Investigation of the role of the ubiquitin proteasome pathway in dengue virus life cycle 4

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Chapter 4: Discussion
4.1 Preface

Egress from the infected cell is perhaps one of the most ill defined parts of the DENV
life cycle. Previous work has demonstrated that this process occurs through
exocytosis and is hence dependent on expression of the exocyst complex (Chen et al,
2011). This thesis clarifies that the expression of the exocyst complex is regulated at
the translational level, at least in part, by the UPR (Figure 4-1). To ensure successful
completion of its life cycle, DENV relies on the proteasome or increased expression
of components of the UPP to alleviate ER stress, the inhibition of which leads to the
decoupling of infectious virus production from RNA replication.













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Figure 4-1. Schematic diagram of findings. 1. Proteasome inhibitors prevent
polyubiquitylated misfolded proteins to be degraded by the proteasome. 2-3.
Accumulation of misfolded proteins stresses the cell and activates the PERK
pathway. 4. Activation of this pathway phosphorylates eIF2α. 5. Translational
attenuation occurs and results in decreased levels of TC10 and EXOC7. 6. Dengue
egress is inhibited due to the reduction in protein levels of these host factors
necessary for virus egress.
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4.2 Unfolded protein response during flavivirus infection

The ER is an extensive membranous network that serves different specialized
functions, such as intracellular signal transduction and calcium storage. In addition,
most secreted and transmembrane proteins enter the lumen of the ER prior to being
secreted for maturation. To maintain homeostasis in the ER, the ER has evolved three
mechanistically distinct pathways collectively called the UPR.

Under ER stress, ER chaperone immunoglobulin heavy chain binding protein (BiP),
plays a central role in the activation of PERK, activating transcription factor 6 (ATF-
6) and the ER transmembrane protein kinase/endoribonuclease (IRE-1) pathways
(Ron & Walter, 2007; Schroder & Kaufman, 2005; Shen & Prywes, 2005). PERK is
an ER-localized type I transmembrane protein and the PERK pathway functions as a

first-response mechanism induced by various stressors and attenuates global protein
synthesis via phosphorylation of eIF2α (Wek et al, 2006).

PERK activation also induces the activation of C/EBP homologous protein (CHOP)
and growth arrest and DNA damage-inducible protein (GADD34). In the case of
sustained ER stress, CHOP is responsible for apoptosis of the cells. Alternatively,
CHOP can also function as a pro-survival transcription factor leading to induction of
GADD34, a subunit of protein phosphatase 1c (PP1c) that targets the
dephosphorylation of phosphorylated eIF2α (eIF2α-P) (Rutkowski et al, 2006).
Failure to suppress ER stress leads to activation of the ATF6 and IRE1 pathways,
which act to alleviate the accumulation of misfolded proteins by up-regulating host
factors that increase the capacity of the ER to handle the synthesis of nascent proteins
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(Ron & Walter, 2007).

The life cycle of DENV and other members of the Flaviviridae family depend heavily
on the host ER to translate, replicate, and package their genome (Lindenbach et al,
2007). If ER stress hampers the completion of its life cycle, DENV must thus be able
to modulate the ER stress response to survive. Indeed, several studies have shown that
DENV infection modulates the ER stress response in a time-dependent manner
(Paradkar et al, 2011; Pena & Harris, 2011; Umareddy et al, 2007) (Yu et al, 2006).
Early DENV2 infection has been shown to trigger and then suppress PERK-mediated
eIF2α phosphorylation, and the IRE1 and ATF6 pathways were then activated in the
later stages of infection (Pena & Harris, 2011). Consequently, inhibition of the
proteasome could induce additional UPR that then overcomes the ability of DENV to
regulate ER stress. Critically, inducing ER stress with an agonist without inhibiting
proteasome function recapitulated the observed down-regulation of EXOC7 and TC10
protein levels along with the decoupling of infectious virus production from viral

RNA replication. Supporting our data, salubrinal, a drug that inhibits eIF2α
dephosphorylation, thereby increasing phosphorylated eIF2α levels was previously
shown to reduce the production of infectious viruses (Umareddy et al, 2007).

