Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism

Mangal, Joslyn L.; Inamdar, Sahil; Yang, Yi; Dutta, Subhadeep; Wankhede, Mamta; Shi, Xiaojian; Gu, Haiwei; Green, Matthew; Rege, Kaushal; Curtis, Marion; Acharya, Abhinav P.

doi:10.1039/d0tb00790k

Title: Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism

Abstract

Metabolites control immune cell functions, and delivery of these metabolites in a sustained manner may be able to modulate function of the immune cells. In this study, alpha-ketoglutarate (aKG) and diol based polymeric-microparticles (termed paKG MPs) were synthesized to provide sustained release of aKG and promote an immunosuppressive cellular phenotype. Notably, after association with dendritic cells (DCs), paKG MPs modulated the intracellular metabolic-profile/pathways, and decreased glycolysis and mitochondrial respiration in vitro. These metabolic changes resulted in modulation of MHC-II, CD86 expression in DCs, and altered the frequency of regulatory T cells (Tregs), and T-helper type-1/2/17 cells in vitro. In conclusion, this unique strategy of intracellular delivery of key-metabolites in a sustained manner provides a new direction in immunometabolism field-based immunotherapy with potential applications in different diseases associated with immune disorders.

Authors:

Mangal, Joslyn L. ^[1]; Inamdar, Sahil ^[1]; Yang, Yi ^[1]; Dutta, Subhadeep ^[1]; Wankhede, Mamta ^[1]; Shi, Xiaojian ^[2]; Gu, Haiwei ^[2];

^[1]; Rege, Kaushal ^[1]; Curtis, Marion ^[3];

^[1]

Arizona State Univ., Tempe, AZ (United States)
Arizona State Univ., Phoenix, AZ (United States)
Mayo Clinic, Scottsdale, AZ (United States)

Publication Date:: Mon May 11 00:00:00 EDT 2020

Research Org.:: Arizona State Univ., Tempe, AZ (United States)

Sponsoring Org.:: USDOE Advanced Research Projects Agency - Energy (ARPA-E); National Institutes of Health (NIH)

OSTI Identifier:: 1638930

Alternate Identifier(s):: OSTI ID: 1630184

Grant/Contract Number:: AR0001103; 1R01EB020690

Resource Type:: Accepted Manuscript

Journal Name:: Journal of Materials Chemistry. B

Additional Journal Information:: Journal Volume: 8; Journal Issue: 24; Journal ID: ISSN 2050-750X

Publisher:: Royal Society of Chemistry

Country of Publication:: United States

Language:: English

Subject:: 36 MATERIALS SCIENCE

Citation Formats


                    Mangal, Joslyn L., Inamdar, Sahil, Yang, Yi, Dutta, Subhadeep, Wankhede, Mamta, Shi, Xiaojian, Gu, Haiwei, Green, Matthew, Rege, Kaushal, Curtis, Marion, and Acharya, Abhinav P. Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism.  United States: N. p., 2020. 
Web.  doi:10.1039/d0tb00790k.

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                    Mangal, Joslyn L., Inamdar, Sahil, Yang, Yi, Dutta, Subhadeep, Wankhede, Mamta, Shi, Xiaojian, Gu, Haiwei, Green, Matthew, Rege, Kaushal, Curtis, Marion, & Acharya, Abhinav P. Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism.  United States.  https://doi.org/10.1039/d0tb00790k

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                    Mangal, Joslyn L., Inamdar, Sahil, Yang, Yi, Dutta, Subhadeep, Wankhede, Mamta, Shi, Xiaojian, Gu, Haiwei, Green, Matthew, Rege, Kaushal, Curtis, Marion, and Acharya, Abhinav P. Mon .  
"Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism".  United States.  https://doi.org/10.1039/d0tb00790k.  https://www.osti.gov/servlets/purl/1638930.

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@article{osti_1638930,

  title        = {Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism},

  author       = {Mangal, Joslyn L. and Inamdar, Sahil and Yang, Yi and Dutta, Subhadeep and Wankhede, Mamta and Shi, Xiaojian and Gu, Haiwei and Green, Matthew and Rege, Kaushal and Curtis, Marion and Acharya, Abhinav P.},

  abstractNote = {Metabolites control immune cell functions, and delivery of these metabolites in a sustained manner may be able to modulate function of the immune cells. In this study, alpha-ketoglutarate (aKG) and diol based polymeric-microparticles (termed paKG MPs) were synthesized to provide sustained release of aKG and promote an immunosuppressive cellular phenotype. Notably, after association with dendritic cells (DCs), paKG MPs modulated the intracellular metabolic-profile/pathways, and decreased glycolysis and mitochondrial respiration in vitro. These metabolic changes resulted in modulation of MHC-II, CD86 expression in DCs, and altered the frequency of regulatory T cells (Tregs), and T-helper type-1/2/17 cells in vitro. In conclusion, this unique strategy of intracellular delivery of key-metabolites in a sustained manner provides a new direction in immunometabolism field-based immunotherapy with potential applications in different diseases associated with immune disorders.},

  doi          = {10.1039/d0tb00790k},

  journal      = {Journal of Materials Chemistry. B},

  number       = 24,

  volume       = 8,

  place        = {United States},

  year         = {Mon May 11 00:00:00 EDT 2020},

  month        = {Mon May 11 00:00:00 EDT 2020}

}

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https://doi.org/10.1039/d0tb00790k

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Similar Records

Title: Metabolite releasing polymers control dendritic cell function by modulating their energy metabolism

Abstract

Citation Formats

α-ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming journal, July 2017

Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons journal, November 2010

Fibroblasts Mobilize Tumor Cell Glycogen to Promote Proliferation and Metastasis journal, January 2019

