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Laboratory of Virology, Wageningen University, Binnenhaven 11, 6709 PD Wageningen, The Netherlands
Correspondence
Just M. Vlak
just.vlak{at}wur.nl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The family encompasses two genera, Nucleopolyhedrovirus (NPV) and Granulovirus (GV). Recently, a new baculovirus classification has been proposed, consisting of four genera: Alphabaculovirus (lepidopteran NPVs), Betabaculovirus (lepidopteran GVs), Gammabaculovirus (hymenopteran NPVs) and Deltabaculovirus (dipteran NPVs) (Jehle et al., 2006). The proposed genus Alphabaculovirus can be subdivided further into group I and II NPVs, based on phylogenetic analysis of the viral DNA (Bulach et al., 1999; Hayakawa et al., 2000; Herniou et al., 2001, 2003).
Baculoviruses produce two distinct virion phenotypes: occlusion-derived virus (ODV) and budded virus (BV) (Volkman & Summers, 1977). ODVs are present in occlusion bodies and are able to infect midgut epithelial cells by direct membrane fusion (Granados, 1978; Granados & Lawler, 1981; Horton & Burand, 1993). BVs infect insect cells via receptor-mediated endocytosis and are responsible for systemic spread of the virus in the insect (Hefferon et al., 1999; Volkman & Goldsmith, 1985). The BVs of alphabaculovirus group I NPVs, e.g. Autographa californica multiple NPV (AcMNPV) and Orgyia pseudotsugata (Op)MNPV, contain a major envelope protein, GP64. This protein is involved in attachment of BVs to the cell, is required for low-pH-triggered membrane fusion during virus entry and is necessary later in the process of infection for efficient budding of progeny nucleocapsids (NCs) into the haemolymph or cell-culture supernatant (Blissard & Wenz, 1992; Hefferon et al., 1999; Oomens & Blissard, 1999).
Recent data from complete genomic sequences of a growing number of baculoviruses suggest that all group I NPVs possess a gp64-like gene, whereas group II NPVs, beta-, gamma- and deltabaculoviruses lack this gene. For three group II NPVs, Spodoptera exigua (Se)MNPV, Lymantria dispar (Ld)MNPV and Helicoverpa armigera (Hear)NPV, it has been shown that low-pH-mediated membrane fusion is mediated by a novel type of envelope fusion protein, called F (IJkel et al., 2000; Pearson et al., 2000; Long et al., 2006b). Like several mammalian viral envelope fusion proteins, the baculovirus F protein must be cleaved post-translationally by a proprotein convertase (furin) to become fusiogenic (Lung et al., 2002; Westenberg et al., 2002). Homologues of the F gene have been identified in other group II NPVs, in beta- and deltabaculoviruses and in members of the insect retrovirus family Errantiviridae, but also exist in group I NPVs (Herniou et al., 2003; Malik et al., 2000; Rohrmann & Karplus, 2001; Terzian et al., 2001). In the genome of group I NPVs, a truncated F homologue is present (Ac23 homologues). Its translation product is found on the envelope of BVs, but has been shown to be dispensable for viral replication and pathogenesis (Lung et al., 2003; Pearson et al., 2001).
Recently, it was shown that the F proteins of the group II NPVs SeMNPV, LdMNPV and HearNPV are capable of substituting functionally for GP64 in AcMNPV (Long et al., 2006b; Lung et al., 2002). An AcMNPV bacmid lacking the gp64 gene was unable to produce BVs after transfection into insect cells (Monsma et al., 1996), whereas this defect could be rescued by insertion of the SeMNPV, LdMNPV or HearNPV f gene (Long et al., 2006b; Lung et al., 2002). GP64 homologues are also found on Thogoto and Dhori viruses, which are tick-transmitted orthomyxoviruses that replicate in both ticks and mammals (Freedman-Faulstich & Fuller, 1990; Morse et al., 1992). It has therefore been suggested that the group I NPVs have acquired the gp64 gene later during evolution, either from the host or from another insect-infecting virus (Lung et al., 2002; Morse et al., 1992), thereby getting a selective advantage due to increased efficiency of either virus–receptor interaction and virus entry, or virus budding, obviating the need for a functional F protein. However, experimental evidence to support this view is lacking.
