Functional analysis of an immune gene of Spodoptera littoralis by RNAi

Lelio, Ilaria Di; Varricchio, Paola; Prisco, Gennaro Di; Marinelli, A.; Lasco, Valentina; Caccia, Silvia; Casartelli, Morena; Giordana, B.; Rao, Rosa; Gigliotti, Silvia; Pennacchio, Francesco

doi:10.1016/j.jinsphys.2014.03.008

Cited by 34 publications

(38 citation statements)

References 39 publications

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“…Previous work has shown that 102 Sl is directly involved in the regulation of encapsulation and melanization reactions by S. littoralis larvae (35). Because nodulation is an important antimicrobial immune response that shows functional similarity to the encapsulation of large foreign intruders (36), it was reasonable to investigate whether silencing of the 102 Sl gene in S. littoralis larvae has any effect on nodulation and, as a consequence, on the proliferation of microbial pathogens.…”

Section: Resultsmentioning

confidence: 99%

“…We have recently discovered that in Lepidoptera, regulation of the encapsulation and melanization process is mediated in part by a molecular scaffold composed of amyloid fibers (37), and that the RNAi-mediated silencing of the gene encoding the amyloidogenic protein (102 Sl) disrupts these immune responses (35). Here we have demonstrated that in S. littoralis, the nodulation/suppression of microbes is similarly affected by the silencing of this gene, whereas the phagocytic activity of hemocytes and the humoral antimicrobial response remain unaltered.…”

Section: Discussionmentioning

confidence: 99%

“…Silencing of the 102 Sl gene by RNAi and the assessment of its transcription level by qRT-PCR were performed as described previously (35).…”

Section: Methodsmentioning

confidence: 99%

“…To circumvent the problems associated with the manipulation of the midgut microbiota with antibiotics (22)(23)(24)(25)(27)(28)(29)(30)(31) or of the immune response with immunosuppressive molecules (26,34), both of which have unpredictable multiple effects, we performed selective RNAi-mediated silencing of an immune gene (102 Sl, 102 Spodoptera littoralis), recently identified in Spodoptera littoralis (35). This gene is highly expressed in the immune cells circulating in the hemolymph (i.e., hemocytes) and modulates their incorporation in multilayered capsules formed around foreign intruders entering the body cavity (i.e., the hemocoel) (35). The final result is the encapsulation of large objects and the nodulation of bacterial cells or aggregates, which are eventually suppressed by localized production of melanin and other toxic compounds on their surface (36,37).…”

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confidence: 99%

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Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism

Caccia¹,

Lelio

Storia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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147

122

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Bacillus thuringiensis is a widely used bacterial entomopathogen producing insecticidal toxins, some of which are expressed in insect-resistant transgenic crops. Surprisingly, the killing mechanism of B. thuringiensis remains controversial. In particular, the importance of the septicemia induced by the host midgut microbiota is still debated as a result of the lack of experimental evidence obtained without drastic manipulation of the midgut and its content. Here this key issue is addressed by RNAi-mediated silencing of an immune gene in a lepidopteran host Spodoptera littoralis, leaving the midgut microbiota unaltered. The resulting cellular immunosuppression was characterized by a reduced nodulation response, which was associated with a significant enhancement of host larvae mortality triggered by B. thuringiensis and a Cry toxin. This was determined by an uncontrolled proliferation of midgut bacteria, after entering the body cavity through toxin-induced epithelial lesions. Consequently, the hemolymphatic microbiota dramatically changed upon treatment with Cry1Ca toxin, showing a remarkable predominance of Serratia and Clostridium species, which switched from asymptomatic gut symbionts to hemocoelic pathogens. These experimental results demonstrate the important contribution of host enteric flora in B. thuringiensis-killing activity and provide a sound foundation for developing new insect control strategies aimed at enhancing the impact of biocontrol agents by reducing the immunocompetence of the host.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

“…Silencing of the 102 Sl gene by RNAi and the assessment of its transcription level by qRT-PCR were performed as described previously (35).…”

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism

Caccia¹,

Lelio

Storia

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

147

122

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“…Moreover, although the processes of clotting and of nodule and capsule formation differ in their final appearance, they share some molecular steps, and both involve melanin biosynthesis (24)(25)(26). Among the immune genes involved in these reactions is a sequence of key importance codes for a protein generating amyloid fibers that mediate encapsulation and strictly localized melanization of nonself material in Lepidoptera (27,28). Here we cloned and characterized the cDNA of the homolog of this gene in Apis mellifera (GenBank accession no.…”

Section: Dwv Infection and Honey Bee Immunosuppressionmentioning

confidence: 99%

A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Prisco

Annoscia

Margiotta

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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204

213

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Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite-virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.Apis mellifera | Varroa destructor | deformed wing virus | mutualistic symbiosis | honeybee colony losses

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