Repulsion of Superinfecting Virions: A Mechanism for Rapid Virus Spread

Science  12 Feb 2010:
Vol. 327, Issue 5967, pp. 873-876
DOI: 10.1126/science.1183173

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Viral Superspreaders

Viruses are thought to spread across a lawn of cells by an iterative process of infection, replication, and release. If this were the case, the rate of spread would be limited by the viral replication kinetics. Now, Doceul et al. (p. 873, published online 21 January; see the Perspective by Pickup) describe a spreading mechanism used by vaccinia virus that is not restricted by viral replication kinetics and that causes a dramatic acceleration of spread. Early after infection, vaccinia virus proteins A33 and A36 are expressed as a complex on the cell surface. This marks the cell as infected and causes superinfecting virions to be repelled by the formation of actin projections beneath the virus particle. Virions are repelled from infected cells repeatedly until an uninfected cell is reached and are thus pushed further away from the origin of infection to accelerate dissemination.


Viruses are thought to spread across susceptible cells through an iterative process of infection, replication, and release, so that the rate of spread is limited by replication kinetics. Here, we show that vaccinia virus spreads across one cell every 75 minutes, fourfold faster than its replication cycle would permit. To explain this phenomenon, we found that newly infected cells express two surface proteins that mark cells as infected and, via exploitation of cellular machinery, induce the repulsion of superinfecting virions away toward uninfected cells. Mechanistically, early expression of proteins A33 and A36 was critical for virion repulsion and rapid spread, and cells expressing these proteins repelled exogenous virions rapidly. Additional spreading mechanisms may exist for other viruses that also spread faster than predicted by replication kinetics.

  • * These authors contributed equally to this work.

  • Present address: Radboud University Nijmegen, Nijmegen Centre for Molecular Life Sciences, 6500 HB Nijmegen, The Netherlands.

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