Viruses as probes for systems analysis of cellular signalling, cytoskeleton reorganization and endocytosis

Current Opinion in Microbiology

Volumn 8, Issue 3, 2005, Pages 331-337

  Pelkmans, Lucas ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

ANALYTIC METHOD; CELL STRUCTURE; CYTOSKELETON; DIFFRACTION; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; GENOMICS; HOST CELL; MAMMAL; MEMBRANE TRANSPORT; MICROBIAL KINETICS; MICROSCOPY; MICROTUBULE; MOLECULAR PROBE; NONHUMAN; PROTEIN STRUCTURE; REVIEW; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; SYSTEM ANALYSIS;

CYTOLOGICAL TECHNIQUES; CYTOSKELETON; ENDOCYTOSIS; SIGNAL TRANSDUCTION; VIRUSES;

MAMMALIA;

EID: 20444488145     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2005.02.018     Document Type: Review

References (43)

1. A. Helenius, J. Kartenbeck, K. Simons, and E. Fries On the entry of Semliki forest virus into BHK-21 cells J Cell Biol 84 1980 404 420
2. M. Suomalainen, M.Y. Nakano, S. Keller, K. Boucke, R.P. Stidwill, and U.F. Greber Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus J Cell Biol 144 1999 657 672
3. L. Pelkmans, J. Kartenbeck, and A. Helenius Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER Nat Cell Biol 3 2001 473 483
4. M. Lakadamyali, M.J. Rust, H.P. Babcock, and X. Zhuang Visualizing infection of individual influenza viruses Proc Natl Acad Sci USA 100 2003 9280 9285
5. P. Desai, and S. Person Incorporation of the green fluorescent protein into the herpes simplex virus type 1 capsid J Virol 72 1998 7563 7568
6. D. McDonald, M.A. Vodicka, G. Lucero, T.M. Svitkina, G.G. Borisy, M. Emerman, and T.J. Hope Visualization of the intracellular behavior of HIV in living cells J Cell Biol 159 2002 441 452
7. A.R. Reynolds, C. Tischer, P.J. Verveer, O. Rocks, and P.I. Bastiaens EGFR activation coupled to inhibition of tyrosine phosphatases causes lateral signal propagation Nat Cell Biol 5 2003 447 453
8. D.L. Evers, X. Wang, and E.S. Huang Cellular stress and signal transduction responses to human cytomegalovirus infection Microbes Infect 6 2004 1084 1093
9. X. Wang, S.M. Huong, M.L. Chiu, N. Raab-Traub, and E.S. Huang Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus Nature 424 2003 456 461
10. P.P. Di Fiore, and G. Scita Eps8 in the midst of GTPases Int J Biochem Cell Biol 34 2002 1178 1183
11. U.F. Greber Signalling in viral entry Cell Mol Life Sci 59 2002 608 626
12. O. Meier, K. Boucke, S.V. Hammer, S. Keller, R.P. Stidwill, S. Hemmi, and U.F. Greber Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake J Cell Biol 158 2002 1119 1131
13. V. Marjomaki, V. Pietiainen, H. Matilainen, P. Upla, J. Ivaska, L. Nissinen, H. Reunanen, P. Huttunen, T. Hyypia, and J. Heino Internalization of Echovirus 1 in Caveolae J Virol 76 2002 1856 1865
14. P. Upla, V. Marjomaki, P. Kankaanpaa, J. Ivaska, T. Hyypia, F.G. Van Der Goot, and J. Heino Clustering induces a lateral redistribution of α2β1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization Mol Biol Cell 15 2004 625 636 This study shows that the multivalent clustering of certain integrin combinations induces their redistribution into caveolae. Not only might this be the mechanism for how echovirus 1 gets sequestered into caveolae but it also suggests how caveolae might be able to regulate integrin function, a link that was long known to exist.
15. B. Tsai, J.M. Gilbert, T. Stehle, W. Lencer, T.L. Benjamin, and T.A. Rapoport Gangliosides are receptors for murine polyoma virus and SV40 EMBO J 22 2003 4346 4355 Old literature predicted that murine polyoma virus and SV40 virus use protein and lipid components as cellular receptors; this study identified the lipid component - gangliosides. These lipids are enriched in caveolae and in lipid rafts, which explains, in part, their modes of viral entry. Nevertheless, differences to other ganglioside-binding ligands as well as the strong ability to activate signalling cascades suggest that additional receptors, which have not yet been identified, are involved.
16. L. Pelkmans, D. Puntener, and A. Helenius Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae Science 296 2002 535 539
17. W.C. Breau, W.J. Atwood, and L.C. Norkin Class I major histocompatibility proteins are an essential component of the simian virus 40 receptor J Virol 66 1992 2037 2045
18. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat Rev Mol Cell Biol 1 2000 31 39
