Smoking changes adaptive immunity with persistent effects

Violaine Saint-André (), Bruno Charbit, Anne Biton, Vincent Rouilly, Céline Possémé, Anthony Bertrand, Maxime Rotival, Jacob Bergstedt, Etienne Patin, Matthew L. Albert, Lluis Quintana-Murci and Darragh Duffy ()
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Violaine Saint-André: Université Paris Cité
Bruno Charbit: Université Paris Cité
Anne Biton: Université Paris Cité, Bioinformatics and Biostatistics Hub
Vincent Rouilly: DATACTIX
Céline Possémé: Université Paris Cité
Anthony Bertrand: Université Paris Cité
Maxime Rotival: Université Paris Cité, CNRS UMR2000, Human Evolutionary Genetics Unit
Jacob Bergstedt: Université Paris Cité, CNRS UMR2000, Human Evolutionary Genetics Unit
Etienne Patin: Université Paris Cité, CNRS UMR2000, Human Evolutionary Genetics Unit
Matthew L. Albert: Octant Biosciences
Lluis Quintana-Murci: Université Paris Cité, CNRS UMR2000, Human Evolutionary Genetics Unit
Darragh Duffy: Université Paris Cité

Nature, 2024, vol. 626, issue 8000, 827-835

Abstract: Abstract Individuals differ widely in their immune responses, with age, sex and genetic factors having major roles in this inherent variability1–6. However, the variables that drive such differences in cytokine secretion—a crucial component of the host response to immune challenges—remain poorly defined. Here we investigated 136 variables and identified smoking, cytomegalovirus latent infection and body mass index as major contributors to variability in cytokine response, with effects of comparable magnitudes with age, sex and genetics. We find that smoking influences both innate and adaptive immune responses. Notably, its effect on innate responses is quickly lost after smoking cessation and is specifically associated with plasma levels of CEACAM6, whereas its effect on adaptive responses persists long after individuals quit smoking and is associated with epigenetic memory. This is supported by the association of the past smoking effect on cytokine responses with DNA methylation at specific signal trans-activators and regulators of metabolism. Our findings identify three novel variables associated with cytokine secretion variability and reveal roles for smoking in the short- and long-term regulation of immune responses. These results have potential clinical implications for the risk of developing infections, cancers or autoimmune diseases.

Date: 2024
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DOI: 10.1038/s41586-023-06968-8

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