A cytokine secreted from the suboesophageal body is essential for morphogenesis of the insect head

Abstract

The suboesophageal body of insects was identified over a century ago in the silkworm embryo, but its biological function is still unknown. We discovered that this tissue is differentiated in the earliest embryonic stages of the cabbage armyworm and secretes the insect cytokine, growth-blocking peptide (GBP), transiently from 24 to 60 h after oviposition when gastrulation is in progress. Over-expression of GBP, achieved by microinjection of the GBP gene driven by a cytomegalovirus (CMV) constitutive promoter, resulted in complex deformities of the procephalon (embryonic head). Severe abnormal phenotypes of the head structure were produced by silencing the GBP expression in the embryo by treating with GBP double-stranded RNA: the procephalon-containing optic lobes diminished and completely separated into bilateral halves. This indicates that GBP secreted from the suboesophageal body plays an essential role in the formation of the procephalic domain during early embryogenesis. The cytokine-induced fusion of bilateral procephalic lobes is thought to be evolutionarily conserved at least in insects, because of the widespread occurrence of the suboesophageal body in insect embryos.

Drosophila growth-blocking peptide-like factor mediates acute immune reactions during infectious and non-infectious stress

“…They have diverse functions such as growth retardation1112, paralysis induction131516, cardioacceleration16, cell proliferation2526, embryogenic morphogenesis27, and immune cell stimulation1428. Characterization of some of these peptide cDNAs demonstrated that the ENF peptides are synthesized as a precursor form in which the active peptide is located at the C-terminal region15282930.…”

Characteristics common to a cytokine family spanning five orders of insects

“…Genetic analysis of Drosophila should allow us to determine the function of these peptides using tools that were not available when GBP was studied in Lepidopterans. There is growing evidence that the ENF cytokine family member GBP plays a crucial role in maintaining insect life from embryonic to larval stages (Tsuzuki et al, 2005a(Tsuzuki et al, , 2005b. The many functions of GBPs include morphogenesis, cellular immunity, cardiomotility and larval growth regulation.…”

A Eukaryotic (Insect) Tricistronic mRNA Encodes Three Proteins Selected by Context-dependent Scanning

“…1). Indeed, we have already shown that the ENF peptide gene of M. brassicae plays an essential role on the morphogenesis of the embryonic head portion (30). Additionally, when a higher proportion of PP protein is required for any purpose, it can be achieved by co-expressing the protein from the monocistronic PP mRNA, which was detected throughout the embryogenesis and larval development (Fig.…”

“…The obtained genomic sequences were deposited in the GenBank TM /EMBL/DDBJ databases (accession numbers AB511039, AB511041, and AB511042). The ENF peptide gene sequences of the P. separata (number AB012294) (28) and M. brassicae (AB126696) (30) were also used for analyzing the genomic structure of the uENF1-uENF 2- PP ( ENF peptide) mRNA of the two moths.…”