Prevention of baculovirus-induced apoptosis of BTI-Tn-5B1-4 (Hi5) cells by the p35 gene of Trichoplusia ni multicapsid nucleopolyhedrovirus
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Journal of General Virology (1999), 80, 1841–1845. Printed in Great Britain
.......................................................................................................................................................................................................... SHORT COMMUNICATION
Prevention of baculovirus-induced apoptosis of BTI-Tn-5B1-4
(Hi5) cells by the p35 gene of Trichoplusia ni multicapsid
nucleopolyhedrovirus
Xiaojiang Dai,1 Xianzong Shi,1† Yi Pang1 and Deming Su1, 2
1
Institute of Entomology and State Key Laboratory for Biocontrol, Zhongshan University, Guangzhou 510275, People’s Republic of China
2
Virology Research Unit, Fudan University, Shanghai 200433, People’s Republic of China
factor (Beidler et al., 1995). Thus, it seems the function of P35
A typical apoptosis of BTI-Tn-5B1-4 (Hi5) cells is highly conserved in evolution. The p35 promoter of
induced by Heliothis armigera single capsid nucleo- Autographa californica multicapsid nucleopolyhedrovirus
polyhedrovirus (HaSNPV) infection was completely (AcMNPV) has both early and late regulating elements that
suppressed by coinfection with Trichoplusia ni multi- direct early and late mRNA synthesis (Nissen & Friesen, 1989 ;
capsid nucleopolyhedrovirus polyhedron-negative Dickson & Friesen, 1991). P35 protein is first detected at
recombinant (TnMNPV-SVING) (OCCN) at a low mul- 8–12 h post-infection (p.i.) and accumulates through later
tiplicity of infection (6n5i10N2). To determine stages of infection (24–36 h p.i.) (Hershberger et al., 1992,
whether TnMNPV p35 alone was sufficient to inhibit 1994). P35 protein is found predominantly in the cytosol
the apoptosis, two recombinant plasmids contain- (Hershberger et al., 1994), unlike the mammalian anti-apoptotic
ing the early promoter of p35, or the very late protein BCL-2, which is localized mainly in the membranes of
promoter of TnMNPV polh were constructed to the mitochondria, endoplasmic reticulum or nucleus
study p35 function by transient expression assay. It (Hockenbery et al., 1990). In addition to its role as an inhibitor
was shown that expression of p35 alone could of apoptosis, P35 can stimulate baculovirus DNA replication
partially prevent HaSNPV-induced apoptosis but (Kool et al., 1994), increase transcription from the 39 kDa
did not facilitate HaSNPV replication in Hi5 cells. promoter of AcMNPV (Gong & Guarino, 1994 ; Gong et al.,
The data suggests that both P35 of TnMNPV and 1998) and promote transformation of mouse embryonic
other unknown gene products are required for the fibroblasts (Resnicoff et al., 1998).
suppression of apoptosis and facilitation of HaSNPV A second class of baculovirus genes, iaps (inhibitors of
replication in Hi5 cells. apoptosis), can be found also in both insect viruses and
mammals (Crook et al., 1993 ; Birnbaum et al., 1994). These
genes encode a C3HC4 (or RING) finger motif found in a
In baculoviruses, the products of two viral genes, p35 and number of transcriptional regulatory proteins, as well as two
iap, are involved in the inhibition of apoptosis (Teodoro & additional novel Cys\His motifs called baculovirus iap repeats
Branton, 1997 ; Miller, 1997). The p35 gene product is unique (BIRs) (Crook et al., 1993 ; Birnbaum et al., 1994). Specific amino
for this virus group, inhibiting not only baculovirus-induced acids within the C3HC4 finger and the N-terminal BIR are
apoptosis in insect cells (Clem et al., 1991) but also develop- critical for IAP anti-apoptosis function (Clem & Miller, 1994).
mentally programmed cell death in the nematode Caeno- It is believed that the mechanism by which the p35 product
rhabditis elegans (Sugimoto et al., 1994) and Drosophila flies inhibits apoptosis differs from that of the iaps products. While
(Hay et al., 1994). In addition, P35 can prevent neuronal cell P35 prevents apoptosis by specifically inhibiting CED-3\ICE
death induced by serum or nerve growth factor deprivation in death protease (caspase I), the iaps proteins function at an
mammalian cells (Rabizadeh et al., 1993 ; Martinou et al., 1995) earlier stage in the pathway, probably involving other caspases
and apoptotic cell death induced by Fas and tumour necrosis in addition to caspase I (Seshagiri et al., 1997 ; Vucic et al., 1997 ;
Manji et al., 1997 ; Bertin et al., 1996 ; Ahmad et al., 1997).
