Abstract
Lichen-forming fungi are symbiotic organisms that synthesize unique natural products with potential for new drug leads. Here, we explored the pharmacological activity of six lichen extracts (Evernia prunastri, Pseudevernia furfuracea, Umbilicaria pustulata, Umbilicaria crustulosa, Flavoparmelia caperata, Platismatia glauca) in the context of cancer and inflammation using a comprehensive set of 11 functional and biochemical in vitro screening assays. We assayed intracellular Ca2+ levels and cell migration. For cancer, we measured tumor cell proliferation, cell cycle distribution and apoptosis, as well as the angiogenesis-associated proliferation of endothelial cells (ECs). Targeting inflammation, we assayed leukocyte adhesion onto ECs, EC adhesion molecule expression, as well as nitric oxide production and prostaglandin (PG)E2 synthesis in leukocytes. Remarkably, none of the lichen extracts showed any detrimental influence on the viability of ECs. We showed for the first time that extracts of F. caperata induce Ca2+ signaling. Furthermore, extracts from E. prunastri, P. furfuracea, F. caperata, and P. glauca reduced cell migration. Interestingly, F. caperata extracts strongly decreased tumor cell survival. The proliferation of ECs was significantly reduced by E. prunastri, P. furfuracea, and F. caperata extracts. The extracts did not inhibit the activity of inflammatory processes in ECs. However, the pro-inflammatory activation of leukocytes was inhibited by extracts from E. prunastri, P. furfuracea, F. caperata, and P. glauca. After revealing the potential biological activities of lichen extracts by an array of screening tests, a correlation analysis was performed to evaluate particular roles of abundant lichen secondary metabolites, such as atranorin, physodic acid, and protocetraric acid as well as usnic acid in various combinations. Overall, some of the lichen extracts tested in this study exhibit significant pharmacological activity in the context of inflammation and/or cancer, indicating that the group lichen-forming fungi includes promising members for further testing.
Highlights
Lichenized fungi form mutualistic symbioses with photosynthetic microorganisms, usually green algae or cyanobacteria, and additional fungal and bacterial communities
None of the lichen extracts showed any detrimental influence on the viability of healthy cells
Our results on analyses of E. prunastri, P. furfuracea, F. caperata, and P. glauca are in correlation with the previous reports of lichen substances that can reduce the migratory capacity of cells (Burlando et al, 2009; Ebrahim et al, 2016; Zhou et al, 2017; Seklic et al, 2018)
Summary
Lichenized fungi form mutualistic symbioses with photosynthetic microorganisms, usually green algae or cyanobacteria, and additional fungal and bacterial communities. Secondary metabolites with biological activities protect lichens from being overgrown or eaten (Solhaug et al, 2003; Gauslaa, 2005; Asplund et al, 2015), or from receiving too much UV light (Solhaug et al, 2003). Some of these metabolites might support the symbiosis itself, by forming water repellent coatings on internal hyphae, which facilitate gas exchange between moist thalli and the environment (Huneck, 2003), or by enabling communication among the different partners in the lichen association. The highest diversity of compounds is found in the structural classes depsides and depsidones (Huneck and Yoshimura, 1996)
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