Abstract
Viruses enter host cells via several mechanisms, including endocytosis, macropinocytosis, and phagocytosis. They can also fuse at the plasma membrane and can spread within the host via cell-to-cell fusion or syncytia. The mechanism used by a given viral strain depends on its external topology and proteome and the type of cell being entered. This comparative review discusses the cellular attachment receptors and entry pathways of dsDNA viruses belonging to the families Adenoviridae, Baculoviridae, Herpesviridae and nucleocytoplasmic large DNA viruses (NCLDVs) belonging to the families Ascoviridae, Asfarviridae, Iridoviridae, Phycodnaviridae, and Poxviridae, and giant viruses belonging to the families Mimiviridae and Marseilleviridae as well as the proposed families Pandoraviridae and Pithoviridae. Although these viruses have several common features (e.g., topology, replication and protein sequence similarities) they utilize different entry pathways to infect wide-range of hosts, including humans, other mammals, invertebrates, fish, protozoa and algae. Similarities and differences between the entry methods used by these virus families are highlighted, with particular emphasis on viral topology and proteins that mediate viral attachment and entry. Cell types that are frequently used to study viral entry are also reviewed, along with other factors that affect virus-host cell interactions.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Viruses utilize several mechanisms to enter host cells. This review focuses on the relationships between the external topology of the virions and their entry mechanisms in different cell types, as well as the roles of cellular receptors and viral attachment factors. Ten viral families are discussed, including Adenoviridae, Baculoviridae, Herpesviridae, and nucleocytoplasmic large DNA viruses (NCLDVs). The NCLDVs include large and giant viruses characterized by their large virions and genomes, and can be classified into several distinct families: Ascoviridae, Asfarviridae, Iridoviridae, Mimiviridae, Marseilleviridae, Phycodnaviridae and Poxviridae. They also include members of the proposed families Pandoraviridae and Pithoviridae as well as the recently isolated molivirus and faustovirus [1,2,3,4]. They replicate completely or partially in the cytoplasm and are larger than other viruses. They may also have several common traits, including similarities in their protein sequences and topological features. Figure 1 shows the external topology of each viral family. They might be evolutionary related and share a common ancestor [5, 6]. It has been proposed that the NCLDVs be classified into one order, named “Megavirales” [7], whereas, herpesviruses belong to the order Herpesvirales. Generally, mimiviruses and phycodnaviruses are closely related to pandoraviruses and moliviruses, whereas pithoviruses are related to marseilleviruses, iridoviruses and ascoviruses, and faustovirus are closely related to asfarviruses, [1,2,3,4, 8, 9].
Virus attachment and receptors
Viruses attach to proteins known as cellular receptors or attachment factors on the surface of the host cell [11, 12]. In addition, certain membrane lipids and glycans may be necessary for viral entry. These factors stabilize the virus on the cell surface and allow it to circumvent the cell’s barriers to entry. High-affinity interactions between viral proteins and cellular receptors drive conformational changes in the proteins’ structures that activate signaling cascades and destabilize the plasma membrane, leading to pore formation and internalization of the virus as shown in Figure 2a [13]. These interactions can be initiated by specific motifs or domains in both viral and host proteins. Notable viral protein motifs that facilitate entry by binding to cellular counterparts include the integrin-binding (RGD), endocytosis (PPxY and Yxx[FILV]), and clathrin endocytosis (PWxxW) motifs, where “x” denotes any residue [14]. It is worth noting that a receptor could be accompanied by an additional co-receptor that triggers a particular entry pathway or stabilizes the virus at plasma membrane.
General mechanisms of virus entry
Cells can internalize viruses by endocytosis, as reviewed elsewhere [11,12,13, 15,16,17] and depicted in Figure 2. Alternatively, the virus may fuse with the cell membrane. Several factors determine which entry mechanism will be active, including the cell type and the cellular receptors it displays. Aspects of the virus’ external topology, such as the presence of surface protrusions or glycoproteins, may also affect the entry process. Viruses enter host cells via one of three major pathways:
(A) Fusion: Viral proteins promote the fusion of the virion with the plasma membrane, which then form a pore, and the virion becomes uncoated. Its genomic cargo is then transferred into the cytoplasm [12, 13, 18,19,20,21]. The proteins involved in fusion, so-called fusogens, can be divided into three classes: (i) class I fusogens, which are dominated by α-helical coils; (ii) class II fusogens, which consist predominantly of β-sheets; and (iii) class III fusogens, which feature both secondary structure types.
(B) Cell-cell fusion: Some viruses such as vaccinia virus (VV) and herpes simplex virus (HSV) induce the expression of proteins on the surfaces of infected cells that attract uninfected cells and cause them to fuse with the infected cell at low pH values to form a multinuclear cell known as a syncytium [11, 13, 22, 23]. Syncytium formation represents a very efficient way for a virus to spread within a host: it circumvents the immune response and creates a good site of replication for a nuclear-replicating virus. It should be noted that syncytium formation is not always regarded as an entry mechanism per se.
(C) Endocytosis: Once the cell internalizes the virus, it is then delivered to an acidic pit, a so-called early endosome. The virus then may be transferred into a late endosome and then to a lysosome. Alternatively, due to the low pH value in the lumen of endosomes, the viral membrane can fuse with the endosomal membrane, releasing the viral genome into the cytoplasm [12]. After exiting from endosomes, some adenoviruses or poxviruses may use microtubules for transport within the cytoplasm. Once in cytoplasm, some viruses move toward the nucleus to deliver their cargo inside the nucleus, whereas the NCLDVs usually remain in cytoplasm to initiate their replication cycle. Dynamin GTPase may have a key role in regulating most endocytic pathways. During virus entry, dynamin is deposited in the neck of the endocytic pit toward the cytoplasm leading to the excision of the pit [24, 25]. There are several major endocytosis-based pathways that viruses can use to enter cells and evade the host’s immune system. These pathways differ in terms of the types of particles involved and the molecules that are important in the process. The most important viral entry pathways are as follows:
-
(1)
Phagocytosis (cell eating), which occurs in specialized mammalian cells (so-called professional phagocytes, e.g., dendritic cells and macrophages) that engulf large and essential particles. Viral entry by this pathway typically involves the formation of large extracellular projections, and the internalized virus is taken into a phagosome. Actin and RhoA are typically necessary for this process.
-
(2)
Pinocytosis (cell drinking), which is the process by which cells take up solutes and fluids. Pinocytotic processes can be further classified based on the membrane structures and types of molecules they are associated with. Macropinocytosis is a nonspecific process, and particles internalized by this route may not be essential for the cell. When it is exploited by viruses, interactions between viral proteins and cell receptors activate intracellular signaling and actin rearrangements that form ruffles or filopodia on the external surface of the host cell. The ruffles then close up to form a vesicle known as a macropinosome, which carries the virus into the cytosol. Actin, Rho GTPases (Rac and Cdc42), PI3K, and Na+/H+ exchange are usually required for this pathway, and kinases are required to regulate macropinosome formation and closure. Although dynamin might not be required for some viruses to enter via macropinocytosis, some strains of adenoviruses and poxviruses require dynamin to enter the cell.
-
(3)
Clathrin-mediated endocytosis, which is the process by which the cell internalizes the virus in a clathrin-rich flask-shaped invagination/cavity (vesicle) known as a clathrin-coated pit. The virus is then delivered into the cytoplasm via endosomes. Clathrin and cholesterol are required, and dynamin and transferrin are usually involved in pit formation.
-
(4)
Caveolar/raft endocytosis, which is similar to clathrin-mediated endocytosis but involves pits containing caveolin-1 rather than clathrin. The internalized virus is delivered to the cytoplasm in cave-like bodies known as caveolae or caveosomes, whose internal pH is neutral.
-
(5)
Endocytosis based on other routes. These pathways involve vesicles that contain neither clathrin nor caveolin. However, like the clathrin- and caveolin-based pathways, they generally require dynamin, cholesterol and/or lipids. Interestingly, lymphocytic choriomeningitis virus uses a dynamin-, clathrin-, and caveolin-independent route that is also independent of actin, lipid rafts, and the pH [26, 27].
Mechanisms of attachment and entry utilized by large and giant DNA viruses
Members of all ten viral families covered in the review infect a wide range of potential hosts, including humans, other mammals, invertebrates, fish, protozoa, and algae, causing serious problems in public health, livestock farming, and aquaculture (Table 1). As suggested by this diversity of potential hosts, they can use many different mechanisms to enter host cells, and members of the same viral family may use very different mechanisms to enter a given host cell type. To ensure an efficient virus infection, a virus may utilize more than one mechanism to enter a given host cell.
Adenoviridae
Adenoviruses (Ad) are non-enveloped icosahedral viruses with diameters of 70-90 nm (Fig. 1) that can be divided into seven groups and 50+ serotypes. They harbor 30 to 40-kb linear dsDNA genomes encoding around 45 proteins, and they replicate in the nucleus. Their genomes encode fiber proteins with a conserved N-terminal tail, a shaft, and a globular knob domain. The lengths of these fibers are similar within a serotype, but Ad-F and Ad-G encode two fiber proteins: short and long [28, 29]. The fibers bind to a wide range of cell receptors [30]; upon binding at the plasma membrane, the fibers become detached from the viral core and remain at the surface, while the core enters the cell [30,31,32]. The coxsackie-adenovirus receptor (CAR) is a functional receptor for most Ad strains [33]; it is expressed in the tight junctions in the epithelial cells of some human tissues (brain, heart and pancreas) and various tumor cells, but not in mice or primates [34, 35] (Table 2). The long viral fibers are flexible enough to permit the fiber knob to interact with CAR, bringing the penton base of the viral capsid into contact with integrins in the host cell membrane. Other cellular receptors targeted by adenoviruses include CD46, CD80, CD86, desmoglein-2, heparan sulphate, sialic acid, major histocompatibility complex-1-α2, and vascular cell adhesion molecule-1. Ad-2, Ad-5 and egg drop syndrome virus enter host cells via clathrin-mediated endocytosis [36,37,38], whereas Ad-3, Ad-5 and Ad-35 enter via macropinocytosis [37, 39]. Longer lists of cellular receptors and entry pathways exploited by adenoviruses are given in Tables 2 and 3.
