PMC:7565665 / 1886-12378 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":"1. Introduction\nChronic obstructive and restrictive lung diseases are among the leading causes of mortality worldwide, where acute or recurrent episodes of respiratory exacerbations are not only responsible for significant health care costs and a poor quality of life, but also an increased risk of death [1,2,3,4]. The airway mucosa is a primary route of entry for pathogenic microorganisms (bacteria, virus and/or fungi) and represents an important barrier in preventing the entry of these infectious organisms. In the event that the pathogen evades this mucociliary defense mechanism, the airway epithelial cells utilize complex pathogen clearance mechanisms to restrict the life-threatening exacerbations, where these cells work in collaboration with our immune system, involving both innate and adaptive responses, to launch a robust immune response against the invading pathogens, which if successful, results in pathogen elimination or clearance. Thus, providing proof-of-concept evidence in support of autophagy augmentation strategies for alleviating respiratory exacerbations in chronic obstructive pulmonary disease (COPD), cystic fibrosis (CF), acute lung injury (ALI), acute respiratory distress syndrome (ARDS), and coronavirus disease-2019 (COVID-19).\nA plethora of studies have identified the “autophagy-lysosome pathway”, a major cellular degradation system, as one of the important mechanisms involved in regulating the immune-mediated pathogen clearance mechanisms in several infection models [5,6,7]. Evidence suggests that a specific form of autophagy, called “xenophagy”, is responsible for the elimination of bacterial, viral or fungal pathogens [7,8,9,10]. In general, autophagy (mainly macroautophagy) is one of the two components of the cellular homeostatic machinery called the “proteostasis network (PN)” [11,12,13,14], which could be termed as the “master regulator of cellular well-being”, as it regulates all the processes involved in protein turnover in the cell. The other component of the PN is the ubiquitin-proteasome system (UPS), which deals primarily with the degradation of cellular proteins [15,16,17,18,19] which allows protein turnover and a replacement of misfolded proteins, as well as the regulation of vital regulatory proteins involved in a variety of cellular homeostatic processes. In contrast, the autophagy-lysosome pathway can handle the degradation of much broader and larger cargo, such as protein aggregates, lipids, damaged organelles, or infectious agents such as bacteria and viruses [9,20,21,22,23,24]. These two components of the PN play a vital role in maintaining cellular homeostasis by facilitating the removal of these dysfunctional cellular components while maintaining or replenishing the levels of proteins, lipids, etc., via synthetic machinery. Other proteostatic mechanisms include the unfolded protein response (UPR), small ubiquitin-like modifier (SUMO), and the endoplasmic reticulum (ER)-associated degradation (ERAD) pathways. Both SUMO and ERAD have a role in the trafficking of the misfolded cystic fibrosis transmembrane conductance regulator (CFTR), which is the dysfunctional protein responsible for the pathogenesis of CF [25,26]. Furthermore, the dysregulation of UPR has been shown to lead to an exaggerated inflammatory response that plays a role in CF pathogenesis progression and exacerbations [27]. Therefore, it is evident that any dysregulation of the PN components leads to severe life-threatening diseases that includes proteinopathies, neurodegenerative diseases, age-related disorders, and chronic respiratory diseases such as CF and COPD [11,13,15,28,29,30].\nRespiratory infections serve as a trigger for disease exacerbation, while exposure to tobacco, biomass smoke, and aging, are the leading causes for COPD-emphysema development and progression [4,31,32,33]. We and others have demonstrated that autophagy impairment is the key central mechanism for tobacco, biomass smoke or e-cigarette vapor (eCV) exposure and the age-related induction of inflammatory-oxidative stress, alveolar apoptosis and senescence, leading to COPD-emphysema pathogenesis and progression [33,34,35,36,37,38,39]. Additionally, the above-described causative mechanisms also hamper the pathogen clearance, and thus make the individual more prone to acute or recurrent respiratory infections or exacerbations [35,39,40]. Mechanistically, cigarette smoke (CS)-induced phagocytosis defects involves autophagy impairment, which blunts the clearance and promotes the survival of disease-causing pathogens, thereby facilitating chronic infections or recurrent exacerbations [34,35,36].\nIn addition, we recently demonstrated that exposure to CS and other noxious environmental agents promotes accelerated lung aging, which is another important factor contributing to increased infections in chronic lung disease subjects [33]. In fact, aging per se is responsible for an increased risk of pulmonary infections due to the decline of immunity. Notably, the PN and autophagy are known to decrease over time with age, and therefore, serve a crucial role in determining the increased risk of lung infections in the elderly, by virtue of hampered pathogen clearance mechanisms [13,41]. Therefore, several studies, including our recent reports, demonstrate the therapeutic potential of novel autophagy augmentation strategies for controlling COPD-emphysema pathogenesis and progression [22,42,43].