Awadhesh K Arya, Kinjal Sethuraman, Jaylyn Waddell, Abid R Bhat, Zuha Imtiyaz, Deepa Walia, Yuanyuan Liang, Yong Sung Cha, Yoonsuk Lee, Siamak Moayedi, Douglas Sward, Stephen R Thom
Immune mediators are elevated due to carbon monoxide (CO) poisoning but their role in the development of neurological deficits is unknown. Circulating microparticles (MPs) are elevated in response to CO and correlate with the development of neurological complications. We hypothesized that interleukin (IL)-1β is carried by MPs and contributes to the development of neurological sequelae (NS). Blood-borne IL-1β in CO-poisoned patients is almost exclusively carried by MPs. Healthy humans have 0.8 ± 0.8 (n = 27) MPs/μL bearing IL-1β on the membrane surface. IL-1β-bearing MPs obtained from patients at the time of CO poisoning diagnosis who recover (Global Deterioration Score [GDS] = 1 at 1 month) numbered 35 ± 12/μL (n = 27, p < 0.001 vs. control) and patients who sustained NS (GDS > 1 at 1 month) had 75 ± 38/μL (n = 27; p < 0.001 vs. control and CO-recovered groups). Twice as many MPs carry IL-1β cargo as express surface-bearing IL-1β. The concentration is higher post-CO but does not correlate with NS. Those with NS have 43.8 ± 42.0 pg IL-1β /106 MPs, and those with GDS = 1 have 33.0 ± 32.0 pg/106 MPs, versus controls 5.4 ± 0.3 pg/106 MPs, p < 0.001. In a murine CO model, MPs IL-1β cargo follows similar proportions to humans. Pharmacologic blockade of IL-1β using an IL-1 receptor antagonist or neutralizing anti-IL-1β antibody inhibited neuroinflammation and preserved neurological function. Results demonstrate that brain-derived MPs liberated via the glymphatic system to the peripheral circulation activate neutrophils which are the prime generators of IL-1β-bearing MPs that maintain a cycle of neuroinflammation. Targeting IL-1β disrupts MP-mediated inflammation.