Body Mass Index in Multiple Sclerosis modulates ceramide-induced DNA methylation and disease course
Multiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS. Fifty-four therapy-naive Relapsing Remitting (RR) MS patient...
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| Published in | EBioMedicine Vol. 43; pp. 392 - 410 |
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| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Netherlands
Elsevier B.V
01.05.2019
Elsevier |
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| Abstract | Multiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS.
Fifty-four therapy-naive Relapsing Remitting (RR) MS patients with high and normal BMI received clinical and MRI evaluation. Blood samples were immunophenotyped, and processed for unbiased plasma lipidomic profiling and genome-wide DNA methylation analysis of circulating monocytes. The main findings at baseline were validated in an independent cohort of 91 therapy-naïve RRMS patients. Disease course was evaluated by a two-year longitudinal follow up and mechanistic hypotheses tested in human cell cultures and in animal models of MS.
Higher monocytic counts and plasma ceramides, and hypermethylation of genes involved in negative regulation of cell proliferation were detected in the high BMI group of MS patients compared to normal BMI. Ceramide treatment of monocytic cell cultures increased proliferation in a dose-dependent manner and was prevented by DNA methylation inhibitors. The high BMI group of MS patients showed a negative correlation between monocytic counts and brain volume. Those subjects at a two-year follow-up showed increased T1 lesion load, increased disease activity, and worsened clinical disability. Lastly, the relationship between body weight, monocytic infiltration, DNA methylation and disease course was validated in mouse models of MS.
High BMI negatively impacts disease course in Multiple Sclerosis by modulating monocyte cell number through ceramide-induced DNA methylation of anti-proliferative genes.
This work was supported by funds from the Friedman Brain Institute, NIH, and Multiple Sclerosis Society. |
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| AbstractList | AbstractBackgroundMultiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS. MethodsFifty-four therapy-naive Relapsing Remitting (RR) MS patients with high and normal BMI received clinical and MRI evaluation. Blood samples were immunophenotyped, and processed for unbiased plasma lipidomic profiling and genome-wide DNA methylation analysis of circulating monocytes. The main findings at baseline were validated in an independent cohort of 91 therapy-naïve RRMS patients. Disease course was evaluated by a two-year longitudinal follow up and mechanistic hypotheses tested in human cell cultures and in animal models of MS. FindingsHigher monocytic counts and plasma ceramides, and hypermethylation of genes involved in negative regulation of cell proliferation were detected in the high BMI group of MS patients compared to normal BMI. Ceramide treatment of monocytic cell cultures increased proliferation in a dose-dependent manner and was prevented by DNA methylation inhibitors. The high BMI group of MS patients showed a negative correlation between monocytic counts and brain volume. Those subjects at a two-year follow-up showed increased T1 lesion load, increased disease activity, and worsened clinical disability. Lastly, the relationship between body weight, monocytic infiltration, DNA methylation and disease course was validated in mouse models of MS. InterpretationHigh BMI negatively impacts disease course in Multiple Sclerosis by modulating monocyte cell number through ceramide-induced DNA methylation of anti-proliferative genes. FundThis work was supported by funds from the Friedman Brain Institute, NIH, and Multiple Sclerosis Society. Multiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS. Fifty-four therapy-naive Relapsing Remitting (RR) MS patients with high and normal BMI received clinical and MRI evaluation. Blood samples were immunophenotyped, and processed for unbiased plasma lipidomic profiling and genome-wide DNA methylation analysis of circulating monocytes. The main findings at baseline were validated in an independent cohort of 91 therapy-naïve RRMS patients. Disease course was evaluated by a two-year longitudinal follow up and mechanistic hypotheses tested in human cell cultures and in animal models of MS. Higher monocytic counts and plasma ceramides, and hypermethylation of genes involved in negative regulation of cell proliferation were detected in the high BMI group of MS patients compared to normal BMI. Ceramide treatment of monocytic cell cultures increased proliferation in a dose-dependent manner and was prevented by DNA methylation inhibitors. The high BMI group of MS patients showed a negative correlation between monocytic counts and brain volume. Those subjects at a two-year follow-up showed increased T1 lesion load, increased disease activity, and worsened clinical disability. Lastly, the relationship between body weight, monocytic infiltration, DNA methylation and disease course was validated in mouse models of MS. High BMI negatively impacts disease course in Multiple Sclerosis by modulating monocyte cell number through ceramide-induced DNA methylation of anti-proliferative genes. This work was supported by funds from the Friedman Brain Institute, NIH, and Multiple Sclerosis Society. Multiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS. Fifty-four therapy-naive