Subversion of the actin cytoskeleton during viral infection

Key Points

  • Actin is a ubiquitous cellular protein that forms a foundation for cellular structure and integrity. Viruses are obligate intracellular parasites with a replication cycle that requires them to engage and modify the actin cytoskeleton at all stages, from entry through replication to egress and spread.

  • Oncogenic proteins of transforming viruses interfere with the RHO-family GTPases (actin-signalling molecules) to change cellular dynamics from a quiescent to a mitotic state. The actin cytoskeleton is altered dramatically, cell shape changes, and cell-to-cell contact and matrix adhesion are lost, while podosomes and membrane ruffles appear on the cell surface.

  • Virus-mediated oncogenic transformation can result in metastatic tumours in humans, such as nasopharyngeal, hepatocellular and cervical carcinomas (induced by Epstein–Barr virus, hepatitis B virus and human papillomavirus, respectively). In vitro, viral proteins increase cell migration by disrupting and modulating actin dynamics. The host proteins involved in these interactions may be specific cytoskeletal targets for antimetastatic therapies.

  • Virions often interact with the underlying actin cytoskeleton to gain entry to the cell. Virions may move to entry sites using high-affinity interactions with receptors that are associated with actin filaments inside the cell. Movement is promoted by myosin motors that drive the actin cytoskeleton, pulling the receptor–virion complex across the plasma membrane. Virion entry by endocytic processes or formation of the fusion pore also often involves cortical actin.

  • Actin structures can be modified during viral infection to produce long cellular extensions (for example, filopodia and tunnelling nanotubes). These structures facilitate the long-distance dissemination of a wide range of viruses, including vaccinia virus, herpes simplex viruses, HIV and rotaviruses.

  • Most actin–virus interactions have been discovered in isolated or cultured cell systems. The next generation of research will apply this knowledge to viral infections in vivo to understand the role of viral subversion of the actin cytoskeleton in disease.

Abstract

Viral infection converts the normal functions of a cell to optimize viral replication and virion production. One striking observation of this conversion is the reconfiguration and reorganization of cellular actin, affecting every stage of the viral life cycle, from entry through assembly to egress. The extent and degree of cytoskeletal reorganization varies among different viral infections, suggesting the evolution of myriad viral strategies. In this Review, we describe how the interaction of viral proteins with the cell modulates the structure and function of the actin cytoskeleton to initiate, sustain and spread infections. The molecular biology of such interactions continues to engage virologists in their quest to understand viral replication and informs cell biologists about the role of the cytoskeleton in the uninfected cell.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Actin filament dynamics.
Figure 2: RHO-family GTPase-mediated modelling of the actin cytoskeleton.
Figure 3: Manifestations of actin rearrangement.
Figure 4: Models of entry.
Figure 5: Actin involvement in viral replication and egress.

References

  1. 1

    Pollard, T. D. & Cooper, J. A. Actin, a central player in cell shape and movement. Science 326, 1208–1212 (2009).

    CAS  Article  Google Scholar 

  2. 2

    Weaver, A. M., Young, M. E., Lee, W.-L. & Cooper, J. A. Integration of signals to the Arp2/3 complex. Curr. Opin. Cell Biol. 15, 23–30 (2003).

    CAS  PubMed  Article  Google Scholar 

  3. 3

    Moreau, V. et al. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nature Cell Biol. 2, 441–448 (2000).

    CAS  PubMed  Article  Google Scholar 

  4. 4

    Weisswange, I., Newsome, T. P., Schleich, S. & Way, M. The rate of N-WASP exchange limits the extent of ARP2/3-complex-dependent actin-based motility. Nature 458, 87–91 (2009).

    CAS  PubMed  Article  Google Scholar 

  5. 5

    Carlier, M.-F. et al. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136, 1307–1322 (1997).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6

    DesMarais, V., Macaluso, F., Condeelis, J. & Bailly, M. Synergistic interaction between the Arp2/3 complex and cofilin drives stimulated lamellipod extension. J. Cell Sci. 117, 3499–3510 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7

    Yamashiro, S., Yamakita, Y., Ono, S. & Matsumura, F. Fascin, an actin-bundling protein, induces membrane protrusions and increases cell motility of epithelial cells. Mol. Biol. Cell 9, 993–1006 (1998).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8

    Matsumura, F., Yamashiro-Matsumura, S. & Lin, J. J. Isolation and characterization of tropomyosin-containing microfilaments from cultured cells. J. Biol. Chem. 258, 6636–6644 (1983).

    CAS  PubMed  Google Scholar 

  9. 9

    Uruno, T. et al. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nature Cell Biol. 3, 259–266 (2001).

    CAS  PubMed  Article  Google Scholar 

  10. 10

    Schmitz, A. A., Govek, E. E., Bottner, B. & Van Aelst, L. Rho GTPases: signaling, migration, and invasion. Exp. Cell Res. 261, 1–12 (2000).

    CAS  PubMed  Article  Google Scholar 

  11. 11

    Hall, A. Rho GTPases and the actin cytoskeleton. Science 279, 509–514 (1998).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  12. 12

    Heasman, S. J. & Ridley, A. J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nature Rev. Mol. Cell Biol. 9, 690–701 (2008). A recent and extensive review on the biology of RHO-family GTPases.

    CAS  Article  Google Scholar 

  13. 13

    Gouin, E., Welch, M. D. & Cossart, P. Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8, 35–45 (2005).

    CAS  Article  Google Scholar 

  14. 14

    Münter, S., Way, M. & Frischknecht, F. Signaling during pathogen infection. Sci. STKE 2006, re5 (2006). A comprehensive review on how pathogen infection affects signalling mechanisms.