The activation of individual branches and components of the UPR by other members
of the Flaviviridae family have also been reported. Studies with hepatitis C virus have
demonstrated activation and suppression of the PERK pathway in a time-dependent
manner (Pavio et al, 2003). Also, infection with Japanese encephalitis virus was
shown to induce the IRE pathway, protecting cells from virus-induced cytopathic
effects (Yu et al, 2006), whereas WNV induction of the UPR was shown to lead to
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CHOP-mediated apoptosis (Medigeshi et al, 2007). Taken together, these studies
suggest that flaviviruses have evolved to manipulate the UPR, rendering the UPR as a
potential anti-viral host target. However, no therapeutic that specifically targets the
three sensors of the unfolded protein response, has been licensed, likely due to the
cellular toxicity it may cause.

4.3 Repurposing proteasome inhibitors as an anti-flaviviral therapeutic

On the other hand, proteasome inhibitors are currently indicated in the treatment of
certain hematological malignancies. The much greater sensitivity of myeloma cell
lines and mantle cell lines to proteasome inhibition compared with normal peripheral
blood mononuclear cells is poorly understood. The UPP plays a critical role in
regulating ER stress to enable DENV to complete its life cycle by egressing cells
through exocytosis. Perturbing this pathway is utilized by the Ae. aegypti midgut to
inhibit continued infectious DENV production without harm to itself and this same
approach could potentially be exploited as a therapeutic strategy in dengue.

Indeed, the potency of proteasome inhibition as an anti-dengue strategy is suggested
by the low nanomolar EC
50
of bortezomib, one of the first FDA-approved proteasome
inhibitor, in DENV-infected primary monocytes. Similarly, bortezomib treatment in
an immunocompetent mouse model was able to reduce plasma leakage, the degree of
thrombocytopenia as well as the pro-inflammatory responses. At a mechanistic level,
we have demonstrated that proteasome inhibition could inhibit virus egress and hence
spread within mammals. With a good understanding of its antiviral action, the
potential of bortezomib or other proteasome inhibitors to serve as an anti-dengue or
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even anti-flaviviral therapy will need to be explored in clinical safety and efficacy
trials. Indeed, a known side effect of bortezomib is thrombocytopenia although this is
only observed in multiple myeloma patients after weeks of continuous treatment. As
treatment for dengue would not exceed a week, the side effects observed only after
prolonged therapy may not be clinically relevant for dengue. Therefore, it is also
unlikely that bortezomib would exacerbate the situation in patients who present with
the symptoms of thrombocytopenia.!One limitation, however, is that bortezomib is
given subcutaneously or intravenously to patients. This is not ideal for any anti-
dengue therapeutics, as injections are not recommended for dengue patients having
the tendency to bleed. Opportunely, this problem can be circumvented by the recent
introduction of ixazomib, the first oral proteasome inhibitor that is currently
undergoing Phase 3 clinical studies (Moreau, 2014). Table 4-1 lists the current
development of various proteasome inhibitors undergoing different phases of clinical
trials.

While we have demonstrated the inhibition of virus egress as the antiviral mechanism
effected by proteasome inhibition, it is interesting that proteasome inhibitors may

have other modes of antiviral action. The UPP has also been shown to be critical for
the life cycle of Nipah virus. Inhibition of the proteasome led to impaired nuclear
export of the viral matrix protein to the cytoplasm (Wang et al, 2010). Studies on
retroviruses have also demonstrated that disruption of the proteasome function
depletes the free ubiquitin pool (Mimnaugh et al, 1997), which is necessary for the
ubiquitylation of late domain on Gag protein for proper viral budding (Patnaik et al,
2000; Schubert et al, 2000). While such mechanisms could contribute to our observed
inhibition of DENV replication, our findings suggest another complementary
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mechanism that impairs flaviviral life cycle. Altogether, proteasome inhibition could
be a broad spectrum antiviral approach against viruses that egress cells via exocytosis
or which requires ubiquitylation to regulate the functions of specific viral proteins.

