PMC:7565665 / 53410-58684 JSONTXT

{"target":"http://pubannotation.org/docs/sourcedb/PMC/sourceid/7565665","sourcedb":"PMC","sourceid":"7565665","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7565665","text":"7. CFTR- Autophagy Dysfunction and Pathogenesis of Chronic Obstructive Lung Diseases\nThe homeostatic autophagy process in the airways is prone to dysregulation by a variety of factors such as exposure to first- or second-hand CS [40], eCV [39], biomass smoke [14,43], waterpipe smoke (WPS) [94], wildfire smoke [189], environmental pollution [61], genetic polymorphisms [53,61,149], aging [190], obesity [191,192], and changes in the expression and/or activity of CFTR [22,35,53]. Elevated levels of ROS/RNS ensuing from exposure to the above-described risk factors is the primary driver of autophagy impairment (Figure 1), which is considered a central mechanism for the advent of inflammatory-oxidative stress, cellular senescence, and apoptosis [62,94]. These potentially deleterious changes result in the initiation and progression of COPD-emphysema, as they correlate with the severity of emphysema in COPD subjects [22,33,62]. We and others have demonstrated the important role of transcription factor-EB (TFEB), the master autophagy regulator, in controlling inflammatory-oxidative and immune signaling [34,143,193]. In a relatively recent study, we showed that CS-induced accumulation or trapping of TFEB proteins into perinuclear aggresome bodies prevents it from entering the nucleus and performing its function as an autophagy regulating transcription factor, thereby culminating in autophagy dysfunction [34]. These findings were confirmed in human lung tissue sections from smoker and nonsmoker COPD subjects, where the perinuclear accumulation of TFEB into aggresome bodies increases with emphysema severity [34]. Moreover, smokers showed a more prominent increase in TFEB-aggresome localization as compared to nonsmokers, emphasizing that CS exposure leads to defective autophagy via functional trapping of TFEB into aggresome bodies [34]. It is evident from innumerable studies that a complete loss or decrease in the levels of functional WT-CFTR from the PM due to genetic mutations leads to several deleterious changes in the airways that ultimately results in obstructive lung disease pathogenesis in CF subjects. Specifically, a decrease in/loss of WT-CFTR is causally related to increased ROS-mediated inflammatory-oxidative stress, mucus hypersecretion, elevated ceramide levels, and hampered mucociliary clearance resulting in an increased incident of recurrent and chronic pulmonary infections, all of which result in chronic obstructive pathologies in CF airways [15,51,53,110,194]. It is now well documented that CS exposure [22,40,63,107,108], eCV [39,195], or certain infectious agents [196,197,198] also induce a decrease in the activity or expression of CFTR in the airways and was aptly described as acquired CFTR dysfunction. As expected, CS-induced ROS and the resulting oxidative stress was found to be the main cause of acquired CFTR dysfunction in COPD [62,107,108,109]. Moreover, the mechanistic confirmation of the role of acquired CFTR dysfunction in COPD pathogenesis comes from studies which showed that the pharmacological rescue of mutant CFTR to the PM was able to correct CS-induced inflammatory-oxidative stress, autophagy impairment, and COPD-emphysema pathogenesis [14,42,62]. Another important mechanism which plays a crucial pathogenic role in both CF and COPD-emphysema is ceramide accumulation (Figure 1), and numerous studies have highlighted that a loss or decrease in CFTR and/or CS exposure leads to an increase in ceramide levels [22,52,93,110,182,183,186,188]. Our earlier studies described a direct correlation between a lack of lipid-raft CFTR expression and CS-induced apoptosis along with defective autophagy and the progression of COPD-emphysema via ceramide or lactosylceramide accumulation [93,110]. Lately, we also demonstrated that autophagy augmentation alleviates CS-induced CFTR dysfunction, ceramide accumulation (lipophagy impairment), and resulting COPD-emphysema pathogenesis [22], thus demonstrating that autophagy and CFTR share an interconnected biology crucial for the initiation and progression of chronic lung diseases (Figure 1). We further went on to demonstrate that CS-induced autophagy dysfunction and the dysfunction of its component lipophagy lead to intracellular ceramide accumulation [110]. Meanwhile, acquired CFTR dysfunctions caused ASM activation-dependent membrane ceramide accumulation [22]. The pathogenic role of ceramide has also been implicated in CF lung disease, wherein it mediates the inflammation, apoptosis, and increased susceptibility to P. aeruginosa infection [183,186,199], and is elevated in the airways of CF mice and patients. Mechanistically, it was proven that the ROS-dependent activation of acid sphingomyelinase (ASM) resulted in increased membrane ceramide accumulation [200]. Thus, several ASM inhibitors have been tested and were shown to reduce ceramide accumulation along with resulting infection and inflammation in the lungs of CF mice [186,200]. Therefore, there is strong evidence that CFTR-autophagy dysfunction is a prime factor that promotes multiple host destructive phenomena, including inflammatory-oxidative stress and recurrent infection-related exacerbations, which eventually contribute to chronic obstructive lung disease 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