Prodigiosins from a marine sponge-associated actinomycete attenuate HCl/ethanol-induced gastric lesion via antioxidant and anti-inflammatory mechanisms

Abstract

Gastric ulcer is sores that form in the stomach mucosal layer because of erosion caused by high acid secretion and excessive use of non-steroidal anti-inflammatory drugs. Prodigiosins (PdGs) are red-pigmented secondary metabolites produced by bacteria, including actinomycetes. Butylcycloheptylprodigiosin ( 1 ) and undecylprodigiosin ( 2 ) were identified and isolated from a crude extract of the actinomycete RA2 isolated from the Red Sea Sponge Spheciospongia mastoidea . Chemical structure of 1 and 2 was determined by NMR and mass spectroscopy. Although their antioxidant and anti-inflammatory properties are known, their effect on gastric lesion is unknown. Therefore, this study aimed to investigate gastroprotective effects of PdGs against HCl/ethanol-induced gastric lesion in rats. Oral pretreatment with PdGs (100, 200, and 300 mg/kg) attenuated severity of HCl/ethanol-induced gastric mucosal injury, as evidenced by decreases in gastric lesion index scores, ulceration area, histopathologic abnormality, and neutrophil infiltration. These effects were comparable to those of omeprazole, a standard anti-gastric ulcer agent. HCl/ethanol-induced gastric erosions was associated with tremendous increases in lipid peroxidation, nitric oxide, and pro-inflammatory cytokines and mediators (myeloperoxidase, interleukin-1β, tumor necrosis factor-α, and cyclooxygenase-2), and with significant decreases in enzymatic and non-enzymatic antioxidant activities. However, PdGs ameliorated gastric inflammation and oxidative stress by downregulating nuclear factor kappa B and inducible nitric oxide synthase expression and upregulating heme oxygenase-1 expression. PdGs prevented gastric mucosal apoptosis by downregulating Bax and caspase-3 expression and upregulating Bcl-2 expression, thereby increasing prostaglandin E2 production. Our results suggested that PdGs exerted gastroprotective effects by decreasing the levels of inflammatory mediators, apoptotic markers, and antioxidants.

Production and Potential Applications of Bioconversion of Chitin and Protein-Containing Fishery Byproducts into Prodigiosin: A Review

“…26-1 [ 191 ], Streptoverticillium rubrireticuli [ 181 ], Pseudoalteromonas sp. [ 186 ], Pseudoalteromonas rubra [ 100 ], Actinomycetes [ 146 , 187 ], and a gene recombinant strain of Pseudomonas putida [ 185 , 189 ].…”

Marine Actinomycetes-Derived Secondary Metabolites Overcome TRAIL-Resistance via the Intrinsic Pathway through Downregulation of Survivin and XIAP

“…Following extraction and evaporation of solvent, separation of the crude extract resulted in compounds ( 3 ) and ( 4 ). The chemical structures of both compounds ( Figure 1 B) were found to be undecylprodigiosin ( 3 ) and butylcycloheptylprodigiosin ( 4 ) based on NMR (1H and 13 C NMR) and mass spectra [ 34 ]. Additionally, the structures were confirmed by comparison of their NMR data with the literature [ 43 , 44 ].…”

“…Marine bacterial strains considered in the current study had previously been assigned to actinomycetes based on partial 16S rRNA and morphological appearance [ 31 , 32 , 33 , 34 ]. The actinobacterial strains EGY1 and EGY34 were isolated from sediment samples obtained from the Red Sea, Egypt.…”

Marine Bacteria Is the Cell Factory to Produce Bioactive Pigments: A Prospective Pigment Source in the Ocean

“…Marine V. ruber DSM 14379 isolated by Danevčič et al (2016) exhibited the production of prodigiosin which showed strong bactericidal activity during the exponential phase of B. subtilis and bacteriostatic activity during stationary growth where it interferes with the cytoplasmic membrane and it also induces autolysin activity enhancing the killing of B. subtilis; however it was observed that the decrease of autolysin resulted in the abolished activity of prodigiosin. Abdelfattah et al (2019), testified the antioxidant and antiinflammatory activity of prodigiosin extracted from Actinomyces sp., isolated from sponge S. mastoidea against HCl/ethanol gastric lesion by over-expressing HO-1 resulting in elevated mucous production antioxidant activity, increasing HSP activity, apoptosis inhibition, and stabilizing cellular membrane thus preventing gastric injury. Prodigiosin has also been reported as an algicidal agent.…”