To address this hypothesis experimentally, a group II NPV (SeMNPV) lacking F was pseudotyped with GP64. The f gene of SeMNPV was deleted by using site-specific mutagenesis of an infectious SeMNPV bacmid (Pijlman et al., 2002). Transfection of this f-null bacmid into insect cells showed that the virus replicates in the initially transfected cell, but is no longer able to propagate an infection. Reinsertion of the SeMNPV f gene rescued SeMNPV infectivity fully, but insertion of the gp64 gene failed to rescue BV infectivity.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) was cultured at 27 °C in plastic tissue-culture flasks (Nunc) in Grace's insect medium, pH 5.9–6.1 (Invitrogen), supplemented with 10 % fetal bovine serum (FBS). The SeMNPV isolate (Gelernter & Federici, 1986) was originally obtained from Dr B. A. Federici (Department of Entomology, University of California, CA, USA) and was called SeMNPV-US1 (Muñoz et al., 1998).
Deletion of the SeMNPV f gene by ET recombination in Escherichia coli.
For deletion mutagenesis of the f gene of the SeMNPV-US1 bacmid SeBAC10 (Pijlman et al., 2002), 75- to 77-mer recombineering primers were designed with 50 nt comprising the left or right homology arm on the 5' end. The forward primer was 5'-TTTGGTCGTCGTCGTCGTCGTTGAAATGATACCCTTTGTCGTTGAACTGGCCTTAGGTTTAAGGGCACCAATAACTG-3', with viral flanking sequences [5' untranslated region (UTR)] from nt 12248 to 12297 according to the SeMNPV complete genome sequence (IJkel et al., 1999). The reverse primer was 5'-ATACATTATATATTGTTTTATTTTACTCTACTACTATTACAATCAATCGGCCTAAGGTTCCTGTGCGACGGTTAC-3', with viral flanking sequences (3' UTR) from nt 14545 to 14496. The 3' ends of the primers anneal to the chloramphenicol-resistance gene (cat) of pBeloBac11 (Shizuya et al., 1992; Wang et al., 1997), and a Bsu36I site was designed between the viral and cat sequences (underlined).
PCR on pBeloBac11 was performed by using high-fidelity Expand Long Template PCR (Roche). The expected 1050 bp PCR fragment was gel-purified and digested with DpnI to eliminate residual template plasmid DNA. After a second round of gel purification, about 500 ng PCR product was used for transformation of electrocompetent E. coli DH10β cells containing both SeBAC10 and the plasmid pBAD-
β
, promoting homologous recombination (Fig. 1a), as described previously (Pijlman et al., 2002). The altered sequence at the f locus of the recombinant bacmid, designated SeBAC
F, was confirmed by PCR using primers to the regions flanking the f gene.
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) in the SmaI and KpnI sites of pFastBac Dual (Invitrogen), generating pFBSePolh Dual. The SeMNPV f gene and the AcMNPV gp64 gene, both under the control of the gp64 promoter, were cloned as XbaI/EcoRI and XbaI/SstI fragments from pFBgusSe8 and pFBgusGP64 (Lung et al., 2002) into the SmaI and SstI sites of pFBSePolh Dual. In this procedure, the AcMNPV p10 and polyhedrin promoters were removed, and plasmids pFBSepolh-SeF(pGP64) and pFBSepolh-GP64(pGP64) were obtained, respectively.
The 250 bp upstream of the SeMNPV f open reading frame (ORF) was amplified from pSeBglII-H (IJkel et al., 1999) with primers 5'-AAACCCGGGTTTGGTCGTCGTCGTCGTCGTTG-3' and 5'-TAAGGATCCTATTTTGCTTGCGACTCGGTTCTC-3' (underlined sequences generate SmaI and BamHI restriction sites, respectively), using high-fidelity Expand Long Template PCR (Roche). The PCR fragment was cloned into the SmaI and BamHI sites of pFBSePolh Dual, thereby removing the AcMNPV p10 and polyhedrin promoters and generating pFBSepolh-(pSeF). The SeMNPV f gene and the AcMNPV gp64 gene were cloned as BamHI/NotI and EcoRI/EcoRI fragments from pFBgusSe8 and pFBgusGP64 (Lung et al., 2002) into the BamHI and NotI sites of pFBSePolh-(pSeF), generating pFBSePolh-SeF(pSeF) and pFBSePolh-GP64(pSeF), respectively. For the generation of control bacmids, a vector was generated containing only the SeMNPV polyhedrin gene behind its own promoter. This was done by removing the SeMNPV f promoter as an SmaI/StuI fragment from pFBSepolh-(pSeF), generating pFBSepolh.
