Introduction
Tuberculosis (TB) remains a leading cause of morbidity and mortality worldwide. Individuals with type 2 diabetes (T2D) are at increased risk of developing active TB, tend to present with more severe disease and experience adverse treatment outcomes compared to individuals without T2D co-morbidity. However, the underlying mechanisms responsible for increased susceptibility of T2D patients to TB remain poorly understood.
Objectives
We investigated whether immune dysfunction at the site of infection - the lung - contributes to TB susceptibility in T2D patients.
Methods
We performed bronchoscopies and collected bronchoalveolar lavage fluid (BAL) from TB contacts with and without T2D in South Africa and obtained paired human alveolar macrophages (HAMs) and monocyte-derived macrophages (MDMs) for transcriptomic, epigenetic and functional assays.
Results
Following ex vivo infection with Mycobacterium tuberculosis (Mtb), T2D-HAMs had increased Mtb fold growth and elevated TNF production. BAL fluid from T2D patients contained fewer neutrophils, with neutrophil frequency inversely correlating with Mtb growth in HAMs. Both T2D-HAMs and T2D-MDMs expressed less CD32 compared to control cells, with T2D patients having fewer M1-like MDMs. Mtb-induced gene expression in T2D-HAMs was delayed, but genes involved in negative regulation of neutrophil migration were upregulated, consistent with the reduced neutrophil recruitment to the lung. Epigenetic profiling revealed hypermethylation in T2D-HAM DNA compared to control HAMs, except for hypomethylated TNF signaling genes, aligning with increased TNF production.
Conclusion
Our findings demonstrate that T2D alters early HAM responses to Mtb, characterized by delayed gene transcription, epigenetically driven cytokine dysregulation and impaired neutrophil recruitment – collectively facilitating enhanced Mtb growth. This study provides the first comprehensive investigation of the diabetic HAM phenotype in the context of recent TB exposure, offering mechanistic insights into the increased TB susceptibility observed in T2D patients.