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Journal of Virology, August 2005, p. 10077-10082, Vol. 79, No. 15
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.15.10077-10082.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

The Immediate-Early Protein IE0 of the Autographa californica Nucleopolyhedrovirus Is Not Essential for Viral Replication{dagger}

Lu Liqun,{ddagger} Hadassah Rivkin, and Nor Chejanovsky*

Entomology Department, Institute of Plant Protection, ARO, The Volcani Center, POB 6 Bet Dagan 50250, Israel

Received 2 July 2004/ Accepted 25 April 2005


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ABSTRACT
 
The role of the Autographa californica multiple nucleopolyhedrovirus (AcMNPV) immediate-early protein IE0 in the baculoviral infection is not clear. In this study, we constructed the recombinant virus vAc{Delta}ie0 null for ie0 expression by targeted mutagenesis replacing exon0 with the cat gene. We found that vAc{Delta}ie0 replicated efficiently in Spodoptera littoralis SL2 cells, which are poorly permissive for AcMNPV. In contrast, in Spodoptera frugiperda SF9 cells, which are fully permissive for AcMNPV, vAc{Delta}ie0 DNA replication and budded virus production were delayed. These results and recently published data (X. Dai et al., J. Virol. 78:9633-9644, 2004) indicate that ie0 is not essential for AcMNPV replication but enhances it in permissive SF9 cells.


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TEXT
 
We focus on the ability of the Autographa californica multiple nucleopolyhedrovirus (AcMNPV), of the Baculoviridae family of arthropod viruses, to infect lepidopteran hosts. The AcMNPV-encoded immediate early protein, IE1, plays a crucial role in regulating the viral infection (2, 6, 9, 11, 13, 17, 21, 27, 29). IE1 is a potent transcriptional activator of early genes, including 39K, p35, and he65 (3, 7, 9, 12, 20) and of its own promoter (18), and it is essential for both DNA replication and late gene expression (15, 16, 18, 20, 22, 24-26, 28, 30, 32). IE1 negatively regulates transcription of the immediate-early gene ie0 (18) and the viral genes pe38 and ie2 (9, 19, 20). The role of IE0, the product of ie0, in the viral replication cycle is unclear. IE0 differs from IE1 by the addition of 54 N-terminal amino acids encoded by exon0 (5). ie0 RNA is expressed only during the early phase of infection, and ie1 RNA is expressed during early and late phases of infection (5, 17, 18). IE0 transactivates the ie1 promoter but does not affect expression from its own promoter (18).

Recently, we reported that recombinant AcMNPVs that expressed ie0 at extremely low levels were able to replicate efficiently in poorly permissive Spodoptera littoralis SL2 cells in contrast to wild-type AcMNPV (4, 23). This suggested that in contrast to the wild type, AcMNPV mutants null in ie0 may replicate efficiently in SL2 cells. We addressed this hypothesis by constructing vAc{Delta}ie0 in which the cat gene replaced exon0 and analyzed its ability to replicate in SL2 and in SF9 cells, the latter being fully permissive to AcMNPV. For this purpose, we utilized targeted mutagenesis as described before (1). Briefly, the Escherichia coli strain BJ-pFP, bearing the recombinant bacterial artificial chromosome plasmid (BACmid) AcFastpolh (23) was transformed with a 2.1-kb SnaBI-SalI fragment containing (i) the 5'- and 3'-flanking sequences of exon0 (AcMNPV map units 91.5 and 92.1, respectively [17]) and (ii) the cat gene replacing exon0. This was achieved by cloning cat into a new BamHI site created in the ie0 promoter region at –31 bp upstream of the ATG start and an existing ClaI site located 120 bp downstream of this ATG (23).

Recombinant BACmid DNA was prepared from transformed bacterial cells resistant to kanamycin and chloramphenicol (1). SF9 cells (106) were transfected with 200 ng of BACmid DNA, and the recombinant virus vAc{Delta}ie0 (Fig. 1A) was obtained after plaque purification of budded viruses present in the supernatant of the cells (1). PCR analysis with primer pair CAT5' (5'-ATGGAGAAAAAAACACTG-3') and CAT3' (5'-TTACGCCCCGCCCT-3') confirmed the presence of cat in the genome of vAc{Delta}ie0 (Fig. 1B, lane 4). The construct vAciePCAT, which bears the cat gene 3' downstream of ie0 promoter but 5' upstream of exon0 (24), served as the positive control (Fig. 1B, lane 3). As expected, cat was not amplified in the absence of viral DNA template or with the use of the AcMNPV genome (Fig. 1B, lanes 1 and 2, respectively). The presence of ie0 was analyzed by PCR using the primers IE0L (5'-CCGGAATTCTATGATAAGAACCAGC-3') and IE0R (5'-GTGTCAACTTGCAACTGCTGAGCTTCTGC-3'). The ie0 coding fragment of exon0 was detected in AcMNPV and vAciePCAT genomes but not in the genome of vAc{Delta}ie0 (Fig. 1B, lanes 6, 7, and 8, respectively). The orientation of the cat gene relative to the ie0 promoter was confirmed by PCR with the primers CAT5' and IE0R2 (5'-GAATAAATGCCATA GGCTCTG-3) (data not shown).