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Drug!
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Table 4-1 Current developments of proteasome inhibitors undergoing different
phases of clinical trials.
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4.4 Learning from Ae. aegypti mosquito

Unlike infection in humans, dengue infection in mosquitoes is nonpathogenic. It is
interesting that the mosquito midgut down-regulates several components of the UPP
naturally to inhibit persistent infectious DENV production. One explanation may be
transcriptomic changes in the mosquito midgut upon ingestion of a bloodmeal or

during its gonotrophic cycle. Both UBE2A and DDB1 act upstream of the proteasome
in the UPP; the former belonging to the E2 ubiquitin-conjugating enzyme family
(Jentsch et al, 1987), and the latter functioning as an adaptor molecule for the cullin 4-
ubiquitin E3 ligase complex (Higa et al, 2006). UBE2A targets several short-lived
regulatory proteins for polyubiquitylation and subsequent turnover by the 26S
proteasome (Jentsch et al, 1987). DDB1 has been shown to facilitate the
ubiquitination and subsequent proteasome-mediated degradation of STATs for the
Rubulavirus genus of Paramyxoviridae (Precious et al, 2005; Ulane et al, 2005).

Our findings are concordant with previous studies in female mosquitoes where
various UPP-specific genes such as TSG101 (AAEL012515), NEDD4 (AAEL002536)
and SCF ubiquitin ligase (AAEL004691) have also been identified as critical host
factors for DENV replication (Guo et al, 2010; Mairiang et al, 2013; Sim &
Dimopoulos, 2010). Due to genetic variability across various mosquito strains and
DENV-2 strains, as well as variation in the methodology of the experiments such as
data analysis and time-points used, it is unsurprising that the UPP-specific genes
detected in these studies were not the same individual genes. As these molecules
function to signal for the activation of the effector of the UPP, the proteasome, we
reasoned that DENV is dependent on the pathway rather than signaling intermediates
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for successful completion of its life cycle. Down-regulation of several genes in the
UPP, along with the midgut barrier (Gomez-Machorro et al, 2004), forms a major part
of the mosquito’s response that restricts DENV infection. Multiple quantitative trait
loci have been associated with the midgut barrier, but the operating mechanisms of
specific genes involved remain to be fully determined (Black et al, 2002). Mosquito
genes and physiological pathways related to innate immunity, redox activity, fat,
protein and carbohydrate production and metabolism were found to be modulated in
response to DENV infection (Behura et al, 2011; Tchankouo-Nguetcheu et al, 2010).

These observations come from multiple studies of specific mosquito tissues and time
points following infection, and used different combinations of Ae. aegypti strains and
DENV-2 strains. It will be interesting to analyze the RNAseq data on the mosquito
midgut transcriptome during DENV infection and compare these results with existing
data available. Studying how these responses limit DENV infection without any
apparent harm to the mosquito (Fragkoudis et al, 2009), which contrast with the
human host response to DENV that is intimately linked with dengue pathogenesis
(Whitehorn & Simmons, 2011), offers a hitherto unexplored opportunity for
therapeutic discovery.

4.5 Beyond the anti-viral effects of bortezomib: Potential use as an adjuvant

In the scope of this thesis, we show that bortezomib inhibited virus egress and
induced apoptosis in primary monocytes. This raises the possibility that DENV
‘trapped’ in the cells could firstly, increase MHC presentation of viral antigens in
infected cells and secondly, allow cross-presentation of viral antigen via apoptotic
cells. The former is unlikely because bortezomib was demonstrated to down-regulate
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cell surface HLA (human leukocyte antigen) class I expression of monocytes (Shi et
al, 2008). Preliminary results from our studies suggest that although inflammatory
responses were reduced in bortezomib-treated mice, IFNγ levels were increased
instead. This is suggestive of elevated T cell and NK (natural killer) cell activity and
future work could be performed to examine if bortezomib could indeed induce NK
cells, T cells and antibody responses against DENV in immunocompetent mice. If this
possibility is true, it is plausible to use bortezomib as an adjuvant to raise adaptive
immunity when co-injected with partially attenuated DENV. The antiviral action of
bortezomib will limit the number of cycles of infection in the host while enhancing
the acquired immune response against DENV.

4.6 Conclusion

In conclusion, the UPP plays a critical role in regulating ER stress to enable DENV to
complete its life cycle by egressing cells through exocytosis. Perturbing this pathway
is utilised by the Aedes aegypti midgut to inhibit continued infectious DENV
production without harm to itself and this same approach could potentially be
exploited as a therapeutic strategy in dengue.
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References

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