Relapsing Remitting (RR) MS patients with high and normal BMI received clinical and MRI evaluation. Blood samples were immunophenotyped, and processed for unbiased plasma lipidomic profiling and genome-wide DNA methylation analysis of circulating monocytes. The main findings at baseline were validated in an independent cohort of 91 therapy-naïve RRMS patients. Disease course was evaluated by a two-year longitudinal follow up and mechanistic hypotheses tested in human cell cultures and in animal models of MS. Higher monocytic counts and plasma ceramides, and hypermethylation of genes involved in negative regulation of cell proliferation were detected in the high BMI group of MS patients compared to normal BMI. Ceramide treatment of monocytic cell cultures increased proliferation in a dose-dependent manner and was prevented by DNA methylation inhibitors. The high BMI group of MS patients showed a negative correlation between monocytic counts and brain volume. Those subjects at a two-year follow-up showed increased T1 lesion load, increased disease activity, and worsened clinical disability. Lastly, the relationship between body weight, monocytic infiltration, DNA methylation and disease course was validated in mouse models of MS. High BMI negatively impacts disease course in Multiple Sclerosis by modulating monocyte cell number through ceramide-induced DNA methylation of anti-proliferative genes. FUND: This work was supported by funds from the Friedman Brain Institute, NIH, and Multiple Sclerosis Society. Multiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS.BACKGROUNDMultiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study addresses the effect of BMI on the epigenome of monocytes and disease course in MS.Fifty-four therapy-naive Relapsing Remitting (RR) MS patients with high and normal BMI received clinical and MRI evaluation. Blood samples were immunophenotyped, and processed for unbiased plasma lipidomic profiling and genome-wide DNA methylation analysis of circulating monocytes. The main findings at baseline were validated in an independent cohort of 91 therapy-naïve RRMS patients. Disease course was evaluated by a two-year longitudinal follow up and mechanistic hypotheses tested in human cell cultures and in animal models of MS.METHODSFifty-four therapy-naive Relapsing Remitting (RR) MS patients with high and normal BMI received clinical and MRI evaluation. Blood samples were immunophenotyped, and processed for unbiased plasma lipidomic profiling and genome-wide DNA methylation analysis of circulating monocytes. The main findings at baseline were validated in an independent cohort of 91 therapy-naïve RRMS patients. Disease course was evaluated by a two-year longitudinal follow up and mechanistic hypotheses tested in human cell cultures and in animal models of MS.Higher monocytic counts and plasma ceramides, and hypermethylation of genes involved in negative regulation of cell proliferation were detected in the high BMI group of MS patients compared to normal BMI. Ceramide treatment of monocytic cell cultures increased proliferation in a dose-dependent manner and was prevented by DNA methylation inhibitors. The high BMI group of MS patients showed a negative correlation between monocytic counts and brain volume. Those subjects at a two-year follow-up showed increased T1 lesion load, increased disease activity, and worsened clinical disability. Lastly, the relationship between body weight, monocytic infiltration, DNA methylation and disease course was validated in mouse models of MS.FINDINGSHigher monocytic counts and plasma ceramides, and hypermethylation of genes involved in negative regulation of cell proliferation were detected in the high BMI group of MS patients compared to normal BMI. Ceramide treatment of monocytic cell cultures increased proliferation in a dose-dependent manner and was prevented by DNA methylation inhibitors. The high BMI group of MS patients showed a negative correlation between monocytic counts and brain volume. Those subjects at a two-year follow-up showed increased T1 lesion load, increased disease activity, and worsened clinical disability. Lastly, the relationship between body weight, monocytic infiltration, DNA methylation and disease course was validated in mouse models of MS.High BMI negatively impacts disease course in Multiple Sclerosis by modulating monocyte cell number through ceramide-induced DNA methylation of anti-proliferative genes. FUND: This work was supported by funds from the Friedman Brain Institute, NIH, and Multiple Sclerosis Society.INTERPRETATIONHigh BMI negatively impacts disease course in Multiple Sclerosis by modulating monocyte cell number through ceramide-induced DNA methylation of anti-proliferative genes. FUND: This work was supported by funds from the Friedman Brain Institute, NIH, and Multiple Sclerosis Society. |
| Author | Morstein, Johannes Castro, Kamilah Amatruda, Mario Watson, Corey T. Kosa, Peter Katz Sand, Ilana Casaccia, Patrizia Inglese, Matilde Petracca, Maria Chen, Emily Y. Trauner, Dirk Bielekova, Bibiana Kiebish, Michael A. Ntranos, Achilles |
| AuthorAffiliation | f Department of Chemistry, New York University, NY, New York, United States of America c Advanced Science Research Center at The Graduate Center of The City University of New York and Inter-Institutional Center for Glial Biology at Icahn School of Medicine New York, New York, United States of America d Neuroimmunological Disease Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, United States of America e BERG, LLC. Framingham, MA, United States of America a Department of Neuroscience, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America g Department of Biochemistry and Molecular Genetics, University of Louisville, Louisville, KY, United States of America b Department of Neurology, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America |