Herpesviridae (order Herpesvirales)
Herpesviruses (HVs) have an enveloped icosahedral virion (150-200 nm) containing a 120 to 240-kb linear dsDNA genome encoding 100-200 proteins (see Figure 1 and Table 1). They replicate in the nucleus. The >70 known members of this family include eight human pathogens: HSV-1, HSV-2, CMV, EBV, KSHV, VZV, HHV-6 and HHV-7. HVs are rich in glycoproteins (GPs) that can form heterodimeric complexes to facilitate attachment and entry [55, 56]. Several proteins are involved in their attachment, including viral GPs (gB, gC, gD, gH/gL, and the gH/gL/gO complex) and host cell proteins such as HVEM, integrins, heparan sulphate, syndecan, and neuropilin [57,58,59,60,61,62]. HVEM was the first recognized receptor for HSV-1/2 gD (see Table 3). HV has a bacteriophage-like short tail whose role in entry is currently unknown [63]. Interestingly, an analysis of cytomegalovirus (CMV) showed that the genomes of clinical samples contain at least 19 genes that are absent in laboratory-acclimated strains [64]. Three of these missing proteins, UL128, UL130 and UL131, contribute to viral entry by binding to gH/gL [64,65,66,67,68,69]. HVs generally enter host cells by endocytosis or fusion with the plasma membrane [149, 71,72,73,74,75,76,77]. HSV-1, CMV, EBV, KSHV and VZV enter via endocytosis [78, 61, 79,80,81,82,83,84,85,86,87]. KSHV has been observed to enter endothelial cells by pinocytosis [88] but enters monocytes via some other mechanism that may involve heparan sulphate, integrins, and the induction of Src and PI3 K signaling [89]. Details on the entry mechanisms of HVs and receptors mediating their attachment and entry can be found in Table 3.
Baculoviridae
Baculoviruses are arthropod-specific enveloped virus with nucleocapsid dimensions of 21 × 260 nm (Fig. 1). They have circular dsDNA genomes of 80-180 kb that encode 100-180 proteins and replicate in the nucleus. They are used in biocontrol against insects, and as vectors for gene transfer and protein expression. Consequently, their entry into insect, human, and cancer cells has an increasing biological impact (see Tables 1 and 3). Two baculovirus phenotypes have been characterized: budded and occlusion-derived. Viruses of this family express two crucial fusogens, gp64 (class III) and F (class I), which are functionally analogous and can both trigger low-pH membrane fusion during endocytosis. There are evidences that gp64 facilitate virus entry and fusion with the plasma membrane [167,168,169,170]. Bombyx mori nucleopolyhedrovirus (BmNPV) enters Bombyx mori (BmN) cells via cholesterol-dependent macropinocytosis [171], while Autographa californica multiple nucleopolyhedrovirus (AcMNPV) grown in Spodoptera frugiperda (sf9) cells enters human hepatocarcinoma (HepG2) and embryonic kidney (293) cell lines via a dynamin-, raft- and RhoA-dependent phagocytosis-like mechanism [172], but clathrin-mediated endocytosis or macropinocytosis may not be involved in the virus uptake. However, recombinant AcMNPV from sf21 cells enters BHK-21 cells via low-pH clathrin-mediated endocytosis [173]. Additionally, a pseudotyped vesicular stomatitis virus (VSV) encoding gp64 grown in Sf9 cells enters the Huh7 and 293 cells via macropinocytosis and endocytosis, which is mediated by viral gp64, and cellular cholesterol, dynamin and clathrin [169]. This process also requires the host cell proteins HSPG and syndecan-1 [174], as well as cholesterol [169, 175].
Poxviridae
Poxviruses are widely distributed enveloped viruses (∼360 × 270 × 250 nm) that replicate in the cytoplasm (Fig. 1) [176]. They harbor a 130 to 375-kb linear genome that encodes ~200 proteins. Vaccinia virus (VV) is a prototypic virus of this class that was used as a smallpox vaccine. It exists in three forms [177, 178]. The first is the mature virion (MVs, also known as the intracellular mature virus, IMV or INV), which has a brick-shaped structure; it is the most abundant, stable and simple form and is active in host-host transmission. The second form is the wrapped virion (WV or intracellular enveloped virus, IEV), which contains an MV core wrapped in two membranes. WVs travel to the cell periphery via microtubules and fuse with the plasma membrane, and they are then released by exocytosis as the third form, the extracellular virion (EV, or cell-associated extracellular enveloped virus, CEV, or extracellular enveloped virus, EEV), which is specialized for exiting and cell-to-cell transmission within the host.
Four proteins are used for attachment to the cell surface (A26, A27, D8 and H3), and the MV displays the so-called entry-fusion complex (EFC), which consists of 11 proteins (A16L, A21L, A28L, F9, G3L, G9R, H2, J5, L1R, L5R and O3L). These proteins interact with one another and mediate virus-cell fusion, membrane disruption, and cell-to-cell fusion [176, 179, 180] (Tables 3 and 4). Inhibition of any of these proteins destabilizes the complex and hence perturbs viral entry. MV enters host cells via endocytosis or fusion with the plasma membrane, leaving the virus in endosomes [179,180,181,182,183,184] (see Table 3). Notably, the mechanisms of fusion for MVs and EVs at the plasma membrane and endosome are identical, and both require EFC proteins. VV (MV/EV), WR, and IHD-J enter HeLa cells via macropinocytosis [132, 134,135,136,137,138,139] and have also been suggested to enter via a parallel endocytotic mechanism [138]. In Drosophila, VV enters DL1 cells by macropinocytosis [147], but it enters S2 cells via endocytosis [148].
Giant viruses (Mimiviridae and Marseilleviridae)
These families comprise the largest known viruses, so-called giant viruses (GVs). They have genomes of ~0.5-2.5 Mb that encode 400-2500 proteins, and they replicate in the cytoplasm. Representatives of these families have been isolated from diverse habitats, including bronchoalveolar lavage fluid [204] and stools [205] from patients with pneumonia, insects [206], and leeches [207] (for a detailed review, see reference [208], [209]). The nature of the relationship between giant viruses and pneumonia remains to be elucidated [209,210,211,212]. Briefly, the giant viruses were detected by serological and genomic methods in patients with respiratory symptoms. Moreover, recent images show giant virus- and virus factory-like structures in number of human cells [213].
Mimivirus virions are 500 nm in diameter, with a 1 Mb dsDNA genome encoding 900 proteins. Their surfaces are completely covered with fibers (120 nm long) attached to the capsid via a disc-shaped feature except at one capsid vertex (Fig. 1). The outer fibers may play some role in the virus’ attachment to or entry into host cells [214, 215], but the details of its mechanisms of attachment and entry are unknown. Proteomic and gene silencing experiments revealed that the fibres consist of at least four proteins (R135, L725, L829, and R856); viruses in which any of these proteins are silenced exhibit short and deformed fibers [214, 216,217,218,219], as shown in Figure 3. Further structural analysis showed that R135 is a component of the fibers and is required for host cell entry [219]. In addition, a electron microscopy showed that L725 aggregates form fibre-like architectures [217]. The fibers’ shape differs from that in other viruses, and the fiber proteins exhibit no sequence similarity to proteins encoded by other viruses. It should be noted that some giant viruses lack external fibers – for instance, marseilleviruses (which are 200 nm in diameter with 350-kb circular dsDNA genomes) have topologies similar to those of mimiviruses but have only short (12 nm) or no fibers [216].
Mimiviruses enter amoebae or macrophages via a phagocytosis-like mechanism that depends on dynamin, actin and PI3-K [220, 221]. Unlike poxviruses, the entire virion with fiber can be seen inside the host. Further analyses showed that individual Marseillevirus virions enter A. castellanii cells via phagocytosis or in vesicles, endocytosis and micropinocytosis, were also suggested, but remain to be investigated [222]. Because the closely related Mimiviruses enter cells via phagocytosis, it seems very plausible that Marseillevirus could also enter via such a mechanism. It should be noted that the original host of most giant virus strains, including APMV, is not known; neither amoebae nor macrophages are their natural hosts. The tropism of these viruses and their interactions with their natural host cells thus remain to be elucidated.
Phycodnaviridae
The Phycodnaviridae are marine enveloped viruses with dimensions of 100-220 nm that have 330 to 560-kb linear dsDNA genomes and replicate in the cytoplasm of algae (Fig. 1). Despite having algal hosts, their entry pathways resemble those used by bacteriophages and animal viruses. Paramecium bursaria chlorella virus (PBCV-1) attaches to host cells via a viral vertex and degrades the host cell wall at the site of attachment like a bacteriophage [223]. To this end, it encodes chitinases, chitosanase, β -1,3-glucanase, and alginase enzymes that catalyze cell wall lysis [224]; it also encodes potassium ion channel proteins, which have a putative role in entry [225, 226]. After entry, PBCV leaves an empty shell at the cell surface. Another member of this family, Emiliania huxleyi virus 86, enters host cells via endocytosis or fusion of the outer lipid membrane surrounding the capsid, which is similar to animal virus entry [227]. The intact virion can be seen in the cytoplasm before the capsid breaks down to release the genome. Ectocarpus fasciculatus virus infects zoospores or gametes of brown algae that lack cell walls [228]. It fuses with the outer plasma membrane of the host cell, leaving the capsid outside the cell surface, and injects its genomic cargo into the cytoplasm.
Asfarviridae
These are enveloped viruses (175-215 nm, see Figure 1) with 170 to 190-kb linear dsDNA genomes encoding around 150 genes. They infect macrophages and monocytes of pigs and argasid ticks, and they replicate in the nucleus and/or cytoplasm. The early steps in the binding and entry of African swine fever virus (ASFV) into host cells are largely unknown [229]. The ASFV-E70 and Ba71V strains enter Vero cells and macrophages by low-pH-, dynamin-, and clathrin-dependent endocytosis, which requires actin, small GTPase Rab7 and PI3-K. Additionally, cholesterol may be needed to liberate the virus from endosomes into the cytoplasm [230,231,232,233,234]. There is also evidence that ASFV can enter via macropinocytosis, which requires actin, kinases and Na+/H+ exchange [235].
Iridoviridae
The iridoviruses include both enveloped and non-enveloped viruses with dimensions of 120-350 nm that replicate in the cytoplasm of insect and fish cells (Fig. 1). They harbor 100 to 200-kb linear dsDNA genomes with circularly permuted and redundant termini. The enveloped viruses fuse with the cell membrane of the host cell, whereas the non-enveloped viruses enter via endocytic pathways [236] (see Table 3). Frog virus 3, tiger frog virus, and infectious spleen and kidney necrosis virus enter BHK-21, HepG2 and Mandarin fish fry cells, respectively, by endocytosis [159,160,161,162]. The VP088 protein encoded by SGIV facilitates both endocytosis and macropinocytosis into a grouper spleen cell line [163, 164].
Ascoviridae
These viruses (~130 nm diameter, 200-400 nm in length) infect invertebrates; they replicate in the nucleus and harbor 150 to 190-kb circular dsDNA genomes that encode 180 proteins (Fig. 1). They are phylogenetically related to iridoviruses, and their entry mechanisms are obscure. However, Heliothis virescens ascovirus-3e infections are known to require actin rearrangement [237].
