Pleiotropic consequences of metabolic stress for the major histocompatibility complex class II molecule antigen processing and presentation machinery

Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we...

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Published in	Immunity (Cambridge, Mass.) Vol. 54; no. 4; pp. 721 - 736.e10
Main Authors	Clement, Cristina C., Nanaware, Padma P., Yamazaki, Takahiro, Negroni, Maria Pia, Ramesh, Karthik, Morozova, Kateryna, Thangaswamy, Sangeetha, Graves, Austin, Kim, Hei Jung, Li, Tsai Wanxia, Vigano’, Marco, Soni, Rajesh K., Gadina, Massimo, Tse, Harley Y., Galluzzi, Lorenzo, Roche, Paul A., Denzin, Lisa K., Stern, Lawrence J., Santambrogio, Laura
Format	Journal Article
Language	English
Published	United States Elsevier Inc 13.04.2021 Elsevier Limited
Subjects	advanced glycation end products Age Animal models Animals Antigen presentation Antigen Presentation - immunology Antigen processing antigen processing and presentation Antigen-Presenting Cells - immunology Antigens Arthritis Cardiovascular disease CD4+ T cells Complications Dendritic cells Diabetes Diabetes mellitus Diabetes Mellitus, Experimental - immunology Diabetes Mellitus, Type 2 - immunology Disease Models, Animal Efficiency Epitopes Epitopes - immunology Female Glycosylation High fat diet Histocompatibility Antigens Class II - immunology Hyperglycemia hyperinsulinemia Hyperlipidemia Lipid peroxidation Lipids Lymphatic system Lymphocytes Major histocompatibility complex Male Mass spectrometry Metabolic disorders Metabolic syndrome MHC class II Mice Mice, Inbred C57BL Obesity oxidative posttranslational modifications Pathogenesis Peptides Peptides - immunology Phosphorylation Protein Binding - immunology Proteins Scientific imaging Stress, Physiological - immunology Sugar dendritic cells hyperinsulinemia oxidative posttranslational modifications antigen processing and presentation MHC class II diabetes advanced glycation end products obesity CD4+ T cells CD4(+) T cells
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ISSN	1074-7613 1097-4180 1097-4180
DOI	10.1016/j.immuni.2021.02.019

