Research Article: Invasion of midgut epithelial cells by a persistently transmitted virus is mediated by sugar transporter 6 in its insect vector

Date Published: July 27, 2018

Publisher: Public Library of Science

Author(s): Faliang Qin, Wenwen Liu, Nan Wu, Lu Zhang, Zhongkai Zhang, Xueping Zhou, Xifeng Wang, John Carr.


Insect transmission is obligatory for persistently transmitted viruses because the vector insect is the only means of virus spread in nature. The insect midgut is the first major barrier limiting virus acquisition, but the mechanisms by which viruses are able to cross the cell membrane and then infect the midgut epithelial cells of the insect have not been elucidated completely. Here, we found that the outer capsid or nucleocapsid protein (NP) of three viruses can interact and colocalize with sugar transporter 6 that is highly expressed in the midgut of Laodelphax striatellus (LsST6). In contrast, LsST6 did not interact with the NP of rice grassy stunt virus, which cannot be transmitted by the same planthopper. LsST6 not only altered the cellular location of viral proteins and then colocalized with them in the cell membrane, but also mediated the entry of rice stripe virus (RSV) particles into Spodoptera frugiperda 9 (Sf9) cells that expressed the heterologous gene LsST6. We further showed that RSV particles initially bound to the cell membrane of midgut epithelial cells where it colocalized with LsST6, and then invaded the cytoplasm. When LsST6 expression was knocked down, viral titre, acquisition percentage and transmission efficiency of the treated insect decreased significantly, but virus replication was not affected. This work thus uncovered a strategy by which LsST6 mediates viral entry into midgut epithelial cells and leads to successful transmission by the insect vector.

Partial Text

Many viruses persistently transmitted by arthropods cause serious diseases in plants, animals and humans. More than 76% of plant viruses and 40% of mammalian viruses are transmitted to the hosts by specific arthropods, mainly planthoppers, aphids, mosquitoes, and ticks [1, 2]. Frequent epidemics of viral diseases in rice, wheat and vegetables are largely attributed to high populations and viral transmission efficiency of the insect vectors [3–6]. Similarly, viruses that cause diseases in humans and animals such as dengue fever, Zika fever and Japanese encephalitis, are vectored by different species of Aedes mosquitoes and are endemic in many areas of the developing world [7–10]. Understanding the virus–insect vector interaction and transmission mechanisms will provide important information on the epidemics of the diseases caused by plant and animal arboviruses and lead to the development of better control strategies.

The insect midgut consists mainly of a single layer of epithelial cells, with extensive microvilli on the lumen side and a porous basal lamina on the hemocoel side [37, 38]. The midgut absorbs the nutrients necessary for insect survival and provides an environment for the development and multiplication of viruses and parasites [39, 40]. The midgut epithelial cells have been identified as the initial infection site and the first barrier to virus invasion [1, 13, 41]. Our results on the distribution of RSV particles in the alimentary canal over time also demonstrated that the midgut epithelial cells of L. striatellus served as the initial infection site of RSV. After successful invasion of the midgut, RSV began its replication process, then spread into neighboring cells.