Ionic mitigation of CD4


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
04 02 2022
Historique:
received: 08 10 2021
accepted: 24 12 2021
entrez: 5 2 2022
pubmed: 6 2 2022
medline: 11 3 2022
Statut: epublish

Résumé

T helper (Th) cells provide immunity to pathogens but also contribute to detrimental immune responses during allergy and autoimmunity. Th2 cells mediate asthmatic airway inflammation and Th1 cells are involved in the pathogenesis of multiple sclerosis. T cell activation involves complex transcriptional networks and metabolic reprogramming, which enable proliferation and differentiation into Th1 and Th2 cells. The essential trace element zinc has reported immunomodulatory capacity and high zinc concentrations interfere with T cell function. However, how high doses of zinc affect T cell gene networks and metabolism remained so far elusive. Herein, we demonstrate by means of transcriptomic analysis that zinc aspartate (UNIZINK), a registered pharmaceutical infusion solution with high bioavailability, negatively regulates gene networks controlling DNA replication and the energy metabolism of murine CD3/CD28-activated CD4

Identifiants

pubmed: 35121767
doi: 10.1038/s41598-022-04827-6
pii: 10.1038/s41598-022-04827-6
pmc: PMC8816938
doi:

Substances chimiques

Cell Cycle Proteins 0
Immunomodulating Agents 0
Zinc Compounds 0
Aspartic Acid 30KYC7MIAI
zinc aspartate 4OC7QTI23H

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1943

Informations de copyright

© 2022. The Author(s).