    PubMed  Google Scholar 

  15. 15

    Favoreel, H. W., Enquist, L. W. & Feierbach, B. Actin and Rho GTPases in herpesvirus biology. Trends Microbiol. 15, 426–433 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16

    Fleissner, E. & Tress, E. Chromatographic and electrophoretic analysis of viral proteins from hamster and chicken cells transformed by Rous sarcoma virus. J. Virol. 11, 250–262 (1973). The earliest work on RSV-induced cytoskeletal changes.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    McNutt, N. S., Culp, L. A. & Black, P. H. Contact-inhibited revertant cell lines isolated from SV40-transformed cells. IV. Microfilament distribution and cell shape in untransformed, transformed, and revertant Balb-c 3T3 cells. J. Cell Biol. 56, 412–428 (1973). The earliest report on SV40-induced cell transformation and morphological changes.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18

    Goldman, R. D., Chang, C. & Williams, J. F. Properties and behavior of hamster embryo cells transformed by human adenovirus type 5. Cold Spring Harb. Symp. Quant. Biol. 39, 601–614 (1975).

    PubMed  Article  Google Scholar 

  19. 19

    Wang, E. & Goldberg, A. R. Changes in microfilament organization and surface topogrophy upon transformation of chick embryo fibroblasts with Rous sarcoma virus. Proc. Natl Acad. Sci. USA 73, 4065–4069 (1976). The earliest demonstration of the gradual changes in cell morphology that occur as a result of cell transformation.

    CAS  PubMed  Article  Google Scholar 

  20. 20

    Jackson, P. & Bellett, A. J. Relationship between organization of the actin cytoskeleton and the cell cycle in normal and adenovirus-infected rat cells. J. Virol. 63, 311–318 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21

    Hall, A. The cytoskeleton and cancer. Cancer Metastasis Rev. 28, 5–14 (2009).

    PubMed  Article  Google Scholar 

  22. 22

    Marchisio, P. C., Capasso, O., Nitsch, L., Cancedda, R. & Gionti, E. Cytoskeleton and adhesion patterns of cultured chick embryo chondrocytes during cell spreading and Rous sarcoma virus transformation. Exp. Cell Res. 151, 332–343 (1984).

    CAS  PubMed  Article  Google Scholar 

  23. 23

    Boschek, C. B. et al. Early changes in the distribution and organization of microfilament proteins during cell transformation. Cell 24, 175–184 (1981).

    CAS  PubMed  Article  Google Scholar 

  24. 24

    McClain, D. A., Maness, P. F. & Edelman, G. M. Assay for early cytoplasmic effects of the src gene product of Rous sarcoma virus. Proc. Natl Acad. Sci. USA 75, 2750–2754 (1978).

    CAS  PubMed  Article  Google Scholar 

  25. 25

    Kellie, S., Horvath, A. R. & Elmore, M. A. Cytoskeletal targets for oncogenic tyrosine kinases. J. Cell Sci. 99, 207–211 (1991).

    CAS  PubMed  Google Scholar 

  26. 26

    Rohrschneider, L. R. Adhesion plaques of Rous sarcoma virus-transformed cells contain the src gene product. Proc. Natl Acad. Sci. USA 77, 3514–3518 (1980).

    CAS  PubMed  Article  Google Scholar 

  27. 27

    Shriver, K. & Rohrschneider, L. Organization of pp60src and selected cytoskeletal proteins within adhesion plaques and junctions of Rous sarcoma virus-transformed rat cells. J. Cell Biol. 89, 525–535 (1981).

    CAS  PubMed  Article  Google Scholar 

  28. 28

    Hiura, K., Lim, S. S., Little, S. P., Lin, S. & Sato, M. Differentiation dependent expression of tensin and cortactin in chicken osteoclasts. Cell Motil. Cytoskeleton 30, 272–284 (1995).

    CAS  PubMed  Article  Google Scholar 

  29. 29

    Sefton, B. M., Hunter, T., Ball, E. H. & Singer, S. J. Vinculin: a cytoskeletal target of the transforming protein of Rous sarcoma virus. Cell 24, 165–174 (1981).

    CAS  PubMed  Article  Google Scholar 

  30. 30

    Yoo, Y., Ho, H. J., Wang, C. & Guan, J. L. Tyrosine phosphorylation of cofilin at Y68 by v-Src leads to its degradation through ubiquitin-proteasome pathway. Oncogene 29, 263–272 (2010).

    CAS  PubMed  Article  Google Scholar 

  31. 31

    Burns, S., Thrasher, A. J., Blundell, M. P., Machesky, L. & Jones, G. E. Configuration of human dendritic cell cytoskeleton by Rho GTPases, the WAS protein, and differentiation. Blood 98, 1142–1149 (2001).

    CAS  Article  Google Scholar 

  32. 32

    Hai, C. M., Hahne, P., Harrington, E. O. & Gimona, M. Conventional protein kinase C mediates phorbol-dibutyrate-induced cytoskeletal remodeling in a7r5 smooth muscle cells. Exp. Cell Res. 280, 64–74 (2002).

    CAS  PubMed  Article  Google Scholar 

  33. 33

    Moreau, V., Tatin, F., Varon, C. & Genot, E. Actin can reorganize into podosomes in aortic endothelial cells, a process controlled by Cdc42 and RhoA. Mol. Cell Biol. 23, 6809–6822 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. 34

    Sato, T. et al. Identification of the membrane-type matrix metalloproteinase MT1-MMP in osteoclasts. J. Cell Sci. 110, 589–596 (1997).

