Neurotoxic effects of sublethal concentrations of cyanobacterial extract containing anatoxin-a(s) on Nauphoeta cinerea cockroaches

• Published in: Ecotoxicology and environmental safety Vol. 171; pp. 138 - 145
• Main Authors: dos Santos, Douglas Silva, Rosa, Maria Eduarda, Zanatta, Ana Paula, Oliveira, Raquel Soares, de Almeida, Carlos Gabriel Moreira, Leal, Allan Pinto, Sanz, Miriam, Fernandes, Kelly Afonsina, de Souza, Velci Queiroz, de Assis, Denis Reis, Pinto, Ernani, Belo, Cháriston André Dal
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier Inc 30.04.2019
• Subjects: Anatoxin-a(s); Anticholinesterase activity; Central nervous system neurotoxicity; Neuromuscular blockade; Organophosphate compounds; Trichlorfon; AChE; ACh; Trichlorfon; Anatoxin-a(s); GLU; OPs; Central nervous system neurotoxicity; GABA; Neuromuscular blockade; Tn; Organophosphate compounds; WHO; CECA; Anticholinesterase activity
• ISSN: 0147-6513; 1090-2414
• DOI: 10.1016/j.ecoenv.2018.12.068

The detection of cyanotoxins, such as the anatoxin-a(s), is essential to ensure the biological safety of water environments. Here, we propose the use of Nauphoeta cinerea cockroaches as an alternative biological model for the biomonitoring of the activity of anatoxin-a(s) in aquatic systems. In order to validate our proposed model, we compared the effects of a cyanobacterial extract containing anatoxin-a(s) (CECA) with those of the organophosphate trichlorfon (Tn) on biochemical and physiological parameters of the nervous system of Nauphoeta cinerea cockroaches. In brain homogenates from cockroaches, CECA (5 and 50 μg/g) inhibited acetylcholinesterase (AChE) activity by 53 ± 2% and 51 ± 7%, respectively, while Tn (5 and 50 μg/g) inhibited AChE activity by 35 ± 4% and 80 ± 9%, respectively (p < 0.05; n = 6). Moreover, CECA at concentrations of 5, 25, and 50 µg/g decreased the locomotor activity of the cockroaches, diminishing the distance travelled and increasing the frequency and duration of immobile episodes similarly to Tn (0.3 μg/g) (p < 0.05, n = 40, respectively). CECA (5, 25 and 50 μg/g) induced an increase in the leg grooming behavior, but not in the movement of antennae, similarly to the effect of Tn (0.3 μg/g). In addition, both CECA (50 µg/200 μl) and Tn (0.3 µg/200 μl) induced a negative chronotropism in the insect heart (37 ± 1 and 47 ± 8 beats/min in 30 min, respectively) (n = 9, p > 0.05). Finally, CECA (50 µg/g), Tn (0.3 µg/g) and neostigmine (50 µg/g) caused significant neuromuscular failure, as indicated by the monitoring of the in vivo neuromuscular function of the cockroaches, during 100 min (n = 6, p < 0.05, respectively). In conclusion, sublethal doses of CECA provoked entomotoxicity. The Tn-like effects of CECA on Nauphoeta cinerea cockroaches encompass both the central and peripheral nervous systems in our insect model. The inhibitory activity of CECA on AChE boosts a cascade of signaling events involving octopaminergic/dopaminergic neurotransmission. Therefore, this study indicates that this insect model could potentially be used as a powerful, practical, and inexpensive tool to understand the impacts of eutrophication and for orientating decontamination processes. [Display omitted] •Sublethal doses of CECA produce behavioral alterations in Nauphoeta cinerea cockroaches.•CECA inhibition of AChE alters the insect octopaminergic/dopaminergic signaling.•CECA causes neuromuscular failure in Nauphoeta cinerea similarly to trichlorfon.•Nauphoeta cinerea cockroaches are a suitable model for risk assessment of cyanobacteria.