PMC:7346000 / 3893-11059 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7346000","sourcedb":"PMC","sourceid":"7346000","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7346000","text":"2. Immunology\nDissecting the complex pathogenesis of CAPA requires a molecular understanding of the physiological processes whereby infection with SARS-CoV-2 facilitates fungal pathogenesis. Similar to other SARS coronaviruses, SARS-CoV-2 targets and invades epithelial cells and type II pneumocytes through binding of the SARS spike protein to the angiotensin-converting enzyme 2 (ACE2) receptors [11]. Cleavage of the S1/S2 domain by the type 2 transmembrane protease TMPRSS2 leads to the activation of the spike protein [12], thereby facilitating viral entry into the target cell via ACE2. Besides its role as a SARS virus receptor, ACE2 was also demonstrated to be required for protection from severe acute lung injury in ARDS [13]. In support of this, an insertion/deletion polymorphism that affects ACE activity was associated with ARDS susceptibility and outcome [14]. Whether the preceding interaction of SARS-CoV-2 with host cells, by disrupting the regulation of the renin-angiotensin system and or the kallikrein-kinin system, contributes to the development of CAPA, is not known.\nViral entry and infection elicit an immune response, which is initiated by the establishment of an inflammatory cascade by innate immune cells. Although the receptor(s) and signaling pathways involved in the immune recognition of Aspergillus and the downstream production of inflammatory mediators are relatively well characterized [15], not much is known regarding how the immune system senses and responds to SARS-CoV-2. Based on the available knowledge for infections with other coronaviruses, two possible mechanisms can be anticipated and are likely to explain the development of ARDS and consequently CAPA. The first involves the release of danger-associated molecular patterns (DAMPs), signal molecules released by dying or damaged cells that act as endogenous danger signals to promote and exacerbate the immune and inflammatory response leading to lung injury [16]. It is noteworthy that DAMPs have also been shown to regulate inflammation in fungal diseases [17]. The DAMP/receptor for advanced glycation end-products axis was found to integrate with Toll-like receptors (TLRs) to generate and amplify the inflammatory response in experimental aspergillosis [18]. Moreover, recipients of allogeneic stem-cell transplantation harboring genetic variants underlying a hyperactivation of danger signaling in response to infection displayed an increased risk of developing IPA [19]. This emerging concept could help explain fungal pathogenesis in conditions of exuberant inflammation such as that observed in COVID-19 patients and highlights DAMP targeting as potential immunomodulatory strategy in CAPA.\nA second possibility involves the collateral effects of recognition pathways required for the activation of antiviral immunity that may, paradoxically, contribute to an inflammatory environment that favors secondary infections. ACE2 is not well expressed on immune cells and SARS-CoV are recognized by TLR4 and TLR3, leading to the activation of MyD88- or TRIF-mediated signaling, respectively [20,21]. Of note, this may be potentiated in the presence of Aspergillus spp. which activate TLR4/MyD88/TRIF through the cleavage of fibrinogen [22]. It is likely that SARS-CoV-2 may elicit, to a large extent, overlapping signaling pathways towards the production of inflammatory cytokines. In addition, the activation of the inflammasome by SARS-CoV and the consequent production of IL-1β is an event that contributes further to the hyperinflammatory response [23]. A transcriptome analysis of COVID-19 patients revealed an early immune response characterized by a marked upregulation of the IL-1 pathway, even after respiratory function nadir [24]. The possibility that IL-1 and related pro-inflammatory pathways could serve as therapeutic targets was demonstrated by the favorable responses in severe COVID-19 patients with secondary hemophagocytic lymphohistiocytosis treated with the interleukin-1 receptor antagonist anakinra [25]. Similar findings were also disclosed in acute leukemia patients with COVID-19 [26]. Likewise, IL-1 blockade with anakinra has also been found to ameliorate inflammation in both chronic granulomatous disease [27] and cystic fibrosis [28], and in either case, to restrain susceptibility to infection or colonization by Aspergillus. Therefore, the early hyperactivation of the IL-1 pathway induced by the SARS-CoV-2 infection may be a major factor establishing a highly permissive inflammatory environment that favors fungal pathogenesis.\nBesides IL-1, increased levels of IL-6 have also been consistently reported in severe cases of COVID-19 [29,30], with an impact on immune cell function and the anti-viral mechanisms of immune cells [31]. An enhanced production of IL-6 is also observed in epithelial cells following infection with A. fumigatus, suggesting that, at least in some patients, the co-infection may contribute to the increased levels of this cytokine in severe COVID-19 patients [32]. In a large patient series of COVID-19 patients with ARDS, the use of the IL-6 receptor antagonist tocilizumab was recently reported to promote rapid and sustained responses associated with significant clinical improvement [33]. However, such clinical approach could paradoxically enhance the predisposition to CAPA, similar to animal models of IL-6 deficiency subjected to experimental aspergillosis [34]. For this reason, ongoing trials are addressing the combined use of IL-6 antagonists and antifungal prophylaxis in severe COVID-19 patients.\nAn emerging body of evidence supports therefore an increased systemic inflammatory reaction in patients with severe SARS-CoV-2 infection who are more likely to develop CAPA. In this regard, increased levels of circulating proinflammatory cytokines, such as TNF, were observed in patients requiring intensive care, compared to those with milder infections [35]. Other studies, however, have also unveiled marked defects in immune cell populations, namely T-lymphocytes, as another factor explaining the immune dysfunction in patients with COVID-19 [36]. This suggests that while sustained innate immune function leads to hyperinflammation [37], lymphocyte numbers decline, and their function may be defective. In this regard, severe lymphocytopenia was among the factors in a risk score model that predicted the development of invasive mold disease in patients with hematological malignances [38]. It is thus reasonable to speculate that in elderly individuals or with co-morbidities, defective immune responses to SARS-CoV-2 may allow unrestricted viral replication which, in turn, elicits hyperinflammation and severe complications such as ARDS [39], besides establishing favorable conditions for the acquisition of secondary infections, such as CAPA.\nWhile there is much to be learned about CAPA, our current understanding of the pathophysiology of other coinfections with respiratory viruses such as influenza [40] provides an important framework towards the effective design of immunotherapeutic approaches and the identification of the patients that could benefit the most from 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