    CAS  PubMed  Google Scholar 

  35. 35

    Saltel, F. et al. Invadosomes: Intriguing structures with promise. Eur. J. Cell Biol. 90, 100–107 (2011). A recent review about invadopodia, connecting earlier observations and nomenclature with recent literature.

    CAS  PubMed  Article  Google Scholar 

  36. 36

    Albiges-Rizo, C., Destaing, O., Fourcade, B., Planus, E. & Block, M. R. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 122, 3037–3049 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. 37

    Felice, G. R., Eason, P., Nermut, M. V. & Kellie, S. pp60v-src association with the cytoskeleton induces actin reorganization without affecting polymerization status. Eur. J. Cell Biol. 52, 47–59 (1990).

    CAS  PubMed  Google Scholar 

  38. 38

    Carley, W. W., Lipsky, M. G. & Webb, W. W. Regulation and drug insensitivity of F-actin association with adhesion areas of transformed cells. J. Cell Physiol. 117, 257–265 (1983).

    CAS  PubMed  Article  Google Scholar 

  39. 39

    Owada, M. K. et al. Occurrence of caldesmon (a calmodulin-binding protein) in cultured cells: comparison of normal and transformed cells. Proc. Natl Acad. Sci USA 81, 3133–3137 (1984).

    CAS  PubMed  Article  Google Scholar 

  40. 40

    Wang, E., Yin, H. L., Krueger, J. G., Caliguiri, L. A. & Tamm, I. Unphosphorylated gelsolin is localized in regions of cell-substratum contact or attachment in Rous sarcoma virus-transformed rat cells. J. Cell Biol. 98, 761–771 (1984).

    CAS  PubMed  Article  Google Scholar 

  41. 41

    Hendricks, M. & Weintraub, H. Tropomyosin is decreased in transformed cells. Proc. Natl Acad. Sci. USA 78, 5633–5637 (1981).

    CAS  PubMed  Article  Google Scholar 

  42. 42

    Ostap, E. M. Tropomyosins as discriminators of myosin function. Adv. Exp. Med. Biol. 644, 273–282 (2008).

    CAS  PubMed  Article  Google Scholar 

  43. 43

    Bernstein, B. W. & Bamburg, J. R. Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actin-depolymerizing factor (ADF). Cell Motil. 2, 1–8 (1982).

    CAS  PubMed  Article  Google Scholar 

  44. 44

    Graessmann, A., Graessmann, M., Tjian, R. & Topp, W. C. Simian virus 40 small-t protein is required for loss of actin cable networks in rat cells. J. Virol. 33, 1182–1191 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45

    Nunbhakdi-Craig, V., Craig, L., Machleidt, T. & Sontag, E. Simian virus 40 small tumor antigen induces deregulation of the actin cytoskeleton and tight junctions in kidney epithelial cells. J. Virol. 77, 2807–2818 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 46

    Endter, C. & Dobner, T. Cell transformation by human adenoviruses. Curr. Top. Microbiol. Immunol. 273, 163–214 (2004).

    CAS  PubMed  Google Scholar 

  47. 47

    Nielsch, U., Fognani, C. & Babiss, L. E. Adenovirus E1A-p105(Rb) protein interactions play a direct role in the initiation but not the maintenance of the rodent cell transformed phenotype. Oncogene 6, 1031–1036 (1991).

    CAS  PubMed  Google Scholar 

  48. 48

    Bellett, A. J., Jackson, P., David, E. T., Bennett, E. J. & Cronin, B. Functions of the two adenovirus early E1A proteins and their conserved domains in cell cycle alteration, actin reorganization, and gene activation in rat cells. J. Virol. 63, 303–310 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49

    Fischer, R. S. & Quinlan, M. P. While E1A can facilitate epithelial cell transformation by several dominant oncogenes, the C-terminus seems only to regulate rac and cdc42 function, but in both epithelial and fibroblastic cells. Virology 269, 404–419 (2000).

    CAS  PubMed  Article  Google Scholar 

  50. 50

    Bachvaroff, R. J., Klein, G. & Rapaport, F. T. Alterations in cell characteristics in relation to malignant transformation. Transplant Proc. 11, 1055–1059 (1979).

    CAS  PubMed  Google Scholar 

  51. 51

    Lamelin, J. P., Williams, E. H., Souissi, T., De-The, G. & Gabbiani, G. Smooth muscle antibody in Burkitt's lymphoma and in nasopharyngeal carcinoma. Clin. Exp. Immunol. 28, 157–162 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    Bachvaroff, R. J., Miller, F. & Rapaport, F. T. Appearance of cytoskeletal components on the surface of leukemia cells and of lymphocytes transformed by mitogens and Epstein–Barr virus. Proc. Natl Acad. Sci. USA 77, 4979–4983 (1980).

    CAS  PubMed  Article  Google Scholar 

  53. 53

    Smalheiser, N. R. Proteins in unexpected locations. Mol. Biol. Cell 7, 1003–1014 (1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54

    Arnoys, E. J. & Wang, J. L. Dual localization: proteins in extracellular and intracellular compartments. Acta Histochem. 109, 89–110 (2007).

    CAS  PubMed  Article  Google Scholar 

  55. 55

    Mosialos, G. et al. Epstein-Barr virus infection induces expression in B lymphocytes of a novel gene encoding an evolutionarily conserved 55-kilodalton actin-bundling protein. J. Virol. 68, 7320–7328 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56

    Ishikawa, R., Yamashiro, S., Kohama, K. & Matsumura, F. Regulation of actin binding and actin bundling activities of fascin by caldesmon coupled with tropomyosin. J. Biol. Chem. 273, 26991–26997 (1998).