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  		FIG. 1. Structure of recombinant AcMNPVs. (A) Genomic organization. The dashed lines indicate the site of insertion of the cat gene (box). The boxes show the locations of the ie0 coding regions (exon0 and exon1) and ie1 and me53 genes and their correspondent promoters (upper arrows). IE0L, IE0R, IE0R2, CAT5', and CAT3' primers were utilized for PCR analysis. H, HinDIII restriction enzyme site; B, BamH I restriction enzyme site; S, SalI restriction enzyme site. (B) PCR analysis using cat or exon0 primers (CAT5' and CAT3' or IE0L and IE0R, respectively). Lanes 1 and 5, no template; lanes 2 and 6, AcMNPV; lanes 3 and 7, vAcie0PCAT (see reference 23); lanes 4 and 8, vAc{Delta}ie0. Molecular markers are indicated on the left. Arrows, PCR products.

vAc{Delta}ie0 was viable in SL2 and SF9 cells. We examined if IE0 was synthesized in vAc{Delta}ie0-infected SL2 and SF9 cells by immunoblot analysis with anti-IE0/IE1 antiserum (23). To distinguish between IE0 and IE1, we utilized the plasmids phspie0 and phspie1 (bearing ie0 and ie1, respectively, under the control of the heat shock promoter from Drosophila) (10). phspie0 was constructed by hybrid PCR to obtain fusion of exon0 and exon1 (5). The 140-bp exon0 sequence was amplified from pBgl-11 bearing an intact ie0 (23) with the primers IE0L (containing an EcoRI site) and IE0R. The 5' 200-bp sequence of exon1, containing 152 bp of the ie1 5' coding sequence and an additional 48 bp specific to ie0 5' upstream and contiguous to ie1, was amplified from pAcie1 (3) with the primers IE1L2 (5'-CAGCAGTTGCAAGTTGAC-3') and IE1R2 (5'-TCGCTGTCAGATATCACCG-3') bearing an EcoRV site. A mixture of the amplified DNA from these PCRs served as PCR template to obtain the fused ie0 5' N-terminal coding sequence (340 bp) using the IE0L1 and IE1R2 primers. The resultant product was digested with EcoRI-EcoRV and cloned in phsp70ie1 digested with the above enzymes to obtain pHspie0 that bore the complete ie0 open reading frame (ORF).

Transfection of SL2 cells with phspie1, which bears only ie1 (23), enabled us to identify IE1 by polyacrylamide gel electrophoresis (PAGE) and subsequent immunoblot analysis (Fig. 2A, lane 10). IE1 and IE0 accumulated to approximately equal levels throughout the infection of SL2 cells with AcMNPV (Fig. 2A, lanes 2 to 5). In vAc{Delta}ie0-infected SL2 cells, IE1 was detectable at 4 h and it accumulated during the infection (Fig. 2A, lanes 6 to 9). As expected, no IE1 or IE0 was detected in mock-infected cells (Fig. 2A, lane 1).



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  		FIG. 2. Synthesis of IE1 and IE0 in SF9 and SL2 cells infected with vAc{Delta}ie0 and AcMNPV. SL2 (A) or SF9 (B) cells (105) were infected with AcMNPV or vAc{Delta}ie0 at a multiplicity of infection (MOI) of 5 or transfected with phspie0 and phspie1. m.i., mock-infected cells. At various time points (indicated on top of each panel), the cells were harvested and the samples were subjected to sodium dodecyl sulfate-PAGE and immunoblot analysis with anti-IE1/IE0 antiserum. Molecular mass markers are shown on the left. Arrows on the right show the positions of IE0 and IE1.

