PMC:7144273 / 16499-30045
Annnotations
{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7144273","sourcedb":"PMC","sourceid":"7144273","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7144273","text":"MSCs in respiratory virus-related lung injury: pre-clinical evidence\nThere is a large body of literature demonstrating efficacy of either systemic or direct intratracheal MSC administration in pre-clinical models of respiratory diseases, including those involving acute lung injury induced by bacteria or bacterial products (endotoxins) or other means [35]. The models include rodents and large animals (pigs and sheep), as well as explanted human lungs. A range of approaches have been utilised for dose, dosing and MSC source, with MSCs from bone marrow, adipose tissue, umbilical cord, cord blood and placenta being investigated. A recent systematic review indicated that BM-MSCs and UC-MSCs were more effective than AD-MSCs in reducing mortality in pre-clinical acute lung injury models [36].\nHowever, there are only a small number of pre-clinical studies investigating effects of MSC administration in pre-clinical models of respiratory virus infections. These have been further limited to influenza viruses, have produced conflicting results, and have not as yet directly addressed coronavirus respiratory infections (table 1). Notably, two earlier studies found MSCs not to be protective against influenza respiratory infections in mice. Darwish et al. [37] assessed the effects of a single systemic administration in immunocompetent mice of either syngeneic murine BM-MSCs or xenogeneic human BM-MSCs on lung injury induced by mouse-adapted H1N1 or swine-origin pandemic H1N1. Two different doses of MSCs (2.5×105 or 5×105 cells·mouse−1) were administered at different time-points after virus administration (days −2, 0, 2 and 5 post infection (p.i.)). Using survival and different measures of lung inflammation as outcome end-points on day 7 p.i., neither syngeneic nor xenogeneic MSC administration, either alone or as an adjuvant therapy with oseltamivir, was effective either when administered prophylactically prior to virus inoculation, or when therapeutically administered. Similarly, Gotts et al. [38] assessed the effect of both systemic and intratracheal administration of human and mouse MSCs (5×105 cells·mouse−1), administered in two doses, either earlier (days 2 and 3 p.i.) or later (days 5 and 6 p.i.), in mouse-adapted H1N1-induced lung injury in immunocompetent mice. However, MSCs did not improve influenza-mediated lung injury, regardless of administration route.\nTABLE 1 Pre-clinical studies of MSCs in respiratory virus-related lung injury\nFirst author, year [ref.] Experimental model, route of infection, type of virus MSC source, passage, number, administration route, timing of treatment Time of outcome analysis Adjuvant therapy Outcome Mechanisms of action Control group\nDarwish, 2013 [37] C57BL/6 mice aged 7–10 weeks, i.n. infection, influenza A/PuertoRico/8/34 (mouse- adapted H1N1) or influenza A/Mexico/410 8/2009 (swine-origin pandemic H1N1) Mouse BM-MSCs (P6–P9) or human BM- MSCs (P3), 2.5×105 or 5×105 cells·mouse−1, i.v. (tail vein), single dose, days −2, 0, 2 or 5 post infection Day 7 or when euthanasia criteria were met Oseltamivir 2.5 mg·kg−1, oral gavage, once daily for 5 days Prophylactic and therapeutic syngeneic and xenogeneic administration of MSCs failed to improve survival, failed to affect weight loss, and failed to decrease lung parenchyma inflammation and BALF cell counts Nonspecified (soluble mediators) No\nGotts, 2014 [38] C57BL/6 mice aged 7–10 weeks, i.n. infection, influenza A/Puerto Rico/8/34 (mouse-adapted H1N1) Mouse BM-MSCs (≤P7) or human BM-MSCs (≤P7), 5×105 cells·mouse−1, i.v. (retro-orbital injection) or i.t. (data not shown); two doses: 1) days 5 and 6 post infection, 2) days 2 and 3 post infection (data not shown) Days 7, 9 or 11 No Mouse MSCs prevented influenza-induced thrombocytosis and caused a modest reduction in lung viral load on day 7; early (data not shown) and late syngeneic and xenogeneic i.v. administration of MSCs failed to affect weight loss, failed to decrease lung water, failed to decrease BALF inflammation, and failed to improve lung histology; i.t. administration increased severity of model (data not shown) Nonspecified (soluble mediators) No\nChan, 2016 [39] BALB/c mice aged 6–8 weeks (young) or 8–12 months (old), i.n. infection, influenza A/Hong Kong/486/1997(H5N1) Human BM-MSCs (passage not mentioned), 5×105 cells·mouse−1, i.v., single dose, day 5 post infection Days 7, 