\nAutophagy plays a crucial role in the elimination of pathogens, and the pharmacological disruption of autophagy has been shown to impair host defense against Pseudomonas aeruginosa (P. aeruginosa), while the induction of autophagy facilitates P. aeruginosa clearance from murine lungs [5,44,45].\nAdditionally, autophagy-related 7 (ATG7)-dependent autophagy is reported to have a significant role in murine host resistance to Klebsiella pneumoniae, an important respiratory track pathogen [46]. Similarly, during a pulmonary infection with Chlamydia pneumoniae in mice, autophagy restricts inflammasome activation, while mice deficient in autophagy demonstrate an increased mortality, highlighting the protective role of autophagy [47]. Immunity against viral infections in the airways is also regulated by autophagy. For example, autophagy deficiency promotes interleukin (IL)-17-mediated lung pathology in mice infected with respiratory syncytial virus (RSV) [48]. Furthermore, a recent study demonstrates that IL-22 inhibits RSV production by blocking the virus-mediated suppression of cellular autophagy [49]. Moreover, recent studies on Middle East respiratory syndrome (MERS) coronavirus [50] provide proof-of-concept evidence on the therapeutic potential of autophagy modulating drugs for combating the SARS-COV2 infection, cytokine storm, and pathogenesis of severe ARDS-like COVID-19 fatal lung disease.\nAnother elaborately studied example where autophagy regulates inflammatory-oxidative stress, inflammation, and infection-mediated disease exacerbations is CF. CF is a genetic disorder, wherein the ΔF508-CFTR is the most common mutation leading to lack of membrane-resident functional CFTR, where the absence of the functional CFTR on the plasma membrane (PM) deteriorates the pathogen clearance ability in CF subjects, leading to persistent infections and chronic inflammation, culminating into a catastrophic lung function decline [51,52,53]. Studies in CF cell lines and knockout mice suggest that the absence of CFTR by itself is sufficient to promote a pro-inflammatory milieu, at least in part, by the activation of nuclear factor kappa-light-chain-enhancer of activated B cells (NFκB) signaling [54,55,56,57]. Moreover, a transient transfection of wild type (WT)-CFTR reduced tumor necrosis factor α (TNFα)-mediated NFκB activation, confirming the anti-inflammatory role of CFTR [55]. Furthermore, a P. aeruginosa infection in CF mice leads to a more pronounced NFκB-mediated inflammatory response and pathogenesis of CF-related lung disease [51,58]. Thus, membrane-resident functional CFTR is demonstrated to be a critical regulator of innate and adaptive immune responses, in addition to its classical role as an ion transporter.\nA recent comprehensive article summarizes the role of dysfunctional CFTR in the controlling cellular signaling pathways used by innate immune cells for combating infections such as airway epithelial cells, neutrophils, monocytes, and macrophages [59]. Additionally, we and others have shown a clear role of membrane-CFTR in regulating the function of adaptive immune cells, such as CD3+ T cells, CD4+ T cells, CD4+FoxP3+ regulatory T cells (T regs), and B cells [59]. A recent intriguing study found that CFTR dysfunction in platelets leads to aberrant transient receptor potential cation channel subfamily C member 6 (TRPC6)-dependent platelet activation, which was proposed as a major driver of CF-lung inflammation and impaired bacterial clearance [60].\nThus, autophagy plays a vital role in limiting lung infections, and it is evident that a complete or partial absence of functional CFTR leads to autophagy impairment. Mechanistically, CFTR loss or dysfunction results in the reactive oxygen species (ROS)-mediated activation of transglutaminase-2 (TGM-2), and inactivation of the Beclin-1 complex, thereby causing autophagy impairment [61]. Apart from the genetic loss or dysfunction of CFTR, exposure to CS also leads to decreased CFTR activity and expression in vitro, in animal models and in smokers with or without COPD, primarily via ROS-dependent mechanisms [22,42,62,63]. This acquired CFTR dysfunction results in increased inflammatory-oxidative stress, apoptosis, cellular senescence, defective autophagy, and impaired mucociliary clearance, all hallmarks of COPD.\nTo summarize, we and others have demonstrated that autophagy augmentation has the potential to not only control CFTR dysfunction-mediated pathologies in CF and COPD, but also allows the clearance of opportunistic infections while balancing immune regulation to avoid recurrent exacerbations and disease progression. This provides a potential to tailor autophagy augmentation for acute and respiratory exacerbations in CF, COPD, ALI/ARDS and COVID-19, etc. Hence, we focus here on the role of autophagy in pulmonary infections and immune dysfunction, where the therapeutic potential of novel autophagy augmenting strategies to alleviate lung disease pathogenesis and respiratory exacerbations is 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