Conclusion and future perspectives
Viruses enter host cells via several mechanisms, depending on the host cell type and viral strain. Concerns about the risks of viral outbreaks have prompted efforts to characterize emerging pathogens and predict the emergence and properties of new viruses. A further motivating factor for such studies is the possibility of developing non-cytotoxic antiviral drugs that act outside host cells by preventing viral attachment or entry rather than disrupting viral replication inside cells. This review details the entry pathways exploited by large dsDNA viruses. Their entry pathways are affected by several factors, including the external topology of the virions (particularly the presence of surface protrusions and their topology), the targeted cell type, the cellular receptors that are present, and the viral protein content.
While viruses from the same viral family often have similar topologies and encode proteins with similar sequences and structures, they may still use different entry mechanisms. As mentioned in Table 3, the virus protein(s) may bind to one or more receptors and co-receptors (see herpesviruses for examples). The binding may activate number of factors (proteins/pathways) that are relevant to infection. These factors could be characteristics of other entry pathways (see, for example, entry of KSHV). Additionally, the MV form of vaccinia virus can enter cells by direct fusion with either the plasma membrane or the membrane of a vesicle after endocytosis.
It is worth emphasizing that additional factors could affect the entry mechanism. Among these factors is protein sequence similarity; some viral proteins exhibit functional and structural similarities despite having little or no sequence similarity. For example, the HSV-1 protein gB is a class III fusogen that resembles (especially in its post-fusion conformation) the gG protein of the RNA rhabdovirus VSV and the baculovirus protein gp64 [72, 238,239,240,241]. Additionally, the EBV protein gp42 is a functional homolog of HSV gD, but the two share no sequence similarity [110]. The functional motifs of viral proteins appear to play central roles in determining the entry pathways available to specific viruses, so their analysis could enable prediction of entry pathways and virus-host cell interactions [14, 242]. Closely related viruses that infect the same host generally have similar functional motif profiles [242]. Another factor that may be important is ubiquitination of viral proteins inside host cells, which can affect infection and microtubule trafficking. For instance, the adenovirus protein VI recruits Nedd4 E3 ubiquitin ligases via interactions involving its PPxY motif [14, 61, 243, 244]. Biophysical factors may also affect viral entry. For example, the entry of CMV into vascular endothelial cells is promoted by low levels of shear stress [245]. Similarly, the fusion of the enveloped HSV requires a negative curvature of the lipid bilayer and can thus be suppressed by factors that prevent the formation of such negative curvature [246].
Differences in observed entry pathways for different strains or different samples of the same viral strain may be due to differences in experimental design and conditions [61], the use of a non-physiological host in vitro (e.g., non-wild-type cells), or the use of a laboratory strain whose gene content differs from that of the wild-type virus, as in the case of CMV [64]. It is generally accepted that cell lines (i.e., immortalized cells) often differ genetically and phenotypically from cells in native tissues (or primary cells). Consequently, the type of cell used when studying viral entry may profoundly affect the results obtained. It has also been shown that baculoviruses grown in different insect cell types enter mammalian cells via different mechanisms [247]. These results clearly show that there are several aspects of viral entry into host cells that are very poorly understood. Comparative studies could potentially shed important light on this topic and help to clarify unknown aspects of virus-host cell interactions. In addition, more comprehensive information on viral topology and protein sequences will help to understand virus tropism. Further studies in this area should focus on predicting viral entry mechanisms and the evolution of interactions between host cells and viruses. Efforts should also be made to identify optimal experimental conditions for viral entry in different cell types and for different viral families.
Abbreviations
- dsDNA:
-
double-stranded DNA
- CHO:
-
Chinese hamster ovary
- DC:
-
dendritic cell
- EnC:
-
endothelial cell
- EpC:
-
epithelial cell
- FbC:
-
fibroblast cell
- VV:
-
vaccinia virus
- WR:
-
VV Western Reserve
- IHD-J:
-
International Health Department-J
- AcMNPV:
-
Autographa californica multiple nucleopolyhedrovirus
- BmNPV:
-
Bombyx mori nucleopolyhedrovirus
- ISKNV:
-
infectious spleen and kidney necrosis virus
- SGIV:
-
Singapore grouper iridovirus
- ASFV:
-
African swine fever virus
- HHV:
-
Human herpesvirus
- HSV:
-
herpes simplex virus type 1 or 2 (HSV-1 or HSV-2, also known as HHV-1 and HHV-2, respectively)
- VZV:
-
varicella-zoster virus (or HHV-3)
- EBV:
-
Epstein-Barr virus (or HHV-4)
- CMV:
-
cytomegalovirus or human CMV (HCMV or HHV-5)
- KSHV:
-
Kaposi’s sarcoma-associated HV (HHV-8)
- VSV:
-
vesicular stomatitis virus
- CAR:
-
coxsackie-adenovirus receptor
- DSG2:
-
desmoglein-2
- ESCRT:
-
endosomal sorting complexes required for transport
- GAGs:
-
glycosaminoglycan
- GD1a:
-
disialogangliotetraosylceramide
- HLA:
-
human leukocyte antigen
- HS:
-
heparan sulphate
- HSPG:
-
heparan sulphate proteoglycans
- HVEM:
-
herpesvirus entry mediator
- IFN:
-
interferon
- MHC:
-
major histocompatibility complex
- PGs:
-
proteoglycans
- PI3-K:
-
phosphatidylinositol 3-kinase
- PILR-α:
-
paired immunoglobulin-like receptor alpha
- PS:
-
phosphatidylserine
- VCAM-1:
-
vascular cell adhesion molecule 1
References
Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C, Garin J, Claverie JM, Abergel C (2013) Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341(6143):281–286. doi:10.1126/science.1239181
Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, Lescot M, Poirot O, Bertaux L, Bruley C, Coute Y, Rivkina E, Abergel C, Claverie JM (2014) Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci USA 111(11):4274–4279. doi:10.1073/pnas.1320670111
Legendre M, Lartigue A, Bertaux L, Jeudy S, Bartoli J, Lescot M, Alempic JM, Ramus C, Bruley C, Labadie K, Shmakova L, Rivkina E, Coute Y, Abergel C, Claverie JM (2015) In-depth study of Mollivirus sibericum, a new 30,000-year-old giant virus infecting Acanthamoeba. Proc Natl Acad Sci USA 112(38):E5327–E5335. doi:10.1073/pnas.1510795112
Reteno DG, Benamar S, Khalil JB, Andreani J, Armstrong N, Klose T, Rossmann M, Colson P, Raoult D, La Scola B (2015) Faustovirus, an asfarvirus-related new lineage of giant viruses infecting amoebae. J Virol 89(13):6585–6594. doi:10.1128/jvi.00115-15
Nasir A, Caetano-Anolles G (2015) A phylogenomic data-driven exploration of viral origins and evolution. Sci Adv 1(8):e1500527. doi:10.1126/sciadv.1500527
Aherfi S, Colson P, La Scola B, Raoult D (2016) Giant viruses of amoebas: an update. Front Microbiol 7:349. doi:10.3389/fmicb.2016.00349
Colson P, De Lamballerie X, Yutin N, Asgari S, Bigot Y, Bideshi DK, Cheng XW, Federici BA, Van Etten JL, Koonin EV, La Scola B, Raoult D (2013) “Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch Virol 158(12):2517–2521. doi:10.1007/s00705-013-1768-6
Yutin N, Koonin EV (2013) Pandoraviruses are highly derived phycodnaviruses. Biol Direct 8:25. doi:10.1186/1745-6150-8-25
Fischer MG, Allen MJ, Wilson WH, Suttle CA (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 107(45):19508–19513. doi:10.1073/pnas.1007615107
Hulo C, de Castro E, Masson P, Bougueleret L, Bairoch A, Xenarios I, Le Mercier P (2011) ViralZone: a knowledge resource to understand virus diversity. Nucleic Acids Res 39(Database issue):D576–D582. doi:10.1093/nar/gkq901
Marsh M, Helenius A (2006) Virus entry: open sesame. Cell 124(4):729–740. doi:10.1016/j.cell.2006.02.007
Grove J, Marsh M (2011) The cell biology of receptor-mediated virus entry. J Cell Biol 195(7):1071–1082. doi:10.1083/jcb.201108131
Dimitrov DS (2004) Virus entry: molecular mechanisms and biomedical applications. Nat Rev Microbiol 2(2):109–122. doi:10.1038/nrmicro817
Sobhy H (2016) A review of functional motifs utilized by viruses. Proteomes 4(1):3. doi:10.3390/proteomes4010003
Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422(6927):37–44. doi:10.1038/nature01451
Mercer J, Helenius A (2009) Virus entry by macropinocytosis. Nat Cell Biol 11(5):510–520. doi:10.1038/ncb0509-510
Vazquez-Calvo A, Saiz JC, McCullough KC, Sobrino F, Martin-Acebes MA (2012) Acid-dependent viral entry. Virus Res 167(2):125–137. doi:10.1016/j.virusres.2012.05.024
Kielian M, Rey FA (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4(1):67–76
Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15(7):690–698