Références

Ruterbusch, M. et al. In vivo CD4(+) T cell differentiation and function: Revisiting the Th1/Th2 paradigm. Annu. Rev. Immunol. 38, 705–725 (2020).
pubmed: 32340571 doi: 10.1146/annurev-immunol-103019-085803
Hammad, H. & Lambrecht, B. N. The basic immunology of asthma. Cell 184(9), 2521–2522 (2021).
pubmed: 33930297 doi: 10.1016/j.cell.2021.04.019
Mattiuzzi, C. & Lippi, G. Worldwide asthma epidemiology: insights from the global health data exchange database. Int. Forum Allergy Rhinol. 10(1), 75–80 (2020).
pubmed: 31645084 doi: 10.1002/alr.22464
Willame, C. et al. Incidence rates of autoimmune diseases in European Healthcare Databases: a contribution of the advance project. Drug Saf. 44(3), 383–395 (2021).
pubmed: 33462778 pmcid: 7892524 doi: 10.1007/s40264-020-01031-1
Anzilotti, C. et al. An essential role for the Zn2+ transporter ZIP7 in B cell development. Nat. Immunol. 20(3), 350–361 (2019).
pubmed: 30718914 pmcid: 6561116 doi: 10.1038/s41590-018-0295-8
Gammoh, N. Z. & Rink, L. Zinc in infection and inflammation. Nutrients 9(6), 624 (2017).
pmcid: 5490603 doi: 10.3390/nu9060624
Haase, H. & Schomburg, L. You’d Better Zinc-Trace Element Homeostasis in Infection and Inflammation. Nutrients 11(9), 2078 (2019).
pmcid: 6770902 doi: 10.3390/nu11092078
Hojyo, S. et al. Zinc transporter SLC39A10/ZIP10 controls humoral immunity by modulating B-cell receptor signal strength. Proc. Natl. Acad. Sci. USA 111(32), 11786–11791 (2014).
pubmed: 25074919 pmcid: 4136588 doi: 10.1073/pnas.1323557111
Kim, B. & Lee, W. W. Regulatory role of zinc in immune cell signaling. Mol. Cells 44(5), 335–341 (2021).
pubmed: 33986184 pmcid: 8175146 doi: 10.14348/molcells.2021.0061
Brooks, W. A. et al. Zinc for severe pneumonia in very young children: Double-blind placebo-controlled trial. Lancet 363(9422), 1683–1688 (2004).
pubmed: 15158629 doi: 10.1016/S0140-6736(04)16252-1
Chasapis, C. T. et al. Recent aspects of the effects of zinc on human health. Arch Toxicol 94(5), 1443–1460 (2020).
pubmed: 32394086 doi: 10.1007/s00204-020-02702-9
Cvijanovich, N. Z. et al. Safety and dose escalation study of intravenous zinc supplementation in pediatric critical illness. JPEN J. Parenter. Enteral. Nutr. 40(6), 860–868 (2016).
pubmed: 25700179 doi: 10.1177/0148607115572193
Perera, M. et al. Randomised controlled trial for high-dose intravenous zinc as adjunctive therapy in SARS-CoV-2 (COVID-19) positive critically ill patients: Trial protocol. BMJ Open 10(12), 580 (2020).
doi: 10.1136/bmjopen-2020-040580
Wessels, I., Rolles, B. & Rink, L. The Potential impact of zinc supplementation on COVID-19 pathogenesis. Front. Immunol. 11, 1712 (2020).
pubmed: 32754164 pmcid: 7365891 doi: 10.3389/fimmu.2020.01712
Guttek, K. et al. Zinc aspartate suppresses proliferation and Th1/Th2/Th17 cytokine production of pre-activated human T cells in vitro. J. Trace Elem. Med. Biol. 49, 86–90 (2018).
pubmed: 29895377 doi: 10.1016/j.jtemb.2018.05.003
Maywald, M., Wessels, I. & Rink, L. Zinc signals and immunity. Int. J. Mol. Sci. 18(10), 1 (2017).
doi: 10.3390/ijms18102222
Rosenkranz, E. et al. Zinc enhances the number of regulatory T cells in allergen-stimulated cells from atopic subjects. Eur. J. Nutr. 56(2), 557–567 (2017).
pubmed: 26589301 doi: 10.1007/s00394-015-1100-1
Sanna, A. et al. Zinc status and autoimmunity: A systematic review and meta-analysis. Nutrients 10(1), 68 (2018).
pmcid: 5793296 doi: 10.3390/nu10010068
Seo, H. M. et al. Serum zinc status and its association with allergic sensitization: The Fifth Korea national health and nutrition examination survey. Sci. Rep. 7(1), 12637 (2017).
pubmed: 28974756 pmcid: 5626772 doi: 10.1038/s41598-017-13068-x
Stoye, D. et al. Zinc aspartate suppresses T cell activation in vitro and relapsing experimental autoimmune encephalomyelitis in SJL/J mice. Biometals 25(3), 529–539 (2012).
pubmed: 22350510 doi: 10.1007/s10534-012-9532-z
Almeida, L. et al. Metabolic pathways in T cell activation and lineage differentiation. Semin. Immunol. 28(5), 514–524 (2016).
pubmed: 27825556 doi: 10.1016/j.smim.2016.10.009
Buck, M. D., O’Sullivan, D. & Pearce, E. L. T cell metabolism drives immunity. J. Exp. Med. 212(9), 1345–1360 (2015).
pubmed: 26261266 pmcid: 4548052 doi: 10.1084/jem.20151159
Slack, M., Wang, T. & Wang, R. T cell metabolic reprogramming and plasticity. Mol. Immunol. 68, 507–512 (2015).
pubmed: 26277274 pmcid: 4679442 doi: 10.1016/j.molimm.2015.07.036
Vaeth, M. et al. Store-operated Ca(2+) entry controls clonal expansion of T cells through metabolic reprogramming. Immunity 47(4), 664–679 (2017).
pubmed: 29030115 pmcid: 5683398 doi: 10.1016/j.immuni.2017.09.003
Reinhold, D. et al. Zinc aspartate induces IL-16 secretion and apoptosis in human T cells. Biomedicines 9(3), 1 (2021).
