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Functional evidence for physiological mechanisms to circumvent neurotoxicity of cardenolides in an adapted and a non-adapted hawk-moth species.
- Source :
-
Proceedings. Biological sciences [Proc Biol Sci] 2013 Mar 20; Vol. 280 (1759), pp. 20123089. Date of Electronic Publication: 2013 Mar 20 (Print Publication: 2013). - Publication Year :
- 2013
-
Abstract
- Because cardenolides specifically inhibit the Na(+)K(+)-ATPase, insects feeding on cardenolide-containing plants need to circumvent this toxic effect. Some insects such as the monarch butterfly rely on target site insensitivity, yet other cardenolide-adapted lepidopterans such as the oleander hawk-moth, Daphnis nerii, possess highly sensitive Na(+)K(+)-ATPases. Nevertheless, larvae of this species and the related Manduca sexta are insensitive to injected cardenolides. By radioactive-binding assays with nerve cords of both species, we demonstrate that the perineurium surrounding the nervous tissue functions as a diffusion barrier for a polar cardenolide (ouabain). By contrast, for non-polar cardenolides such as digoxin an active efflux carrier limits the access to the nerve cord. This barrier can be abolished by metabolic inhibitors and by verapamil, a specific inhibitor of P-glycoproteins (PGPs). This supports that a PGP-like transporter is involved in the active cardenolide-barrier of the perineurium. Tissue specific RT-PCR demonstrated expression of three PGP-like genes in hornworm nerve cords, and immunohistochemistry further corroborated PGP expression in the perineurium. Our results thus suggest that the lepidopteran perineurium serves as a diffusion barrier for polar cardenolides and provides an active barrier for non-polar cardenolides. This may explain the high in vivo resistance to cardenolides observed in some lepidopteran larvae, despite their highly sensitive Na(+)K(+)-ATPases.
- Subjects :
- ATP Binding Cassette Transporter, Subfamily B chemistry
ATP Binding Cassette Transporter, Subfamily B genetics
ATP Binding Cassette Transporter, Subfamily B metabolism
Adaptation, Physiological
Amino Acid Sequence
Animals
Base Sequence
Food Chain
Hemolymph metabolism
Insect Proteins chemistry
Insect Proteins genetics
Insect Proteins metabolism
Larva growth & development
Larva physiology
Moths growth & development
Nerium chemistry
Peripheral Nerves physiology
Permeability
Polymerase Chain Reaction
Sodium-Potassium-Exchanging ATPase metabolism
Species Specificity
Digoxin metabolism
Moths physiology
Neurotoxins metabolism
Ouabain metabolism
Subjects
Details
- Language :
- English
- ISSN :
- 1471-2954
- Volume :
- 280
- Issue :
- 1759
- Database :
- MEDLINE
- Journal :
- Proceedings. Biological sciences
- Publication Type :
- Academic Journal
- Accession number :
- 23516239
- Full Text :
- https://doi.org/10.1098/rspb.2012.3089