White JM, Delos SE, Brecher M, Schornberg K (2008) Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol 43(3):189–219
Backovic M, Jardetzky TS (2009) Class III viral membrane fusion proteins. Curr Opin Struct Biol 19(2):189–196
Sattentau Q (2008) Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6(11):815–826. doi:10.1038/nrmicro1972
Zhong P, Agosto LM, Munro JB, Mothes W (2013) Cell-to-cell transmission of viruses. Curr Opin Virol 3(1):44–50
Ramachandran R (2011) Vesicle scission: dynamin. Semin Cell Dev Biol 22(1):10–17. doi:10.1016/j.semcdb.2010.09.001
Cocucci E, Gaudin R, Kirchhausen T (2014) Dynamin recruitment and membrane scission at the neck of a clathrin-coated pit. Mol Biol Cell 25(22):3595–3609. doi:10.1091/mbc.E14-07-1240
Rojek JM, Perez M, Kunz S (2008) Cellular entry of lymphocytic choriomeningitis virus. J Virol 82(3):1505–1517
Quirin K, Eschli B, Scheu I, Poort L, Kartenbeck J, Helenius A (2008) Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 378(1):21–33
Yeh HY, Pieniazek N, Pieniazek D, Gelderblom H, Luftig RB (1994) Human adenovirus type 41 contains two fibers. Virus Res 33(2):179–198
Jones MS 2nd, Harrach B, Ganac RD, Gozum MM, Dela Cruz WP, Riedel B, Pan C, Delwart EL, Schnurr DP (2007) New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81(11):5978–5984. doi:10.1128/JVI.02650-06
Wolfrum N, Greber UF (2013) Adenovirus signalling in entry. Cell Microbiol 15(1):53–62. doi:10.1111/cmi.12053
Moyer CL, Wiethoff CM, Maier O, Smith JG, Nemerow GR (2011) Functional genetic and biophysical analyses of membrane disruption by human adenovirus. J Virol 85(6):2631–2641. doi:10.1128/JVI.02321-10
Corjon S, Gonzalez G, Henning P, Grichine A, Lindholm L, Boulanger P, Fender P, Hong SS (2011) Cell entry and trafficking of human adenovirus bound to blood factor X is determined by the fiber serotype and not hexon:heparan sulfate interaction. PLoS One 6(5):e18205. doi:10.1371/journal.pone.0018205
Roelvink PW, Lizonova A, Lee JG, Li Y, Bergelson JM, Finberg RW, Brough DE, Kovesdi I, Wickham TJ (1998) The coxsackievirus–adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J Virol 72(10):7909–7915
Law LK, Davidson BL (2005) What does it take to bind CAR? Mol Ther 12(4):599–609. doi:10.1016/j.ymthe.2005.05.017
Seiradake E, Henaff D, Wodrich H, Billet O, Perreau M, Hippert C, Mennechet F, Schoehn G, Lortat-Jacob H, Dreja H, Ibanes S, Kalatzis V, Wang JP, Finberg RW, Cusack S, Kremer EJ (2009) The cell adhesion molecule “CAR” and sialic acid on human erythrocytes influence adenovirus in vivo biodistribution. PLoS Pathog 5(1):e1000277. doi:10.1371/journal.ppat.1000277
Wickham TJ, Mathias P, Cheresh DA, Nemerow GR (1993) Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73(2):309–319. doi:10.1016/0092-8674(93)90231-E
Amstutz B, Gastaldelli M, Kalin S, Imelli N, Boucke K, Wandeler E, Mercer J, Hemmi S, Greber UF (2008) Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J 27(7):956–969. doi:10.1038/emboj.2008.38
Huang J, Tan D, Wang Y, Liu C, Xu J, Wang J (2015) Egg drop syndrome virus enters duck embryonic fibroblast cells via clathrin-mediated endocytosis. Virus Res 210:69–76. doi:10.1016/j.virusres.2015.07.014
Guzman E, Taylor G, Hope J, Herbert R, Cubillos-Zapata C, Charleston B (2016) Transduction of skin-migrating dendritic cells by human adenovirus 5 occurs via an actin-dependent phagocytic pathway. J Gen Virol. doi:10.1099/jgv.0.000581
Wang H, Liaw YC, Stone D, Kalyuzhniy O, Amiraslanov I, Tuve S, Verlinde CL, Shayakhmetov D, Stehle T, Roffler S, Lieber A (2007) Identification of CD46 binding sites within the adenovirus serotype 35 fiber knob. J Virol 81(23):12785–12792. doi:10.1128/JVI.01732-07
Persson BD, Muller S, Reiter DM, Schmitt BB, Marttila M, Sumowski CV, Schweizer S, Scheu U, Ochsenfeld C, Arnberg N, Stehle T (2009) An arginine switch in the species B adenovirus knob determines high-affinity engagement of cellular receptor CD46. J Virol 83(2):673–686. doi:10.1128/JVI.01967-08
Cupelli K, Muller S, Persson BD, Jost M, Arnberg N, Stehle T (2010) Structure of adenovirus type 21 knob in complex with CD46 reveals key differences in receptor contacts among species B adenoviruses. J Virol 84(7):3189–3200. doi:10.1128/JVI.01964-09
Sirena D, Lilienfeld B, Eisenhut M, Kalin S, Boucke K, Beerli RR, Vogt L, Ruedl C, Bachmann MF, Greber UF, Hemmi S (2004) The human membrane cofactor CD46 is a receptor for species B adenovirus serotype 3. J Virol 78(9):4454–4462
Fleischli C, Verhaagh S, Havenga M, Sirena D, Schaffner W, Cattaneo R, Greber UF, Hemmi S (2005) The distal short consensus repeats 1 and 2 of the membrane cofactor protein CD46 and their distance from the cell membrane determine productive entry of species B adenovirus serotype 35. J Virol 79(15):10013–10022. doi:10.1128/JVI.79.15.10013-10022.2005
Marttila M, Persson D, Gustafsson D, Liszewski MK, Atkinson JP, Wadell G, Arnberg N (2005) CD46 is a cellular receptor for all species B adenoviruses except types 3 and 7. J Virol 79(22):14429–14436. doi:10.1128/JVI.79.22.14429-14436.2005
Fleischli C, Sirena D, Lesage G, Havenga MJ, Cattaneo R, Greber UF, Hemmi S (2007) Species B adenovirus serotypes 3, 7, 11 and 35 share similar binding sites on the membrane cofactor protein CD46 receptor. J Gen Virol 88(Pt 11):2925–2934. doi:10.1099/vir.0.83142-0
Short JJ, Vasu C, Holterman MJ, Curiel DT, Pereboev A (2006) Members of adenovirus species B utilize CD80 and CD86 as cellular attachment receptors. Virus Res 122(1–2):144–153. doi:10.1016/j.virusres.2006.07.009
Wang H, Li ZY, Liu Y, Persson J, Beyer I, Moller T, Koyuncu D, Drescher MR, Strauss R, Zhang XB, Wahl JK 3rd, Urban N, Drescher C, Hemminki A, Fender P, Lieber A (2011) Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat Med 17(1):96–104. doi:10.1038/nm.2270
Dechecchi MC, Tamanini A, Bonizzato A, Cabrini G (2000) Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology 268(2):382–390
Robinson CM, Zhou X, Rajaiya J, Yousuf MA, Singh G, Deserres JJ, Walsh MP, Wong S, Seto D, Dyer DW, Chodosh J, Jones MS (2013) Predicting the next eye pathogen: analysis of a novel adenovirus. MBio 4(2):e00595-00512. doi:10.1128/mBio.00595-12
Hong SS, Karayan L, Tournier J, Curiel DT, Boulanger PA (1997) Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J 16(9):2294–2306. doi:10.1093/emboj/16.9.2294
Burmeister WP, Guilligay D, Cusack S, Wadell G, Arnberg N (2004) Crystal structure of species D adenovirus fiber knobs and their sialic acid binding sites. J Virol 78(14):7727–7736. doi:10.1128/JVI.78.14.7727-7736.2004
Chu Y, Heistad D, Cybulsky MI, Davidson BL (2001) Vascular cell adhesion molecule-1 augments adenovirus-mediated gene transfer. Arterioscler Thromb Vasc Biol 21(2):238–242
Nilsson EC, Storm RJ, Bauer J, Johansson SM, Lookene A, Angstrom J, Hedenstrom M, Eriksson TL, Frangsmyr L, Rinaldi S, Willison HJ, Pedrosa Domellof F, Stehle T, Arnberg N (2011) The GD1a glycan is a cellular receptor for adenoviruses causing epidemic keratoconjunctivitis. Nat Med 17(1):105–109. doi:10.1038/nm.2267
Cooper RS, Heldwein EE (2015) Herpesvirus gB: a finely tuned fusion machine. Viruses 7(12):6552–6569. doi:10.3390/v7122957
Heldwein EE (2016) gH/gL supercomplexes at early stages of herpesvirus entry. Curr Opin Virol 18:1–8. doi:10.1016/j.coviro.2016.01.010
Akula SM, Pramod NP, Wang FZ, Chandran B (2002) Integrin alpha3beta1 (CD 49c/29) is a cellular receptor for Kaposi’s sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108(3):407–419
Pertel PE (2002) Human herpesvirus 8 glycoprotein B (gB), gH, and gL can mediate cell fusion. J Virol 76(9):4390–4400
Wang FZ, Akula SM, Pramod NP, Zeng L, Chandran B (2001) Human herpesvirus 8 envelope glycoprotein K8.1A interaction with the target cells involves heparan sulfate. J Virol 75(16):7517–7527
Birkmann A, Mahr K, Ensser A, Yaguboglu S, Titgemeyer F, Fleckenstein B, Neipel F (2001) Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J Virol 75(23):11583–11593
Chakraborty S, Veettil MV, Chandran B (2012) Kaposi’s sarcoma associated herpesvirus entry into target cells. Front Microbiol 3:6
Yang E, Arvin AM, Oliver SL (2016) Role for the alphaV integrin subunit in Varicella–Zoster virus-mediated fusion and infection. J Virol 90(16):7567–7578. doi:10.1128/jvi.00792-16
Schmid MF, Hecksel CW, Rochat RH, Bhella D, Chiu W, Rixon FJ (2012) A tail-like assembly at the portal vertex in intact herpes simplex type-1 virions. PLoS Pathog 8(10):e1002961. doi:10.1371/journal.ppat.1002961
Cha TA, Tom E, Kemble GW, Duke GM, Mocarski ES, Spaete RR (1996) Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J Virol 70(1):78–83
Adler B, Scrivano L, Ruzcics Z, Rupp B, Sinzger C, Koszinowski U (2006) Role of human cytomegalovirus UL131A in cell type-specific virus entry and release. J Gen Virol 87(Pt 9):2451–2460
Ryckman BJ, Rainish BL, Chase MC, Borton JA, Nelson JA, Jarvis MA, Johnson DC (2008) Characterization of the human cytomegalovirus gH/gL/UL128-131 complex that mediates entry into epithelial and endothelial cells. J Virol 82(1):60–70
Hahn G, Revello MG, Patrone M, Percivalle E, Campanini G, Sarasini A, Wagner M, Gallina A, Milanesi G, Koszinowski U, Baldanti F, Gerna G (2004) Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 78(18):10023–10033