Transfection of bacmids.
The inserts of the donor plasmids were transposed into the attTn7 transposition sites of the SeMNPV bacmids SeBacF and SeBAC10 (Fig. 1b
), or into the gp64-null AcMNPV bacmid (Lung et al., 2002), according to the Bac-to-Bac manual (Invitrogen). Transposition was confirmed by PCR as described previously (Westenberg et al., 2004).
Se301 cells (5.0x105) were seeded into 35 mm tissue-culture plates (Nunc). The cells were transfected with approximately 1 µg bacmid DNA, using 10 µl Cellfectin (Invitrogen). After 5 days, the cells were transferred to a T75 flask (Nunc) and, subsequently, one-third of the cells were transferred every 5 days to a new T75 flask until 90 % of the cells contained polyhedra. The insect-cell supernatants were clarified by centrifugation at 4000 g for 10 min and subsequently passed through a 0.45 µm filter. The presence of infectious BVs in the supernatant was investigated by infecting 1.0x106 Se301 cells in a T25 flask with 500 µl supernatant. Finally, the genotype of the BVs was verified by PCR.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Lung et al., 2002). To determine whether the reverse was also possible, a recently constructed SeMNPV bacmid (Pijlman et al., 2002) was modified by deleting the f gene (Se8). The f ORF and its promoter were deleted from the SeMNPV bacmid SeBac10 by ET recombination (Muyrers et al., 1999), using a PCR-amplified DNA fragment containing a cat cassette flanked by 50 bp of sequence 200 bp upstream of the translational start codon and 50 bp downstream of the stop codon (Fig. 1a). Bacterial colonies resistant for chloramphenicol (insert) and kanamycin (bacmid) were selected. The colonies were analysed for successful recombination by PCR using primers flanking the recombination sites and by sequencing the amplified DNA fragments (data not shown). The generated SeBacF DNA was transformed into E. coli DH10β cells, together with the plasmid pMON7124, encoding a Tn7 transposase, which can facilitate transposition of gene cassettes into the bacmid (Luckow et al., 1993).
To investigate whether the f gene is necessary for efficient budding and propagation of infection, the SeMNPV polyhedrin gene was inserted into SeBac10 and SeBacF bacmids at its original locus by Tn7-based transposition to mark successful infection (Fig. 1b) (Luckow et al., 1993). Se301 cells were transfected with the generated bacmids SeBac10/Sepolh and SeBacF/Sepolh. As a positive control, wild-type SeMNPV DNA was also transfected in parallel. Polyhedra were observed 1 week post-transfection (p.t.) in cells initially transfected with SeMNPV wild-type DNA, whilst 2 weeks p.t., approximately 90 % of the cells contained polyhedra (Fig. 2a). A significant delay was observed for cells transfected with SeBac10Sepolh, where 90 % was reached approximately 3 weeks p.t. (Fig. 2b). The presence of infectious BVs in the supernatants of the polyhedron-containing cell culture was demonstrated by infecting healthy Se301 cells with the supernatants (Fig. 2d, e). Cells initially transfected with SeBacFSepolh did contain polyhedra at 3 weeks p.t. (Fig. 2c), but subculturing of the cells showed that the virus did not spread to other cells (Fig. 2f). Therefore, it can be concluded that the SeMNPV f gene is essential for virus propagation in cell culture and probably in insects.
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FSepolh-SeF(pSeF). This bacmid was generated by transposing the f gene under the control of its own promoter, together with the polyhedrin gene, into SeBacF (Fig. 1b). Transfection of the bacmid resulted in the formation of polyhedra in the majority of cells 3 weeks p.t. (Fig. 3a) and the production of infectious BVs was demonstrated upon passaging the supernatant (Fig. 3d). This shows that the f-null SeMNPV bacmid could be rescued by its own f gene and that a viable virus was generated. Further, the experiment shows that the homologous repeat region hr1, essential for viral replication (Broer et al., 1998), and gp16, expressing a nuclear membrane protein with unknown function (Gross et al., 1993), both flanking the f gene in SeMNPV, were probably not affected by the deletion of f.
