Masaya Matsuda, Yuya Sannomiya, Osamu Kaminuma, Takeshi Nabe
Severe asthma is characterized by persistent airway inflammation, irreversible airway remodeling, and reduced responsiveness to glucocorticoids. Subepithelial fibrosis, a major determinant of progressive lung function decline, remains mechanistically undefined. Evidence identifies group 2 innate lymphoid cells (ILC2s) as key contributors to fibrotic airway remodeling. Importantly, ILC2s in severe asthma are not simply increased in number but functionally reprogrammed into a pathogenic, profibrotic state. We summarize evidence for pathogenic ILC2s and discuss three defining properties distinguishing them from homeostatic ILC2s. First, pathogenic ILC2s acquire a fibrogenic phenotype marked by increased IL-13, IL-4, IL-5, and amphiregulin, promoting fibroblast activation and matrix deposition. Second, they exhibit enhanced proliferative capacity driven by cell cycle-related (CDK4/6) and transcriptional (CDK8/19) cyclin-dependent kinases, expanding the pathogenic pool. Third, JAK-STAT5-Bcl-xL and PI3K-Akt-mTORC1 signaling confers resistance to glucocorticoid-induced apoptosis, enabling persistence despite corticosteroid therapy. Together, these properties provide a mechanistic framework linking chronic type 2 inflammation to persistent airway fibrosis. We also discuss therapeutic strategies targeting alarmins, cytokines, CDKs, and steroid-resistance signaling, and highlight open questions on ILC2 heterogeneity. Future single-cell and spatial transcriptomic studies will determine whether these properties arise within a common ILC2 population or distinct subsets, informing precision therapies for severe asthma.