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Open Access Research article

The natural insect peptide Neb-colloostatin induces ovarian atresia and apoptosis in the mealworm Tenebrio molitor

Elżbieta Czarniewska1*, Grzegorz Rosiński1, Elżbieta Gabała23 and Mariola Kuczer4

Author Affiliations

1 Department of Animal Physiology & Development, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland

2 Department of Cell Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland

3 Current address: Research Centre of Quarantine, Invasive & Genetically Modified Organisms, Węgorka 20, 60-318 Poznań, Poland

4 Faculty of Chemistry, Wrocław University, Joliot-Curie 14, 50-383 Wroclaw, Poland

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BMC Developmental Biology 2014, 14:4  doi:10.1186/1471-213X-14-4

Published: 30 January 2014

Abstract

Background

The injection of Neb-colloostatin into T. molitor females causes gonadoinhibitory effects on ovarian development. This peptide inhibits intercellular space formation (patency) in follicular epithelium and results in slowed vitellogenesis, delayed ovulation, reduced number of eggs laid and presumably cell death in the terminal follicles. However, as does the form of cell death in the terminal follicle, the mode of action of Neb-colloostatin remains unknown.

Results

We tested Neb-colloostatin for a sterilizing effect on females of Tenebrio molitor. We report that injection of nanomolar doses of Neb-colloostatin induce ovarian follicle atresia in 4-day old females during their first gonadotropic cycle. Light microscope observations revealed morphological changes in the ovary: after Neb-colloostatin injection the terminal oocytes are significantly smaller and elicit massive follicle resorption, but the control terminal follicles possess translucent ooplasm in oocytes at different stages of vitellogenesis. A patency is visible in follicular epithelium of the control vitellogenic oocytes, whereas peptide injection inhibits intercellular space formation and, in consequence, inhibits vitellogenesis. Confocal and electron microscope examination showed that peptide injection causes changes in the morphology indicating death of follicular cells. We observed F-actin cytoskeleton disorganization, induction of caspase activity, changes in chromatin organization and autophagic vacuole formation. Moreover, the apical cytoplasm of follicular cells is filled with numerous free ribosomes, probably indicating a higher demand for protein biosynthesis, especially in preparation for autophagic vacuole formation. On the other hand, the process of polyribosomes formation is inhibited, indicating the contributing effect of this hormone.

Conclusion

Neb-colloostatin induces atresia in the mealworm ovary. Degeneration of T. molitor follicles includes changes in morphology and viability of follicular cells, and oosorption as a consequence of these changes.

Keywords:
Insect ovary; Neb-colloostatin; Gonadoinhibitory peptide; Follicle atresia; Apoptosis; Autophagy