doi: 10.3390/biomedicines9030246
Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28(1), 27–30 (2000).
pubmed: 10592173 pmcid: 102409 doi: 10.1093/nar/28.1.27
Dimova, D. K. & Dyson, N. J. The E2F transcriptional network: Old acquaintances with new faces. Oncogene 24(17), 2810–2826 (2005).
pubmed: 15838517 doi: 10.1038/sj.onc.1208612
Lei, M. The MCM complex: Its role in DNA replication and implications for cancer therapy. Curr. Cancer Drug Targets 5(5), 365–380 (2005).
pubmed: 16101384 doi: 10.2174/1568009054629654
Satyanarayana, A. & Kaldis, P. Mammalian cell-cycle regulation: Several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28(33), 2925–2939 (2009).
pubmed: 19561645 doi: 10.1038/onc.2009.170
Buck, M. D. et al. Metabolic instruction of immunity. Cell 169(4), 570–586 (2017).
pubmed: 28475890 pmcid: 5648021 doi: 10.1016/j.cell.2017.04.004
Qin, Q. et al. Lisa: inferring transcriptional regulators through integrative modeling of public chromatin accessibility and ChIP-seq data. Genome Biol. 21(1), 32 (2020).
pubmed: 32033573 pmcid: 7007693 doi: 10.1186/s13059-020-1934-6
Delpoux, A. et al. FOXO1 constrains activation and regulates senescence in CD8 T cells. Cell Rep. 34(4), 8674 (2021).
doi: 10.1016/j.celrep.2020.108674
Newton, R. H. et al. Maintenance of CD4 T cell fitness through regulation of Foxo1. Nat. Immunol. 19(8), 838–848 (2018).
pubmed: 29988091 pmcid: 6289177 doi: 10.1038/s41590-018-0157-4
Marchingo, J. M. et al. Quantitative analysis of how Myc controls T cell proteomes and metabolic pathways during T cell activation. Elife 9, 1 (2020).
doi: 10.7554/eLife.53725
Wang, R. et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 35(6), 871–882 (2011).
pubmed: 22195744 pmcid: 3248798 doi: 10.1016/j.immuni.2011.09.021
Gourraud, P. A. et al. The genetics of multiple sclerosis: An up-to-date review. Immunol. Rev. 248(1), 87–103 (2012).
pubmed: 22725956 pmcid: 5967887 doi: 10.1111/j.1600-065X.2012.01134.x
Pividori, M. et al. Shared and distinct genetic risk factors for childhood-onset and adult-onset asthma: Genome-wide and transcriptome-wide studies. Lancet Respir. Med. 7(6), 509–522 (2019).
pubmed: 31036433 pmcid: 6534440 doi: 10.1016/S2213-2600(19)30055-4
Hönscheid, A., Dubben, S., Rink, L. & Haase, H. Zinc differentially regulates mitogen-activated protein kinases in human T cells. J. Nutr. Biochem. 23(1), 18–26 (2012).
pubmed: 21333516 doi: 10.1016/j.jnutbio.2010.10.007
Wong, P. F. & Abubakar, S. High intracellular Zn2+ ions modulate the VHR, ZAP-70 and ERK activities of LNCaP prostate cancer cells. Cell Mol. Biol. Lett. 13(3), p375–p390 (2008).
doi: 10.2478/s11658-008-0009-6
Ishikura, S. et al. The nuclear zinc finger protein Zfat maintains FoxO1 protein levels in peripheral T cells by regulating the activities of autophagy and the Akt signaling pathway. J. Biol. Chem. 291(29), 15282–15291 (2016).
pubmed: 27226588 pmcid: 4946940 doi: 10.1074/jbc.M116.723734
Rosenkranz, E. et al. Induction of regulatory T cells in Th1-/Th17-driven experimental autoimmune encephalomyelitis by zinc administration. J. Nutr. Biochem. 29, 116–123 (2016).
pubmed: 26895672 doi: 10.1016/j.jnutbio.2015.11.010
Kitabayashi, C. et al. Zinc suppresses Th17 development via inhibition of STAT3 activation. Int. Immunol. 22(5), 375–386 (2010).
pubmed: 20215335 doi: 10.1093/intimm/dxq017
Gao, H., Dai, W., Zhao, L., Min, J. & Wang, F. The role of zinc and zinc homeostasis in macrophage function. J. Immunol. Res. 6(2018), 6872621 (2018).
Engelmann, S. et al. T cell-independent modulation of experimental autoimmune encephalomyelitis in ADAP-deficient mice. J. Immunol. 191(10), 4950–4959 (2013).
pubmed: 24101551 doi: 10.4049/jimmunol.1203340
Miller, S. D. & Karpus, W. J. Experimental autoimmune encephalomyelitis in the mouse. Curr. Protoc. Immunol. 15, 1 (2007).
pubmed: 18432984
Laffont, S. et al. Androgen signaling negatively controls group 2 innate lymphoid cells. J. Exp. Med. 214(6), 1581–1592 (2017).
pubmed: 28484078 pmcid: 5461006 doi: 10.1084/jem.20161807
Melgert, B. N. et al. Female mice are more susceptible to the development of allergic airway inflammation than male mice. Clin. Exp. Allergy 35(11), 1496–1503 (2005).
pubmed: 16297148 doi: 10.1111/j.1365-2222.2005.02362.x
Kim, D. I., Song, M. K. & Lee, K. Comparison of asthma phenotypes in OVA-induced mice challenged via inhaled and intranasal routes. BMC Pulm. Med. 19(1), 241 (2019).
pubmed: 31823765 pmcid: 6902567 doi: 10.1186/s12890-019-1001-9
Kujur, W. et al. Caerulomycin A inhibits Th2 cell activity: A possible role in the management of asthma. Sci. Rep. 5, 15396 (2015).
pubmed: 26481184 pmcid: 4612543 doi: 10.1038/srep15396

