Abstract
Vector mosquitoes are responsible for transmission of the majority of arthropod-borne (arbo-) viruses. Virus replication in these vectors needs to be sufficiently high to permit efficient virus transfer to vertebrate hosts. The mosquito immune response therefore is a key determinant for arbovirus transmission. Mosquito antiviral immunity is primarily mediated by the small interfering RNA pathway. Besides this well-established antiviral machinery, the PIWI-interacting RNA (piRNA) pathway processes viral RNA into piRNAs. In recent years, significant progress has been made in characterizing the biogenesis and function of these viral piRNAs. In this review, we discuss these developments, identify knowledge gaps, and suggest directions for future research.
Highlights
Vector mosquitoes are responsible for transmission of the majority of arthropod-borne viruses
Since Piwi preferentially associates with PIWI-interacting RNA (piRNA) containing a uridine at the first nucleotide position, both sense and antisense viral piRNAs (vpiRNAs) produced in these cells bear a 1U bias (Table 1)
PIWI-dependence of vpiRNAs has been established for dengue, Sindbis, and Semliki Forest virus (Alphavirus genus, Togaviridae family) [31,32,36] and direct association with PIWI proteins has been demonstrated for Sindbis virus–derived piRNAs [32]
Summary
Mosquitoes and other hematophagous arthropods transmit important human and animal viruses, some of which are responsible for debilitating diseases such as dengue, chikungunya, and Zika [1]. MicroRNAs comprise an independent class of small RNAs that may be involved in the cellular response to arboviral infections by regulation of host immune genes [23] They are produced from genome-encoded stem-loop RNA structures in a Dicer-1- and Ago1-dependent manner, akin to siRNA biogenesis [24]. Since Piwi preferentially associates with piRNAs containing a uridine at the first nucleotide position, both sense and antisense vpiRNAs produced in these cells bear a 1U bias (Table 1). In combination with the predisposition of Zuc to cleave directly 50 of uridine residues, this causes Aub to associate predominantly with 1U antisense piRNAs. A subset of PIWI proteins, including Aub and silkworm Siwi, have an additional preference for target RNAs carrying an adenosine directly opposite of the first position of the piRNA [66,67]. PIWI-dependence of vpiRNAs has been established for dengue, Sindbis, and Semliki Forest virus (Alphavirus genus, Togaviridae family) [31,32,36] and direct association with PIWI proteins has been demonstrated for Sindbis virus–derived piRNAs [32]
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