| AuthorAffiliation_xml | – name: b Department of Neurology, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – name: g Department of Biochemistry and Molecular Genetics, University of Louisville, Louisville, KY, United States of America – name: a Department of Neuroscience, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – name: e BERG, LLC. Framingham, MA, United States of America – name: c Advanced Science Research Center at The Graduate Center of The City University of New York and Inter-Institutional Center for Glial Biology at Icahn School of Medicine New York, New York, United States of America – name: f Department of Chemistry, New York University, NY, New York, United States of America – name: d Neuroimmunological Disease Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, United States of America |
| Author_xml | – sequence: 1 givenname: Kamilah surname: Castro fullname: Castro, Kamilah organization: Department of Neuroscience, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – sequence: 2 givenname: Achilles surname: Ntranos fullname: Ntranos, Achilles organization: Department of Neurology, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – sequence: 3 givenname: Mario surname: Amatruda fullname: Amatruda, Mario organization: Advanced Science Research Center at The Graduate Center of The City University of New York and Inter-Institutional Center for Glial Biology at Icahn School of Medicine New York, New York, United States of America – sequence: 4 givenname: Maria surname: Petracca fullname: Petracca, Maria organization: Department of Neurology, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – sequence: 5 givenname: Peter surname: Kosa fullname: Kosa, Peter organization: Neuroimmunological Disease Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, United States of America – sequence: 6 givenname: Emily Y. surname: Chen fullname: Chen, Emily Y. organization: BERG, LLC. Framingham, MA, United States of America – sequence: 7 givenname: Johannes orcidid: 0000-0002-6940-288X surname: Morstein fullname: Morstein, Johannes organization: Department of Chemistry, New York University, NY, New York, United States of America – sequence: 8 givenname: Dirk surname: Trauner fullname: Trauner, Dirk organization: Department of Chemistry, New York University, NY, New York, United States of America – sequence: 9 givenname: Corey T. surname: Watson fullname: Watson, Corey T. organization: Department of Biochemistry and Molecular Genetics, University of Louisville, Louisville, KY, United States of America – sequence: 10 givenname: Michael A. surname: Kiebish fullname: Kiebish, Michael A. organization: BERG, LLC. Framingham, MA, United States of America – sequence: 11 givenname: Bibiana surname: Bielekova fullname: Bielekova, Bibiana organization: Neuroimmunological Disease Section, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, United States of America – sequence: 12 givenname: Matilde surname: Inglese fullname: Inglese, Matilde organization: Department of Neurology, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – sequence: 13 givenname: Ilana surname: Katz Sand fullname: Katz Sand, Ilana organization: Department of Neurology, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America – sequence: 14 givenname: Patrizia orcidid: 0000-0002-4785-9264 surname: Casaccia fullname: Casaccia, Patrizia email: patrizia.casaccia@asrc.cuny.edu organization: Department of Neuroscience, Icahn School of Medicine at Mount Sinai, NY, New York, United States of America |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30981648$$D View this record in MEDLINE/PubMed |
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| Snippet | Multiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early life. This study... AbstractBackgroundMultiple Sclerosis (MS) results from genetic predisposition and environmental variables, including elevated Body Mass Index (BMI) in early... |
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| SubjectTerms | Advanced Basic Science Animals Biomarkers Body Mass Index Brain - pathology Ceramides - metabolism Ceramides - pharmacology Disease Models, Animal Disease Progression Disease Susceptibility DNA Methylation - drug effects Epigenesis, Genetic Epigenetics Epigenomics - methods Female Humans Immunity Internal Medicine Leukocyte Count Lipid Metabolism - drug effects Lipids Lipids - blood Male Metabolome Metabolomics - methods Mice Monocytes - drug effects Monocytes - immunology Monocytes - metabolism Multiple Sclerosis - diagnostic imaging Multiple Sclerosis - etiology Multiple Sclerosis - metabolism Multiple Sclerosis - pathology Neurodegeneration Obesity Obesity - complications Obesity - metabolism Organ Size Research paper Transcription, Genetic |
| Title | Body Mass Index in Multiple Sclerosis modulates ceramide-induced DNA methylation and disease course |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S2352396419302324 https://www.clinicalkey.es/playcontent/1-s2.0-S2352396419302324 https://dx.doi.org/10.1016/j.ebiom.2019.03.087 https://www.ncbi.nlm.nih.gov/pubmed/30981648 https://www.proquest.com/docview/2210008032 https://pubmed.ncbi.nlm.nih.gov/PMC6557766 |
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