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Abstract	Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class II molecule antigen processing and presentation machinery in vivo under conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC class II-peptide binding, and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC class II immunopeptidome of Ob/Ob mice on a high-fat diet compared with controls, including changes in the presentation of an apolipoprotein B100 peptide associated previously with T2D and metabolic syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC class II antigen presentation that may contribute to T2D complications. [Display omitted] •Oxidative post-translational modifications (PTMs) are observed in T2D subjects•PTMs were mapped to the MHC class II antigen processing and presentation machinery•PTMs affected epitope-specific antigen processing and MHC class II presentation•Increased presentation of an APO-B peptide associated with clinical complications of T2D Hyperglycemia and hyperlipidemia during diabetes and metabolic syndrome induce protein oxidative post-translational modifications (PTMs) that affect the MHC class II processing and presentation machinery. Clement et al. reveal that these PTMs are linked to epitope-specific changes in the MHC class II peptidome, with increased presentation of an apolipoprotein B100 peptide, contributing to diabetes-related complications.
AbstractList	Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class II molecule antigen processing and presentation machinery in vivo under conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC class II-peptide binding, and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC class II immunopeptidome of Ob/Ob mice on a high-fat diet compared with controls, including changes in the presentation of an apolipoprotein B100 peptide associated previously with T2D and metabolic syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC class II antigen presentation that may contribute to T2D complications. [Display omitted] •Oxidative post-translational modifications (PTMs) are observed in T2D subjects•PTMs were mapped to the MHC class II antigen processing and presentation machinery•PTMs affected epitope-specific antigen processing and MHC class II presentation•Increased presentation of an APO-B peptide associated with clinical complications of T2D Hyperglycemia and hyperlipidemia during diabetes and metabolic syndrome induce protein oxidative post-translational modifications (PTMs) that affect the MHC class II processing and presentation machinery. Clement et al. reveal that these PTMs are linked to epitope-specific changes in the MHC class II peptidome, with increased presentation of an apolipoprotein B100 peptide, contributing to diabetes-related complications. SummaryHyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class II molecule antigen processing and presentation machinery in vivo under conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC class II-peptide binding, and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC class II immunopeptidome of Ob/Ob mice on a high-fat diet compared with controls, including changes in the presentation of an apolipoprotein B100 peptide associated previously with T2D and metabolic syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC class II antigen presentation that may contribute to T2D complications. Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class II molecule antigen processing and presentation machinery in vivo under conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC class II-peptide binding, and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC class II immunopeptidome of Ob/Ob mice on a high-fat diet compared with controls, including changes in the presentation of an apolipoprotein B100 peptide associated previously with T2D and metabolic syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC class II antigen presentation that may contribute to T2D complications.Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class II molecule antigen processing and presentation machinery in vivo under conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC class II-peptide binding, and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC class II immunopeptidome of Ob/Ob mice on a high-fat diet compared with controls, including changes in the presentation of an apolipoprotein B100 peptide associated previously with T2D and metabolic syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC class II antigen presentation that may contribute to T2D complications. Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids, and proteins, favoring protein glycation, glycoxidation, and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class II molecule antigen processing and presentation machinery in vivo under conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC class II-peptide binding, and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC class II immunopeptidome of Ob/Ob mice on a high-fat diet compared with controls, including changes in the presentation of an apolipoprotein B100 peptide associated previously with T2D and metabolic syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC class II antigen presentation that may contribute to T2D complications. Hyperglycemia and hyperlipidemia are often observed in patients with Type II Diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence is the non-enzymatic reaction between sugars, lipids and proteins, favoring protein glycation, glycoxidation and lipoxidation. Here, we identified oxidative alterations in key components of the major histocompatibility complex (MHC) class-II molecule antigen processing and presentation machinery in vivo , in conditions of hyperglycemia-induced metabolic stress. These modifications were linked to epitope-specific changes in endosomal processing efficiency, MHC-class-II-peptide binding and DM editing activity. Moreover, we observed some quantitative and qualitative changes in the MHC-class-II immunopeptidome of Ob/Ob and mice on a high fat diet as compared to controls, including changes in the presentation of an apolipoprotein B100 peptide previously associated with T2D and metabolic-syndrome-related clinical complications. These findings highlight a link between glycation reactions and altered MHC-class-II antigen presentation that may contribute to T2D complications. Hyperglycemia and hyperlipidemia during diabetes and metabolic syndrome induce protein oxidative post-translational modifications (PTMs) that affect the MHC-class-II processing and presentation machinery. Clement et al. reveal that these PTMs are linked to epitope-specific changes in the MHC-class-II peptidome, with increased presentation of an apolipoprotein B100 peptide, contributing to diabetes-related complications.
Author	Ramesh, Karthik Nanaware, Padma P. Graves, Austin Galluzzi, Lorenzo Vigano’, Marco Santambrogio, Laura Tse, Harley Y. Negroni, Maria Pia Clement, Cristina C. Morozova, Kateryna Kim, Hei Jung Gadina, Massimo Stern, Lawrence J. Yamazaki, Takahiro Denzin, Lisa K. Li, Tsai Wanxia Soni, Rajesh K. Roche, Paul A. Thangaswamy, Sangeetha
AuthorAffiliation	1 Department of Radiation Oncology, Weill Cornell Medicine, New York, NY, US 5 Experimental Immunology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, US 4 Child Health Institute of New Jersey, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ, US 8 Proteomics and Macromolecular Crystallography Shared Resource, Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center, New York, NY 9 Department of Microbiology and Immunology, Cardiovascular Research Institute, Wayne State University School of Medicine, Detroit 3 Immunology and Microbiology Program, University of Massachusetts Medical School, Worcester, MA, US 7 Orthopaedic Biotechnology Lab, Galeazzi Orthopedic Institute for Care and Scientific Research, Milan, Italy 10 Sandra and Edward Meyer Cancer Center, New York, NY, USA 6 Translational Immunology Section, National Institute of Arthritis Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD, U
AuthorAffiliation_xml	– name: 9 Department of Microbiology and Immunology, Cardiovascular Research Institute, Wayne State University School of Medicine, Detroit – name: 11 Caryl and Israel Englander Institute for Precision Medicine, New York, NY, USA – name: 4 Child Health Institute of New Jersey, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ, US – name: 1 Department of Radiation Oncology, Weill Cornell Medicine, New York, NY, US – name: 5 Experimental Immunology Branch, National Cancer Institute, National Institutes of Health, Bethesda, MD, US – name: 6 Translational Immunology Section, National Institute of Arthritis Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD, US – name: 7 Orthopaedic Biotechnology Lab, Galeazzi Orthopedic Institute for Care and Scientific Research, Milan, Italy – name: 3 Immunology and Microbiology Program, University of Massachusetts Medical School, Worcester, MA, US – name: 8 Proteomics and Macromolecular Crystallography Shared Resource, Herbert Irving Comprehensive Cancer Center, Columbia University Irving Medical Center, New York, NY – name: 10 Sandra and Edward Meyer Cancer Center, New York, NY, USA – name: 2 Department of Pathology, University of Massachusetts Medical School, Worcester, MA, US
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Keywords	dendritic cells hyperinsulinemia oxidative posttranslational modifications antigen processing and presentation MHC class II diabetes advanced glycation end products obesity CD4+ T cells CD4(+) T cells
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Snippet	Hyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical... SummaryHyperglycemia and hyperlipidemia are often observed in individuals with type II diabetes (T2D) and related mouse models. One dysmetabolic biochemical... Hyperglycemia and hyperlipidemia are often observed in patients with Type II Diabetes (T2D) and related mouse models. One dysmetabolic biochemical consequence...
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SubjectTerms	advanced glycation end products Age Animal models Animals Antigen presentation Antigen Presentation - immunology Antigen processing antigen processing and presentation Antigen-Presenting Cells - immunology Antigens Arthritis Cardiovascular disease CD4+ T cells Complications Dendritic cells Diabetes Diabetes mellitus Diabetes Mellitus, Experimental - immunology Diabetes Mellitus, Type 2 - immunology Disease Models, Animal Efficiency Epitopes Epitopes - immunology Female Glycosylation High fat diet Histocompatibility Antigens Class II - immunology Hyperglycemia hyperinsulinemia Hyperlipidemia Lipid peroxidation Lipids Lymphatic system Lymphocytes Major histocompatibility complex Male Mass spectrometry Metabolic disorders Metabolic syndrome MHC class II Mice Mice, Inbred C57BL Obesity oxidative posttranslational modifications Pathogenesis Peptides Peptides - immunology Phosphorylation Protein Binding - immunology Proteins Scientific imaging Stress, Physiological - immunology Sugar
Title	Pleiotropic consequences of metabolic stress for the major histocompatibility complex class II molecule antigen processing and presentation machinery
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