Molluscicidal activity and physiological toxicity of quaternary benzo[c]phenanthridine alkaloids (QBAs) from Macleaya cordata fruits on Oncomelania hupensis

Wenshan Ke, Chang Tu, Dezhi Cao, Xiong Lin, Qiqiang Sun and Qian Zhang

PLOS Neglected Tropical Diseases, 2019, vol. 13, issue 10, 1-16

Abstract: Schistosomiasis is a serious worldwide parasitic disease. One of the best ways to control schistosomiasis is to control the population of Oncomelania hupensis snails. We sought to identify a high-efficiency biogenic molluscicide against Oncomelania with low toxicity, to avoid chemical molluscicide contamination and toxicity in aquatic organisms. We extracted quaternary benzo[c]phenanthridine alkaloids (QBAs) from Macleaya cordata fruits. Molluscicidal activity of the QBAs against Oncomelania was determined using bioassay. Our results showed that the extracted QBAs had a strong molluscicidal effect. In treatment of O. hupensis with QBAs for 48 h and 72 h, the lethal concentration (LC50) was 2.89 mg/L and 1.29 mg/L, respectively. The molluscicidal activity of QBAs was close to that of niclosamide (ethanolamine salt), indicating that QBAs have potential development value as novel biogenic molluscicides. We also analyzed physiological toxicity mechanisms by examining the activity of several important detoxification enzymes. We measured the effect of the extracted QBAs on the activities of glutathione S-transferase (GST), carboxylesterase (CarE), acid phosphatase (ACP), and alkaline phosphatase (AKP) in the liver of O. hupensis. We found that the effects of QBAs on detoxification metabolism in O. hupensis were time and concentration dependent. The activities of GST, CarE, AKP, and ACP in the liver of snails increased significantly in the early stage of treatment (24 h), but decreased sharply in later stages (120 h), compared with these activities in controls. GST, CarE, AKP, and ACP activity in the liver of snails treated with LC50 QBAs for 120 h decreased by 62.3%, 78.1%, 59.2%, and 68.6%, respectively. Our results indicate that these enzymes were seriously inhibited by the extracted QBAs and the detoxification and metabolic functions of the liver gradually weakened, leading to poisoning, which could be the main cause of death in O. hupensis snails.Author summary: Quaternary benzo[c]phenanthridine alkaloids (QBAs) have antimicrobial, antifungal, anti-inflammatory, and anticancer activities (anticancer, antibiosic, and antiphlogistic functions) and have been explored for use as bioantibiotics in livestock. Macleaya cordata fruits have a high QBA content. We isolated QBAs from M. cordata to evaluate molluscicidal activity against Oncomelania and to analyze the physiological toxicity mechanisms. Our results showed that QBAs had strong molluscicidal activity, similar to that of niclosamide. The activities of several important detoxification enzymes (glutathione S-transferase, carboxylesterase, acid phosphatase, and alkaline phosphatase) in the liver of O. hupensis snails were severely inhibited by QBAs. The detoxification and metabolic liver functions gradually weakened via poisoning, which could be the main cause of death in these snails. In China, there are abundant wild plant resources of M. cordata, which is often used in traditional Chinese medicine. QBAs comprising a natural combination of sanguinarine and chelerythrine bisulfate in about a 2:1 ratio had stronger molluscicidal activity than sanguinarine alone. This natural composition could serve as a scientific basis for future development of novel biomolluscicides using these active ingredients and proportions, which could provide an environmentally friendly alternative to the problem of contamination with chemical molluscicides used to combat schistosomiasis in endemic areas.

Date: 2019
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pntd00:0007740

DOI: 10.1371/journal.pntd.0007740

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