Egg chorion tanning in Aedes aegypti mosquito

doi:10.1016/0300-9629(94)90231-3

Comparative Biochemistry and Physiology Part A: Physiology

Volume 109, Issue 4, December 1994, Pages 835-843

Comparative Biochemi...

https://doi.org/10.1016/0300-9629(94)90231-3 Get rights and content

Abstract

The biochemical pathway of egg chorion tanning in the mosquito, Aedes aegypti, is described and compared with chorion protein crosslinking in Drosophila and silkmoths and the biochemical pathways of cuticular tanning in insects. Phenol oxidase, dopa decarboxylase and tyrosine are critical components involved in egg chorion tanning in A. aegypti. Tanning of the mosquito egg chorion is initiated following activation of phenol oxidase, which then catalyzes the hydroxylation of tyrosine to dopa and further oxidizes dopa and dopamine to their respective o-quinones. Because intramolecular cyclization is much slower in dopaminequinone than dopaquinone, the chance to react with external nucleophiles to participate in protein crosslinking reactions also is much greater in dopaminequinone than dopaquinone. This might partly explain the necessity for the involvement of dopa decarboxylase in mosquito chorion tanning. Intramolecular cyclization of dopaquinone and dopaminequinone to form dopachrome and dopaminechrome, respectively, the structural rearrangement of these aminochromes to produce 5,6-dihydroxyindole, and the subsequent oxidation of 5,6-dihydroxyindole by phenol oxidase also lead to melanin formation during egg chorion tanning.