10 or 18 No In older mice, but not younger mice, allogeneic MSCs increased survival, reduced weight loss, reduced lung histopathological lesions, increased M2 macrophages in BALF, reduced lung pro-inflammatory cytokines and chemokines (MCP-1, MCP-3, MIP-1α, RANTES, IL-4, IL-17, TNF-α), but did not reduce lung virus titres Paracrine soluble mediators, partially due to Ang-1 and KGF secretion NIH 3T3 mouse embryo fibroblasts\nLi, 2016 [16] C57BL/6 mice aged 6–8 weeks, i.n. infection, avian influenza virus Hong Kong/2108/2003 (H9N2) Mouse BM-MSCs (P3–P10), 1×105 cells·mouse−1, i.v. (tail vein), single dose, 30 min or day 1 post infection Day 3 No Regardless of time of administration, syngeneic MSCs did not reduce lung virus titration, increased survival rate, decreased lung oedema, decreased histological injury, and improved gas exchange; early and late administration reduced BALF and serum cytokines (IL-6 and TNF-α); early administration reduced BALF chemokine (GM-CSF), reduced BALF and serum chemokines and cytokines (MIG, IL-1α, IFN-γ), and increased anti-inflammatory cytokine IL-10 in BALF and serum Nonspecified (soluble mediators) No\nKhatri, 2018 [40] White Duroc crossbred pigs aged 8 weeks, i.n. infection, influenza virus swine/TX/98 (H3N2) and swine/MN/08 (H1N1) Pig BM-MSC extracellular vesicles (P3–P5), 80 μg·kg−1 body weight (produced by 10×106 MSCs), i.t., single dose, 12 h post infection Days 1 or 3 No BM-MSC-derived extracellular vesicles decreased virus shedding in nasal swabs, reduced influenza virus replication in the lungs, prevented virus-induced production of pro-inflammatory cytokines (TNF-α, CXCL-10), and reduced histological injury and lung oedema Nonspecified (extracellular vesicles) No\nLoy, 2019 [41] BALB/c mice aged 6–8 weeks, i.n. infection, influenza A/Hong Kong/486/1997 (H5N1) Human UC-MSCs (≤P7) 5×105 cells·mouse−1, i.v., single dose, day 5 post infection Days 7, 10, 14 or 18 No UC-MSCs failed to decrease lung virus titration, failed to increase survival rate, reduced body weight loss, decreased lung oedema, and decreased BALF cytokines (IP-10, MCP-1, RANTES, IL-1β) Paracrine soluble mediators, partially due to Ang-1 and HGF secretion NIH 3T3 mouse embryo fibroblasts\nMSCs: mesenchymal stem (stromal) cells; i.n.: intranasal; i.v.: intravenous; i.t.: intratracheal; BM: bone marrow-derived; UC: umbilical cord-derived; BALF: bronchoalveolar lavage fluid; MCP: monocyte chemoattractant; MIP: macrophage inflammatory protein; RANTES: regulated upon activation, normal T-cell expressed and presumably secreted; IL: interleukin; TNF: tumour necrosis factor; Ang-1: angiopoietin-1; KGF: keratinocyte growth factor; GM-CSF: granulocyte–macrophage colony-stimulating factor; MIG: monokine induced by interferon-γ; IFN: interferon; CXCL-10: C-X-C motif chemokine 10; IP-10: interferon γ-induced protein 10; HGF: hepatocyte growth factor.In contrast, more recent studies have demonstrated protective effects of systemic MSC administration in rodent and pig models of influenza respiratory infections. Chan et al. [39] found, through in vitro assays, that MSCs improved the dysregulated alveolar fluid clearance and protein permeability induced by H5N1 and H7N9 influenza viruses, in part by releasing soluble mediators that upregulated sodium and chloride transporters. Systemic administration of 5×105 human BM-MSCs per mouse on day 5 p.i. in immunocompetent mice aged 8–12 months infected with influenza A (H5N1) reduced virus-induced mortality (until day 18 p.i.), weight loss (days 6–10 p.i.), lung oedema (day 7 p.i.), bronchoalveolar lavage fluid (BALF) CD4+ T-cells and natural killer (NK) cells (day 7 p.i.), lung histopathological lesions (day 18 p.i.), and pro-inflammatory cytokines and chemokines (day 7 p.i.), without reducing lung virus titres (days 7 and 10 p.i.). They further found that Ang-1 and KGF released by MSCs were important, but not enough to attenuate the effects of viral infection on alveolar fluid clearance and permeability. However, in young mice (aged 6–8 weeks), no effects were observed in mortality and body weight loss. Thus, the data suggest that systemic MSC administration may provide benefit in older patients who are at higher risk for severe pulmonary illness caused by H5N1. Why this was less effective in younger mice is not clear at present.