Interaction of a Densovirus with Glycans of the Peritrophic Matrix Mediates Oral Infection of the Lepidopteran Pest Spodoptera frugiperda

Abstract

The success of oral infection by viruses depends on their capacity to overcome the gut epithelial barrier of their host to crossing over apical, mucous extracellular matrices. As orally transmitted viruses, densoviruses, are also challenged by the complexity of the insect gut barriers, more specifically by the chitinous peritrophic matrix, that lines and protects the midgut epithelium; how capsids stick to and cross these barriers to reach their final cell destination where replication goes has been poorly studied in insects. Here, we analyzed the early interaction of the Junonia coenia densovirus (JcDV) with the midgut barriers of caterpillars from the pest Spodoptera frugiperda. Using combination of imaging, biochemical, proteomic and transcriptomic analyses, we examined in vitro, ex vivo and in vivo the early interaction of the capsids with the peritrophic matrix and the consequence of early oral infection on the overall gut function. We show that the JcDV particle rapidly adheres to the peritrophic matrix through interaction with different glycans including chitin and glycoproteins, and that these interactions are necessary for oral infection. Proteomic analyses of JcDV binding proteins of the peritrophic matrix revealed mucins and non-mucins proteins including enzymes already known to act as receptors for several insect pathogens. In addition, we show that JcDV early infection results in an arrest of N-Acetylglucosamine secretion and a disruption in the integrity of the peritrophic matrix, which may help viral particles to pass through. Finally, JcDV early infection induces changes in midgut genes expression favoring an increased metabolism including an increased translational activity. These dysregulations probably participate to the overall dysfunction of the gut barrier in the early steps of viral pathogenesis. A better understanding of early steps of densovirus infection process is crucial to build biocontrol strategies against major insect pests.

Recent trends in insect gut immunity

“…The E75 transcription factor induces transcriptional HPx1 activation, and HPx1 knockdown accelerates DUOX-NADPH oxidase’s gut reactive oxygen species (ROS) production, thereby enhancing the immunological sensing of microbial infection ( 31 ). The peritrophic membrane of insects, exposed mucins and non-mucin protein receptors, functions as a binding site for various insect pathogens, such as Junonia coenia densovirus ( JcDV ) ( 32 ). Different protein classes within the insect PM exhibit distinct activities: Class I PM proteins contribute to PM integrity and function; Class II proteins faintly interact with the PM through adsorption; Class III proteins are released under harsher conditions; and Class IV proteins are covalently linked to other PM proteins or chitin, making their removal challenging ( 33 ).…”

Viruses of the Fall Armyworm Spodoptera frugiperda: A Review with Prospects for Biological Control

“…Furthermore, some densoviruses have been successfully used to control insect pests [88]. Junonia coenia densovirus (JcDV), originally isolated from the buckeye butterfly J. coenia, can orally infect S. frugiperda larvae by rapidly binding to the peritrophic matrix of the insect midgut through interaction with different glycans, including chitin and glycoproteins [89]. In addition, JcDV also interferes with midgut gene expression, which leads to dysfunction of the gut barrier [89].…”

“…Junonia coenia densovirus (JcDV), originally isolated from the buckeye butterfly J. coenia, can orally infect S. frugiperda larvae by rapidly binding to the peritrophic matrix of the insect midgut through interaction with different glycans, including chitin and glycoproteins [89]. In addition, JcDV also interferes with midgut gene expression, which leads to dysfunction of the gut barrier [89]. JcDV rescued from lysate of insect cells transfected with JcDV infectious clone caused mortality in second instar of S. frugiperda [51].…”

New Insights into Parvovirus Research

“…The initial phases of virus–cell interaction are a relevant matter of investigation. The interaction of Junonia coenia densovirus with the midgut barriers of caterpillars has been analysed in detail, to yield a picture of the initial phases of infection that involve binding to host glycans and later disruption of the peritrophic matrix, as presented in [13]. Concerning the human pathogenic parvovirus B19, its very selective tropism for erythroid progenitor cells critically depends on the presence of a specific receptor for the VP1 unique region, but the subsequent steps that are also critical to the outcome of infection still need to be further characterised.…”