    CAS  PubMed  Article  Google Scholar 

  57. 57

    Tseng, Y., Fedorov, E., McCaffery, J. M., Almo, S. C. & Wirtz, D. Micromechanics and ultrastructure of actin filament networks crosslinked by human fascin: a comparison with α-actinin. J. Mol. Biol. 310, 351–366 (2001).

    CAS  PubMed  Article  Google Scholar 

  58. 58

    Spender, L. C. et al. Cell target genes of Epstein–Barr virus transcription factor EBNA-2: induction of the p55α regulatory subunit of PI3-kinase and its role in survival of EREB2.5 cells. J. Gen. Virol. 87, 2859–2867 (2006).

    CAS  PubMed  Article  Google Scholar 

  59. 59

    Tan, T. L. et al. Rac1 GTPase is activated by hepatitis B virus replication — involvement of HBX. Biochim. Biophys. Acta 1783, 360–374 (2008).

    CAS  PubMed  Article  Google Scholar 

  60. 60

    Lara-Pezzi, E. et al. The hepatitis B virus X protein (HBx) induces a migratory phenotype in a CD44-dependent manner: possible role of HBx in invasion and metastasis. Hepatology 33, 1270–1281 (2001).

    CAS  PubMed  Article  Google Scholar 

  61. 61

    Charette, S. T. & McCance, D. J. The E7 protein from human papillomavirus type 16 enhances keratinocyte migration in an Akt-dependent manner. Oncogene 26, 7386–7390 (2007).

    CAS  PubMed  Article  Google Scholar 

  62. 62

    Wu, R., Coniglio, S. J., Chan, A., Symons, M. H. & Steinberg, B. M. Up-regulation of Rac1 by epidermal growth factor mediates COX-2 expression in recurrent respiratory papillomas. Mol. Med. 13, 143–150 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63

    Medeiros, N. A., Burnette, D. T. & Forscher, P. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nature Cell Biol. 8, 215–226 (2006).

    CAS  PubMed  Article  Google Scholar 

  64. 64

    Lehmann, M. J., Sherer, N. M., Marks, C. B., Pypaert, M. & Mothes, W. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 170, 317–325 (2005). The earliest description of viral surfing as it relates to viral entry and infection.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. 65

    Schelhaas, M. et al. Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog. 4, e1000148 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  66. 66

    Mercer, J. & Helenius, A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320, 531–535 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  67. 67

    Huang, K.-C., Yasruel, Z., Guérin, C., Holland, P. C. & Nalbantoglu, J. Interaction of the Coxsackie and adenovirus receptor (CAR) with the cytoskeleton: binding to actin. FEBS Lett. 581, 2702–2708 (2007).

    CAS  PubMed  Article  Google Scholar 

  68. 68

    Coyne, C. B. & Bergelson, J. M. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124, 119–131 (2006).

    CAS  Article  Google Scholar 

  69. 69

    Meier, O. & Greber, U. F. Adenovirus endocytosis. J. Gene Med. 6, S152–S163 (2004). An essential review covering virus-induced cytoskeletal changes and endocytosis.

    PubMed  Article  Google Scholar 

  70. 70

    Mercer, J., Schelhaas, M. & Helenius, A. Virus entry by endocytosis. Ann. Rev. Biochem. 79, 803–833 (2010).

    CAS  PubMed  Article  Google Scholar 

  71. 71

    Greene, W. & Gao, S.-J. Actin dynamics regulate multiple endosomal steps during Kaposi's sarcoma-associated herpesvirus entry and trafficking in endothelial cells. PLoS Pathog. 5, e1000512 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  72. 72

    Quinn, K. et al. Rho GTPases modulate entry of Ebola virus and vesicular stomatitis virus pseudotyped vectors. J. Virol. 83, 10176–10186 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. 73

    Cureton, D. K., Massol, R. H., Saffarian, S., Kirchhausen, T. L. & Whelan, S. P. J. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 5, e1000394 (2009). A visually stunning analysis of VSV entry and the role of actin.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  74. 74

    Brandenburg, B. et al. Imaging poliovirus entry in live cells. PLoS Biol. 5, e183 (2007).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  75. 75

    Vaughan, J. C., Brandenburg, B., Hogle, J. M. & Zhuang, X. Rapid actin-dependent viral motility in live cells. Biophys. J. 97, 1647–1656 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. 76

    Veiga, E. & Cossart, P. The role of clathrin-dependent endocytosis in bacterial internalization. Trends Cell Biol. 16, 499–504 (2006).

    CAS  PubMed  Article  Google Scholar 

  77. 77

    Kallewaard, N. L., Bowen, A. L. & Crowe, J. E. Jr. Cooperativity of actin and microtubule elements during replication of respiratory syncytial virus. Virology 331, 73–81 (2005).

    CAS  PubMed  Article  Google Scholar 

  78. 78

    Wurth, M. A. et al. The actin cytoskeleton inhibits pore expansion during PIV5 fusion protein-promoted cell–cell fusion. Virology 404, 117–126 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79

    Pastey, M. K., Gower, T. L., Spearman, P. W., Crowe, J. E. Jr. & Graham, B. S. A RhoA-derived peptide inhibits syncytium formation induced by respiratory syncytial virus and parainfluenza virus type 3. Nature Med. 6, 35–40 (2000).

    CAS  PubMed  Article  Google Scholar 

  80. 80

    Schowalter, R. M. et al. Rho GTPase activity modulates paramyxovirus fusion protein-mediated cell–cell fusion. Virology 350, 323–334 (2006).

