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Open AccessArticle

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

1
Ecole Pratique des Hautes Etudes (EPHE), PSL Research Univ, DGIMI, Univ Montpellier, INRA, 34095 Montpellier, France
2
Diversité des Génomes et Interactions Microorganismes Insectes (DGIMI), Univ Montpellier, INRA, 34095 Montpellier, France
3
Estructura de Recerca Interdisciplinar en Biotecnologia I Biomedicina (ERI-BIOTECMED, Deaprtment of Genetics Faculty of Biological Sciences Univ Valencia, 46100 Burjassot, Spain
4
BioCampus, Univ Montpellier, CNRS, INSERM, 34000 Montpellier, France
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Unité de Glycobiologie Structurale et Fonctionnelle (UGSF) Univ Lille, CNRS, UMR 8576—UGSF, 59000 Lille, France
6
Institut Européen des Membranes (IEM), Univ Montpellier, CBRS, ENSCM, 34095 Montpellier, France
*
Authors to whom correspondence should be addressed.
Viruses 2019, 11(9), 870; https://doi.org/10.3390/v11090870
Received: 2 August 2019 / Revised: 9 September 2019 / Accepted: 11 September 2019 / Published: 17 September 2019
(This article belongs to the Special Issue New Insights into Parvovirus Research)
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. View Full-Text
Keywords: insect; Lepidoptera; insect parvovirus; chitin; peritrophins; glycans; biocontrol insect; Lepidoptera; insect parvovirus; chitin; peritrophins; glycans; biocontrol
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Pigeyre, L.; Schatz, M.; Ravallec, M.; Gasmi, L.; Nègre, N.; Clouet, C.; Seveno, M.; El Koulali, K.; Decourcelle, M.; Guerardel, Y.; Cot, D.; Dupressoir, T.; Gosselin-Grenet, A.-S.; Ogliastro, M. Interaction of a Densovirus with Glycans of the Peritrophic Matrix Mediates Oral Infection of the Lepidopteran Pest Spodoptera frugiperda. Viruses 2019, 11, 870.

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