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F, generating SeBacFSepolh-GP64(pSeF) (Fig. 1b). Polyhedra were observed 3 weeks p.t. in Se301 cells that were initially transfected with this bacmid (Fig. 3b), but the infection did not spread to other cells. Transfer of the supernatant to fresh cells did not result in a secondary infection, suggesting that no infectious BVs were produced (Fig. 3e).
To exclude the possibility that the absence of spread was not due to low GP64 expression being governed by the SeMNPV f promoter or to less optimal replication of the bacmid, two ‘control’ bacmids, SeBacFSepolh-SeF(pGP64) and SeBacFSepolh-GP64(pGP64), were generated, from which either the F protein or the GP64 protein is expressed under the control of the AcMNPV gp64 promoter. Polyhedron-containing cells were observed when cells were transfected with f-null bacmid expressing the F protein (Fig. 3c), and transfer of the supernatant to fresh cells resulted in a secondary infection (Fig. 3f), indicating that the gp64 promoter is also able to drive f gene expression in SeMNPV. Despite this observation, rescue of f-null SeMNPV bacmid by gp64 under the control of its own promoter was not detected, as polyhedra were only observed in the initially transfected cells (Fig. 3g) and not in cells incubated with the supernatant (Fig. 3j).
Expression of GP64 in insect cells
To verify whether functional GP64 could be expressed from the donor plasmids pFBSePolh-GP64(pSeF) and pFBSePolh-GP64(pGP64), the expression cassettes were transposed into a gp64-null AcMNPV bacmid. Se301 cells were transfected with the originating bacmids AcBacgp64SePolh-GP64(pSeF) and AcBacgp64SePolh-GP64(pGP64), respectively. Five days p.t., polyhedron-containing cells were observed (Fig. 3h, i). Cell supernatants were clarified and used to infect healthy Se301 cells. Three days post-infection, infected cells were observed, as determined by the presence of polyhedra (Fig. 3k, l), indicating that infectious viruses were made and, more importantly, that GP64 had been expressed. So, in principle, GP64 could be expressed from SeBacFSepolh-SeF(pGP64) and SeBacFSepolh-GP64(pGP64) as well in Se301 cells, but was not able to form budded SeMNPV virions.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Pseudotyping of baculoviruses was performed successfully for the first time with vesicular stomatitis virus G (VSV-G) protein in AcMNPV BVs (Barsoum et al., 1997) and could even substitute for GP64 (Mangor et al., 2001), although viral propagation in insect cells was greatly reduced. However, neither pseudotyping experiment seemed to alter the host range of AcMNPV. GP64 is involved in viral attachment to host cells, is required during virus entry and is necessary for efficient budding of progeny NCs (Blissard & Wenz, 1992; Hefferon et al., 1999; Oomens & Blissard, 1999). GP64 is present in all group I NPVs. Group II NPVs lack the GP64 protein and use F proteins as envelope fusion protein (IJkel et al., 2000; Pearson et al., 2000). It has been postulated that, during evolution, the gp64 gene was inserted into some baculoviruses (now group I NPVs), giving these a selective advantage due to increased efficiency either of virus–receptor interactions or of virus entry or budding, obviating the need for a functional F protein (Lung et al., 2002; Morse et al., 1992). The question was whether this assumption could be approached experimentally and validated.
It has previously been shown that AcMNPV could be pseudotyped with certain group II NPV F proteins, which substituted for the functions of GP64 (Long et al., 2006b; Lung et al., 2002). These experiments indicated that the group II NPV F proteins are functionally analogous to GP64 in an AcMNPV virion. In the current study, however, it was found that the AcMNPV GP64 protein cannot substitute readily for the F protein in SeMNPV (Fig. 3c, d) in functional terms. Viral propagation could be rescued by reinsertion of an SeMNPV f gene in an f-null SeMNPV bacmid (Fig. 3a, b), confirming that the f gene is essential for BV production and systemic spread of the virus of a group II NPV. This is in contrast to the F homologue (Ac23) in the group I NPV AcMNPV, where this protein can be deleted without affecting viral replication or pathogenesis in cell culture or infected animals (Lung et al., 2003).
