PMC:7321036 / 86-8224 JSONTXT

{"target":"http://pubannotation.org/docs/sourcedb/PMC/sourceid/7321036","sourcedb":"PMC","sourceid":"7321036","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7321036","text":"gent of the coronavirus disease 2019 (COVID-19) pandemic, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has infected millions and killed hundreds of thousands of people worldwide, highlighting an urgent need to develop antiviral therapies. Here we present a quantitative mass spectrometry-based phosphoproteomics survey of SARS-CoV-2 infection in Vero E6 cells, revealing dramatic rewiring of phosphorylation on host and viral proteins. SARS-CoV-2 infection promoted casein kinase II (CK2) and p38 MAPK activation, production of diverse cytokines, and shutdown of mitotic kinases, resulting in cell cycle arrest. Infection also stimulated a marked induction of CK2-containing filopodial protrusions possessing budding viral particles. Eighty-seven drugs and compounds were identified by mapping global phosphorylation profiles to dysregulated kinases and pathways. We found pharmacologic inhibition of the p38, CK2, CDK, AXL, and PIKFYVE kinases to possess antiviral efficacy, representing potential COVID-19 therapies.\n\nGraphical Abstract\n\nHighlights\n• Phosphoproteomics analysis of SARS-CoV-2-infected cells uncovers signaling rewiring\n• Infection promotes host p38 MAPK cascade activity and shutdown of mitotic kinases\n• Infection stimulates CK2-containing filopodial protrusions with budding virus\n• Kinase activity analysis identifies potent antiviral drugs and compounds\n\nPhosphoproteomics analysis of SARS-CoV-2-infected Vero E6 cells reveals host cellular pathways hijacked by viral infection, leading to the identification of small molecules that target dysregulated pathways and elicit potent antiviral efficacy.\n\nIntroduction\nSevere acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an enveloped positive-sense RNA virus that belongs to the lineage B Betacoronavirus family. It is closely related to SARS-CoV, the causative agent of SARS, which emerged in the human population in 2002 (79% genetic similarity), and several SARS-related coronaviruses that circulate in bats (up to 98% genetic similarity) (Lai et al., 2020; Zhou et al., 2020). The pathophysiology of severe coronavirus disease 2019 (COVID-19) is similar to that of severe disease caused by SARS-CoV and is characterized by acute respiratory distress and excessive inflammation capable of inducing respiratory failure, multi-organ failure, and death (Wong et al., 2004; Zhang et al., 2020).\nTo enter host cells, the SARS-CoV-2 spike (S) protein binds to an ACE2 receptor on the target cell and is subsequently primed by a serine protease, TMPRSS2, that cleaves the S protein and allows fusion of viral and lysosomal membranes (Hoffmann et al., 2020). Following entry, viral genomic RNA is translated to produce the polyproteins ORF1a and ORF1ab, which are subsequently cleaved by viral proteases into non-structural proteins that form the viral replication/transcription complex (RTC). Extensive remodeling of the host endoplasmic reticulum leads to formation of double-membrane vesicles, within which viral RNA synthesis occurs. The viral RNA genome is replicated by transcription of the negative-strand genomic RNA template, whereas subgenomic mRNAs are transcribed and translated to produce structural and accessory proteins. Structural proteins and viral genomes assemble at the endoplasmic reticulum-Golgi intermediate compartment (ERGIC) (de Haan and Rottier, 2005), followed by transport to the cell surface for release by exocytosis (Fehr and Perlman 2015).