Hijacking of the Ubiquitin/Proteasome Pathway by the HIV Auxiliary Proteins
Abstract
:1. Introduction
2. The Ubiquitin-Proteasome System
- (1)
- Some cellular E3 ubiquitin ligases recognize viral proteins and induce their ubiquitination, which can have a positive effect on viral replication. For instance, ubiquitination of the p6 domain of the HIV-1 Gag polyprotein is important for the interaction of p6 with the ESCRT machinery. However, the mono-ubiquitination of lysine residues within the p6 domain (K27 and K33) does not seem to be sufficient to facilitate budding of new virions, the latter being also dependent on the cumulative ubiquitination of NC-p2 (NucleoCapsid-peptide 2) domain [21,22,23,24]. Ubiquitination of the HIV-1 accessory protein Tat by cellular E3 ligases stimulates transcription of viral RNA [25,26].
- (2)
- Ubiquitination of viral proteins can also induce their degradation, thereby blocking the viral life cycle. This is a strategy used by certain restriction factors. The polymerase PB1 (Protein Binding 1) of the Influenza A virus (IAV) for example is ubiquitinated (K48-linked ubiquitin) by the cellular E3 ubiquitin ligase TRIM32 (TRIpartite Motif-containing protein 32), followed by its degradation by the proteasome [27]. This seems to be a general mechanism as PB1 proteins derived from various IAV serotypes (H1N1 (Hemagglutinin 1 Neuraminidase 1), H3N2, H5N1 or H7N9) associate with TRIM32 in multiple cell types and this suggests that PB1 has not yet adapted to avoid TRIM32 targeting [28]. The Human herpesvirus type I (HSV-1) capsid protein Vp5 has also been shown to be degraded by the ubiquitin proteasome system, leaving the viral genome exposed to innate immune sensors [29]. Interestingly, TRIM5α was reported to inhibit HSV-1 and -2 replication at an early stage of the infection cycle [30], suggesting a role for this or related protein in cytosolic sensing of herpesvirus capsids.
- (3)
- Certain viruses have evolved to recruit the cellular E3 ligases to induce the degradation of cellular proteins that might have harmful effects on the viral life cycle. For instance, the protein E6 of Human papillomavirus (HPV) recruits the cellular E3 ubiquitin ligase E6-AP to induce ubiquitination and degradation of p53, thereby allowing viral replication [31,32]. The NSP1 (Non-Structural RNA binding protein 1) protein of Rotaviruses subverts the Skp1-Cul1-Fbox (SCF) E3 ligase to induce the ubiquitination and degradation of β-TrCP (β-Transducin repeat Containing Protein). β-TrCP is by itself a substrate adaptor of an E3 ligase and its degradation leads to accumulation of the NF-ϰB inhibitor IϰB, resulting in inhibition of the NF-ϰB induced antiviral responses [33,34]. These mechanisms are important for HIV replication and will be detailed in Section 5.
- (4)
- Other viruses directly encode their own E3 ligases. Kaposi sarcoma herpesvirus (KSHV) protein K3 and K5 (RING-CH family of ligases) ubiquitinate MHC-I (Major Histocompatibility Complex I), resulting in its down-regulation from the cell surface through a clathrin-dependent sorting pathway to an endolysosomal compartment [35,36]. This endolysosomal sorting requires K63-linked instead of K48-linked polyubiquitin chains [19]. Another well-known example is the ICP0 protein (Infected Cell Protein 0) of HSV-1, an E3 ubiquitin ligase which induces the degradation of the ND10 (Nuclear Domain 10) nuclear body components PML (Promyelocytic Leukemia Protein) and Sp100 through the UPS, thereby avoiding antiviral sensing [37,38]. ICP0 has also been shown to have a RING-independent E3 ligase activity that polyubiquitinates the E2 enzyme cdc34. ICP0 influences many cellular pathways and is required for the activation of most viral and many cellular genes, for reactivation from latency and suppression of innate immunity [19].
- (5)
- Finally, ubiquitin modifications can be reversed by the isopeptide-bond specific proteolytic activity of DUBs. In addition to cellular DUBs, it has been reported that various virus families code their own DUBs (Coronavirus, Herpesvirus etc.) to evade host antiviral immune response and promote virus replication (for a recent review see [1]). For instance, in the herpesviridae family, a variety of DUBs play an important role in the virus life cycle (e.g., UL36USP (Ubiquitin Ligase 36 Ubiquitin Specific Protease) of HSV-1, tegument protein pUL48 of human cytomegalovirus (HCMV)). Regarding HIV-1, a recent study reported that several cellular DUBs (USP7 and USP47, Ubiquitin Specific Protease family) play an important role in its replication by regulating Gag processing and thus the infectivity of released virions and simultaneously the entry of Gag into the UPS and MHC-I pathway [39]. Moreover, this study showed that treatment with DUB inhibitors targeting USP47 causes a general Gag processing defect, indicating that USP47 interacts with Gag and prevents its entry into the UPS. Similarly, proteasome inhibitors have been shown to impact HIV-1 replication by reducing the release and maturation of infectious particles [40,41] or by suppressing its transcription [42]. Taken together, these studies suggest a potential antiretroviral activity of DUB and proteasome inhibitors.
3. The HIV Life Cycle
4. Cellular Factors Mediating Viral Restriction Using the UPS
4.1. TRIM5α
4.2. March8
5. Counteraction of Restriction Factors by Viral Auxiliary Proteins Using the UPS
5.1. Vif
5.2. Vpx
5.3. Vpu
6. Other Cellular Proteins Targeted by the Hijacked UPS
7. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Seissler, T.; Marquet, R.; Paillart, J.-C. Hijacking of the Ubiquitin/Proteasome Pathway by the HIV Auxiliary Proteins. Viruses 2017, 9, 322. https://doi.org/10.3390/v9110322
Seissler T, Marquet R, Paillart J-C. Hijacking of the Ubiquitin/Proteasome Pathway by the HIV Auxiliary Proteins. Viruses. 2017; 9(11):322. https://doi.org/10.3390/v9110322
Chicago/Turabian StyleSeissler, Tanja, Roland Marquet, and Jean-Christophe Paillart. 2017. "Hijacking of the Ubiquitin/Proteasome Pathway by the HIV Auxiliary Proteins" Viruses 9, no. 11: 322. https://doi.org/10.3390/v9110322