    CAS  PubMed  Article  Google Scholar 

  81. 81

    Iyengar, S., Hildreth, J. E. K. & Schwartz, D. H. Actin-dependent receptor colocalization required for human immunodeficiency virus entry into host cells. J. Virol. 72, 5251–5255 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. 82

    Yoder, A. et al. HIV envelope-CXCR4 signaling activates cofilin to overcome cortical actin restriction in resting CD4 T Cells. Cell 134, 782–792 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  83. 83

    Jimenez-Baranda, S. et al. Filamin-A regulates actin-dependent clustering of HIV receptors. Nature Cell Biol. 9, 838–846 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. 84

    Harmon, B., Campbell, N. & Ratner, L. Role of Abl kinase and the Wave2 signaling complex in HIV-1 entry at a post-hemifusion step. PLoS Pathog. 6, e1000956 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  85. 85

    Clement, C. et al. A novel role for phagocytosis-like uptake in herpes simplex virus entry. J. Cell Biol. 174, 1009–1021 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. 86

    Smith, J. L., Lidke, D. S. & Ozbun, M. A. Virus activated filopodia promote human papillomavirus type 31 uptake from the extracellular matrix. Virology 381, 16–21 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  87. 87

    Cantin, R., Methot, S. & Tremblay, M. J. Plunder and stowaways: incorporation of cellular proteins by enveloped viruses. J. Virol. 79, 6577–6587 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  88. 88

    Burke, E., Mahoney, N. M., Almo, S. C. & Barik, S. Profilin is required for optimal actin-dependent transcription of respiratory syncytial virus genome RNA. J. Virol. 74, 669–675 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. 89

    Klauschies, F. et al. Viral infectivity and intracellular distribution of matrix (M) protein of canine distemper virus are affected by actin filaments. Arch. Virol. 115, 1503–1508 (2010).

    Article  CAS  Google Scholar 

  90. 90

    Bucher, D. et al. M protein (M1) of influenza virus: antigenic analysis and intracellular localization with monoclonal antibodies. J. Virol. 63, 3622–3633 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91

    Harpen, M., Barik, T., Musiyenko, A. & Barik, S. Mutational analysis reveals a noncontractile but interactive role of actin and profilin in viral RNA-dependent RNA synthesis. J. Virol. 83, 10869–10876 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  92. 92

    Arhel, N. et al. Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nature Methods 3, 817–824 (2006).

    CAS  Article  Google Scholar 

  93. 93

    Bukrinskaya, A., Brichacek, B., Mann, A. & Stevenson, M. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188, 2113–2125 (1998). A biochemical analysis of the association between actin and HIV particles at different stages post-entry.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. 94

    Fackler, O. T. & Kräusslich, H.-G. Interactions of human retroviruses with the host cell cytoskeleton. Curr. Opin. Microbiol. 9, 409–415 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. 95

    Jolly, C., Mitar, I. & Sattentau, Q. J. Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J. Virol. 81, 5547–5560 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  96. 96

    Sasaki, H., Ozaki, H., Karaki, H. & Nonomura, Y. Actin filaments play an essential role for transport of nascent HIV-1 proteins in host cells. Biochem. Biophys. Res. Commun. 316, 588–593 (2004).

    CAS  PubMed  Article  Google Scholar 

  97. 97

    Chen, C. et al. Association of Gag multimers with filamentous actin during equine infectious anemia virus assembly. Curr. HIV Res. 5, 315–323 (2007).

    CAS  PubMed  Article  Google Scholar 

  98. 98

    Tyrrell, D. L. & Ehrnst, A. Transmembrane communication in cells chronically infected with measles virus. J. Cell Biol. 81, 396–402 (1979).

    CAS  PubMed  Article  Google Scholar 

  99. 99

    Takimoto, T. & Portner, A. Molecular mechanism of paramyxovirus budding. Virus Res. 106, 133–145 (2004).

    CAS  PubMed  Article  Google Scholar 

  100. 100

    Miazza, V., Mottet-Osman, G., Startchick, S., Chaponnier, C. & Roux., L. Sendai virus induced cytoplasmic actin remodeling correlates with efficient virus particle production. Virology 410, 7–16 (2011).

    CAS  PubMed  Article  Google Scholar 

  101. 101

    Bohn, W., Rutter, G., Hohenberg, H., Mannweiler, K. & Nobis, P. Involvement of actin filaments in budding of measles virus: studies on cytoskeletons of infected cells. Virology 149, 91–106 (1986). A study producing high-quality electron micrographs that demonstrate the directional alignment of actin filaments with measles virions.

    CAS  PubMed  Article  Google Scholar 

  102. 102

    Stallcup, K. C., Raine, C. S. & Fields, B. N. Cytochalasin B inhibits the maturation of measles virus. Virology 124, 59–74 (1983).

    CAS  PubMed  Article  Google Scholar 

  103. 103

    Forest, T., Barnard, S. & Baines, J. D. Active intranuclear movement of herpesvirus capsids. Nature Cell Biol. 7, 429–431 (2005).

    CAS  PubMed  Article  Google Scholar 

  104. 104

    Feierbach, B., Piccinotti, S., Bisher, M., Denk, W. & Enquist, L. W. Alpha-herpesvirus infection induces the formation of nuclear actin filaments. PLoS Pathog. 2, e85 (2006).

    PubMed  PubMed Central  Article  Google Scholar 

  105. 105

    Simpson-Holley, M., Colgrove, R. C., Nalepa, G., Harper, J. W. & Knipe, D. M. Identification and functional evaluation of cellular and viral factors involved in the alteration of nuclear architecture during herpes simplex virus 1 infection. J. Virol. 79, 12840–12851 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. 106

    Wagenaar, F. et al. The US3-encoded protein kinase from pseudorabies virus affects egress of virions from the nucleus. J. Gen. Virol. 76, 1851–1859 (1995).

