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Viral Apoptotic Mimicry Is an Immune Evasion Viral Apoptotic Mimicry Mechanism Used by Hepatitis B Virus (HBV)

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Viral Apoptotic Mimicry Is an Immune Evasion Viral Apoptotic Mimicry Mechanism Used by Hepatitis B Virus (HBV) PROGRESS (REF. 13), when they hypothesized that viral apoptotic mimicry is an immune evasion Viral apoptotic mimicry mechanism used by hepatitis B virus (HBV). The premise being that during chronic HBV Ali Amara and Jason Mercer infection, large-scale production of non- infectious subviral particles, composed of Abstract | As opportunistic pathogens, viruses have evolved many elegant phosphatidylserine-rich host membranes strategies to manipulate host cells for infectious entry and replication. Viral and viral membrane proteins, would be able apoptotic mimicry, defined by the exposure of phosphatidylserine — a marker for to suppress adaptive immunity through apoptosis — on the pathogen surface, is emerging as a common theme used by interactions between phosphatidylserine and cellular apoptotic clearance receptors. enveloped viruses to promote infection. Focusing on the four best described Since Vanlandschoot and Leroux-Roels’ examples (vaccinia virus, dengue virus, Ebola virus and pseudotyped lentivirus), we prediction more than a decade ago, viral summarize our current understanding of apoptotic mimicry as a mechanism for apoptotic mimicry has been experimentally virus entry, binding and immune evasion. We also describe recent examples of confirmed for several enveloped viruses. non-enveloped viruses that use this mimicry strategy, and discuss future directions These include alphaviruses, flaviviruses, filo- viruses, some arenaviruses, baculoviruses, and how viral apoptotic mimicry could be targeted therapeutically. poxviruses and rhabdoviruses14–21 (TABLE 1). By containing phosphatidylserine within Through millions of years of coexistence of an anti-inflammatory response. The their membranes, these viruses effectively with their hosts, viruses have evolved to externalization of phosphatidylserine on mimic apoptotic cells, thereby subverting exploit the essential functions of the cells apoptotic cells was recently shown to depend apoptotic clearance mechanisms to facilitate that they invade, such as endocytosis, on caspase-mediated cleavage of the phos- virus entry or infection. For many viruses secretion, cell division and apoptosis. Viral pholipid flippase ATP11C5. When external- that use apoptotic mimicry, their cellular pathogens use many mechanisms to evade ized, phosphatidylserine can be recognized phosphatidylserine receptors have been or subvert apoptosis, including inactivation by subsets of receptors on the surface of identified, and the role of this strategy in of apoptotic sensors, molecular mimicry of both professional and non-professional virus infection has been characterized apoptotic regulators and perturbation of phagocytes (reviewed in REF. 6). These spe- (reviewed in REF. 22). caspase cleavage (reviewed in REF. 1). It was cialized receptors perform two functions: Interestingly, accumulating evidence sug- recently shown that viruses also hijack apop- they trigger the signalling cascades and gests that apoptotic mimicry can facilitate totic recognition and clearance mechanisms actin rearrangements that are required for infection by several different mechanisms. In for their own means. By eliminating abnor- the endocytic engulfment, trafficking and this Progress article, we discuss recent stud- mal or harmful cells, dampening immune degradation of apoptotic debris, and they ies indicating that viral apoptotic mimicry responses and assuring normal tissue and concomitantly initiate the production of promotes virus entry, enhances virus bind- organ formation during development, the anti-inflammatory cytokines while suppres­ ing to host cells or dampens host immune clearance of apoptotic cells serves an essen- sing the transcription of pro-inflammatory responses, depending on the virus and the tial function in all multicellular organisms cytokines7–9 (BOX 1). phosphatidylserine receptor or receptors that (reviewed in REF. 2). Not surprisingly, this Given these properties, it is easy to envi- are engaged. Recent findings suggest that process is highly conserved and, importantly, sion why a virus would evolve to use a strat- both enveloped and non-enveloped viruses actively anti-inflammatory3. egy of apoptotic mimicry. By masquerading can use this strategy, so we introduce the To distinguish dead and dying cells as apoptotic debris, viruses could directly terms classic and non-classic apoptotic from their healthy counterparts, phosphati- engage the apoptotic clearance machinery. mimicry, respectively. Focusing on the dylserine, which is a negatively charged This would in turn trigger uptake by endo- best described examples to date, we review phospholipid, is exposed