Wang D, Shenk T (2005) Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci USA 102(50):18153–18158
Patrone M, Secchi M, Fiorina L, Ierardi M, Milanesi G, Gallina A (2005) Human cytomegalovirus UL130 protein promotes endothelial cell infection through a producer cell modification of the virion. J Virol 79(13):8361–8373
Heldwein EE, Krummenacher C (2008) Entry of herpesviruses into mammalian cells. Cell Mol Life Sci 65(11):1653–1668
Connolly SA, Jackson JO, Jardetzky TS, Longnecker R (2011) Fusing structure and function: a structural view of the herpesvirus entry machinery. Nat Rev Microbiol 9(5):369–381
Eisenberg RJ, Atanasiu D, Cairns TM, Gallagher JR, Krummenacher C, Cohen GH (2012) Herpes virus fusion and entry: a story with many characters. Viruses 4(5):800–832
Salameh S, Sheth U, Shukla D (2012) Early events in herpes simplex virus lifecycle with implications for an infection of lifetime. Open Virol J 6:1–6
Gardner TJ, Tortorella D (2016) Virion glycoprotein-mediated immune evasion by human cytomegalovirus: a sticky virus makes a slick getaway. Microbiol Mol Biol Rev 80(3):663–677. doi:10.1128/mmbr.00018-16
Shannon-Lowe C, Rowe M (2014) Epstein Barr virus entry; kissing and conjugation. Curr Opin Virol 4:78–84. doi:10.1016/j.coviro.2013.12.001
Agelidis AM, Shukla D (2015) Cell entry mechanisms of HSV: what we have learned in recent years. Future Virol 10(10):1145–1154. doi:10.2217/fvl.15.85
Gillet L, Frederico B, Stevenson PG (2015) Host entry by gamma-herpesviruses—lessons from animal viruses? Curr Opin Virol 15:34–40. doi:10.1016/j.coviro.2015.07.007
Ryckman BJ, Jarvis MA, Drummond DD, Nelson JA, Johnson DC (2006) Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J Virol 80(2):710–722
Chen J, Rowe CL, Jardetzky TS, Longnecker R (2012) The KGD motif of Epstein–Barr virus gH/gL is bifunctional, orchestrating infection of B cells and epithelial cells. MBio 3(1). doi:10.1128/mBio.00290-11
Li Q, Spriggs MK, Kovats S, Turk SM, Comeau MR, Nepom B, Hutt-Fletcher LM (1997) Epstein–Barr virus uses HLA class II as a cofactor for infection of B lymphocytes. J Virol 71(6):4657–4662
Wang X, Hutt-Fletcher LM (1998) Epstein–Barr virus lacking glycoprotein gp42 can bind to B cells but is not able to infect. J Virol 72(1):158–163
Wang HB, Zhang H, Zhang JP, Li Y, Zhao B, Feng GK, Du Y, Xiong D, Zhong Q, Liu WL, Du H, Li MZ, Huang WL, Tsao SW, Hutt-Fletcher L, Zeng YX, Kieff E, Zeng MS (2015) Neuropilin 1 is an entry factor that promotes EBV infection of nasopharyngeal epithelial cells. Nat Commun 6:6240. doi:10.1038/ncomms7240
Kirschner AN, Omerovic J, Popov B, Longnecker R, Jardetzky TS (2006) Soluble Epstein–Barr virus glycoproteins gH, gL, and gp42 form a 1:1:1 stable complex that acts like soluble gp42 in B-cell fusion but not in epithelial cell fusion. J Virol 80(19):9444–9454
Tugizov SM, Berline JW, Palefsky JM (2003) Epstein–Barr virus infection of polarized tongue and nasopharyngeal epithelial cells. Nat Med 9(3):307–314
Inoue N, Winter J, Lal RB, Offermann MK, Koyano S (2003) Characterization of entry mechanisms of human herpesvirus 8 by using an Rta-dependent reporter cell line. J Virol 77(14):8147–8152
Akula SM, Naranatt PP, Walia NS, Wang FZ, Fegley B, Chandran B (2003) Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) infection of human fibroblast cells occurs through endocytosis. J Virol 77(14):7978–7990
Rappocciolo G, Hensler HR, Jais M, Reinhart TA, Pegu A, Jenkins FJ, Rinaldo CR (2008) Human herpesvirus 8 infects and replicates in primary cultures of activated B lymphocytes through DC-SIGN. J Virol 82(10):4793–4806
Raghu H, Sharma-Walia N, Veettil MV, Sadagopan S, Chandran B (2009) Kaposi’s sarcoma-associated herpesvirus utilizes an actin polymerization-dependent macropinocytic pathway to enter human dermal microvascular endothelial and human umbilical vein endothelial cells. J Virol 83(10):4895–4911
Kerur N, Veettil MV, Sharma-Walia N, Sadagopan S, Bottero V, Paul AG, Chandran B (2010) Characterization of entry and infection of monocytic THP-1 cells by Kaposi’s Sarcoma Associated Herpesvirus (KSHV): role of heparan sulfate, DC-SIGN, integrins and signaling. Virology 406(1):103–116
Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, Hemmi S, Greber UF (2002) Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 158(6):1119–1131. doi:10.1083/jcb.200112067
Kalin S, Amstutz B, Gastaldelli M, Wolfrum N, Boucke K, Havenga M, DiGennaro F, Liska N, Hemmi S, Greber UF (2010) Macropinocytotic uptake and infection of human epithelial cells with species B2 adenovirus type 35. J Virol 84(10):5336–5350. doi:10.1128/JVI.02494-09
Nicola AV, McEvoy AM, Straus SE (2003) Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol 77(9):5324–5332
Nicola AV, Hou J, Major EO, Straus SE (2005) Herpes simplex virus type 1 enters human epidermal keratinocytes, but not neurons, via a pH-dependent endocytic pathway. J Virol 79(12):7609–7616
Nicola AV, Straus SE (2004) Cellular and viral requirements for rapid endocytic entry of herpes simplex virus. J Virol 78 (14):7508-7517. doi:10.1128/JVI.78.14.7508-7517.2004
Shukla SY, Singh YK, Shukla D (2009) Role of nectin-1, HVEM, and PILR-alpha in HSV-2 entry into human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 50(6):2878–2887
Satoh T, Arii J, Suenaga T, Wang J, Kogure A, Uehori J, Arase N, Shiratori I, Tanaka S, Kawaguchi Y, Spear PG, Lanier LL, Arase H (2008) PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132(6):935–944
Geraghty RJ, Krummenacher C, Cohen GH, Eisenberg RJ, Spear PG (1998) Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280(5369):1618–1620
Cocchi F, Menotti L, Mirandola P, Lopez M, Campadelli-Fiume G (1998) The ectodomain of a novel member of the immunoglobulin subfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex virus types 1 and 2 in human cells. J Virol 72(12):9992–10002
Zhang N, Yan J, Lu G, Guo Z, Fan Z, Wang J, Shi Y, Qi J, Gao GF (2011) Binding of herpes simplex virus glycoprotein D to nectin-1 exploits host cell adhesion. Nat Commun 2:577. doi:10.1038/ncomms1571
Gianni T, Salvioli S, Chesnokova LS, Hutt-Fletcher LM, Campadelli-Fiume G (2013) alphavbeta6- and alphavbeta8-integrins serve as interchangeable receptors for HSV gH/gL to promote endocytosis and activation of membrane fusion. PLoS Pathog 9(12):e1003806. doi:10.1371/journal.ppat.1003806
Gianni T, Leoni V, Campadelli-Fiume G (2013) Type I interferon and NF-kappaB activation elicited by herpes simplex virus gH/gL via alphavbeta3 integrin in epithelial and neuronal cell lines. J Virol 87(24):13911–13916. doi:10.1128/jvi.01894-13
Montgomery RI, Warner MS, Lum BJ, Spear PG (1996) Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87(3):427–436
Stiles KM, Whitbeck JC, Lou H, Cohen GH, Eisenberg RJ, Krummenacher C (2010) Herpes simplex virus glycoprotein D interferes with binding of herpesvirus entry mediator to its ligands through downregulation and direct competition. J Virol 84(22):11646–11660
Bacsa S, Karasneh G, Dosa S, Liu J, Valyi-Nagy T, Shukla D (2011) Syndecan-1 and syndecan-2 play key roles in herpes simplex virus type-1 infection. J Gen Virol 92(Pt 4):733–743
Petermann P, Rahn E, Thier K, Hsu MJ, Rixon FJ, Kopp SJ, Knebel-Morsdorf D (2015) Role of nectin-1 and herpesvirus entry mediator as cellular receptors for herpes simplex virus 1 on primary murine dermal fibroblasts. J Virol 89(18):9407–9416. doi:10.1128/jvi.01415-15
Karaba AH, Kopp SJ, Longnecker R (2011) Herpesvirus entry mediator and nectin-1 mediate herpes simplex virus 1 infection of the murine cornea. J Virol 85(19):10041–10047
Bello-Morales R, Crespillo AJ, Praena B, Tabares E, Revilla Y, Garcia E, Fraile-Ramos A, Baron W, Krummenacher C, Lopez-Guerrero JA (2016) Role of proteolipid protein in HSV-1 entry in oligodendrocytic cells. PLoS One 11(1):e0147885. doi:10.1371/journal.pone.0147885
Gianni T, Amasio M, Campadelli-Fiume G (2009) Herpes simplex virus gD forms distinct complexes with fusion executors gB and gH/gL in part through the C-terminal profusion domain. J Biol Chem 284(26):17370–17382
Arii J, Goto H, Suenaga T, Oyama M, Kozuka-Hata H, Imai T, Minowa A, Akashi H, Arase H, Kawaoka Y, Kawaguchi Y (2010) Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1. Nature 467(7317):859–862
Kirschner AN, Sorem J, Longnecker R, Jardetzky TS (2009) Structure of Epstein–Barr virus glycoprotein 42 suggests a mechanism for triggering receptor-activated virus entry. Structure 17(2):223–233
Tiwari V, Clement C, Xu D, Valyi-Nagy T, Yue BY, Liu J, Shukla D (2006) Role for 3-O-sulfated heparan sulfate as the receptor for herpes simplex virus type 1 entry into primary human corneal fibroblasts. J Virol 80(18):8970–8980
Santoro F, Kennedy PE, Locatelli G, Malnati MS, Berger EA, Lusso P (1999) CD46 is a cellular receptor for human herpesvirus 6. Cell 99(7):817–827
Mori Y, Yang X, Akkapaiboon P, Okuno T, Yamanishi K (2003) Human herpesvirus 6 variant A glycoprotein H-glycoprotein L-glycoprotein Q complex associates with human CD46. J Virol 77(8):4992–4999