\nLi et al. [16] investigated the impact of a low dose (105 cells·mouse−1) of murine BM-MSCs in avian influenza virus (H9N2)-induced lung injury in young immunocompetent mice. A single intravenous administration led, on day 3 p.i., to reduction in mortality, lung oedema and histological injury, as well as in BALF and serum chemokines and cytokines, and to improved gas exchange and levels of anti-inflammatory mediators, although it did not reduce lung virus titration when administered either 30 min or 24 h after infection induction. Differences between early and later administration of MSCs were only observed in some BALF and serum inflammatory mediators. Only early administration reduced BALF levels of GM-CSF, reduced BALF and serum monokine induced by IFN-γ (MIG), IL-1α and IFN-γ, and increased levels of BALF and serum IL-10. Both early and later administration led to reduction of BALF and serum IL-6 and tumour necrosis factor-α. This might reflect that early administration seems more geared towards prevention of cell infection and inflammation, rather than dealing with more clinically relevant sequelae of epithelial infection. Avian influenza virus infection can trigger a very intense pro-inflammatory response compared to other influenza viruses; thus, Li et al. [16] speculated that the beneficial effects might be a specific consequence of different pathogenic features, compared to swine-origin H1N1 infection.\nLoy et al. [41] found that UC-MSCs were more effective than human BM-MSCs at restoring impaired alveolar fluid clearance and permeability, in in vitro airway epithelial cell models. These effects were partially mediated through MSC secretion of Ang-1 and hepatocyte growth factor. The authors subsequently compared administration of UC-MSCs to BM-MSCs (5×105 cells·mouse−1, day 5 p.i.) in experimental lung injury induced by influenza A (H5N1) infection in female immunocompetent mice aged 6–8 weeks. Despite failure to reduce virus titre and increase survival rate, a single dose of UC-MSCs decreased body weight loss (days 16 and 17 p.i.), lung oedema (days 10 and 14 p.i.) and inflammation (day 7 p.i.) in H5N1-induced lung injury.\nMSC-derived extracellular vesicles have been demonstrated to have comparable results, and in some cases are more effective than MSCs themselves in ameliorating inflammation and injury in a range of pre-clinical lung injury models [42, 43]. Khatri et al. [40] found that systemic administration of extracellular vesicles isolated from pig BM-MSCs was safe and reduced virus shedding in nasal swabs, influenza replication in the lungs, BALF pro-inflammatory cytokines and chemokines, and histopathological changes, when administered 12 h after viral inoculation in a mixed swine (H3N2, H1N1) and avian (H9N5, H7N2) influenza-induced pig lung injury model. These findings suggest systemic extracellular vesicle administration as a potential cell-free strategy for use in respiratory virus-induced lung injuries.\nThere are as yet no pre-clinical data investigating effects of MSC administration in models of coronavirus respiratory infection, mostly due to the lack of an established animal model. SARS-CoV-2 replication was observed in several non-human primates and in inbred strains of mice following intranasal infection, but these models failed to show clinical signs of pulmonary disease as seen in humans [44]. Mice transgenic for human ACE2, infected with SARS-CoV-2, demonstrated virus replication in the lungs, as well as interstitial pneumonia with lymphocyte and monocyte infiltration into the alveolar interstitium and accumulation of macrophages in alveolar spaces [45]. While this model requires further evaluation, it might facilitate the testing of therapeutics including cell-based therapies for COVID-19. Recently, a non-human primate model for SARS-CoV-2 was able to reflect the same clinical signs, viral replication and pathology observed in humans, with comparable levels of mortality, and might be a valuable model for further evaluation [46].\nOverall, it remains unclear whether the varying results reflect the differing features of each approach, including differences in the host (age), in the MSCs (source, number, route of administration), and in the virus-specific inflammatory patterns. Infection of the administered MSCs by the viruses, particularly the avian influenza viruses, might explain the lack of effectiveness observed in some in vivo studies, but MSC infection after their administration in vivo has not yet been investigated. In order to bypass the impact of viruses on MSCs, extracellular vesicles might be an option for further studies. Clearly, further pre-clinical studies must be done to evaluate the infectiveness of MSCs by coronaviruses and the impact of MSCs in coronavirus-induced lung injury 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