Mitochondria: An Integrative Hub Coordinating Circadian Rhythms, Metabolism, the Microbiome, and Immunity

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2020 Mar 3

PMID 32117978

Citations 25

Authors

Bruno A Aguilar-Lopez

Maria Maximina Bertha Moreno-Altamirano

Hazel M Dockrell

Michael R Duchen

Francisco Javier Sanchez-Garcia

Affiliations

Soon will be listed here.

Abstract

There is currently some understanding of the mechanisms that underpin the interactions between circadian rhythmicity and immunity, metabolism and immune response, and circadian rhythmicity and metabolism. In addition, a wealth of studies have led to the conclusion that the commensal microbiota (mainly bacteria) within the intestine contributes to host homeostasis by regulating circadian rhythmicity, metabolism, and the immune system. Experimental studies on how these four biological domains interact with each other have mainly focused on any two of those domains at a time and only occasionally on three. However, a systematic analysis of how these four domains concurrently interact with each other seems to be missing. We have analyzed current evidence that signposts a role for mitochondria as a key hub that supports and integrates activity across all four domains, circadian clocks, metabolic pathways, the intestinal microbiota, and the immune system, coordinating their integration and crosstalk. This work will hopefully provide a new perspective for both hypothesis-building and more systematic experimental approaches.

Citing Articles

The Role of Insulin Within the Socio-Psycho-Biological Framework in Type 2 Diabetes-A Perspective from Psychoneuroimmunology.

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The interplay between mitochondria, the gut microbiome and metabolites and their therapeutic potential in primary mitochondrial disease.

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Vitamin-mediated interaction between the gut microbiome and mitochondria in depression: A systematic review-based integrated perspective.

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Conservation Mitonuclear Replacement: Facilitated mitochondrial adaptation for a changing world.

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Zhao X, Zhang J, Liu J, Chen Q, Cai C, Miao X Aging (Albany NY). 2023; 15(22):12794-12816.

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References

Peng H, Guerau-de-Arellano M, Mehta V, Yang Y, Huss D, Papenfuss T . Dimethyl fumarate inhibits dendritic cell maturation via nuclear factor κB (NF-κB) and extracellular signal-regulated kinase 1 and 2 (ERK1/2) and mitogen stress-activated kinase 1 (MSK1) signaling. J Biol Chem. 2012; 287(33):28017-26. PMC: 3431702. DOI: 10.1074/jbc.M112.383380. View

Baixauli F, Acin-Perez R, Villarroya-Beltri C, Mazzeo C, Nunez-Andrade N, Gabande-Rodriguez E . Mitochondrial Respiration Controls Lysosomal Function during Inflammatory T Cell Responses. Cell Metab. 2015; 22(3):485-98. PMC: 5026297. DOI: 10.1016/j.cmet.2015.07.020. View

Kabat A, Srinivasan N, Maloy K . Modulation of immune development and function by intestinal microbiota. Trends Immunol. 2014; 35(11):507-17. PMC: 6485503. DOI: 10.1016/j.it.2014.07.010. View

Gomez-Cabanas L, Lopez-Cotarelo P, Criado-Garcia O, Murphy M, Boya P, Rodriguez-Fernandez J . Immunological Synapse Formation Induces Mitochondrial Clustering and Mitophagy in Dendritic Cells. J Immunol. 2019; 202(6):1715-1723. DOI: 10.4049/jimmunol.1800575. View

Rescigno M . Intestinal microbiota and its effects on the immune system. Cell Microbiol. 2014; 16(7):1004-13. DOI: 10.1111/cmi.12301. View

Moisoi N, Klupsch K, Fedele V, East P, Sharma S, Renton A . Mitochondrial dysfunction triggered by loss of HtrA2 results in the activation of a brain-specific transcriptional stress response. Cell Death Differ. 2008; 16(3):449-64. DOI: 10.1038/cdd.2008.166. View

