Vitellogenin in inflammation and immunity in social insects

Abstract

Social insects, such as the honey bee and ants, form vast colonies that are only rivalled by human settlements. Living in dense, often stationary groups is prone to increase disease transmission. Yet, social insect queens and certain worker types can lead lengthy lives compared to the life span of most solitary insects. Social insects appear to have modified insulin/insulin like signaling pathway that regulates insect life history. This modification results in extremely elevated levels of the multifunctional lipoprotein vitellogenin in the individuals with longer life span. Vitellogenin is an egg-yolk precursor, but it also regulates caste-related behaviors in social insects, has shielding effects in inflammation and infection, and it is a mediator of transgenerational immunity. Here, we compile what is known about the life span and immune actions of vitellogenin and the evolution of this protein in the honey bee and ants. Recently we identified proteins homologous to vitellogenin in several Hymenopteran species, and showed that at least one of these vitellogenin-like proteins can have a protective role similar to vitellogenin in the honey bee. The newly identified vitellogenin homologs hint that the regulation of social insect life span can be more complex than thought before.

Changes in vitellogenin expression caused by nematodal and fungal infections in insects

“…The humoral response includes production of various compounds, such as eicosanoids, phenoloxidases, proteinases, proteinase inhibitors and a wide selection of antimicrobial peptides and proteins (Jiang, 2008;Beckage, 2008). The list of the protective compounds also includes Vgs, whose involvement in insect defense systems has recently been described in several insect species (Havukainen et al, 2013;Singh et al, 2013;Salmela et al, 2015;Salmela and Sundstrom, 2017;Park et al, 2018). We have found in this study that in the firebug P. apterus, Vg is probably also involved in the defense reaction against the entomopathogenic nematode S. carpocapsae and, partially, against the fungus I. fumosorosea.…”

“…However, low levels of Vgs have been identified in males of several insect species, including the firebug Pyrrhocoris apterus (Nemec et al, 1993). Several recent studies suggested that Vgs play an important role not only in reproduction but also in other aspects of insect biology, such as the caste differentiation process in social insects, wound healing, protection against oxidative stress, immunity and life span regulation (Havukainen et al, 2013;Singh et al, 2013;Salmela et al, 2015;Salmela and Sundstrom, 2017;Park et al, 2018). Studies in the silkworm and honeybee reported strong antibacterial activity of Vg against gram-positive and gram-negative bacteria (Singh et al, 2013), showing that Vg bound to bacterial cells and destroyed them.…”

Gene expression is stronger associated with behaviour than with age and fertility in ant workers

“…In other social insects, this linkage between JH, Vg and behaviour is similar [23,38–40], absent [41] or reversed [42–44]. Moreover, Vg underwent multiple duplications in ants with different orthologs taking over specific functions in the regulation of fertility and behaviour [31,45–49]. In honey bees, the foraging gene is highly expressed in the optical lobes and mushroom bodies of forager’ brains [50,51], causing an elevated sucrose responsiveness and the onset of foraging behaviour [52,53].…”

Young but not defenceless: antifungal activity during embryonic development of a social insect

“…This yolk precursor is known to have antimicrobial activity and plays a role in immunity across a variety of taxonomical groups (e.g. [32,[40][41][42]47,[49][50][51]). Our results indicate that E1 embryos, which probably have the highest concentration of maternally contributed vitellogenins before becoming metabolized during embryogenesis, reduced conidia germination by approximately 10% (figure 4b).…”