Barriers to success: How baculoviruses establish efficient systemic infections

Abstract

The mechanisms used by baculoviruses to exit the midgut and cause systemic infection of their insect hosts have been debated for decades. After being ingested, baculoviruses reach the midgut, where several host barriers need to be overcome in order to establish successful infection. One of these barriers is the basal lamina, a presumably virus-impermeable extracellular layer secreted by the epithelial cells lining the midgut and trachea. This review discusses new evidence that demonstrates how these viruses breach the basal lamina and establish efficient systemic infections. The biochemical mechanisms involved in dismantling basal lamina during baculovirus infection may also provide new insights into the process of basal lamina remodeling in invertebrate and vertebrate animals.

The scope of the crustacean immune system for disease control

“…For example, infections with Vibrio harveyi are known to cause extensive pathology and tissue inflammation in the gut and hepatopancreas in shrimp (Jiranvanichpaisal et al, 2010) and the gut is an area of localised changes in gene expression following infection (Soonthornchai et al, 2010). As recently described by Passarelli & Hall (2011) the midgut epithelia is also exploited by insect baculoviruses to escape from the midgut environment before removal by host epithelial cell sloughing. Knowledge of crustacean gut immunity is very limited, in part because of the dominant focus on the haemolymph and haemocytes as the main site of immune reactivity.…”

Recent Advances in Our Knowledge of Baculovirus Molecular Biology and Its Relevance for the Registration of Baculovirus-Based Products for Insect Pest Population Control

“…Sequence data from gammabaculoviruses failed to identify homologues to the alphabaculovirus fusion proteins, GP64 or F-protein (Duffy et al, 2006;Lauzon et al, 2006), indicating the absence of the BV phenotype. Also lacking in gammabaculoviruses are viral fibroblast growth factor (vfgf) homologues (Jehle et al, 2006), that have been shown to accelerate the establishment of systemic infections in alphabaculoviruses (Detvisitsakun et al, 2007;Passarelli, 2011). (See section 3.7.)…”

“…The BL serves as structural support for regenerating epidermal cells that replace senescing cells that were sloughed off during development or physical assaults to the gut and as a separation between the sterile hemocoelic organs and the midgut, thus preventing the passage of natural microbiota and pathogens acquired during feeding. A model for AcMNPV breaching of the BL has recently been proposed (Means & Passarelli, 2010;Passarelli, 2011). The tracheal system is the insect respiratory system and the first cells to be infected by BVs are the tracheoblasts (Engerhard et al, 1994;Kirkpatrick et al, 1994;Washburn et al, 1995) which are highly motile, singlecell tracheal projections that respond to signaling from oxygen deficient cells and organs.…”

“…To branch to other cells and tissues, tracheoblasts are thought to degrade the BL by secreting enzymes. Baculoviruses are the only viruses known to encode FGF signaling molecules (Passarelli, 2011). Conserved only in alphabaculoviruses and betabaculoviruses, but absent in midgut-restricted gammabaculoviruses and deltabaculoviruses, viral FGF (vFGF) has been shown to accelerate BV exit from midgut cells and secondary infection by rerouting the host respiratory system to the midgut epithelium by mimicking host FGF.…”

The Baculoviral Genome

“…Conversely, this gene is absent in Gamma and Deltabaculoviruses which cause midgut-restricted infections. Interestingly, it was found that the presence of v-fgf accelerates larval death as knockouts of these genes in AcMNPV and BmNPV caused a retardation in host death compared to infection with wild type viruses (Passarelli, 2011).…”