\nAlthough much about SARS-CoV-2 biology can be inferred based on similarity to SARS-CoV, SARS-CoV-2 is a novel coronavirus with unique properties that contribute to its pandemic-scale spread. Unlike SARS-CoV, SARS-CoV-2 infection is commonly asymptomatic, particularly in the younger population (Guan et al., 2020), and contagious prior to symptom onset (Rothe et al., 2020; Peiris et al., 2003; Bai et al., 2020). These characteristics contribute to the difficulty of containing SARS-CoV-2 spread through public health strategies and amplify the need to develop vaccines and therapies to protect against and treat COVID-19. Clinical management of COVID-19 is largely limited to infection prevention and supportive care. So far, remdesivir, a broad-spectrum antiviral agent, is the only medication approved for emergency use to treat COVID-19 by the US Food and Drug Administration (FDA) (Grein et al., 2020). Although the evidence supporting remdesivir use in patients with advanced COVID-19 is promising, there remains an urgent need for potent SARS-CoV-2 therapeutic agents, especially those that could be given in an outpatient setting, to effectively combat the COVID-19 pandemic.\nProteomics approaches that globally quantify changes in protein abundance and phosphorylation are powerful tools to elucidate mechanisms of viral pathogenesis by providing a snapshot of how cellular pathways and processes are rewired upon infection (Johnson et al., 2020). Importantly, the functional outcomes of many phosphorylation events are well annotated, especially for kinases where phosphorylation directly regulates their activity. State-of-the-art bioinformatics approaches can then be employed to readily identify regulated kinases from phosphorylation profiles, many of which are likely to be established drug targets with therapeutic potential (Ochoa et al., 2016, 2020). Here we present a quantitative survey of the global phosphorylation and protein abundance landscape of SARS-CoV-2 infection, map phosphorylation changes to disrupted kinases and pathways, and use these profiles to rapidly prioritize drugs and compounds with the potential to treat SARS-CoV-2 infection.\n\nResults\n\nPhosphorylation Signaling Represents a Primary Host Response to SARS-CoV-2 Infection\nTo determine how SARS-CoV-2 hijacks host-protein signaling, a global phosphoproteomics experiment was performed in Vero E6 cells, a cell line originating from the kidney of a female African green monkey (Chlorocebus sabaeus) (Osada et al., 2014). This cell line was selected because of its high susceptibility to SARS-CoV-2 infection (Harcourt et al., 2020). Cells were harvested in biological triplicate at 6 time points after SARS-CoV-2 infection (0, 2, 4, 8, 12, or 24 h) or after mock infection at 0 or 24 h (Figure 1 A). Using a data-independent acquisition (DIA) proteomics approach, each sample was then partitioned and analyzed for changes in global protein abundance or phosphorylation (data available in Table S1). Chlorocebus sabaeus and human protein sequences were aligned, and phosphorylation sites and protein identifiers were mapped to their respective human protein orthologs. Phosphorylation fold changes calculated using the 0- or 24-h mock control were highly comparable (correlation coefficient r = 0.77); therefore, the 0-h mock control was used for all subsequent comparisons.\nFigure 1 Global Proteomics of Phosphorylation and Abundance Changes upon SARS-CoV-2 Infection\n(A) Vero E6 cells were infected with SARS-CoV-2 (MOI 1.0). After 1 h of viral uptake, cells were harvested (0 h) or, subsequently, after 2, 4, 8, 12, or 24 h. As a control, Vero E6 cells were also mock infected for 1 h and harvested immediately thereafter (0 h) or after 24 h of mock infection. All conditions were performed in biological triplicate. Following cell harvest, cells were lysed, and proteins were digested into peptides. Aliquots of all samples were analyzed by mass spectrometry (MS) to measure changes in protein abundance upon infection, whereas the remaining sample was enriched for phosphorylated peptides and subsequently analyzed to measure changes in phosphorylation signaling. A DIA approach was used for all MS acquisitions. Last, all phosphorylation sites and protein identifiers were mapped to their respective human protein orthologs.\n(B) Principal-component analysis (PCA) of phosphorylation replicates after removing outliers. See also Figure S1.\n(C) Correlation of protein abundance (AB) and phosphorylation sites (PHs) between replicates within a biological condition (red) and across biological conditions (black). Boxplots depict median (horizonal lines), interquartile 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