Santoro F, Greenstone HL, Insinga A, Liszewski MK, Atkinson JP, Lusso P, Berger EA (2003) Interaction of glycoprotein H of human herpesvirus 6 with the cellular receptor CD46. J Biol Chem 278(28):25964–25969
Tanaka Y, Suenaga T, Matsumoto M, Seya T, Arase H (2013) Herpesvirus 6 glycoproteins B (gB), gH, gL, and gQ are necessary and sufficient for cell-to-cell fusion. J Virol 87 (19):10900-10903. doi:10.1128/JVI.01427-13
Secchiero P, Sun D, De Vico AL, Crowley RW, Reitz MS Jr, Zauli G, Lusso P, Gallo RC (1997) Role of the extracellular domain of human herpesvirus 7 glycoprotein B in virus binding to cell surface heparan sulfate proteoglycans. J Virol 71(6):4571–4580
Compton T, Nepomuceno RR, Nowlin DM (1992) Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 191(1):387–395
Wang X, Huong SM, Chiu ML, Raab-Traub N, Huang ES (2003) Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 424(6947):456–461
Feire AL, Koss H, Compton T (2004) Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc Natl Acad Sci USA 101(43):15470–15475
Wang X, Huang DY, Huong SM, Huang ES (2005) Integrin alphavbeta3 is a coreceptor for human cytomegalovirus. Nat Med 11(5):515–521
Tugizov S, Navarro D, Paz P, Wang Y, Qadri I, Pereira L (1994) Function of human cytomegalovirus glycoprotein B: syncytium formation in cells constitutively expressing gB is blocked by virus-neutralizing antibodies. Virology 201(2):263–276
Kinzler ER, Compton T (2005) Characterization of human cytomegalovirus glycoprotein-induced cell–cell fusion. J Virol 79(12):7827–7837
Zhou M, Lanchy JM, Ryckman BJ (2015) Human cytomegalovirus gH/gL/gO promotes the fusion step of entry into all cell types, whereas gH/gL/UL128-131 broadens virus tropism through a distinct mechanism. J Virol 89(17):8999–9009. doi:10.1128/jvi.01325-15
Tanner J, Weis J, Fearon D, Whang Y, Kieff E (1987) Epstein–Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 50(2):203–213
Miller N, Hutt-Fletcher LM (1992) Epstein–Barr virus enters B cells and epithelial cells by different routes. J Virol 66(6):3409–3414
Speck P, Haan KM, Longnecker R (2000) Epstein–Barr virus entry into cells. Virology 277(1):1–5. doi:10.1006/viro.2000.0624
Nemerow GR, Wolfert R, McNaughton ME, Cooper NR (1985) Identification and characterization of the Epstein–Barr virus receptor on human B lymphocytes and its relationship to the C3d complement receptor (CR2). J Virol 55(2):347–351
Chesnokova LS, Nishimura SL, Hutt-Fletcher LM (2009) Fusion of epithelial cells by Epstein–Barr virus proteins is triggered by binding of viral glycoproteins gHgL to integrins alphavbeta6 or alphavbeta8. Proc Natl Acad Sci USA 106(48):20464–20469
Veettil MV, Kumar B, Ansari MA, Dutta D, Iqbal J, Gjyshi O, Bottero V, Chandran B (2016) ESCRT-0 component Hrs promotes macropinocytosis of Kaposi’s Sarcoma-Associated Herpesvirus in human dermal microvascular endothelial cells. J Virol 90(8):3860–3872. doi:10.1128/jvi.02704-15
Wang FZ, Akula SM, Sharma-Walia N, Zeng L, Chandran B (2003) Human herpesvirus 8 envelope glycoprotein B mediates cell adhesion via its RGD sequence. J Virol 77(5):3131–3147
AlHajri SM, Cunha CW, Nicola AV, Aguilar HC, Li H, Taus NS (2017) Ovine Herpesvirus 2 Glycoproteins B, H, and L Are Sufficient for, and Viral Glycoprotein Ov8 Can Enhance, Cell-Cell Membrane Fusion. J Virol 91 (6). doi:10.1128/JVI.02454-16
Townsley AC, Weisberg AS, Wagenaar TR, Moss B (2006) Vaccinia virus entry into cells via a low-pH-dependent endosomal pathway. J Virol 80(18):8899–8908. doi:10.1128/JVI.01053-06
Locker JK, Kuehn A, Schleich S, Rutter G, Hohenberg H, Wepf R, Griffiths G (2000) Entry of the two infectious forms of vaccinia virus at the plasma membrane is signaling-dependent for the IMV but not the EEV. Mol Biol Cell 11(7):2497–2511
Mercer J, Helenius A (2008) Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320(5875):531–535. doi:10.1126/science.1155164
Huang CY, Lu TY, Bair CH, Chang YS, Jwo JK, Chang W (2008) A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J Virol 82(16):7988–7999. doi:10.1128/JVI.00894-08
Mercer J, Knebel S, Schmidt FI, Crouse J, Burkard C, Helenius A (2010) Vaccinia virus strains use distinct forms of macropinocytosis for host-cell entry. Proc Natl Acad Sci USA 107(20):9346–9351. doi:10.1073/pnas.1004618107
Schmidt FI, Bleck CK, Helenius A, Mercer J (2011) Vaccinia extracellular virions enter cells by macropinocytosis and acid-activated membrane rupture. EMBO J 30(17):3647–3661. doi:10.1038/emboj.2011.245
Schroeder N, Chung CS, Chen CH, Liao CL, Chang W (2012) The lipid raft-associated protein CD98 is required for vaccinia virus endocytosis. J Virol 86(9):4868–4882. doi:10.1128/JVI.06610-11
Sandgren KJ, Wilkinson J, Miranda-Saksena M, McInerney GM, Byth-Wilson K, Robinson PJ, Cunningham AL (2010) A differential role for macropinocytosis in mediating entry of the two forms of vaccinia virus into dendritic cells. PLoS Pathog 6(4):e1000866. doi:10.1371/journal.ppat.1000866
Izmailyan R, Hsao JC, Chung CS, Chen CH, Hsu PW, Liao CL, Chang W (2012) Integrin beta1 mediates vaccinia virus entry through activation of PI3K/Akt signaling. J Virol 86(12):6677–6687. doi:10.1128/JVI.06860-11
Laliberte JP, Moss B (2010) Lipid membranes in poxvirus replication. Viruses 2(4):972–986. doi:10.3390/v2040972
Villa NY, Bartee E, Mohamed MR, Rahman MM, Barrett JW, McFadden G (2010) Myxoma and vaccinia viruses exploit different mechanisms to enter and infect human cancer cells. Virology 401(2):266–279. doi:10.1016/j.virol.2010.02.027
Hiley CT, Chard LS, Gangeswaran R, Tysome JR, Briat A, Lemoine NR, Wang Y (2013) Vascular endothelial growth factor A promotes vaccinia virus entry into host cells via activation of the Akt pathway. J Virol 87 (5):2781-2790
Chan WM, Bartee EC, Moreb JS, Dower K, Connor JH, McFadden G (2013) Myxoma and vaccinia viruses bind differentially to human leukocytes. J Virol 87 (8):4445-4460
Byrd D, Amet T, Hu N, Lan J, Hu S, Yu Q (2013) Primary human leukocyte subsets differentially express vaccinia virus receptors enriched in lipid rafts. J Virol 87(16):9301–9312
Haga IR, Pechenick Jowers T, Griffiths SJ, Haas J, Beard PM (2014) TRAF2 facilitates vaccinia virus replication by promoting rapid virus entry. J Virol 88(7):3664–3677
Moser TS, Jones RG, Thompson CB, Coyne CB, Cherry S (2010) A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog 6(6):e1000954. doi:10.1371/journal.ppat.1000954
Bengali Z, Satheshkumar PS, Yang Z, Weisberg AS, Paran N, Moss B (2011) Drosophila S2 cells are non-permissive for vaccinia virus DNA replication following entry via low pH-dependent endocytosis and early transcription. PLoS One 6(2):e17248. doi:10.1371/journal.pone.0017248
Whitbeck JC, Foo CH, Ponce de Leon M, Eisenberg RJ, Cohen GH (2009) Vaccinia virus exhibits cell-type-dependent entry characteristics. Virology 385(2):383–391. doi:10.1016/j.virol.2008.12.029
Bengali Z, Townsley AC, Moss B (2009) Vaccinia virus strain differences in cell attachment and entry. Virology 389(1–2):132–140. doi:10.1016/j.virol.2009.04.012
Bengali Z, Satheshkumar PS, Moss B (2012) Orthopoxvirus species and strain differences in cell entry. Virology 433(2):506–512
Morizono K, Xie Y, Olafsen T, Lee B, Dasgupta A, Wu AM, Chen IS (2011) The soluble serum protein Gas6 bridges virion envelope phosphatidylserine to the TAM receptor tyrosine kinase Axl to mediate viral entry. Cell Host Microbe 9(4):286–298. doi:10.1016/j.chom.2011.03.012
Doceul V, Hollinshead M, van der Linden L, Smith GL (2010) Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327(5967):873–876. doi:10.1126/science.1183173
Turner PC, Moyer RW (2006) The cowpox virus fusion regulator proteins SPI-3 and hemagglutinin interact in infected and uninfected cells. Virology 347(1):88–99. doi:10.1016/j.virol.2005.11.012
Wagenaar TR, Moss B (2007) Association of vaccinia virus fusion regulatory proteins with the multicomponent entry/fusion complex. J Virol 81(12):6286–6293. doi:10.1128/JVI.00274-07
Turner PC, Moyer RW (2008) The vaccinia virus fusion inhibitor proteins SPI-3 (K2) and HA (A56) expressed by infected cells reduce the entry of superinfecting virus. Virology 380(2):226–233. doi:10.1016/j.virol.2008.07.020
Laliberte JP, Moss B (2014) A novel mode of poxvirus superinfection exclusion that prevents fusion of the lipid bilayers of viral and cellular membranes. J Virol 88(17):9751–9768. doi:10.1128/JVI.00816-14
Wagenaar TR, Ojeda S, Moss B (2008) Vaccinia virus A56/K2 fusion regulatory protein interacts with the A16 and G9 subunits of the entry fusion complex. J Virol 82(11):5153–5160. doi:10.1128/JVI.00162-08
Guo CJ, Liu D, Wu YY, Yang XB, Yang LS, Mi S, Huang YX, Luo YW, Jia KT, Liu ZY, Chen WJ, Weng SP, Yu XQ, He JG (2011) Entry of tiger frog virus (an Iridovirus) into HepG2 cells via a pH-dependent, atypical, caveola-mediated endocytosis pathway. J Virol 85(13):6416–6426. doi:10.1128/JVI.01500-10
Braunwald J, Nonnenmacher H, Tripier-Darcy F (1985) Ultrastructural and biochemical study of frog virus 3 uptake by BHK-21 cells. J Gen Virol 66 ( Pt 2):283-293