    CAS  PubMed  Article  Google Scholar 

  107. 107

    Ohkawa, T., Volkman, L. E. & Welch, M. D. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J. Cell Biol. 190, 187–195 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  108. 108

    Roberts, K. L. & Baines, J. D. Myosin Va enhances secretion of herpes simplex virus 1 virions and cell surface expression of viral glycoproteins. J. Virol. 84, 9889–9896 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. 109

    Sattentau, Q. Avoiding the void: cell-to-cell spread of human viruses. Nature Rev. Microbiol. 6, 815–826 (2008). A comprehensive review about the hurdles of cell-to-cell spread of viruses.

    CAS  Article  Google Scholar 

  110. 110

    Damsky, C. H., Sheffield, J. B., Tuszynski, G. P. & Warren, L. Is there a role for actin in virus budding? J. Cell Biol. 75, 593–605 (1977).

    CAS  PubMed  Article  Google Scholar 

  111. 111

    Akiyama, T. et al. Substrate specificities of tyrosine-specific protein kinases toward cytoskeletal proteins in vitro. J. Biol. Chem. 261, 14797–14803 (1986).

    CAS  PubMed  Google Scholar 

  112. 112

    Carlson, L. A. et al. Cryo electron tomography of native HIV-1 budding sites. PLoS Pathog. 6, e1001173 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  113. 113

    Maldarelli, F., King, N. W. Jr. & Yagi, M. J. Effects of cytoskeletal disrupting agents on mouse mammary tumor virus replication. Virus Res. 7, 281–295 (1987).

    CAS  PubMed  Article  Google Scholar 

  114. 114

    Eugenin, E. A., Gaskill, P. J. & Berman, J. W. Tunneling nanotubes (TNT) are induced by HIV-infection of macrophages: a potential mechanism for intercellular HIV trafficking. Cell. Immunol. 254, 142–148 (2009).

    CAS  PubMed  Article  Google Scholar 

  115. 115

    Sherer, N. M. et al. Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nature Cell Biol. 9, 310–315 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. 116

    Haller, C., Rauch, S. & Fackler, O. T. HIV-1 Nef employs two distinct mechanisms to modulate Lck subcellular localization and TCR induced actin remodeling. PLoS ONE 2, e1212 (2007).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  117. 117

    Nobile, C. et al. HIV-1 Nef inhibits ruffles, induces filopodia, and modulates migration of infected lymphocytes. J. Virol. 84, 2282–2293 (2010).

    CAS  PubMed  Article  Google Scholar 

  118. 118

    Stolp, B., Abraham, L., Rudolph, J. M. & Fackler, O. T. Lentiviral Nef proteins utilize PAK2-mediated deregulation of cofilin as a general strategy to interfere with actin remodeling. J. Virol. 84, 3935–3948 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. 119

    Stolp, B. et al. HIV-1 Nef interferes with host cell motility by deregulation of cofilin. Cell Host Microbe 6, 174–186 (2009).

    CAS  PubMed  Article  Google Scholar 

  120. 120

    Rauch, S., Pulkkinen, K., Saksela, K. & Fackler, O. T. Human immunodeficiency virus type 1 nef recruits the guanine exchange factor Vav1 via an unexpected interface into plasma membrane microdomains for association with p21-activated kinase 2 activity. J. Virol. 82, 2918–2929 (2008).

    CAS  PubMed  Article  Google Scholar 

  121. 121

    Minnebruggen, G. V., Favoreel, H. W., Jacobs, L. & Nauwynck, H. J. Pseudorabies virus US3 protein kinase mediates actin stress fibre breakdown. J. Virol. 77, 9074–9080 (2003).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  122. 122

    Favoreel, H. W. et al. Alphaherpesvirus use and misuse of cellular actin and cholesterol. Vet. Microbiol. 143, 2–7 (2010).

    CAS  PubMed  Article  Google Scholar 

  123. 123

    Favoreel, H. W., Van Minnebruggen, G., Adriaensen, D. & Nauwynck, H. J. Cytoskeletal rearrangements and cell extensions induced by the US3 kinase of an αherpesvirus are associated with enhanced spread. Proc. Natl Acad. Sci. USA 102, 8990–8995 (2005). An investigation that demonstrates the direct induction of cytoskeletal extensions by a herpesvirus protein kinase.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  124. 124

    Van den Broeke, C.l. et al. Alphaherpesvirus US3-mediated reorganization of the actin cytoskeleton is mediated by group A p21-activated kinases. Proc. Natl Acad. Sci.USA 106, 8707–8712 (2009).

    CAS  PubMed  Article  Google Scholar 

  125. 125

    Deruelle, M. J. & Favoreel, H. W. Keep it in the subfamily: the conserved alphaherpesvirus US3 protein kinase. J. Gen. Virol. 92, 18–30 (2010).