Curtis A, Bellet M, Sassone-Corsi P, ONeill L . Circadian clock proteins and immunity. Immunity. 2014; 40(2):178-86. DOI: 10.1016/j.immuni.2014.02.002. View

Castanon-Cervantes O, Wu M, Ehlen J, Paul K, Gamble K, Johnson R . Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol. 2010; 185(10):5796-805. PMC: 2974025. DOI: 10.4049/jimmunol.1001026. View

Peterson B, Campbell J, Ilkayeva O, Grimsrud P, Hirschey M, Newgard C . Remodeling of the Acetylproteome by SIRT3 Manipulation Fails to Affect Insulin Secretion or β Cell Metabolism in the Absence of Overnutrition. Cell Rep. 2018; 24(1):209-223.e6. PMC: 6093627. DOI: 10.1016/j.celrep.2018.05.088. View

10.

Huang B, Gudi R, Wu P, Harris R, Hamilton J, Popov K . Isoenzymes of pyruvate dehydrogenase phosphatase. DNA-derived amino acid sequences, expression, and regulation. J Biol Chem. 1998; 273(28):17680-8. DOI: 10.1074/jbc.273.28.17680. View

11.

Reinke H, Asher G . Crosstalk between metabolism and circadian clocks. Nat Rev Mol Cell Biol. 2019; 20(4):227-241. DOI: 10.1038/s41580-018-0096-9. View

12.

Imai S, Guarente L . It takes two to tango: NAD and sirtuins in aging/longevity control. NPJ Aging Mech Dis. 2017; 2:16017. PMC: 5514996. DOI: 10.1038/npjamd.2016.17. View

13.

Shen X, Peter E, Bir S, Wang R, Kevil C . Analytical measurement of discrete hydrogen sulfide pools in biological specimens. Free Radic Biol Med. 2012; 52(11-12):2276-83. PMC: 4413934. DOI: 10.1016/j.freeradbiomed.2012.04.007. View

14.

Dudek-Wicher R, Junka A, Bartoszewicz M . The influence of antibiotics and dietary components on gut microbiota. Prz Gastroenterol. 2018; 13(2):85-92. PMC: 6040098. DOI: 10.5114/pg.2018.76005. View

15.

Chang P, Hao L, Offermanns S, Medzhitov R . The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A. 2014; 111(6):2247-52. PMC: 3926023. DOI: 10.1073/pnas.1322269111. View

16.

Prochnicki T, Latz E . Inflammasomes on the Crossroads of Innate Immune Recognition and Metabolic Control. Cell Metab. 2017; 26(1):71-93. DOI: 10.1016/j.cmet.2017.06.018. View

17.

Kespohl M, Vachharajani N, Luu M, Harb H, Pautz S, Wolff S . The Microbial Metabolite Butyrate Induces Expression of Th1-Associated Factors in CD4 T Cells. Front Immunol. 2017; 8:1036. PMC: 5581317. DOI: 10.3389/fimmu.2017.01036. View

18.

Sulen A, Gullaksen S, Bader L, McClymont D, Skavland J, Gavasso S . Signaling effects of sodium hydrosulfide in healthy donor peripheral blood mononuclear cells. Pharmacol Res. 2016; 113(Pt A):216-227. DOI: 10.1016/j.phrs.2016.08.018. View

19.

Mollica M, Raso G, Cavaliere G, Trinchese G, De Filippo C, Aceto S . Butyrate Regulates Liver Mitochondrial Function, Efficiency, and Dynamics in Insulin-Resistant Obese Mice. Diabetes. 2017; 66(5):1405-1418. DOI: 10.2337/db16-0924. View

20.

Schloder J, Berges C, Luessi F, Jonuleit H . Dimethyl Fumarate Therapy Significantly Improves the Responsiveness of T Cells in Multiple Sclerosis Patients for Immunoregulation by Regulatory T Cells. Int J Mol Sci. 2017; 18(2). PMC: 5343807. DOI: 10.3390/ijms18020271. View