Author for correspondence : Yi Pang. In China, Heliothis armigera single nucleocapsid nucleo-
Fax j86 20 8403 7472. e-mail LS12!zsu.edu.cn polyhedrovirus (HaSNPV) was first described in 1978 (Cai,
1978) and was later developed as the first commercial
† Present address : Department of Entomology & Nematology, insecticide against the cotton bollworm in more than 20
University of Florida, PO Box 110620, Gainesville, FL 32611-0620, provinces (Li & Pang, 1990 ; Zhang et al., 1994). Restriction
USA. fragment length polymorphism in several HaSNPV isolates
0001-6158 # 1999 SGM BIEB
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(a) Republic of China). TnMNPV polyhedron-negative recom-
binant virus TnMNPV-SVI−G (OCC−) was constructed in our
laboratory (Wang et al., 1991). TnMNPV (Kelly & Lescott,
1981) was donated by D. C. Kelly (NERC Institute of Virology
and Environmental Microbiology, Oxford, UK) and has a very
similar genome and protein structure to AcMNPV (Miller &
Dawes, 1978 ; Wang & Kelly, 1983). Trichoplusia ni cell line
BTI-Tn-5B1-4 (Hi5) (Granados et al., 1994) was donated by R.
R. Granados (Boyce Thompson Institute, USA) and Heliothis
zea cell line Hz-IB3 (McIntosh & Ignoffo, 1983) by Quhou
Chen (Central China Normal University, People’s Republic of
China). All cells were propagated at 27 mC in TC-100 medium
(b) supplemented with 10 % foetal bovine serum (Gibco).
TnMNPV-SVI−G was replicated in Hi5 while HaSNPV was
replicated in Hz-IB3 cells. The virus titre was determined by
plaque assay as previously described (O’Reilly et al., 1992).
Isolation of apoptotic DNA fragments was as described by
Herrmann et al. (1994).
Hi5 cells were coinfected with HaSNPV (at an m.o.i. of 5)
and TnMNPV-SVI−G (at an m.o.i. of 5). As a control, Hi5 cells
were infected with HaSNPV alone at an m.o.i. of 5. Light
microscopic observations and the presence or absence of DNA
ladders indicated that the cells coinfected with HaSNPV and
TnMNPV-SVI−G did not undergo apoptosis even by 72 h p.i.
(Fig. 1 a). In these cells, polyhedra (OCC+) were detected in
Fig. 1. (a) Prevention of HaSNPV-induced apoptosis of Hi5 cells by about 30 % of the coinfected cells 72 h p.i., while the other 70 %
TnMNPV-SVI−G. M, Molecular mass marker (λDNA/EcoRIjHindIII) ; A, of cells showed typical virus-infected cytopathic effect with a
uninfected Hi5 cells ; B, Hi5 cells coinfected with TnNPV-SVI−G and
HaSNPV at 72 h p.i., showing complete inhibition of HaSNPV-induced polyhedron-negative phenotype (OCC−). Since the TnMNPV
apoptosis of Hi5 cells by TnNPV-SVI−G ; C, Hi5 cells infected with TnNPV- recombinant virus TnMNPV-SVI−G (OCC−) was used in the
SVI−G at an m.o.i. of 5, 48 h p.i., no apoptosis observed ; D, Hi5 cells coinfection, the presence of polyhedra was due to spread of the
infected with HaSNPV at an m.o.i. of 5, 48 h p.i., showing the
characteristic DNA ladder. (b) Dosage–effect analysis of TnMNPV-SVI−G HaSNPV. The supernatant from the coinfected cells was
for prevention of HaSNPV-induced apoptosis in Hi5 cells. HaSNPV- infective to both Hz-IB3 and Hi5 cells (data not shown),
induced apoptosis was completely inhibited when Hi5 cells were indicating that coinfection of HaSNPV and TnMNPV not only
coinfected with HaSNPV at an m.o.i. of 5 and TnMNPV-SVI−G at an m.o.i.