The inability of the f-null bacmid to propagate an infection could not be rescued by the introduction of AcMNPV gp64 either downstream of the authentic SeMNPV f promoter or downstream of the AcMNPV gp64 promoter. To exclude the possibility that propagation was affected by a deletion in the SeMNPV bacmid that could have been generated during transposition and transformation in E. coli, four different bacmid clones of SeBacFSepolh-GP64(pSeF) and SeBacFSepolh-GP64(pGP64F) were transfected into insect cells. However, none of the bacmids was able to propagate an infection, whereas the f-repair SeMNPV bacmid was able to do so each time. The ability to express GP64 from these bacmids was demonstrated by the insertion of the same expression cassettes into a gp64-null AcMNPV virus, restoring full BV infectivity (Fig. 3e, f). If GP64 is expressed in an SeMNPV background, the level of this expression can only be very low. Western blot analysis using -GP64 on Se301 cells transfected with the SeMNPV bacmids was not sensitive enough to detect GP64, also due to the low transfection rates (<0.1 %).
Despite the observation in this report that GP64 is not able to replace F functionally in SeMNPV, it has been demonstrated that GP64 can be inserted into the group II NPV HearNPV, but only when it carries an authentic f gene (Liang et al., 2005). GP64 meets the requirements of an envelope glycoprotein that is independently able to insert into a membrane and form envelopes, as in pseudotyped lentiviruses (Kumar et al., 2003). Human immunodeficiency virus type 1 (HIV-1) does not require its envelope protein (Env) for virion budding. However, the generated virions were not infectious (Shioda & Shibuta, 1990). Budding of retroviruses seems to occur at ordered lipid microdomains, called lipid rafts (Briggs et al., 2003). It is possible that, when expressed in mammalian cells, GP64 may end up in these lipid rafts and thereby in the envelope of lentiviruses. Recent experiments, however, indicate that GP64 does not seem to be associated with lipid rafts in insect cells (Zhang et al., 2003). In the context of group II NPVs, GP64 may not function on its own because it lacks essential interaction with other proteins to form BVs.
In contrast to HIV-1, the major envelope protein E2 of alphaviruses is absolutely required for efficient budding (Owen & Kuhn, 1997). One hypothesis to explain the synergistic roles of various proteins in the budding process is the push–pull model (Mebatsion et al., 1996). The push represents the role of the matrix and perhaps other proteins on the inner surface of the plasma membrane, and the pull represents the role of the membrane proteins within and on the exterior of the membrane. The concerted or synergistic effects of the two components may accomplish budding. In this respect, it is possible that SeMNPV and perhaps all group II NPV NCs require a special interaction with the F protein to provoke budding, whereas this interaction is not needed for the incorporation of the SeMNPV F protein in AcMNPV BVs.
A possible candidate for this interaction may be the cytoplasmic tail domain (CTD) of the group II NPV F-like proteins. This CTD ranges in length from about 54 to 78 aa. In GP64-like proteins, this domain is much smaller, i.e. 3–8 aa, and probably inert (Oomens & Blissard, 1999). It has been shown for HearNPV (a group II NPV) that, except for the C-terminal 16 aa, the CTD of an F protein is important for virus spread from cell to cell (Long et al., 2006a). Whilst the HearNPV F protein without its CTD is unable to do this in the context of HearNPV, it still rescues infectivity of gp64-null AcMNPV. The long CTDs of the F-like proteins could possess one or more specific protein motifs required for interaction with the viral NCs, whereas these motifs are absent in the rather short CTDs of GP64-like proteins.
The involvement of CTDs of viral envelope proteins in the budding process has indeed been supported for a number of other viruses, including Sendai virus (Ali & Nayak, 2000), influenza A virus (Bilsel et al., 1993), VSV (Robison & Whitt, 2000), Mason–Pfizer monkey virus (Song et al., 2003) and Semliki Forest virus (Zhao et al., 1994). It is plausible that there is an interaction between the CTD of F and one or more viral NC proteins that are specific for group II NPVs. The putative protein Se107 (ORF 107 in SeMNPV), with a nuclear-localization signal and present only in group II NPVs (Herniou et al., 2003), may be a candidate for such a protein. Group II NPVs share another unique gene, Se30. The putative translation product of this gene seems to have a signal peptide and transmembrane domain and it is therefore possible that this protein is translocated to the cell membrane and acts in conjunction with F in virion assembly and virus budding.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 30 July 2007;
accepted 17 October 2007.
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