We also studied the pattern of accumulation of IE1 and IE0 in SF9 cells. Control cells transfected with phspie0 showed the polypeptide corresponding to IE0 (Fig. 2B, lane 2). AcMNPV-infected SF9 cells showed approximately equal steady-state levels of IE0 and IE1 at 4 h postinfection (Fig. 2B, lanes 3 and 4). IE1 steady-state levels increased and became higher than those of IE0 at later times in infection (Fig. 2B, lanes 5 to 6). vAc{Delta}ie0-infected or mock-infected SF9 cells did not show production of IE0 as expected (Fig. 2B, lanes 7 to 10 and 1, respectively). The steady-state levels of IE1 increased significantly in AcMNPV- and vAc{Delta}ie0-infected SF9 cells from 8 to 16 h postinfection (Fig. 2B, compare lanes 4 and 5 and lanes 8 and 9, respectively), reflecting the transition from the early to the late phase of infection.

vAc{Delta}ie0 showed an ie1 expression pattern similar to that of vAcie0PCAT in SL2 cells, and we have shown previously that the latter virus replicated better than AcMNPV in this system (23). Thus, we compared vAc{Delta}ie0 and AcMNPV replication in SL2 cells. vAc{Delta}ie0-infected SL2 cells yielded budded viruses at levels above 106 PFU/ml by 72 hpi; these levels were similar to those of vAcie0PCAT and in contrast to the very low titers of AcMNPV (Fig. 3A). However, we noted a reduced rate in budded virus production for vAc{Delta}ie0- compared to vAcie0PCAT-infected SL2 cells (Fig. 3A). Restoration of the deleted ie0 to vAc{Delta}ie0 resulted in lower budded virus yields in SL2, as observed for AcMNPV (data not shown). In infected SF9 cells, titers of vAc{Delta}ie0 and vAcie0PCAT were 12- to 15-fold lower than that of the wild-type virus (Fig. 3B). We analyzed the rate of budded virus production in SF9 cells between 12 and 24 h postinfection, at 2-h intervals, and found that the rate of synthesis of budded viruses was about 104 PFU/ml per hour for vAc{Delta}ie0 and 105 PFU/ml per hour for AcMNPV (data not shown). From the above results, we concluded that the deletion of the ie0 coding region of exon0 affected the rate of budded virus production.



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  		FIG. 3. Budded-virus yields from vAc{Delta}ie0-, vAcie0PCAT-, and AcMNPV-infected SL2 (A) and SF9 (B) cells. The cells were infected at an MOI of 0.5, and budded viruses (BV) were collected from the cells at the indicated time points after infection and titrated in SF9 cells. The data are the average results of three independent experiments. Error bars indicate standard deviations.

Subsequently, we analyzed the production of polyhedrin and polyhedra by vAc{Delta}ie0-infected SL2 and SF9 cells. Microscopic observation showed polyhedra in the nuclei of vAc{Delta}ie0-infected SL2 and SF9 cells at 72 hpi (Fig. 4A, panels a and b, respectively). AcMNPV-infected SL2 cells did not produce polyhedra, as we reported previously (10, 23), in contrast to wild-type virus-infected SF9 cells (Fig. 4A, panels c and d, respectively). Moreover, polyhedrin accumulated to similar levels in SL2 cells infected with vAc{Delta}ie0 and vAcie0PCAT, and its steady-state levels were about 100-fold higher than those observed with AcMNPV-infected cells (Fig. 4B, lanes 1, 2, and 3, respectively).




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  		FIG. 4. (A) Light micrographs of SL2 (a and c) and SF9 (b and d) cells infected with vAc{Delta}ie0 (a and b) or AcMNPV (c and d) at an MOI of 5 at 72 hours postinfection (hpi; bar, 3 µm). (B) Western blots of infected cells at an MOI of 5 with vAc{Delta}ie0 (lanes 1 and 4), vAcie0PCAT (lanes 2 and 5), or AcMNPV (lanes 3 and 6). Extracts of infected SL2 (lanes 1 to 3) and SF9 (lanes 4 to 6) cells harvested at 48 hpi, subjected to sodium dodecyl sulfate-PAGE, and immunoblotted with anti-polyhedrin antiserum. Ph, polyhedrin. Molecular mass markers are indicated on the left.

In SF9 cells infected with vAc{Delta}ie0, the steady-state levels of polyhedrin were comparable to those produced by vAcie0PCAT and AcMNPV (Fig. 4B, lanes 4, 5, and 6, respectively), but the appearance of polyhedra was delayed for another 24 h with respect to AcMNPV (data not shown).

To determine whether the deletion of ie0 had an effect on earlier steps of AcMNPV replication, we followed the onset and steady-state levels of DNA produced throughout infection by dot blot analysis using a fluorescein-labeled fragment of the AcMNPV polyhedrin gene (Renaissance Random Primer fluorescein labeling kit; Perkin-Elmer Life Sciences). Under our experimental conditions, we were able to detect vAcie0PCAT and vAc{Delta}ie0 DNA in virus-infected SF9 cells at 12 h and 14 h postinfection, respectively, 2 and 4 hours later than AcMNPV DNA (Fig. 5A, spots 5B, 6C, and 4A, respectively). Steady-state levels of vAcie0PCAT and vAc{Delta}ie0 DNA levels increased significantly till 24 h after infection. Thus, partial or total suppression of production of IE0 correlated with delayed viral DNA replication, suggesting that the early phase of the infection was indeed affected as well.



