PMC:7565665 / 41681-48225 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7565665","sourcedb":"PMC","sourceid":"7565665","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7565665","text":"5. Autophagy-Mediated CFTR and Immune Response Dysfunction\nThe genetic loss of CFTR or a decrease in its expression and/or activity due to environmental insults such as CS leads to autophagy dysfunction. An investigation of CFTR-deficient mice or cells isolated from CF subjects revealed an intrinsic defect in autophagy in the absence of CFTR, and the mechanism of defective CFTR-mediated autophagy impairment via the ROS-TG2-Beclin-1 pathway is well established [22,42,53,150]. Supporting studies demonstrate that autophagy augmentation restores CS-induced CFTR dysfunction, inflammatory-oxidative stress, ceramide accumulation, and COPD-emphysema pathogenesis by rescuing aggresome-bound mutant ΔF508-CFTR to the plasma membrane (PM) [22,35]. Conversely, restoring CFTR levels by S-nitrosoglutathione (GSNO) augmentation corrects CS-induced autophagy dysfunction, inflammatory-oxidative stress and COPD-emphysema features [62]. These findings not only highlight the intricate relationship between CFTR and autophagy but also provide a unique therapeutic opportunity to control exacerbations and chronic lung disease progression. Several reports have suggested that the inherently elevated inflammatory-oxidative stress in CF cells, primarily due to activated NFκB signaling, could be dampened by autophagy augmentation [124,160]. Moreover, it’s conceivable that CFTR dysfunction leads to impaired pathogen clearance, as the autophagy-mediated degradation of both intracellular and extracellular pathogens (xenophagy) is well demonstrated [35,45,58,151,161]. An alternate mechanism called LC3-associated phagocytosis (LAP) is also described, which is similar to the normal macroautophagy pathway but does not involve the formation of a double membrane autophagosome [7,162]. Nonetheless, LAP assists in the processing of both intracellular and extracellular pathogens, through the recruitment of LC3 to the phagosomal membrane and subsequent delivery to lysosomes for terminal degradation [7,151,162].\nAutophagy per se plays a very crucial role in regulating innate and adaptive immunity both in normal conditions and in response to pathogen challenges. Autophagy directly governs key aspects of the innate immune activation, including the secretion of inflammatory mediators, such as cytokines, which are essential to combat different microbial pathogens [7,8,9,84]. The “inflammasome” is a cytoplasmic multiprotein complex that detects pathogenic microorganisms or other cellular stresses and activates potent pro-inflammatory cytokines such as IL-1β and IL-18 [87,133]. Although inflammasome activation is an early innate response to protect the host, its prolonged activation can lead to severe hyperinflammation and tissue injury [47,130]. Recent studies suggest that autophagy is a negative regulator of inflammasome activation as a deficiency of autophagy components such as LC3B or Beclin-1 promotes NLRP3-dependent inflammasome activation [47,130,133]. Apart from its regulation of inflammasome, autophagy also suppresses the overactivation of other inflammation-inducing factors such as NFκB, suggesting a general protective role of autophagy in keeping a check of uncontrolled innate immune activation that may contribute to lung injury [11,37,38,54,55]. In the adaptive immune system, functional autophagy is required for the survival, development, maturation, and function of immune cells such as CD4+ T cells, CD8+ T cells, B cells, neutrophils, and monocytes [7,9,84,163,164,165]. Moreover, in dendritic cells (DC’s), antigen processing and presentation to MHC-II is dependent on the autophagic generation of suitable peptides [9,20,88,163,164,165]. Additionally, antigen presentation to CD8+ T cells on MHC-I is also dependent on autophagy, thus implicating its indispensable role in generating an adequate immune response to bacterial and viral pathogens [163,164,165]. Hence, autophagy promotes adequate antigen presentation to T cells in numerous infection models, thereby facilitating a robust adaptive immune response and further demonstrating the necessary functional role autophagy plays in infections.\nThe lack of functional CFTR in macrophages results in an increased production of inflammatory cytokines, and impaired pathogen clearance capacity. The diminished expression of HLA-DQ and HLA-DR (MHC-II molecules) on monocytes derived from ΔF508-CFTR homozygous CF subjects [166], might explain the impaired pathogen clearance ability of CF macrophages. In addition, CFTR deficiency has been implicated in diminished Treg effector function and a more pronounced Th2-biased immune response [167]. The CF defect has also been shown to affect the activation of neutrophils [168], which are the cells responsible for the first line of defense in the airways. Although, airway epithelial cells and lung-resident macrophages sense the invading pathogens and secrete a plethora of factors to induce the recruitment and activation of neutrophils, neutrophils from CF subjects have diminished phagocytic potentials by virtue of the reduced cell surface expression of toll-like receptors (TLRs) and disrupted chloride transport to the phagolysosome [169,170]. Thus the CFTR mutation in CF results in impaired bacterial killing [171]. Moreover, CF neutrophils also demonstrate an increased capacity to release their primary granule contents such as MPO and neutrophil elastase (NE). The uncontrolled release of these enzymes causes lung tissue damage and severe airway inflammation. We have shown that P. aeruginosa LPS-induced MPO levels can be reduced by treatment with the histone deacetylase (HDAC) inhibitor, suberoylanilide hydroxamic acid (SAHA), plausibly by restoring the trafficking of ΔF508-CFTR, suggesting that a functional CFTR is required to keep a tab on uncontrolled neutrophil activation [172]. Mechanistically, an absence or dysfunction of CFTR in neutrophils results in the deactivation of the guanosine triphosphate (GTP)-binding protein Rab27a, which causes impaired granule exocytosis [168,172]. Several studies now agree that the pharmacological inhibition of CFTR or the mutant ΔF508-CFTR is sufficient to cause deregulated neutrophil activation via the activation of the NFκB pathway, resulting in hyperinflammation [172].\nTherefore, autophagy and CFTR share an intimate relationship in terms of regulating the immune response against infections. Moreover, the rescue of mutant CFTR to the PM corrects the autophagy-mediated immune dysfunction, controlling chronic lung disease pathogenesis (Figure 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