19. L. Pelkmans, T. Burli, M. Zerial, and A. Helenius Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic Cell 118 2004 767 780
20. N. Cheshenko, B. Del Rosario, C. Woda, D. Marcellino, L.M. Satlin, and B.C. Herold Herpes simplex virus triggers activation of calcium-signaling pathways J Cell Biol 163 2003 283 293
21. T.D. Pollard, and G.G. Borisy Cellular motility driven by assembly and disassembly of actin filaments Cell 112 2003 453 465
22. S. Cudmore, P. Cossart, G. Griffiths, and M. Way Actin-based motility of vaccinia virus Nature 378 1995 636 638
23. L.G. Tilney, and D.A. Portnoy Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes J Cell Biol 109 1989 1597 1608
24. B.M. Ward, and B. Moss Vaccinia virus intracellular movement is associated with microtubules and independent of actin tails J Virol 75 2001 11651 11663
25. C. Morgan, H.M. Rose, and B. Mednis Electron microscopy of herpes simplex virus. I. Entry J Virol 2 1968 507 516
26. C. Morgan, H.S. Rosenkranz, and B. Mednis Structure and development of viruses as observed in the electron microscope. V. Entry and uncoating of adenovirus J Virol 4 1969 777 796
27. M. Marsh, E. Bolzau, and A. Helenius Penetration of Semliki Forest virus from acidic prelysosomal vacuoles Cell 32 1983 931 940
28. •] show that virus particles are able to polymerize a clathrin coat directly under their site at which they are attached to the plasma membrane. The mechanisms and signals involved to induce 'committed' polymerization of a full clathrin coat can now be tested.
29. •].
30. Z. Richterova, D. Liebl, M. Horak, Z. Palkova, J. Stokrova, P. Hozak, J. Korb, and J. Forstova Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei J Virol 75 2001 10880 10891
31. A.A. Richards, E. Stang, R. Pepperkok, and R.G. Parton Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection Mol Biol Cell 13 2002 1750 1764
32. ••].
33. S.B. Sieczkarski, and G.R. Whittaker Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis J Virol 76 2002 10455 10464
34. ••], foremost the one from Nicola et al., have successfully and convincingly challenged dogmatic views in the virus entry field. They show that viruses that were believed to fuse directly with the plasma membrane are actually more efficient at entering the cell via endocytosis. Although this might be specific for HeLa cells, which were used in both studies, it shows that HIV and HSV-1 are able to hijack the endocytic machinery with important implications for strategies to fight these viral infections.
35. ••].
36. B. Sodeik, M.W. Ebersold, and A. Helenius Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus J Cell Biol 136 1997 1007 1021
37. T.P. Newsome, N. Scaplehorn, and M. Way SRC mediates a switch from microtubule- to actin-based motility of vaccinia virus Science 306 2004 124 129
38. S. Gasman, Y. Kalaidzidis, and M. Zerial RhoD regulates endosome dynamics through Diaphanous-related Formin and Src tyrosine kinase Nat Cell Biol 5 2003 195 204
39. L.A. Cameron, P.A. Giardini, F.S. Soo, and J.A. Theriot Secrets of actin-based motility revealed by a bacterial pathogen Nat Rev Mol Cell Biol 1 2000 110 119
40. J.B. Alberts, and G.M. Odell In silico reconstitution of Listeria propulsion exhibits nano-saltation PLoS Biol 2 2004 e412
41. D. Thomann, J. Dorn, P.K. Sorger, and G. Danuser Automatic fluorescent tag localization II: improvement in super-resolution by relative tracking J Microsc 211 2003 230 248
42. M.C. Adams, A. Matov, D. Yarar, S.L. Gupton, G. Danuser, and C.M. Waterman-Storer Signal analysis of total internal reflection fluorescent speckle microscopy (TIR-FSM) and wide-field epi-fluorescence FSM of the actin cytoskeleton and focal adhesions in living cells J Microsc 216 2004 138 152
43. Pelkmans L, Fava E, Hannes M, Grabner H, Habermann B, Krausz E, Zerial M: Genome-wide analysis of human kinases in endocytosis reveals extensive integration with signalling networks. Nature 2005, in press. This study is the first to systematically compare the host (human) cellular genes that are involved in two different infectious virus entry pathways using RNAi methodology. By doing this, major differences between the regulatory principles of the endocytic pathways they hijack are revealed. In general, when expanded to several viral systems and complete host genomes, such studies can lead to a re-classification of virus families according to the host machineries they hijack, and could change our view on anti-viral treatments, focussing on the host instead of on the pathogen.