Auteurs

Anna Krone (A)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Yan Fu (Y)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Simon Schreiber (S)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Johanna Kotrba (J)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Loisa Borde (L)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Aileen Nötzold (A)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Christoph Thurm (C)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Jonas Negele (J)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Tobias Franz (T)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Sabine Stegemann-Koniszewski (S)

Experimental Pneumology, Department of Pneumology, University Hospital Magdeburg/Medical Faculty, Otto-von-Guericke-University, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Jens Schreiber (J)

Experimental Pneumology, Department of Pneumology, University Hospital Magdeburg/Medical Faculty, Otto-von-Guericke-University, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Christoph Garbers (C)

Institute of Pathology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Aniruddh Shukla (A)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.

Robert Geffers (R)

Genome Analytics, Helmholtz-Center for Infection Research (HZI), Braunschweig, Germany.

Burkhart Schraven (B)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Dirk Reinhold (D)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Anne Dudeck (A)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Annegret Reinhold (A)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Andreas J Müller (AJ)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany.
Intravital Microscopy of Infection and Immunity, Helmholtz-Center for Infection Research (HZI), Braunschweig, Germany.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany.

Sascha Kahlfuss (S)

Institute of Molecular and Clinical Immunology, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany. sascha.kahlfuss@med.ovgu.de.
Institute of Medical Microbiology and Hospital Hygiene, Medical Faculty, Otto-von-Guericke University Magdeburg, Magdeburg, Germany. sascha.kahlfuss@med.ovgu.de.
Health Campus Immunology, Infectiology and Inflammation (GCI3), Medical Faculty, Otto-Von-Guericke University Magdeburg, Magdeburg, Germany. sascha.kahlfuss@med.ovgu.de.
Center for Health and Medical Prevention (CHaMP), Otto-von-Guericke-University, Magdeburg, Germany. sascha.kahlfuss@med.ovgu.de.

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