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The molecular programs underpinning 'tolerance' and 'resistance' in health and viral infection

ABSTRACT: The molecular programs underpinning 'tolerance' and 'resistance' in health and viral infection

PROVIDER: PRJNA728967 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR14510500.fastq.gz	Fastqsanger.gz
	SRR14510600.fastq.gz	Fastqsanger.gz
	SRR14510501.fastq.gz	Fastqsanger.gz
	SRR14510601.fastq.gz	Fastqsanger.gz
	SRR14510502.fastq.gz	Fastqsanger.gz

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The molecular programs underpinning ‘tolerance’ and ‘resistance’ in health and viral infection

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The molecular programs underpinning 'tolerance' and 'resistance' in health and viral infection

Project description:The immune protection against invading pathogens is governed by pathogen elimination (‘resistance’) and by limitation of tissue damage that results from host-pathogen interactions (‘tolerance’). However, distinct molecular states of resistance and tolerance remain obscure. Here, we collected longitudinal lung transcriptomes and clinical phenotypes of disease severity during influenza A virus (IAV) infection across 39 genetically-distinct mouse strains (32 strains of time series data and additional 7 strains with selected time points). Using transcriptional diversity in this data, we uncovered two key programs that together describe the cellular states for resistance and tolerance. The identified programs offer an unprecedented comprehensive view on shared and distinct roles of resistance and tolerance for the regulation of immune defense – for instance, we identified an antagonistic regulation of resistance and tolerance on protein production. Importantly, the framework reveals that both inflammatory states and the healthy steady state are remarkably diverse in resistance and tolerance levels, with implications on disease severity: a baseline state (before infection) of high tolerance and low resistance results in increased severity of IAV infection. Overall, our work provides a framework for the study of resistance and tolerance that could aid in clinical diagnosis and disease management.

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Project description:Tissues are exposed to diverse inflammatory challenges that shape future inflammatory responses. While cellular metabolism regulates immune function, how metabolism programs and stabilizes immune states within tissues and tunes susceptibility to inflammation is poorly understood. Here, we describe an innate immune metabolic switch that programs long-term intestinal tolerance. Intestinal interleukin-18 (IL-18) stimulation elicited tolerogenic macrophages by preventing their proinflammatory glycolytic polarization via metabolic reprogramming to fatty acid oxidation (FAO). FAO reprogramming was triggered by IL-18 activation of SLC12A3 (NCC), leading to sodium influx, release of mitochondrial DNA, and activation of stimulator of interferon genes (STING). FAO was maintained in macrophages by a bistable switch that encoded memory of IL-18 stimulation and by intercellular positive feedback that sustained the production of macrophage-derived 2'3'-cyclic GMP-AMP (cGAMP) and epithelial-derived IL-18. Thus, a tissue-reinforced metabolic switch encodes durable immune tolerance in the gut and may enable reconstructing compromised immune tolerance in chronic inflammation.

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