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  		FIG. 5. Dot blot analysis of AcMNPV, vAcie0PCAT, and vAc{Delta}ie0 DNA replication in SF9 cells. Rows A to C, lanes 1 to 10, lysates of AcMNPV-, vAcie0PCAT-, and vAc{Delta}ie0-infected SF9 cells (MOI of 0.5) at 2, 4, 8, 10, 12, 14, 16, 18, 20, and 24 hpi, respectively. Row D, lanes 1 to 8, 200, 40, 8, 1.6, 0.5, 0.1, 0.02, and 0.004 ng of control AcMNPV DNA, respectively; lanes 9 and 10, extracts from mock-infected cells.

ie0 mRNA consists of 114 nucleotides (nt) from the 5' end of exon0, spliced to join the entire ie1 coding region and an additional upstream 48 nt adjacent to the ie1 ORF (17). Also, exon0 encodes a putative protein, ORF141 (8). Deletion of ie0 resulted in a concomitant deletion of the N terminus of ORF141 (8). Thus, the phenotype of our vAc{Delta}ie0 mutant could be attributed to different functions of IE0 and ORF141 in the viral replication cycle. ORF141 was correlated with the ability of AcMNPV to bud from permissive SF9 cells (8), and this is consistent with our finding that the rate of budded virus production of vAc{Delta}ie0 was about 10-fold lower than that of AcMNPV. On the other hand, the delay that we observed in the onset of viral DNA synthesis in SF9 cells infected with vAcie0PCAT or with vAc{Delta}ie0 (Fig. 5) may be due to the deficiency of these mutants to produce IE0. This conclusion is further supported by the recent finding by Dai et al. (8) that a knock-out mutant in ORF141 that was not defective in production of IE0 did not show delay in the onset of DNA synthesis.

Our results, obtained by infecting cells SL2 and SF9 cells with vAc{Delta}ie0 and vAcie0PCAT, show that IE0 is not essential for viral replication. Thus, in AcMNPV-permissive SF9 cells, IE0 may contribute to modulate the IE1 function early in infection. This could be achieved by IE0-mediated transactivation of the ie1 promoter and/or by its association with IE1 as suggested before (20, 21, 31). In SL2 cells poorly permissive for AcMNPV, the IE0 regulatory function appears to be lost, no transition from the early to the late phase of production of IE1 is observed, and the viral infection is aborted. Moreover, in this system, accumulation of IE0 interferes with the viral infection since its deletion allows completing the viral cycle (this work and reference 22). Taken together, the above data suggest that IE0 regulates the IE1-function by its association with IE1 and other SF9 cellular factors, but not SL2 cellular factors. Formation of a complex between IE0 and IE1 could be required in the early phase of infection, but if the accumulation of IE0 late in infection is comparable to that of IE1, the above complex could be an obstacle not leaving enough IE1 available (in the form of IE1-IE1 dimers [24]) to enable completion of AcMNPV's replication cycle. Rescue of production of viral progeny in these cells could be achieved by reducing or eliminating the accumulation of IE0 (reference 23 and Fig. 2A, respectively). This hypothesis is consistent with the observed antagonistic effects of coexpression of ie0 and ie1 on very late gene expression (14).

Finally, the function of the putative ORF141 protein in AcMNPV-infected SL2 cells remains unclear. It is conceivable that further increase in budded virus titers could be achieved by infecting these cells with an AcMNPV null mutant in ie0, bearing an intact ORF141 protein.


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ACKNOWLEDGMENTS
 
We acknowledge support for this research by BARD, under grant no. IS-2999-98 to N.C.


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FOOTNOTES
 
* Corresponding author. Mailing address: Entomology Department, The Institute of Plant Protection, The Volcani Center, POB 6, Bet Dagan 50250, Israel. Phone: 972-3-968-3694. Fax: 972-3-960-4180. E-mail: ninajiq{at}volcani.agri.gov.il. Back

{dagger} Contribution 507/04 from the Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel. Back

{ddagger} Present address: Animal Health Biotechnology Unit, Temasek Life Sciences Laboratory, National University of Singapore, 1 Research Link, Singapore 117604. Back


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Journal of Virology, August 2005, p. 10077-10082, Vol. 79, No. 15
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.15.10077-10082.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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