    PubMed  Article  CAS  Google Scholar 

  126. 126

    Berkova, Z., Crawford, S. E., Blutt, S. E., Morris, A. P. & Estes, M. K. Expression of rotavirus NSP4 alters the actin network organization through the actin remodeling protein cofilin. J. Virol. 81, 3545–3553 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. 127

    Gardet, A., Breton, M., Fontanges, P., Trugnan, G. & Chwetzoff, S. Rotavirus spike protein VP4 binds to and remodels actin bundles of the epithelial brush border into actin bodies. J. Virol. 80, 3947–3956 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  128. 128

    Gardet, A., Breton, M., Trugnan, G. & Chwetzoff, S. Role for actin in the polarized release of rotavirus. J. Virol. 81, 4892–4894 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  129. 129

    Valderrama, F., Cordeiro, J. V., Schleich, S., Frischknecht, F. & Way, M. Vaccinia virus-induced cell motility requires F11L-mediated inhibition of RhoA signaling. Science 311, 377–381 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  130. 130

    Arakawa, Y., Cordeiro, J. V., Schleich, S., Newsome, T. P. & Way, M. The release of vaccinia virus from infected cells requires RhoA-mDia modulation of cortical actin. Cell Host Microbe 1, 227–240 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  131. 131

    Sanderson, C. M., Way, M. & Smith, G. L. Virus-induced cell motility. J. Virol. 72, 1235–1243 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. 132

    Cordeiro, J. V. et al. F11-mediated inhibition of RhoA signalling enhances the spread of vaccinia virus in vitro and in vivo in an intranasal mouse model of infection. PLoS ONE 4, e8506 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  133. 133

    Hiller, G., Weber, K., Schneider, L., Parajsz, C. & Jungwirth, C. Interaction of assembled progeny pox viruses with the cellular cytoskeleton. Virology 98, 142–153 (1979).

    CAS  PubMed  Article  Google Scholar 

  134. 134

    Cudmore, S., Cossart, P., Griffiths, G. & Way, M. Actin-based motility of vaccinia virus. Nature 378, 636–638 (1995). A seminal work on the role of actin-based motility in VV infection.

    CAS  Article  Google Scholar 

  135. 135

    Wolffe, E. J., Weisberg, A. S. & Moss, B. Role for the vaccinia virus A36R outer envelope protein in the formation of virus-tipped actin-containing microvilli and cell-to-cell virus spread. Virology 244, 20–26 (1998).

    CAS  PubMed  Article  Google Scholar 

  136. 136

    Frischknecht, F. et al. Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature 401, 926–929 (1999).

    CAS  PubMed  Article  Google Scholar 

  137. 137

    Scaplehorn, N. et al. Grb2 and Nck act cooperatively to promote actin-based motility of vaccinia virus. Curr. Biol. 12, 740–745 (2002).

    CAS  PubMed  Article  Google Scholar 

  138. 138

    Doceul, V., Hollinshead, M., van der Linden, L. & Smith, G. L. Repulsion of superinfecting virions: a mechanism for rapid virus spread. Science 327, 873–876 (2010). A report that connects the history of VV-mediated actin modulation with long-distance viral spread and the observable phenomenon of plaque formation.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  139. 139

    Reeves, P. M. et al. Variola and monkeypox viruses utilize conserved mechanisms of virion motility and release that depend on Abl and Src family tyrosine kinases. J. Virol. 85, 21–31 (2011).

    CAS  PubMed  Article  Google Scholar 

  140. 140

    Dodding, M. P. & Way, M. Nck- and N-WASP-dependent actin-based motility is conserved in divergent vertebrate poxviruses. Cell Host Microbe 6, 536–550 (2009).

    CAS  PubMed  Article  Google Scholar 

  141. 141

    Murti, K. G., Chen, M. & Goorha, R. Interaction of frog virus 3 with the cytomatrix: III. Role of microfilaments in virus release. Virology 142, 317–325 (1985).

    CAS  PubMed  Article  Google Scholar 

  142. 142

    Jouvenet, N. et al. African swine fever virus induces filopodia-like projections at the plasma membrane. Cell. Microbiol. 8, 1803–1811 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  143. 143

    Champagne, C., Landry, M. C., Gingras, M. C. & Lavoie, J. N. Activation of adenovirus type 2 early region 4 ORF4 cytoplasmic death function by direct binding to Src kinase domain. J. Biol. Chem. 279, 25905–25915 (2004).

    CAS  PubMed  Article  Google Scholar 

  144. 144

    Robert, A. et al. Adenovirus E4orf4 hijacks rho GTPase-dependent actin dynamics to kill cells: a role for endosome-associated actin assembly. Mol. Biol. Cell 17, 3329–3344 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  145. 145

    Amine, A. et al. Novel anti-metastatic action of cidofovir mediated by inhibition of E6/E7, CXCR4 and Rho/ROCK signaling in HPV tumor cells. PLoS ONE 4, e5018 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  146. 146

    Moser, T. S., Jones, R. G., Thompson, C. B., Coyne, C. B. & Cherry, S. A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog. 6, e1000954 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  147. 147

    Ferreira, C. Expression of ubiquitin, actin, and actin-like genes in African swine fever virus infected cells. Virus Res. 44, 11–21 (1996).

    CAS  PubMed  Article  Google Scholar 

  148. 148

    Drenckhahn, D. & Wagner, J. Stress fibres in the splenic sinus endothelium in situ: molecular structure, relationship to the extracellular matrix, and contractility. J. Cell Biol. 102, 1738–1747 (1986).

    CAS  PubMed  Article  Google Scholar 

  149. 149

    Wong, A. J., Pollard, T. D. & Herman, I. M. Actin filament stress fibres in vascular endothelial cells in vivo. Science 219, 867–869 (1983).

    CAS  PubMed  Article  Google Scholar 

  150. 150

    Halliburton, W. D. On muscle-plasma. J. Physiol. 8, 133–202 (1887).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  151. 151

    Straub, F. B. in Studies from the Institute of Medical Chemistry University Szeged Vol. 2 (ed. Szent-Györgyi, A.) 3–15 (Karger, Basel, 1942).

    Google Scholar 

  152. 152

    Jakus, M. A. & Hall, C. E. Studies of actin and myosin. J. Biol. Chem. 167, 705–714 (1947).

