Elsevier

Virology

Volume 112, Issue 2, 30 July 1981, Pages 375-384
Virology

Penetration and uncoating of frog virus 3 (FV3) in cultured rat Kupffer cells

https://doi.org/10.1016/0042-6822(81)90284-1Get rights and content

Abstract

The in vitro interactions between unenveloped frog virus 3 and Kupffer cells have been studied at 37°, a nonpermissive temperature for viral multiplication. Kupffer cells were isolated by collagenase perfusion of rat livers followed by purification of the cells by centrifugal elutriation. Electron microscopic examinations revealed peculiar modes of interaction with the cellular membranes. Two hours after infection most virus particles were present in phagocytic vacuoles or dense and only few in pinocytic vesicles. About 25% of the engulfed virions displayed fusion between the trilaminar internal core membrane and the membrane of the vacuoles resulting in an opening of the shell that allowed dense core material to be released into the cytoplasm. The empty capsids were integrated into the membrane of the vacuole and were often invaded by the endoplasmic reticulum. Some virions fused directly with the plasma membrane allowing their electrondense content to be shed into the cytoplasm from the outside. Finally, some particles came into contact with the plasma membrane through a stalk-like structure which permitted the passage of the dense core material into the cell.

References (30)

  • A. Bingen-Brendel et al.

    Etude morphologique séquentielle du développment du FV3 sur cellules BHK21

    J. Microsc.

    (1971)
  • S. Dales

    Early events in cell-animal virus interaction

    Bacteriol. Rev.

    (1973)
  • S. Dales

    Penetration of animal viruses into cells

  • S. Fazekas De St. Groth

    Viropexis, the mechanism of Influenza virus infection

    Nature (London)

    (1948)
  • J.L. Gendrault et al.

    Interaction of Frog Virus 3 (FV3) with sinusoidal cells

  • Cited by (31)

    • Prior induction of cellular antiviral pathways limits frog virus 3 replication in two permissive Xenopus laevis skin epithelial-like cell lines

      2021, Developmental and Comparative Immunology
      Citation Excerpt :

      Our findings support the use of Xela DS2 and Xela VS2 to replicate FV3 and for use as in vitro models in which interactions between frog skin epithelial cells and FV3 can be examined. FV3 exists as enveloped and non-enveloped/naked virions and is known to enter host cells through receptor-mediated endocytosis (enveloped virions) or fusion at the plasma membrane followed by nucleocapsid injection into the cytoplasm (naked virions) (Braunwald et al., 1985; Gendrault et al., 1981; Houts et al., 1974; Kelly, 1975). In contrast to previous studies that suggest FV3 uses class A scavenger receptors for cellular entry in tadpole cell lines (American toad, wood frog, green frog, bullfrog) and adult X. laevis macrophages (Vo et al., 2019a), Xela DS2 and Xela VS2 do not express appreciable levels of class A scavenger receptor (srai/ii, scara3, scara4, scara5, and marco) transcripts despite being susceptible and permissive to FV3.

    • Ranaviruses and other members of the family Iridoviridae: Their place in the virosphere

      2017, Virology
      Citation Excerpt :

      Although an envelope is not needed to initiate a productive viral infection, the presence or absence of an envelope appears to determine the route of entry and the specific infectivity of the virion. Early studies indicated that enveloped viruses enter by receptor-mediated endocytosis whereas non-enveloped virions initiate infection by binding the plasma membrane with subsequent entry of the viral core into the cytoplasm (Braunwald et al., 1985, 1979; Gendrault et al., 1981; Liu et al., 2016). Recently entry via pinocytosis or caveolin-mediated mechanisms have been proposed (Guo et al., 2011, 2012; Jia et al., 2013; Wang et al., 2014).

    • Delineating the roles of cellular and innate antiviral immune parameters mediating ranavirus susceptibility using rainbow trout cell lines

      2017, Virus Research
      Citation Excerpt :

      FV3 preparations contain both enveloped particles and non-enveloped (naked) particles (Chinchar et al., 2011). While receptor-mediated endocytosis is one of two possible modes of entry, the other being fusion, it is likely the primary route (Gendrault et al., 1981; Braunwald et al., 1985; Chinchar, 2002). Thus, RTG-2 may express more surface receptors, to date of unknown identity, or have higher endocytic activity, to enhance virus attachment and entry respectively.

    • Amphibian (Xenopus laevis) tadpoles and adult frogs mount distinct interferon responses to the Frog Virus 3 ranavirus

      2017, Virology
      Citation Excerpt :

      Interestingly, murine FV3 infection models were employed for hepatitis research over 30 years ago (Gut et al., 1981; Kirn et al., 1982, 1980). While the temperature of 37 °C used for these studies are not permissive to FV3 replication (Aubertin et al., 1973), these studies demonstrated viral cell entry and release of viral content into host cell cytoplasm (Gendrault et al., 1981). In absence of viral replication, the FV3-induced pathology observed in these early studies would have had to stem from pre-packaged factors already present in the FV3 virions.

    View all citing articles on Scopus
    View full text