on the external cytosis and simultaneously dampen the host phosphatidylserine-mediated entry of vac- leaflet of the plasma membrane as a hall- immune response. As many (perhaps all) cinia virus (VACV), Ebola virus (EBOV) mark of programmed cell death4. There cell types are capable of clearing apoptotic and dengue virus (DENV), phosphatidyl- are five key steps involved in the clearance cells10–12, an apoptotic mimicry strategy serine-enhanced binding of lentivirus vec- of apoptotic debris: phosphatidylserine may enable a virus to expand its cell type tors and the dampening of innate immune exposure on the apoptotic cell; engage- tropism without the need to encode specific responses by phosphatidylserine-containing ment of phosphatidylserine receptors on receptor-binding proteins. The idea that pseudotyped lentiviral particles. We also a phagocyte; endocytic engulfment of the viruses might subvert cellular apoptotic discuss how a non-enveloped virus, simian apoptotic cell; intracellular trafficking of the clearance machinery was first proposed by virus 40 (SV40), engages phosphatidylser- phagosome for degradation; and induction Vanlandschoot and Leroux-Roels in 2003 ine receptors for internalization. As all of NATURE REVIEWS | MICROBIOLOGY VOLUME 13 | AUGUST 2015 | 461 © 2015 Macmillan Publishers Limited. All rights reserved PROGRESS Box 1 | Apoptotic clearance obtain a phosphatidylserine-rich membrane. Several enveloped viruses that use apoptotic In a healthy adult, approximately 50 billion cells undergo apoptosis on a daily basis69. Given these mimicry, such as EBOV and Marburg virus vast numbers, it is not surprising that defects in the clearance of apoptotic cells can result in (MARV), have been suggested to bud from various diseases. The major hallmark of apoptosis is exposure of phosphatidylserine on the cell plasma membrane microdomains called surface70. This negatively charged phospholipid is found on the inner leaflet of the plasma membrane in healthy cells26, but during apoptosis, phosphatidylserine is exposed on the external lipid rafts, which are highly enriched for 29,30 leaflet of the plasma membrane. This change in phosphatidylserine localization is mediated by the phosphatidylserine in the external leaflet . inactivation of lipid flippases in combination with activation of calcium-dependent phospholipid Infection by many viruses triggers apoptosis scramblases. of the target cell; thus, it is likely that these Clearance of apoptotic cells is initiated when these phosphatidylserine-enriched membranes viruses acquire phosphatidylserine by bud- engage phosphatidylserine receptors. Two types of phosphatidylserine receptor have been ding from the surface of apoptotic cells, described: those that bind the phospholipid directly and those that use bridging molecules to as has been suggested for the arenavirus associate with it. Direct phosphatidylserine-binding receptors include T cell immunoglobulin and Pichinde virus (PICV)31. In lieu of inducing mucin receptor (TIM) proteins (TIM1, TIM3 and TIM4); the CD300 family members CD300a and apoptosis, cell surface phosphatidylserine CD300f (also known as CLM1); and the seven-transmembrane spanning receptors brain-specific exposure may be the consequence of a virus- angiogenesis inhibitor 1 (BAI1), stabilin 1 and receptor for advanced glycosylation end products induced increase in intracellular calcium (RAGE) (reviewed in REFS 2,71,72). The phosphatidylserine-bridging molecule MFGE8 is used for 32 apoptotic clearance through αvβ3 and αvβ5 integrins73, which are indirect phosphatidylserine concentrations . This rise in calcium levels receptors. Similarly, GAS6 and protein S (PROS) are the bridging molecules that link the indirect can inactivate lipid flippases — proteins phosphatidylserine receptors of the tyrosine protein kinase receptor 3 (TYRO3)–AXL–MER (TAM) that translocate phospholipids between family to phosphatidylserine to mediate apoptotic clearance72. membrane leaflets and thus maintain phos- The mechanism used for the engulfment of apoptotic cells by phagocytes most closely resembles phatidylserine asymmetry — and result in macropinocytosis74. This endocytic mechanism is largely actin driven and regulated by the RHO phosphatidylserine externalization33. It is GTPases RAC1 and CDC42 (REF. 75). Hallmarks of macropinocytosis include vigorous membrane likely that enveloped and non-enveloped 36 ruffling, uptake into loose-fitting fluid-filled vacuoles and bystander endocytosis . Although, the viruses alike would be able to exploit such a molecular details remain incomplete76, genetic screens in Caenorhabditis elegans have identified mechanism; however, as there is no literature components of the signalling pathways that drive RHO GTPase activation and the subsequent cytoskeletal rearrangements needed for clearance64. Once engulfment is complete, the apoptotic to support this theory, it remains
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