    CAS  PubMed  Google Scholar 

  153. 153

    Ohnishi, T. & Tomoko, O. Extraction of actin- and myosin-like proteins from liver mitochondria. J. Biochem. 52, 230–231 (1962).

    CAS  PubMed  Article  Google Scholar 

  154. 154

    Wen, K.-K., Rubenstein, P. A. & DeMali, K. A. Vinculin nucleates actin polymerization and modifies actin filament structure. J. Biol. Chem. 284, 30463–30473 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  155. 155

    Cudmore, S., Reckmann, I., Griffiths, G. & Way, M. Vaccinia virus: a model system for actin-membrane interactions. J. Cell Sci. 109, 1739–1747 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  156. 156

    Spector, I., Shochet, N. R., Blasberger, D. & Kashman, Y. Latrunculins — novel marine macrolides that disrupt microfilament organization and affect cell growth: I. Comparison with cytochalasin D. Cell Motil. Cytoskeleton 13, 127–144 (1989).

    CAS  PubMed  Article  Google Scholar 

  157. 157

    Cooper, J. A. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105, 1473–1478 (1987).

    CAS  PubMed  Article  Google Scholar 

  158. 158

    Saito, S., Watabe, S., Ozaki, H., Fusetani, N. & Karaki, H. Mycalolide B, a novel actin depolymerizing agent. J. Biol. Chem. 269, 29710–29714 (1994).

    CAS  PubMed  Google Scholar 

  159. 159

    Bubb, M. R., Spector, I., Beyer, B. B. & Fosen, K. M. Effects of jasplakinolide on the kinetics of actin polymerization. J. Biol. Chem. 275, 5163–5170 (2000).

    CAS  PubMed  Article  Google Scholar 

  160. 160

    Limouze, J., Straight, A., Mitchison, T. & Sellers, J. Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25, 337–341 (2004).

    CAS  PubMed  Article  Google Scholar 

  161. 161

    Sahai, E. & Olson, M. F. Purification of TAT-C3 exoenzyme. Methods Enzymol. 406, 128–140 (2006).

    CAS  PubMed  Article  Google Scholar 

  162. 162

    Ishizaki, T. et al. Pharmacological properties of Y-27632, a specific inhibitor of Rho-associated kinases. Mol. Pharmacol. 57, 976–983 (2000).

    CAS  PubMed  Google Scholar 

  163. 163

    Klussmann, E., Scott, J., Deacon, S. W. & Peterson, J. R. in Protein-Protein Interactions as New Drug Targets (eds Kass, R. S. & Clancy, C. E.) 431–460 (Springer, Berlin, 2008).

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge M. Way, W. Bohn, K. Gruenwald and K. DeMali for generously providing the original electron micrographs. They also appreciate the guidance and encouragement from all members of the Enquist laboratory. L.W.E. and O.O.K. are supported by the US National Institutes of Health grants R37 NS033506-16 and R01 NS060699-03. M.P.T. is supported by an American Cancer Society Postdoctoral Research Fellowship (PF-10-057-01-MPC).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lynn W. Enquist.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Lynn W. Enquist's homepage

Glossary

Gelsolin

A calcium-activated protein that severs actin filaments.

Lamellipodia

Wide, thin sheets of membrane extending from the cell body; lamellipodia are often associated with the leading edge of motile cells.

Membrane ruffles

Membrane-enclosed, densely packed actin bundles that increase during cell migration or transformation. Ruffles localize to the leading edge of the lamellipodia, giving these structures a flower-like appearance.

Filopodia

Long, thin membranous extensions of the cell with a core of actin filaments.

Podosomes

Dot-like extracellular matrix attachment sites in motile cells. In transformed cells, podosomes aggregate in the presence of serum to form ring- or crescent-shaped rosettes.

Pseudopodia

Large membranous protrusions that are used to promote the movement of highly motile cells; the name is derived from the Greek for 'false-footed'.

Contact inhibition

The inhibition of uncontrolled cell division by cell–cell contact through mitogen-activated protein kinase signalling. Contact inhibition is deregulated in transformed cell populations.

Adherens junctions

Epithelial cell-to-cell junctions that connect the actin cytoskeleton of one cell to the cytoplasm of the neighbouring cell via cadherins and catenins.

Vinculin

A focal-adhesion plaque protein that is associated with the microfilament ends and talin.

Talin

An actin-binding protein associated with adherens junctions, ruffling membranes and other sites of actin–membrane interaction.

α-actinin

A large family of proteins that crosslink and bundle actin filaments in a calcium-dependent manner in non-muscle cells.

Focal adhesions

Macromolecular complexes that connect the actin cytoskeleton to the extracellular matrix by the association of transmembrane integrins with extracellular proteins such as fibronectin.

Caldesmon

A calmodulin-binding and F-actin-binding protein that regulates the function of actin filaments in a calcium-dependent manner.

Clathrin-mediated endocytosis

The process of enveloping extracellular material and bringing it into the cellular cytoplasm within a membranous vesicle. Invagination of the plasma membrane and stabilization of the vesicle is carried out by triskelions of clathrin that polymerize at the membrane surface to induce curvature.

Macropinocytosis

A specialized form of endocytosis that is used by the cell to obtain soluble materials from the extracellular environment.

Actin treadmilling

The act of moving a specific actin monomer, or its position, along an actin filament using active polymerization and depolymerization processes.

Comet tails

Dense structures of actin filaments that are used to propel objects through the cytoplasm or long distances away from the cell.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Taylor, M., Koyuncu, O. & Enquist, L. Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 9, 427–439 (2011). https://doi.org/10.1038/nrmicro2574

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing