 (4) ArticleOpen Access

Dynamic regulation of serum aryl hydrocarbon receptor agonists in MS

Veit Rothhammer, Davis M. Borucki, Maria Isabel Garcia Sanchez, Maria Antonietta Mazzola, Christopher C. Hemond, Keren Regev, Anu Paul, Pia Kivisäkk, Rohit Bakshi, Guillermo Izquierdo, Howard L. Weiner, Francisco J. Quintana
First published June 16, 2017, DOI: https://doi.org/10.1212/NXI.0000000000000359
Veit Rothhammer
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Davis M. Borucki
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Maria Isabel Garcia Sanchez
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Maria Antonietta Mazzola
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Christopher C. Hemond
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Keren Regev
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Anu Paul
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Pia Kivisäkk
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Rohit Bakshi
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Guillermo Izquierdo
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Howard L. Weiner
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Francisco J. Quintana
From the Ann Romney Center for Neurologic Diseases (V.R., D.M.B., M.A.M., C.C.H., K.R., A.P., P.K., R.B., H.L.W., F.J.Q.), Brigham and Women's Hospital, Harvard Medical School, Boston, MA; Molecular Biology Service and MS Unit (M.I.G.S., G.I.), University of Seville, Spain; and Broad Institute of MIT and Harvard (F.J.Q.), Cambridge, MA.
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Full PDF
Citation
Dynamic regulation of serum aryl hydrocarbon receptor agonists in MS
Veit Rothhammer, Davis M. Borucki, Maria Isabel Garcia Sanchez, Maria Antonietta Mazzola, Christopher C. Hemond, Keren Regev, Anu Paul, Pia Kivisäkk, Rohit Bakshi, Guillermo Izquierdo, Howard L. Weiner, Francisco J. Quintana
Neurol Neuroimmunol Neuroinflamm Jul 2017, 4 (4) e359; DOI: 10.1212/NXI.0000000000000359

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    Figure 1 Detection of aryl hydrocarbon receptor ligands from different sources

    Aryl hydrocarbon receptor (AHR) agonistic activity was measured for a collection of AHR ligands from exogenous and exogenous sources, including the pollutant 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) (A), the diet-derived ligand Indole-3-carbinol (I3C) (B), ligands derived from microbial and host tryptophan metabolism Indole (C), Indoxyl-3-sulfate (I3S) (D), Indirubin (E), and 2′Z-Indirubin (F), the mucosal ligand 2-(1′H-indole-3′-carbonyl)-thiazole-4-carboxylic acid methyl ester (ITE) (G), and the endogenous metabolite Kynurenine (H). Data are normalized to 100% (maximum activity per ligand) and are representative of 2 independent experiments.

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    Figure 2 Aryl hydrocarbon receptor ligand levels are decreased in patients with relapsing-remitting MS

    Aryl hydrocarbon receptor (AHR) agonistic activity in serum samples of healthy controls (controls, n = 26) and relapsing-remitting MS (RRMS) patients (RRMS, n = 91) was assessed in duplicates using an AHR ligand–sensitive luciferase assay. Relative activity was calculated by dividing firefly luciferase activity (pGud-Luc) by Renilla luciferase activity (pTK-Renilla). Values are means of duplicate measurements. Lines represent mean and error bars standard error of the mean (SEM). Significance levels were derived using the Student t test. **p < 0.01.

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    Figure 3 Aryl hydrocarbon receptor ligand levels are modulated by disease activity

    Aryl hydrocarbon receptor (AHR) agonistic activity in serum samples of healthy controls (controls, n = 26), relapsing-remitting MS (RRMS) patients during remission (RRMS remission, n = 32), and patients with RRMS with active disease (RRMS active, n = 20) was assessed in duplicates using an AHR ligand–sensitive luciferase assay. Values are means of duplicate measurements. Lines represent mean and error bars standard error of the mean (SEM). Significance levels were derived using 1-way analysis of variance followed by the Tukey multiple comparisons test. ****p < 0.0001.

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    Figure 4 Aryl hydrocarbon receptor ligand levels are increased in clinically isolated syndrome as compared to healthy controls

    Aryl hydrocarbon receptor agonistic activity in serum samples of healthy controls (controls, n = 33) and patients with clinically isolated syndrome (CIS, n = 15) was assessed in duplicates. Values are means of duplicate measurements. Lines represent mean and error bars standard error of the mean (SEM). Significance level was derived by the Student t test. **p < 0.01.

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    Figure 5 Aryl hydrocarbon receptor ligand levels in patients with benign relapsing-remitting MS are unchanged as compared to healthy controls

    Aryl hydrocarbon receptor agonistic activity in serum samples of healthy controls (controls, n = 7) and patients with benign relapsing-remitting MS as defined by low EDSS scores despite longstanding disease (benign MS, n = 11) was assessed in duplicates. Values are means of duplicate measurements. Lines represent mean and error bars standard error of the mean (SEM). Significance level was derived by the Student t test. n.s. = not significant.

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    Figure 6 Dynamic modulation of aryl hydrocarbon receptor ligand levels in patients with relapsing-remitting MS

    (A) Serum aryl hydrocarbon receptor (AHR) agonistic activity is increased during the first relapse of the disease but decreases below control levels in remission. Further relapses increase AHR ligand levels during the relapse. (B) Benign courses of MS have control levels of AHR agonistic activity and might be increased during relapses. RRMS = relapsing-remitting MS.

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