Cholesterol-rich Lipid Rafts Are Required for Release of Infectious Human Respiratory Syncytial Virus Particles

Overview

Journal Virology

Specialty Microbiology

Date 2011 Nov 18

PMID 22088217

Citations 35

Authors

Te-Hung Chang

Jesus Segovia

Ahmed Sabbah

Victoria Mgbemena

Santanu Bose

Affiliations

Soon will be listed here.

Abstract

Cholesterol and sphingolipid enriched lipid raft micro-domains in the plasma membrane play an important role in the life-cycle of numerous enveloped viruses. Although human respiratory syncytial virus (RSV) proteins associate with the raft domains of infected cells and rafts are incorporated in RSV virion particles, the functional role of raft during RSV infection was unknown. In the current study we have identified rafts as an essential component of host cell that is required for RSV infection. Treatment of human lung epithelial cells with raft disrupting agent methyl-beta-cyclodextrin (MBCD) led to drastic loss of RSV infectivity due to diminished release of infectious progeny RSV virion particles from raft disrupted cells. RSV infection of raft deficient Niemann-Pick syndrome type C human fibroblasts and normal human embryonic lung fibroblasts revealed that during productive RSV infection, raft is required for release of infectious RSV particles.

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References

Brown G, Jeffree C, McDonald T, McL Rixon H, Aitken J, Sugrue R . Analysis of the interaction between respiratory syncytial virus and lipid-rafts in Hep2 cells during infection. Virology. 2004; 327(2):175-85. DOI: 10.1016/j.virol.2004.06.038. View

McDonald T, Pitt A, Brown G, McL Rixon H, Sugrue R . Evidence that the respiratory syncytial virus polymerase complex associates with lipid rafts in virus-infected cells: a proteomic analysis. Virology. 2004; 330(1):147-57. DOI: 10.1016/j.virol.2004.09.034. View

Laliberte J, McGinnes L, Peeples M, Morrison T . Integrity of membrane lipid rafts is necessary for the ordered assembly and release of infectious Newcastle disease virus particles. J Virol. 2006; 80(21):10652-62. PMC: 1641742. DOI: 10.1128/JVI.01183-06. View

Silvius J . Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim Biophys Acta. 2003; 1610(2):174-83. DOI: 10.1016/s0005-2736(03)00016-6. View

Ali A, Nayak D . Assembly of Sendai virus: M protein interacts with F and HN proteins and with the cytoplasmic tail and transmembrane domain of F protein. Virology. 2000; 276(2):289-303. DOI: 10.1006/viro.2000.0556. View

Gower T, Graham B . Antiviral activity of lovastatin against respiratory syncytial virus in vivo and in vitro. Antimicrob Agents Chemother. 2001; 45(4):1231-7. PMC: 90448. DOI: 10.1128/AAC.45.4.1231-1237.2001. View

Fleming E, Kolokoltsov A, Davey R, Nichols J, Roberts Jr N . Respiratory syncytial virus F envelope protein associates with lipid rafts without a requirement for other virus proteins. J Virol. 2006; 80(24):12160-70. PMC: 1676292. DOI: 10.1128/JVI.00643-06. View

Henderson L, Lin L, Prasad A, Paul C, Chang T, Maue R . Embryonic striatal neurons from niemann-pick type C mice exhibit defects in cholesterol metabolism and neurotrophin responsiveness. J Biol Chem. 2000; 275(26):20179-87. DOI: 10.1074/jbc.M001793200. View

Bose S, Malur A, Banerjee A . Polarity of human parainfluenza virus type 3 infection in polarized human lung epithelial A549 cells: role of microfilament and microtubule. J Virol. 2001; 75(4):1984-9. PMC: 115145. DOI: 10.1128/JVI.75.4.1984-1989.2001. View

10.

Sabbah A, Chang T, Harnack R, Frohlich V, Tominaga K, Dube P . Activation of innate immune antiviral responses by Nod2. Nat Immunol. 2009; 10(10):1073-80. PMC: 2752345. DOI: 10.1038/ni.1782. View

11.

Harder T, Scheiffele P, Verkade P, Simons K . Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol. 1998; 141(4):929-42. PMC: 2132776. DOI: 10.1083/jcb.141.4.929. View

12.

Leser G, Lamb R . Influenza virus assembly and budding in raft-derived microdomains: a quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology. 2005; 342(2):215-27. DOI: 10.1016/j.virol.2005.09.049. View

13.

Ning Y, Buranda T, Hudson L . Activated epidermal growth factor receptor induces integrin alpha2 internalization via caveolae/raft-dependent endocytic pathway. J Biol Chem. 2006; 282(9):6380-7. DOI: 10.1074/jbc.M610915200. View

14.

Chu B, Ge L, Xie C, Zhao Y, Miao H, Wang J . Requirement of myosin Vb.Rab11a.Rab11-FIP2 complex in cholesterol-regulated translocation of NPC1L1 to the cell surface. J Biol Chem. 2009; 284(33):22481-22490. PMC: 2755969. DOI: 10.1074/jbc.M109.034355. View

15.

Gower T, Pastey M, Peeples M, Collins P, McCurdy L, Hart T . RhoA signaling is required for respiratory syncytial virus-induced syncytium formation and filamentous virion morphology. J Virol. 2005; 79(9):5326-36. PMC: 1082718. DOI: 10.1128/JVI.79.9.5326-5336.2005. View

16.

Avota E, Muller N, Klett M, Schneider-Schaulies S . Measles virus interacts with and alters signal transduction in T-cell lipid rafts. J Virol. 2004; 78(17):9552-9. PMC: 506914. DOI: 10.1128/JVI.78.17.9552-9559.2004. View

17.

Sun X, Whittaker G . Role for influenza virus envelope cholesterol in virus entry and infection. J Virol. 2003; 77(23):12543-51. PMC: 262566. DOI: 10.1128/jvi.77.23.12543-12551.2003. View

18.

Brown G, McL Rixon H, Sugrue R . Respiratory syncytial virus assembly occurs in GM1-rich regions of the host-cell membrane and alters the cellular distribution of tyrosine phosphorylated caveolin-1. J Gen Virol. 2002; 83(Pt 8):1841-1850. DOI: 10.1099/0022-1317-83-8-1841. View

19.

Pastey M, Gower T, Spearman P, Crowe Jr J, Graham B . A RhoA-derived peptide inhibits syncytium formation induced by respiratory syncytial virus and parainfluenza virus type 3. Nat Med. 1999; 6(1):35-40. PMC: 7095870. DOI: 10.1038/71503. View

20.

Robinzon S, Dafa-Berger A, Dyer M, Paeper B, Proll S, Teal T . Impaired cholesterol biosynthesis in a neuronal cell line persistently infected with measles virus. J Virol. 2009; 83(11):5495-504. PMC: 2681928. DOI: 10.1128/JVI.01880-08. View