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Riding apoptotic bodies for cell-cell transmission by African swine fever virus
Abstract:
African swine fever virus (ASFV), a devastating pathogen to the worldwide swine industry, mainly targets macrophage/monocyte lineage, but how the virus enters host cells has remained unclear. Here, we report that ASFV utilizes apoptotic bodies (ApoBDs) for infection and cell-cell transmission. We show that ASFV induces cell apoptosis of primary porcine alveolar macrophages (PAMs) at the late stage of infection to productively shed ApoBDs that are subsequently swallowed by neighboring PAMs to initiate a secondary infection as evidenced by electron microscopy and live-cell imaging. Interestingly, the virions loaded within ApoBDs are exclusively single-enveloped particles that are devoid of the outer layer of membrane and represent a predominant form produced during late infection. The in vitro purified ApoBD vesicles are capable of mediating virus infection of naive PAMs, but the transmission can be significantly inhibited by blocking the "eat-me" signal phosphatidyserine on the surface of ApoBDs via Annexin V or the efferocytosis receptor TIM4 on the recipient PAMs via anti-TIM4 antibody, whereas overexpression of TIM4 enhances virus infection. The same treatment however did not affect the infection by intracellular viruses. Importantly, the swine sera to ASFV exert no effect on the ApoBD-mediated transmission but can partially act on the virions lacking the outer layer of membrane. Thus, ASFV has evolved to hijack a normal cellular pathway for cell-cell spread to evade host responses.
Insights
African swine fever virus (ASFV) uses apoptotic bodies for infection and spread. This mechanism helps the virus evade host immune responses, impacting the global swine industry.
Area of Science:
- Virology
- Cell Biology
- Immunology
Background:
- African swine fever virus (ASFV) causes significant losses in the global swine industry.
- ASFV primarily infects cells of the macrophage/monocyte lineage.
- The mechanism of ASFV entry into host cells was previously unclear.
Purpose of the Study:
- To elucidate the mechanism of ASFV entry and cell-cell transmission.
- To investigate the role of apoptotic bodies in ASFV infection.
- To understand how ASFV evades host immune responses.
Main Methods:
- Electron microscopy and live-cell imaging to observe ASFV infection and transmission.
- In vitro purification of ASFV-loaded apoptotic bodies.
- Inhibition assays using Annexin V and anti-TIM4 antibodies.
- Overexpression studies of the efferocytosis receptor TIM4.
Main Results:
- ASFV induces apoptosis in primary porcine alveolar macrophages (PAMs), leading to the shedding of apoptotic bodies (ApoBDs).
- These ASFV-laden ApoBDs are single-enveloped particles and are engulfed by neighboring PAMs, initiating secondary infections.
- Blocking phosphatidylserine on ApoBDs or the TIM4 receptor on recipient cells inhibits ASFV transmission via ApoBDs.
- ASFV ApoBD-mediated transmission is not affected by swine sera, suggesting a mechanism for immune evasion.
Conclusions:
- ASFV utilizes apoptotic bodies for efficient cell-cell transmission.
- This strategy allows ASFV to evade host immune responses, particularly antibody-mediated neutralization.
- Understanding this pathway is crucial for developing effective control strategies against ASFV.
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