Weight control interventions improve therapeutic efficacy of dacarbazine in melanoma by reversing obesity-induced drug resistance journal, December 2016

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Quantitative Method to Investigate the Balance between Metabolism and Proteome Biomass: Starting from Glycine journal, November 2016

Rationale, Feasibility and Acceptability of Ketogenic Diet for Cancer Treatment journal, September 2017

The microbial metabolite desaminotyrosine protects from influenza through type I interferon journal, August 2017

Metabolic signatures of T-cells and macrophages in rheumatoid arthritis journal, June 2017

Downregulation of L-arginine metabolism in dendritic cells induces tolerance to exogenous antigen journal, January 2017

Targeted metabolic profiling of wounds in diabetic and nondiabetic mice: Wound metabolic profiling journal, May 2015

Suppression of insulin feedback enhances the efficacy of PI3K inhibitors journal, July 2018

Metabolic reprogramming in macrophages and dendritic cells in innate immunity journal, June 2015

Mitochondrial Dysfunction Prevents Repolarization of Inflammatory Macrophages journal, October 2016

Srebp-controlled glucose metabolism is essential for NK cell functional responses journal, September 2017

Glucose Oxidation Is Critical for CD4 + T Cell Activation in a Mouse Model of Systemic Lupus Erythematosus journal, November 2015

Shape Induced Inhibition of Phagocytosis of Polymer Particles journal, June 2008

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Regulation of immune responses by L-arginine metabolism journal, August 2005

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Adhesive substrate-modulation of adaptive immune responses journal, December 2008

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Daily red wine vinegar ingestion for eight weeks improves glucose homeostasis and affects the metabolome but does not reduce adiposity in adults journal, January 2019

A high-throughput microparticle microarray platform for dendritic cell-targeting vaccines journal, September 2009

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Enhanced glycolysis contributes to the pathogenesis of experimental autoimmune neuritis journal, February 2018

3-bromopyruvate ameliorate autoimmune arthritis by modulating Th17/Treg cell differentiation and suppressing dendritic cell activation journal, February 2017

Dendritic cell metabolism journal, December 2014

Metabolic control of TH17 and induced Treg cell balance by an epigenetic mechanism journal, August 2017

Epidermal T Cells and Wound Healing journal, May 2010

α-ketoglutarate orchestrates macrophage activation through metabolic and epigenetic reprogramming
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Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons
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Fibroblasts Mobilize Tumor Cell Glycogen to Promote Proliferation and Metastasis
journal, January 2019

Weight control interventions improve therapeutic efficacy of dacarbazine in melanoma by reversing obesity-induced drug resistance
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Rationale, Feasibility and Acceptability of Ketogenic Diet for Cancer Treatment
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The microbial metabolite desaminotyrosine protects from influenza through type I interferon
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Metabolic signatures of T-cells and macrophages in rheumatoid arthritis
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Downregulation of L-arginine metabolism in dendritic cells induces tolerance to exogenous antigen
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Targeted metabolic profiling of wounds in diabetic and nondiabetic mice: Wound metabolic profiling
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Suppression of insulin feedback enhances the efficacy of PI3K inhibitors
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Metabolic reprogramming in macrophages and dendritic cells in innate immunity
journal, June 2015

Mitochondrial Dysfunction Prevents Repolarization of Inflammatory Macrophages
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Srebp-controlled glucose metabolism is essential for NK cell functional responses
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Glucose Oxidation Is Critical for CD4 ⁺ T Cell Activation in a Mouse Model of Systemic Lupus Erythematosus
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Shape Induced Inhibition of Phagocytosis of Polymer Particles
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journal, December 2015

Database-Assisted Globally Optimized Targeted Mass Spectrometry (dGOT-MS): Broad and Reliable Metabolomics Analysis with Enhanced Identification
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Regulation of immune responses by L-arginine metabolism
journal, August 2005

Impaired Epidermal to Dendritic T Cell Signaling Slows Wound Repair in Aged Skin
journal, November 2016

Adhesive substrate-modulation of adaptive immune responses
journal, December 2008

Deregulated Myc Requires MondoA/Mlx for Metabolic Reprogramming and Tumorigenesis
journal, February 2015

The metabolic engine of endothelial cells
journal, September 2019

Coccidioidomycosis Detection Using Targeted Plasma and Urine Metabolic Profiling
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In Vivo Dynamic Monitoring of Small Molecules with Implantable Polymer-Dot Transducer
journal, June 2016

Adhesive substrates modulate the activation and stimulatory capacity of non-obese diabetic mouse-derived dendritic cells
journal, January 2011

TREM2 Maintains Microglial Metabolic Fitness in Alzheimer’s Disease
journal, August 2017

Daily red wine vinegar ingestion for eight weeks improves glucose homeostasis and affects the metabolome but does not reduce adiposity in adults
journal, January 2019

A high-throughput microparticle microarray platform for dendritic cell-targeting vaccines
journal, September 2009

Inhibition of Glycolysis Reduces Disease Severity in an Autoimmune Model of Rheumatoid Arthritis
journal, September 2018

Dendritic cells modulate burn wound healing by enhancing early proliferation: Dendritic cells in wound healing
journal, January 2016

Enhanced glycolysis contributes to the pathogenesis of experimental autoimmune neuritis
journal, February 2018

3-bromopyruvate ameliorate autoimmune arthritis by modulating Th17/Treg cell differentiation and suppressing dendritic cell activation
journal, February 2017

Dendritic cell metabolism
journal, December 2014

Metabolic control of TH17 and induced Treg cell balance by an epigenetic mechanism
journal, August 2017

Epidermal T Cells and Wound Healing
journal, May 2010