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Most insects reproduce by laying eggs that have an eggshell/chorion secreted by follicle cells, which serves as a protective barrier for developing embryos. Thus, eggshell formation is vital for reproduction. Insect yellow family genes encode for secreted extracellular proteins that perform different, context-dependent functions in different tissues at various stages of development involving, for example, cuticle/eggshell coloration and morphology, molting, courtship behavior and embryo hatching. In this study we investigated the function of two of this family's genes, yellow-g (TcY-g) and yellow-g2 (TcY-g2), on the formation and morphology of the eggshell of the red flour beetle, Tribolium castaneum. Real-time PCR analysis revealed that both TcY-g and TcY-g2 were specifically expressed in the ovarioles of adult females. Loss of function produced by injection of double-stranded RNA (dsRNA) for either TcY-g or TcY-g2 gene resulted in failure of oviposition. There was no effect on maternal survival. Ovaries dissected from those dsRNA-treated females exhibited ovarioles containing not only developing oocytes but also mature eggs in their egg chambers. However, the ovulated eggs were collapsed and ruptured, resulting in swollen lateral oviducts and calyxes. TEM analysis showed that lateral oviducts were filled with electron-dense material, presumably from some cellular content leakage out of the collapsed eggs. In addition, morphological abnormalities in lateral oviduct epithelial cells and the tubular muscle sheath were evident. These results support the hypothesis that both TcY-g and TcY-g2 proteins are required for maintaining the rigidity and integrity of the chorion, which is critical for resistance to mechanical stress and/or rehydration during ovulation and egg activation in the oviducts of T. castaneum. Because Yellow-g and Yellow-g2 are highly conserved among insect species, both genes are potential targets for development of gene-based insect pest population control methods.
Hardening and tanning of insect ootheca, egg cases, egg sac, chorion, and silk
2022, Advances in Insect Physiology
Citation Excerpt :
While cockroach ootheca and mantid egg cases are hardened solely by the sclerotization process, the lepidopteran insect, Hyalophora egg seems to be stiffened by disulphide crosslinks formed between cysteine-rich fibrillar proteins, rather than by sclerotization process (Tefler, 2009). On the other hand, mosquito eggs seem to be made up of melanin and chitin (Amenya et al., 2010; Farnesi et al., 2015; Li, 1994). In this case, hardening is also assisted by peroxidase mediated dityrosine and trityrosine crosslink formation (Li, 1994).
Insects lay eggs that must survive in nature often several days to months. The eggs need to be protected from desiccation and other harsh environmental challenges. The structural components of eggshells are mostly proteins, but in some cases the polysaccharide, chitin is also used as an essential matrix material. In addition, several eggshells also contain minerals and catecholamine derivatives. Enzymic components often include peroxidase, laccase and/or phenoloxidase and other sclerotizing enzymes. In this review, some of the aspects of eggshell and chorion tanning in insects are reviewed. Four major systems representing different way of hardening are considered. They are hardening of the cockroach ootheca, tanning of the mosquito egg chorion, crosslinking of Drosophila eggshell, and sclerotization of praying mantis egg sacs. Cockroach ootheca, which is devoid of chitin, mostly use sclerotization mechanism to harden its case using 3,4-dihydroxybenzyl alcohol. Mosquito eggs which possess chitin on the other hand, employ both melanisation and peroxidase mediated dityrosine and trityrosine formation for tanning reactions. Drosophila egg chorion primarily utilize peroxidase mediated crosslinking process only. While these three systems seem to differ from the normal sclerotization process employed by most insect cuticles which use N-acetyldopamine and N-β-alanyldopamine as sclerotizing precursors and phenoloxidase (both laccase and o-diphenoloxidase), quinone isomerase, and quinone methide isomerase as the sclerotizing enzymes, the egg sacs of praying mantis recruit a variety of N-acyldopamine derivatives and the two enzymes—phenoloxidase and quinone isomerase—for hardening their sacs. In addition, tanning of silk is also considered briefly in this review. The biochemical mechanisms of these reactions are discussed in detail.
Cuticular sclerotization in insects – A critical review
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Citation Excerpt :
The presence of dityrosine and trityrosine crosslinks has been reported in many systems now. Similarly, the association of peroxidase with cuticular matrix for crosslinking has also been reported extensively (Konstandi et al., 2005, 2006; Li, 1994; Li et al., 1996, 2004; Mindrinos et al., 1980; Zhao et al., 2001). Proteomic studies also reveal the intimate association of peroxidase, phenoloxidase and laccase with cuticular structures (Amenya et al., 2010; Marinotti et al., 2014).
