The Heat Shock Response in the Western Honey Bee (Apis mellifera) is Antiviral

Abstract

Honey bees (Apis mellifera) are an agriculturally important pollinator species that live in easily managed social groups (i.e., colonies). Unfortunately, annual losses of honey bee colonies in many parts of the world have reached unsustainable levels. Multiple abiotic and biotic stressors, including viruses, are associated with individual honey bee and colony mortality. Honey bees have evolved several antiviral defense mechanisms including conserved immune pathways (e.g., Toll, Imd, JAK/STAT) and dsRNA-triggered responses including RNA interference and a non-sequence specific dsRNA-mediated response. In addition, transcriptome analyses of virus-infected honey bees implicate an antiviral role of stress response pathways, including the heat shock response. Herein, we demonstrate that the heat shock response is antiviral in honey bees. Specifically, heat-shocked honey bees (i.e., 42 °C for 4 h) had reduced levels of the model virus, Sindbis-GFP, compared with bees maintained at a constant temperature. Virus-infection and/or heat shock resulted in differential expression of six heat shock protein encoding genes and three immune genes, many of which are positively correlated. The heat shock protein encoding and immune gene transcriptional responses observed in virus-infected bees were not completely recapitulated by administration of double stranded RNA (dsRNA), a virus-associated molecular pattern, indicating that additional virus–host interactions are involved in triggering antiviral stress response pathways.

Multi-tiered Analyses of Honey Bees That Resist or Succumb to Parasitic Mites and Viruses

“…On the other hand, we find important differences between our results and prior reports of particular genes being best correlated with DWV infection or antiviral response. In fact, in several instances genes previously identified as key antivirus responses were not differentially expressed in our study [17,18,[22][23][24][25][26][27][28].…”

Social Fever or General Immune Response? Revisiting an Example of Social Immunity in Honey Bees

“…In some cases, this interaction might be antagonistic, as was observed in the wounding response of adult workers [38]. In other instances, heat stress and immune gene expression are positively correlated, as was demonstrated in adult workers experimentally-infected with virus [39]. Given the amount of pathogen that was delivered to the small colonies, it is likely that a high number of adult workers were exposed and points to the need for further study of the linkage between the immune system and heat and other stress responses in both immature and adult honey bees.…”

Pesticide–Virus Interactions in Honey Bees: Challenges and Opportunities for Understanding Drivers of Bee Declines

“…Other immune system components involved in antiviral defense include autophagy, phagocytosis, and heat shock proteins [133][134][135]. Autophagy is an intracellular mechanism for degrading and recycling cytoplasmic components and occurs through the formation of double-membraned vesicles.…”

“…Phagocytosis is a cellular process by which certain hemocytes (i.e., macrophages/plasmatocytes) degrade dead, infected, or pathogenic cells, and this response can be crucial in eliminating virus-infected cells [134]. Heat shock proteins are part of the organismal stress responses, but their genes are also induced during viral infection to help reduce replication [135]. They also act as chaperones to help facilitate the RNAi antiviral pathway [136].…”