Guo CJ, Wu YY, Yang LS, Yang XB, He J, Mi S, Jia KT, Weng SP, Yu XQ, He JG (2012) Infectious spleen and kidney necrosis virus (a fish iridovirus) enters Mandarin fish fry cells via caveola-dependent endocytosis. J Virol 86(5):2621–2631. doi:10.1128/JVI.06947-11
Jia KT, Wu YY, Liu ZY, Mi S, Zheng YW, He J, Weng SP, Li SC, He JG, Guo CJ (2013) Mandarin fish caveolin 1 interaction with major capsid protein of infectious spleen and kidney necrosis virus and its role in early stages of infection. J Virol 87(6):3027–3038
Wang S, Huang X, Huang Y, Hao X, Xu H, Cai M, Wang H, Qin Q (2014) Entry of a novel marine DNA virus, Singapore grouper iridovirus, into host cells occurs via clathrin-mediated endocytosis and macropinocytosis in a pH-dependent manner. J Virol 88(22):13047–13063. doi:10.1128/JVI.01744-14
Yuan Y, Wang Y, Liu Q, Zhu F, Hong Y (2016) Singapore grouper iridovirus protein VP088 is essential for viral infectivity. Sci Rep 6:31170. doi:10.1038/srep31170
Ao J, Chen X (2006) Identification and characterization of a novel gene encoding an RGD-containing protein in large yellow croaker iridovirus. Virology 355(2):213–222. doi:10.1016/j.virol.2006.07.004
Wu J, Chan R, Wenk MR, Hew CL (2010) Lipidomic study of intracellular Singapore grouper iridovirus. Virology 399(2):248–256. doi:10.1016/j.virol.2010.01.016
Blissard GW, Wenz JR (1992) Baculovirus gp64 envelope glycoprotein is sufficient to mediate pH-dependent membrane fusion. J Virol 66(11):6829–6835
Dong S, Wang M, Qiu Z, Deng F, Vlak JM, Hu Z, Wang H (2010) Autographa californica multicapsid nucleopolyhedrovirus efficiently infects Sf9 cells and transduces mammalian cells via direct fusion with the plasma membrane at low pH. J Virol 84(10):5351–5359. doi:10.1128/JVI.02517-09
Kataoka C, Kaname Y, Taguwa S, Abe T, Fukuhara T, Tani H, Moriishi K, Matsuura Y (2012) Baculovirus GP64-mediated entry into mammalian cells. J Virol 86(5):2610–2620
Kato T, Sugioka S, Itagaki K, Park EY (2016) Gene transduction in mammalian cells using Bombyx mori nucleopolyhedrovirus assisted by glycoprotein 64 of Autographa californica multiple nucleopolyhedrovirus. Sci Rep 6:32283. doi:10.1038/srep32283
Huang J, Hao B, Cheng C, Liang F, Shen X, Cheng X (2014) Entry of Bombyx mori nucleopolyhedrovirus into BmN cells by cholesterol-dependent macropinocytic endocytosis. Biochem Biophys Res Commun 453(1):166–171. doi:10.1016/j.bbrc.2014.09.073
Laakkonen JP, Makela AR, Kakkonen E, Turkki P, Kukkonen S, Peranen J, Yla-Herttuala S, Airenne KJ, Oker-Blom C, Vihinen-Ranta M, Marjomaki V (2009) Clathrin-independent entry of baculovirus triggers uptake of E. coli in non-phagocytic human cells. PLoS One 4(4):e5093
Long G, Pan X, Kormelink R, Vlak JM (2006) Functional entry of baculovirus into insect and mammalian cells is dependent on clathrin-mediated endocytosis. J Virol 80(17):8830–8833
Makkonen KE, Turkki P, Laakkonen JP, Yla-Herttuala S, Marjomaki V, Airenne KJ (2013) 6-o- and N-sulfated syndecan-1 promotes baculovirus binding and entry into mammalian cells. J Virol 87(20):11148–11159. doi:10.1128/jvi.01919-13
Luz-Madrigal A, Asanov A, Camacho-Zarco AR, Sampieri A, Vaca L (2013) A cholesterol recognition amino acid consensus domain in GP64 fusion protein facilitates anchoring of baculovirus to mammalian cells. J Virol 87(21):11894–11907. doi:10.1128/jvi.01356-13
Moss B (2016) Membrane fusion during poxvirus entry. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2016.07.015
Moss B (2006) Poxvirus entry and membrane fusion. Virology 344(1):48–54. doi:10.1016/j.virol.2005.09.037
Smith GL, Vanderplasschen A, Law M (2002) The formation and function of extracellular enveloped vaccinia virus. J Gen Virol 83(Pt 12):2915–2931
Senkevich TG, Moss B (2005) Vaccinia virus H2 protein is an essential component of a complex involved in virus entry and cell–cell fusion. J Virol 79(8):4744–4754. doi:10.1128/JVI.79.8.4744-4754.2005
Moss B (2012) Poxvirus cell entry: how many proteins does it take? Viruses 4(5):688–707. doi:10.3390/v4050688
Laliberte JP, Weisberg AS, Moss B (2011) The membrane fusion step of vaccinia virus entry is cooperatively mediated by multiple viral proteins and host cell components. PLoS Pathog 7(12):e1002446. doi:10.1371/journal.ppat.1002446
Vanderplasschen A, Hollinshead M, Smith GL (1998) Intracellular and extracellular vaccinia virions enter cells by different mechanisms. J Gen Virol 79(Pt 4):877–887
Sodeik B, Krijnse-Locker J (2002) Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host? Trends Microbiol 10(1):15–24. doi:10.1016/S0966-842X(01)02256-9
Schmidt FI, Bleck CK, Reh L, Novy K, Wollscheid B, Helenius A, Stahlberg H, Mercer J (2013) Vaccinia virus entry is followed by core activation and proteasome-mediated release of the immunomodulatory effector VH1 from lateral bodies. Cell Rep 4(3):464–476
Chiu WL, Lin CL, Yang MH, Tzou DL, Chang W (2007) Vaccinia virus 4c (A26L) protein on intracellular mature virus binds to the extracellular cellular matrix laminin. J Virol 81(5):2149–2157. doi:10.1128/JVI.02302-06
Chang SJ, Chang YX, Izmailyan R, Tang YL, Chang W (2010) Vaccinia virus A25 and A26 proteins are fusion suppressors for mature virions and determine strain-specific virus entry pathways into HeLa, CHO-K1, and L cells. J Virol 84(17):8422–8432. doi:10.1128/JVI.00599-10
Chung CS, Hsiao JC, Chang YS, Chang W (1998) A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J Virol 72(2):1577–1585
Kochan G, Escors D, Gonzalez JM, Casasnovas JM, Esteban M (2008) Membrane cell fusion activity of the vaccinia virus A17-A27 protein complex. Cell Microbiol 10(1):149–164. doi:10.1111/j.1462-5822.2007.01026.x
Hsiao JC, Chung CS, Chang W (1999) Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. J Virol 73(10):8750–8761
Lin CL, Chung CS, Heine HG, Chang W (2000) Vaccinia virus envelope H3L protein binds to cell surface heparan sulfate and is important for intracellular mature virion morphogenesis and virus infection in vitro and in vivo. J Virol 74(7):3353–3365
Ojeda S, Senkevich TG, Moss B (2006) Entry of vaccinia virus and cell–cell fusion require a highly conserved cysteine-rich membrane protein encoded by the A16L gene. J Virol 80(1):51–61. doi:10.1128/JVI.80.1.51-61.2006
Townsley AC, Senkevich TG, Moss B (2005) Vaccinia virus A21 virion membrane protein is required for cell entry and fusion. J Virol 79(15):9458–9469
Senkevich TG, Ward BM, Moss B (2004) Vaccinia virus entry into cells is dependent on a virion surface protein encoded by the A28L gene. J Virol 78(5):2357–2366
Nelson GE, Wagenaar TR, Moss B (2008) A conserved sequence within the H2 subunit of the vaccinia virus entry/fusion complex is important for interaction with the A28 subunit and infectivity. J Virol 82(13):6244–6250. doi:10.1128/JVI.00434-08
Shinoda K, Wyatt LS, Moss B (2010) The neutralizing antibody response to the vaccinia virus A28 protein is specifically enhanced by its association with the H2 protein. Virology 405(1):41–49. doi:10.1016/j.virol.2010.05.025
Brown E, Senkevich TG, Moss B (2006) Vaccinia virus F9 virion membrane protein is required for entry but not virus assembly, in contrast to the related L1 protein. J Virol 80(19):9455–9464. doi:10.1128/JVI.01149-06
Izmailyan RA, Huang CY, Mohammad S, Isaacs SN, Chang W (2006) The envelope G3L protein is essential for entry of vaccinia virus into host cells. J Virol 80(17):8402–8410
Ojeda S, Domi A, Moss B (2006) Vaccinia virus G9 protein is an essential component of the poxvirus entry-fusion complex. J Virol 80(19):9822–9830
Chang SJ, Shih AC, Tang YL, Chang W (2012) Vaccinia mature virus fusion regulator A26 protein binds to A16 and G9 proteins of the viral entry fusion complex and dissociates from mature virions at low pH. J Virol 86(7):3809–3818. doi:10.1128/JVI.06081-11
Senkevich TG, Ojeda S, Townsley A, Nelson GE, Moss B (2005) Poxvirus multiprotein entry-fusion complex. Proc Natl Acad Sci USA 102(51):18572–18577. doi:10.1073/pnas.0509239102
Bisht H, Weisberg AS, Moss B (2008) Vaccinia virus L1 protein is required for cell entry and membrane fusion. J Virol 82(17):8687–8694
Townsley AC, Senkevich TG, Moss B (2005) The product of the vaccinia virus L5R gene is a fourth membrane protein encoded by all poxviruses that is required for cell entry and cell–cell fusion. J Virol 79(17):10988–10998
Satheshkumar PS, Moss B (2012) Sequence-divergent chordopoxvirus homologs of the O3 protein maintain functional interactions with components of the vaccinia virus entry-fusion complex. J Virol 86(3):1696–1705. doi:10.1128/JVI.06069-11
Saadi H, Pagnier I, Colson P, Cherif JK, Beji M, Boughalmi M, Azza S, Armstrong N, Robert C, Fournous G, La Scola B, Raoult D (2013) First isolation of mimivirus in a patient with pneumonia. Clin Infect Dis 57(4):e127–e134
Saadi H, Reteno DG, Colson P, Aherfi S, Minodier P, Pagnier I, Raoult D, La Scola B (2013) Shan virus: a new Mimivirus isolated from the stool of a Tunisian patient with pneumonia. Intervirology 56(6):424–429
Boughalmi M, Pagnier I, Aherfi S, Colson P, Raoult D, La Scola B (2013) First isolation of a Marseillevirus in the diptera Syrphidae Eristalis tenax. Intervirology 56(6):386–394
