Non-susceptibility genes to Bombyx densovirus type 1, Nid-1 and nsd-1, affect distinct steps of the viral infection pathway

Kidokoro, Kurako; Ito, Katsuhiko; Ogoyi, Dorington O.; Abe, Hiroaki; Mita, Kazuei; Kadono-Okuda, Keiko

doi:10.1016/j.jip.2009.10.006

Cited by 10 publications

(5 citation statements)

References 6 publications

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“…The next issue will be to characterize the midgut-specific receptor molecule(s). Interestingly, in the silkworm Bombyx mori, two genes conferring resistance to BmDNV-1 have been identified; one, affecting the early recognition step, is a promising midgut receptor candidate gene that remains to be characterized (45). Although Jc-and BmDNV-1 differ in their structures, tissue tropisms, and replication strategies, characterizing both entry pathways in the midgut would be of great interest.…”

Section: Discussionmentioning

confidence: 99%

Densovirus Crosses the Insect Midgut by Transcytosis and Disturbs the Epithelial Barrier Function

Wang

Gosselin-Grenet

Castelli

et al. 2013

J Virol

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g Densoviruses are parvoviruses that can be lethal for insects of different orders at larval stages. Although the horizontal transmission mechanisms are poorly known, densoviral pathogenesis usually starts with the ingestion of contaminated food by the host. Depending on the virus, this leads to replication restricted to the midgut or excluding it. In both cases the success of infection depends on the virus capacity to enter the intestinal epithelium. Using the Junonia coenia densovirus (JcDNV) as the prototype virus and the lepidopteran host Spodoptera frugiperda as an interaction model, we focused on the early mechanisms of infection during which JcDNV crosses the intestinal epithelium to reach and replicate in underlying target tissues. We studied the kinetics of interaction of JcDNV with the midgut epithelium and the transport mechanisms involved. Using several approaches, in vivo, ex vivo, and in vitro, at molecular and cellular levels, we show that JcDNV is specifically internalized by endocytosis in absorptive cells and then crosses the epithelium by transcytosis. As a consequence, viral entry disturbs the midgut function. Finally, we showed that four mutations on the capsid of JcDNV affect specific recognition by the epithelial cells but not their binding.

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Section: Discussionmentioning

confidence: 99%

Densovirus Crosses the Insect Midgut by Transcytosis and Disturbs the Epithelial Barrier Function

Wang

Gosselin-Grenet

Castelli

et al. 2013

J Virol

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“…The midgut was dissected from day 3 fifth instar following exposure to BmDV on day 0 of the fourth instar stage. RT-PCR was performed for 30 cycles with primer sets for + nsd-1 , the NS1 gene of BmDV 20 , and ribosomal 18S as a positive control. ( B ) Immunohistochemical analysis of BmDV in the midgut of transgenic silkworms expressing the nonspliced form of the susceptibility gene + nsd-1 .…”

Section: Resultsmentioning

confidence: 99%

“…In addition, we are currently attempting to isolate another BmDV resistance gene, Nid-1 , by positional cloning. Nid-1 was shown to be required for a virus infection step that occurs after NSD-1 functions 20 . Based on this and our present results, the product of Nid-1 may function within the midgut cells.…”

Section: Discussionmentioning

confidence: 99%

“…We previously identified the nsd-2 gene by positional cloning and found that this gene encodes a putative amino acid transporter that may function as a cell-surface receptor for BmBDV 19 . During BmDV infection, nsd-1 and Nid-1 block the early and late steps of virus infection in the silkworm, respectively 20 . However, neither of these genes has been molecularly identified to date.…”

Section: Introductionmentioning

confidence: 99%

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A single amino acid substitution in the Bombyx-specific mucin-like membrane protein causes resistance to Bombyx mori densovirus

Ito

Kidokoro

Katsuma

et al. 2018

Sci Rep

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Bombyx mori densovirus type 1 (BmDV) is a pathogen that causes flacherie disease in the silkworm. The absolute nonsusceptibility to BmDV among certain silkworm strains is determined independently by two genes, nsd-1 and Nid-1. However, neither of these genes has been molecularly identified to date. Here, we isolated the nsd-1 gene by positional cloning and characterized the properties of its product, NSD-1. Sequence and biochemical analyses revealed that this gene encodes a Bombyx-specific mucin-like glycoprotein with a single transmembrane domain. The NSD-1 protein was specifically expressed in the larval midgut epithelium, the known infection site of BmDV. Sequence analysis of the nsd-1 gene from 13 resistant and 12 susceptible strains suggested that a specific arginine residue in the extracellular tail of the NSD-1 protein was common among susceptible strains. Germline transformation of the susceptible-type nsd-1 (with a single nucleotide substitution) conferred partial susceptibility to resistant larvae, indicating that the + nsd-1 gene is required for the susceptibility of B. mori larvae to BmDV and the susceptibility is solely a result of the substitution of a single amino acid with arginine. Taken together, our results provide striking evidence that a novel membrane-bound mucin-like protein functions as a cell-surface receptor for a densovirus.

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“…About 40 mutant genes have been identified so far by positional cloning or positional cloning combined with other methods. The genes identified are responsible for larval body color ( sch ) 18 , the larval stripe ( cts ) 19 , blood color ( Y and rb ) 20 21 , cocoon color ( Gb ) 22 , pupal and moth color 23 24 ( so and mln ), pathology mutants ( nsd-1 and nsd - 2 ) 25 26 , and moultinism ( mod and nm-g ) 27 28 . These mutants are valuable resources for studying the genetics and gene functions of the silkworm Bombyx mori .…”

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confidence: 99%

Functional Loss of Bmsei Causes Thermosensitive Epilepsy in Contractile Mutant Silkworm, Bombyx mori

Nie

Cheng

Huang

et al. 2015

Sci Rep

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The thermoprotective mechanisms of insects remain largely unknown. We reported the Bombyx mori contractile (cot) behavioral mutant with thermo-sensitive seizures phenotype. At elevated temperatures, the cot mutant exhibit seizures associated with strong contractions, rolling, vomiting, and a temporary lack of movement. We narrowed a region containing cot to ~268 kb by positional cloning and identified the mutant gene as Bmsei which encoded a potassium channel protein. Bmsei was present in both the cell membrane and cytoplasm in wild-type ganglia but faint in cot. Furthermore, Bmsei was markedly decreased upon high temperature treatment in cot mutant. With the RNAi method and injecting potassium channel blockers, the wild type silkworm was induced the cot phenotype. These results demonstrated that Bmsei was responsible for the cot mutant phenotype and played an important role in thermoprotection in silkworm. Meanwhile, comparative proteomic approach was used to investigate the proteomic differences. The results showed that the protein of Hsp-1 and Tn1 were significantly decreased and increased on protein level in cot mutant after thermo-stimulus, respectively. Our data provide insights into the mechanism of thermoprotection in insect. As cot phenotype closely resembles human epilepsy, cot might be a potential model for the mechanism of epilepsy in future.

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Non-susceptibility genes to Bombyx densovirus type 1, Nid-1 and nsd-1, affect distinct steps of the viral infection pathway

Cited by 10 publications

References 6 publications

Densovirus Crosses the Insect Midgut by Transcytosis and Disturbs the Epithelial Barrier Function

Densovirus Crosses the Insect Midgut by Transcytosis and Disturbs the Epithelial Barrier Function

A single amino acid substitution in the Bombyx-specific mucin-like membrane protein causes resistance to Bombyx mori densovirus

Functional Loss of Bmsei Causes Thermosensitive Epilepsy in Contractile Mutant Silkworm, Bombyx mori

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