Sclerotization of cuticle is a vital process for the survival of insects. It is caused by covalent crosslinking of structural proteins and chitin to form hard and often coloured cuticle. During sclerotization, N-acetyldopamine and N-β-alanyldopamine are activated by cuticular enzymes such as phenoloxidase—both laccase and o-diphenoloxidase, peroxidase, quinone isomerase and quinone methide isomerase to reactive intermediates that can form adducts and crosslinks. Four major mechanisms—quinone tanning, quinone methide sclerotization, α,β-sclerotization, and free radical tanning have been identified so far for gluing and bonding the structural proteins with chitin. The biochemistry of the quinone tanning, the first discovered mechanism for hardening is critically evaluated and assessed. The enzymatic and nonenzymatic production of quinone methide, and the critical role of quinone isomerase in quinone methide sclerotization is discussed. The biosynthesis of two sclerotizing precursor associated with α,β-sclerotization is outlined. The critical roles of dehydro N-acetyldopamine and dehydro N-β-alanyldopamine in α,β-sclerotization, and the differential use of N-acetyldopamine and N-β-alanyldopamine in producing coloured versus colourless cuticle is considered. Potential contribution of both peroxidase and laccase for free radical tanning is also briefly examined. The mechanisms of formation of catecholic products in cuticular hydrolysates are investigated. The genes associated with cuticular hardening are briefly described. Sclerotization in other animal systems that use dehydro dopa and its derivatives is also assessed. Melanisation reactions that occur in cuticle and hemolymph and its role in wound healing, defence reactions and cuticular pigmentation is critically evaluated.
Yellow-g and Yellow-g2 proteins are required for egg desiccation resistance and temporal pigmentation in the Asian tiger mosquito, Aedes albopictus
2020, Insect Biochemistry and Molecular Biology
Citation Excerpt :
For instance, the phenoloxidase and dopa decarboxylase activities associated with tyrosine-mediated tanning metabolism (melanization/pigmentation and sclerotization) as well as the dityrosine- or trityrosine-mediated protein cross-linking catalyzed by a peroxidase appear to be required for darkening and hardening of the chorion in Aedes aegypti and Ae. albopictus eggs (Kim et al., 2005; Li, 1994; Li and Christensen, 1993; Li et al., 1996; Li and Li, 2006; Wu et al., 2013). In contrast, the timing of egg desiccation resistance as determined by an egg shrinkage assay (intact or collapsed eggs after 15 min of air-drying) is correlated with serosal cuticle formation (determined by sensitivity to bleach treatment) but not with melanization/darkening of eggs laid not only by Ae.
Eggs from Aedes mosquitoes exhibit desiccation resistance that helps them to survive and spread as human disease vectors throughout the world. Previous studies have suggested that eggshell/chorion melanization and/or serosal cuticle formation are important for desiccation resistance. In this study, using dsRNAs for target genes, we analyzed the functional importance of two ovary-specific yellow genes, AalY-g and AalY-g2, in the resistance to egg desiccation of the Asian tiger mosquito, Aedes albopictus, a species in which neither the timing of the melanization nor temporal development of the serosal cuticle is correlated with desiccation resistance. Injections of dsAalY-g, dsAalY-g2 or dsAalY-g/g2 (co-injection) into adult females have no effect on their fecundity. However, initial melanization is delayed by 1–2 h with the eggshells eventually becoming black similar to that observed in eggs from dsEGFP-injected control females. In addition, the shape of the eggs from dsAalY-g, -g2 and -g/g2-treated females is abnormally crescent-shaped and the outermost exochorion is more fragile and partially peeled off. dsEGFP control eggs, like those from the wild-type strain, acquire resistance to desiccation between 18 and 24 h after oviposition (HAO). In contrast, ~80% of the 24 HAO dsAalY-g and dsAalY-g2 eggs collapse when they are transferred to a low humidity environment. In addition, there is no electron-dense outer endochorion evident in either dsAalY-g or dsAalY-g2 eggs. These results support the hypothesis that AalY-g and AalY-g2 regulate the timing of eggshell darkening and are required for integrity of the exochorion as well as for rigidity, normal morphology and formation of the outer endochorion, a structure that apparently is critical for desiccation resistance of the Ae. albopictus egg.
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The macrophage migration inhibitory factor (MIF) family, consisting of MIF and D-dopachrome tautomerase (DDT) in vertebrates, is evolutionarily ancient and has been found across Kingdoms including vertebrates, invertebrates, plants and bacteria. The mammalian MIF family are chemokines at the top of the inflammatory cascade in combating infections. They also possess enzymatic activities, e.g. DDT catalysis results in the production of 5,6-dihydroxyindole (DHI), a precursor of eumelanin. MIF-like genes are widely distributed, but DDT-like genes have only been described in vertebrates and a nematode. In this report, we cloned a DDT-like gene, for the first time in arthropods, and a second MIF in mud crab. The mud crab MIF family have a three exon/two intron structure as seen in vertebrates. The identification of a DDT-like gene in mud crab and other arthropods suggests that the separation of MIF and DDT preceded the divergence of protostomes and deuterostomes. The MIF family is differentially expressed in tissues of adults and during embryonic development and early life. The high level expression of the MIF family in immune tissues, such as intestine and hepatopancreas, suggests an important role in mud crab innate immunity. Mud crab DDT is highly expressed in early embryos, in megalops and crablets and this coincides with the requirement for melanisation in egg chorion tanning and cuticular hardening in arthropods, suggesting a potential novel role of DDT in melanogenesis via its tautomerase activity to produce DHI in mud crab. The clarification of the presence of both MIF and DDT in this report paves the way for further investigation of their functional roles in immunity and in melanogenesis in mud crab and other arthropods.
Molecular characterization of the cDNA encoding prophenoloxidase-2 (PPO2) and its expression in diamondback moth Plutella xylostella
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Mini reviewEgg chorion tanning in Aedes aegypti mosquito

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Egg chorion tanning in Aedes aegypti mosquito