of 6n5i10−1 or 6n5i10−2 ; HaSNPV-induced apoptosis was not inhibited inhibited completely HaSNPV-triggered apoptotic cell death
when Hi5 cells were coinfected with HaSNPV at an m.o.i. of 5 and but also facilitated HaSNPV replication in Hi5 cells. In the
TnMNPV-SVI−G at an m.o.i. of 6n5i10−4 or 6n5i10−5 ; HaSNPV-induced HaSNPV-infected Hi5 cells, apoptosis appeared at 24 h p.i.
apoptosis was partially inhibited when Hi5 cells were coinfected with
HaSNPV at an m.o.i. of 5 and TnMNPV-SVI−G at an m.o.i. of 6n5i10−3. with a peak of apoptotic mortality (approx. 60 % of cells) at
48 h p.i. (Fig. 1 a). Although a few viral polyhedra were
observed in 5 % of cells, the supernatant of the culture was not
and permissiveness of different cell lines to the replication of infective to Hz-IB3 cells.
HaSNPV have been reported (Wang et al., 1996 ; Zhang et al., To determine the minimum quantity of TnMNPV-SVI−G
1993 ; Sun & Zhang, 1998 ; Liu et al., 1998). Although its required for inhibiting HaSNPV-induced apoptosis of Hi5 cells,
genome is largely unsequenced, several genes have been Hi5 cells were coinfected with HaSNPV (at an m.o.i. of 5) and
characterized in the HaSNPV genome, like polh (Wang et al., TnMNPV-SVI−G at increasing m.o.i. (5–6n5i10−'). Fig. 1 (b)
1996, 1997), chiA (Peng et al., 1998) and egt (Chen et al., 1997). shows that an m.o.i. for TnMNPV-SVI−G as low as 6n5i10−#
To our surprise, when challenged with HaSNPV, the was sufficient for complete inhibition of apoptosis and the
Trichoplusia ni cell line, BTI-Tn-5B1-4 (Hi5) cells underwent facilitation of HaSNPV replication in Hi5 cells.
apoptotic cell death (Pang et al., 1998). In the present study, we To determine whether the TnMNPV P35 alone was
observed that the HaSNPV-induced apoptosis in Hi5 cells was sufficient to inhibit the apoptosis, we constructed two p35
completely suppressed by coinfection with Trichoplusia ni plasmids to study P35 function by transient expression assay.
multicapsid nucleopolyhedrovirus (TnMNPV) and partially The two p35 plasmids were constructed as follows. According
blocked by TnMNPV P35 expression alone. to the reported AcMNPV p35 sequence (Friesen & Miller,
HaSNPV Hubei strain (Cai, 1978) was provided by Zhihong 1987), we amplified the p35 early promoter region and its open
Hu (Institute of Virology, Academia Sinica, Wuhan, People’s reading frame (p35EPO) from the TnMNPV genome using
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On: Fri, 11 Sep 2015 13:26:49Prevention of apoptosis by TnMNPV p35 gene
(a) (b)
Fig. 2. (a) Partial inhibition of HaSNPV-
induced apoptosis by the TnMNPV p35
gene product in Hi5 cells. A, uninfected
Hi5 cells ; B, Hi5 cells infected with
HaSNPV at an m.o.i. of 5, 48 h p.i.,
showing the characteristic DNA ladder ; C,
Hi5 cells transfected with pUC-p35EPO
DNA, and after 24 h infected with
HaSNPV at an m.o.i. of 5, showing partial
inhibition of HaSNPV-induced apoptosis
by pUC-p35EPO in Hi5 cells. (b)
Dosage–effect analysis of pUC-p35EPO for
prevention of HaSNPV-induced apoptosis
in Hi5 cells.
forward primer P1 (5h CGCgaattcATGTGTGTAATCTTT- inoculated onto Hz-IB3 cells. As a result, no infectivity was
CCG 3h), incorporating an EcoRI restriction site, and reverse detected, suggesting that TnMNPV P35 could not facilitate
primer P2 (5h CGCctgcagATGACAAGCAATGAT 3h), incor- DNA replication of HaSNPV in Hi5 cells, and infective budded
porating a PstI restriction site. The amplified sequence was viruses were not detected.