Boughalmi M, Pagnier I, Aherfi S, Colson P, Raoult D, La Scola B (2013) First isolation of a giant virus from wild Hirudo medicinalis leech: Mimiviridae isolation in Hirudo medicinalis. Viruses 5(12):2920–2930
Pagnier I, Reteno DG, Saadi H, Boughalmi M, Gaia M, Slimani M, Ngounga T, Bekliz M, Colson P, Raoult D, La Scola B (2013) A decade of improvements in Mimiviridae and Marseilleviridae isolation from amoeba. Intervirology 56(6):354–363. doi:10.1159/000354556
Kutikhin AG, Yuzhalin AE, Brusina EB (2014) Mimiviridae, Marseilleviridae, and virophages as emerging human pathogens causing healthcare-associated infections. GMS Hyg Infect Control 9(2):Doc16. doi:10.3205/dgkh000236
Zhang XA, Zhu T, Zhang PH, Li H, Li Y, Liu EM, Liu W, Cao WC (2016) Lack of Mimivirus detection in patients with respiratory disease, China. Emerg Infect Dis. doi:10.3201/eid2211.160687
Raoult D, Levasseur A, La Scola B (2017) PCR detection of Mimivirus. Emerg Infect Dis 23(6):1044–1045. doi:10.3201/eid2306.161896
Dornas FP, Boratto PVM, Costa GB, Silva LCF, Kroon EG, La Scola B, Trindade G, Abrahao JS (2017) Detection of mimivirus genome and neutralizing antibodies in humans from Brazil. Arch Virol. doi:10.1007/s00705-017-3455-5
Lusi EA, Maloney D, Caicci F, Guarascio P (2017) Questions on unusual Mimivirus-like structures observed in human cells. F1000Res 6:262. doi:10.12688/f1000research.11007.1
Boyer M, Azza S, Barrassi L, Klose T, Campocasso A, Pagnier I, Fournous G, Borg A, Robert C, Zhang X, Desnues C, Henrissat B, Rossmann MG, La Scola B, Raoult D (2011) Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci 108(25):10296–10301. doi:10.1073/pnas.1101118108
Rodrigues RA, dos Santos Silva LK, Dornas FP, de Oliveira DB, Magalhaes TF, Santos DA, Costa AO, de Macedo Farias L, Magalhaes PP, Bonjardim CA, Kroon EG, La Scola B, Cortines JR, Abrahao JS (2015) Mimivirus fibrils are important for viral attachment to the microbial world by a diverse glycoside interaction repertoire. J Virol 89(23):11812–11819. doi:10.1128/jvi.01976-15
Sobhy H, Scola BL, Pagnier I, Raoult D, Colson P (2015) Identification of giant Mimivirus protein functions using RNA interference. Front Microbiol 6:345. doi:10.3389/fmicb.2015.00345
Sobhy H (2014) Characterization of protein involved in the fibers of Mimivirus. PhD thesis, Universite d’Aix-Marseille, http://www.theses.fr/2014AIXM5029
Sobhy H, Gotthard G, Chabriere E, Raoult D, Colson P (2017) Recombinant expression of Mimivirus L725 ORFan gene product. Acta Virol. doi:10.4149/av_2017_01_123
Klose T, Herbst Dominik A, Zhu H, Max Joann P, Kenttämaa Hilkka I, Rossmann Michael G (2015) A Mimivirus enzyme that participates in viral entry. Structure 23(6):1058–1065. doi:10.1016/j.str.2015.03.023
Ghigo E, Kartenbeck J, Lien P, Pelkmans L, Capo C, Mege JL, Raoult D (2008) Ameobal pathogen mimivirus infects macrophages through phagocytosis. PLoS Pathog 4(6):e1000087. doi:10.1371/journal.ppat.1000087
Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D (2007) Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS One 2(3):e328. doi:10.1371/journal.pone.0000328
Arantes TS, Rodrigues RA, Dos Santos Silva LK, Oliveira GP, de Souza HL, Khalil JY, de Oliveira DB, Torres AA, da Silva LL, Colson P, Kroon EG, da Fonseca FG, Bonjardim CA, La Scola B, Abrahao JS (2016) The large Marseillevirus explores different entry pathways by forming giant infectious vesicles. J Virol 90(11):5246–5255. doi:10.1128/jvi.00177-16
Meints RH, Lee K, Burbank DE, Van Etten JL (1984) Infection of a chlorella-like alga with the virus, PBCV-1: ultrastructural studies. Virology 138(2):341–346
Yanai-Balser GM, Duncan GA, Eudy JD, Wang D, Li X, Agarkova IV, Dunigan DD, Van Etten JL (2010) Microarray analysis of Paramecium bursaria chlorella virus 1 transcription. J Virol 84(1):532–542. doi:10.1128/JVI.01698-09
Wang K, Xie S, Sun B (2011) Viral proteins function as ion channels. Biochim Biophys Acta 1808 2:510–515. doi:10.1016/j.bbamem.2010.05.006
Romani G, Piotrowski A, Hillmer S, Gurnon J, Van Etten JL, Moroni A, Thiel G, Hertel B (2013) A virus-encoded potassium ion channel is a structural protein in the chlorovirus Paramecium bursaria chlorella virus 1 virion. J Gen Virol 94(Pt 11):2549–2556
Mackinder LC, Worthy CA, Biggi G, Hall M, Ryan KP, Varsani A, Harper GM, Wilson WH, Brownlee C, Schroeder DC (2009) A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy. J Gen Virol 90(Pt 9):2306–2316. doi:10.1099/vir.0.011635-0
Maier I, Müller DG, Katsaros C (2002) Entry of the DNA virus, Ectocarpus fasciculatus virus type 1 (Phycodnaviridae), into host cell cytosol and nucleus. Phycol Res 50(3):227–231. doi:10.1046/j.1440-1835.2002.00277.x
Alonso C, Galindo I, Cuesta-Geijo MA, Cabezas M, Hernaez B, Munoz-Moreno R (2013) African swine fever virus-cell interactions: from virus entry to cell survival. Virus Res 173(1):42–57
Hernaez B, Alonso C (2010) Dynamin- and clathrin-dependent endocytosis in African swine fever virus entry. J Virol 84(4):2100–2109. doi:10.1128/JVI.01557-09
Cuesta-Geijo MA, Galindo I, Hernaez B, Quetglas JI, Dalmau-Mena I, Alonso C (2012) Endosomal maturation, Rab7 GTPase and phosphoinositides in African swine fever virus entry. PLoS One 7(11):e48853
Galindo I, Cuesta-Geijo MA, Hlavova K, Munoz-Moreno R, Barrado-Gil L, Dominguez J, Alonso C (2015) African swine fever virus infects macrophages, the natural host cells, via clathrin- and cholesterol-dependent endocytosis. Virus Res 200:45–55. doi:10.1016/j.virusres.2015.01.022
Cuesta-Geijo MA, Chiappi M, Galindo I, Barrado-Gil L, Munoz-Moreno R, Carrascosa JL, Alonso C (2016) Cholesterol flux is required for endosomal progression of African swine fever virions during the initial establishment of infection. J Virol 90(3):1534–1543. doi:10.1128/JVI.02694-15
Hernaez B, Guerra M, Salas ML, Andres G (2016) African swine fever virus undergoes outer envelope disruption, capsid disassembly and inner envelope fusion before core release from multivesicular endosomes. PLoS Pathog 12(4):e1005595. doi:10.1371/journal.ppat.1005595
Sanchez EG, Quintas A, Perez-Nunez D, Nogal M, Barroso S, Carrascosa AL, Revilla Y (2012) African swine fever virus uses macropinocytosis to enter host cells. PLoS Pathog 8(6):e1002754. doi:10.1371/journal.ppat.1002754
Chinchar VG, Yu KH, Jancovich JK (2011) The molecular biology of frog virus 3 and other iridoviruses infecting cold-blooded vertebrates. Viruses 3(10):1959–1985. doi:10.3390/v3101959
Hussain M, Garrad S, Asgari S (2009) The role of actin filaments in ascovirus replication and pathology. Arch Virol 154(11):1737–1743. doi:10.1007/s00705-009-0512-8
Kadlec J, Loureiro S, Abrescia NG, Stuart DI, Jones IM (2008) The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat Struct Mol Biol 15(10):1024–1030
Heldwein EE, Lou H, Bender FC, Cohen GH, Eisenberg RJ, Harrison SC (2006) Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313(5784):217–220
Muggeridge MI (2012) Glycoprotein B of herpes simplex virus 2 has more than one intracellular conformation and is altered by low pH. J Virol 86(12):6444–6456
Vitu E, Sharma S, Stampfer SD, Heldwein EE (2013) Extensive mutagenesis of the HSV-1 gB ectodomain reveals remarkable stability of its postfusion form. J Mol Biol 2836(13):00142–00147
Sobhy H (2016) A bioinformatics pipeline to search functional motifs within whole-proteome data: a case study of poxviruses. Virus Genes. doi:10.1007/s11262-016-1416-9
Wodrich H, Henaff D, Jammart B, Segura-Morales C, Seelmeir S, Coux O, Ruzsics Z, Wiethoff CM, Kremer EJ (2010) A capsid-encoded PPxY-motif facilitates adenovirus entry. PLoS Pathog 6(3):e1000808. doi:10.1371/journal.ppat.1000808
Marvin SA, Wiethoff CM (2012) Emerging roles for ubiquitin in adenovirus cell entry. Biol Cell 104(3):188–198. doi:10.1111/boc.201100096
DuRose JB, Li J, Chien S, Spector DH (2012) Infection of vascular endothelial cells with human cytomegalovirus under fluid shear stress reveals preferential entry and spread of virus in flow conditions simulating atheroprone regions of the artery. J Virol 86(24):13745–13755
Colpitts CC, Ustinov AV, Epand RF, Epand RM, Korshun VA, Schang LM (2013) 5-(Perylen-3-yl)ethynyl-arabino-uridine (aUY11), an arabino-based rigid amphipathic fusion inhibitor, targets virion envelope lipids to inhibit fusion of influenza virus, hepatitis C virus, and other enveloped viruses. J Virol 87(7):3640–3654
O’Flynn NM, Patel A, Kadlec J, Jones IM (2012) Improving promiscuous mammalian cell entry by the baculovirus AcMNPV. Biosci Rep 2012:4
Acknowledgements
I would like to thank professors Philippe Colson (Univ. Aix-Marseille), Bruno Pozzetto (Univ. Jean Monnet), and Bernard Moss (NIAID-NIH).
Author information
Authors and Affiliations
Contributions
HS analysed the data and wrote the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
No known conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by the author.
Informed consent
Not applicable.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Sobhy, H. A comparative review of viral entry and attachment during large and giant dsDNA virus infections. Arch Virol 162, 3567–3585 (2017). https://doi.org/10.1007/s00705-017-3497-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-017-3497-8