Activation of the innate immune system plays a key role in exacerbations of chronic lung disease, yet the potential role of lung fibroblasts in innate immunity and the identity of epithelial danger signals (alarmins) that may contribute to this process are unclear. The objective of the study was to identify lung epithelial derived alarmins released during endoplasmic reticulum stress (ER stress) and oxidative stress and evaluate their potential to induce innate immune responses in lung fibroblasts. We found that treatment of primary human lung fibroblasts (PHLF) with conditioned media from damaged lung epithelial cells significantly upregulated IL-6, IL-8, MCP-1 and GM-CSF expression (p<0.05). This effect was reduced with anti-IL-1α or IL-1Ra but not anti-IL-1β antibody. Co-stimulation with a TLR3 ligand, Poly I:C, significantly accentuated the IL-1α induced inflammatory phenotype in PHLF, and this effect was blocked with IKK2 and TAKi inhibitors. Finally, Il1r1−/− and Il1a−/− mice exhibit reduced BAL neutrophilia and collagen deposition in response to bleomycin treatment. We conclude that IL-1α plays pivotal role in triggering proinflammatory responses in fibroblasts and this process is accentuated in the presence of dsRNA. This mechanism may be important in the repeated cycles of injury and exacerbation in chronic lung disease.