1084 bp in length and had 100 % identity with AcMNPV p35 In our constructs, the two plasmids above did not show
(Shi et al., 1996). The amplificon was doubly digested with significant differences in the inhibition of HaSNPV-induced
EcoRI and PstI and cloned into pUC18 and the expression apoptosis in Hi5 cells, meaning that late expression of p35 in
vector pX3 (Wang et al., 1991), to generate two p35 this case did not further suppress apoptosis.
recombinant plasmids, pUC-p35EPO and pX3-p35EPO. The When the cells were transfected with increasing quantities
former contains the TnMNPV p35 ORF and its own promoter. of plasmid pUC-p35EPO (0n5–10 µg DNA per 2i10& Hi5
The latter contains the TnMNPV p35 ORF driven by its own cells) and then infected with HaSNPV at an m.o.i. of 5 at 24 h
promoter and a very late polh promoter, and the flanking after transfection, the results showed that transfection of
portions of TnMNPV polh (Wang et al., 1991). 2i10& Hi5 cells with 2–5 µg of plasmid pUC-p35EPO resulted
Hi5 cells were transfected using the p35 plasmid DNA as in significant suppression of apoptosis (Fig. 2 b).
described by Kool et al. (1993). A 35 mm tissue culture plate Taken together, our results indicated that the p35 product
was seeded with 2i10& Hi5 cells and incubated at 27 mC of TnMNPV is able to prevent HaSNPV-induced apoptosis of
overnight to allow the cells to attach. Five µg of pUC-p35EPO Hi5 cells ; both the p35 gene product and other unknown gene
or pX3-p35EPO plasmid DNA and 20 µl of Lipofectin reagent products are required to completely suppress the apoptosis
(Gibco BRL) were transfected into the Hi5 cells. After and, at the same time, facilitate HaSNPV replication in Hi5
incubation at 27 mC for 6 h, the DNA-containing medium was cells.
replaced by 1n5 ml of fresh medium, and the cells were It is generally believed that apoptosis provides cells with an
incubated at 27 mC for 24 h. The cells were then infected with effective and final antiviral defence mechanism to prevent virus
HaSNPV at an m.o.i. of 5. As a control, 2i10& cells were infections, and suppression of apoptosis by the expression of
transfected with equimolar amounts of the pUC-18 or pX3 anti-apoptotic genes is expected to promote the replication of
plasmid DNAs respectively, and then infected with HaSNPV viruses and increase the yield of virus progeny (Teodoro &
at an m.o.i. of 5 at 24 h after transfection (data not shown). Branton, 1997 ; Miller, 1997). It had been shown that early
The results showed that p35 products from plasmids pUC- expression of P35 at a low level is sufficient to block apoptosis,
p35EPO (Fig. 2 a) or pX3-p35EPO (data not shown) could while late expression of P35 is required to maintain wild-type
partially prevent HaSNPV-induced apoptosis of Hi5 cells. At virus gene expression and facilitate virus replication
24 h p.i., no apparent apoptosis was observed in cells (Hershberger et al., 1992, 1994). Thus, P35 acts as a host range
transfected with pUC-p35EPO or pX3-p35EPO. From 48 to determinant by suppressing the ability of the infected cells to
72 h p.i., only a few cells transfected with pUC-p35EPO or undergo apoptosis. However, it had been reported that P35
pX3-p35EPO showed apoptosis. In the controls, apoptosis may not be the only host range determinant in the
appeared at 24 h p.i. and progressed to 24–48 h p.i., with a AcMNPV–S. littoralis (SL2) cell system, since it inhibits
peak of apoptotic mortality (approx. 60 % of cells) at 48 h p.i. AcMNPV-induced apoptosis of SL2 cells but does not boost
To determine whether the p35 product from pUC-p35EPO the yield of budded AcMNPV (Gershburg et al., 1997). In the
or pX3-p35EPO could facilitate HaSNPV replication in Hi5 present study, our data also showed that expression of P35
cells, the supernatant from the cells transfected with the could partially inhibit HaSNPV-induced apoptosis in Hi5 cells
plasmids and infected with HaSNPV was collected and but does not facilitate HaSNPV replication.
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Coinfection of Hi5 cells with HaSNPV and TnMNPV- promotor elements mediating early transcription from the 35,000-
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35- and 94-kilodalton protein genes encoded by the HindIII K genomic
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TnMNPV-SVI−G were produced. We tried hard but eventually virus. Journal of Virology 61, 2264–2272.
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HaSNPV and pX3-p35EPO, which contains the flanking Autographa californica nuclear polyhedrosis virus apoptotic suppressor
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