Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis

Journal of Virology

Volumn 76, Issue 20, 2002, Pages 10455-10464

  Sieczkarski, Sara B ^a   Whittaker, Gary R ^a  

^a Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPROMAZINE; CLATHRIN; GENISTEIN; LIGAND; METHYL BETA CYCLODEXTRIN; NYSTATIN; POTASSIUM; PROTEIN; TRANSFERRIN;

ARTICLE; CAVEOLA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; INFLUENZA VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS INFECTION;

ANIMALS; CALCIUM-BINDING PROTEINS; CATTLE; CAVEOLAE; CELL LINE; CHLORPROMAZINE; CLATHRIN; ENDOCYTOSIS; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; INFLUENZA A VIRUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; PHOSPHOPROTEINS; POTASSIUM; RECOMBINANT FUSION PROTEINS; SEMLIKI FOREST VIRUS; TRANSFECTION; TRANSFERRIN;

EID: 0036784565     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.76.20.10455-10464.2002     Document Type: Article

References (59)

1. Ahn, A., D. L. Gibbons, and M. Kielian. 2002. The fusion peptide of Semliki Forest virus associates with sterol-rich membrane domains. J. Virol. 76: 3267-3275.
2. Bayer, N., D. Schober, M. Huttinger, D. Blaas, and R. Fuchs. 2001. Inhibition of clathrin-dependent endocytosis has multiple effects on human rhinovirus serotype 2 cell entry. J. Biol. Chem. 276:3952-3962.
3. Benmerah, A., M. Bayrou, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112:1303-1311.
4. Benmerah, A., B. Begue, A. Dautry-Varsat, and N. Cerf-Bensussan. 1996. The ear of alpha-adaptin interacts with the COOH-terminal domain of the Eps 15 protein. J. Biol. Chem. 271:12111-12116.
5. Benmerah, A., J. Gagnon, B. Begue, B. Megarbane, A. Dautry-Varsat, and N. Cerf-Bensussan. 1995. The tyrosine kinase substrate eps15 is constitutively associated with the plasma membrane adaptor AP-2. J. Cell Biol. 131:1831-1838.
6. Benmerah, A., C. Lamaze, B. Begue, S. L. Schmid, A. Dautry-Varsat, and N. Cerf-Bensussan. 1998. AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol. 140:1055-1062.
7. Benmerah, A., V. Poupon, N. Cerf-Bensussan, and A. Dautry-Varsat. 2000. Mapping of Eps15 domains involved in its targeting to clathrin-coated pits. J. Biol. Chem. 275:3288-3295.
8. Bishop, N. E. 1997. An update on non-clathrin coated endocytosis. Rev. Med. Virol. 7:199-207.
9. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976.
10. Brodsky, F. M., C. Y. Chen, C. Knuehl, M. C. Towler, and D. E. Wakeham. 2001. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17:517-568.
11. Bui, M., G. Whittaker, and A. Helenius. 1996. Effect of M1 protein and low pH on nuclear transport of influenza virus ribonucleoproteins. J. Virol. 70:8391-8401.
12. Carbone, R., S. Fre, G. Iannolo, F. Belleudi, P. Mancini, P. G. Pelicci, M. R. Torrisi, and P. P. Di Fiore. 1997. eps15 and eps15R are essential components of the endocytic pathway. Cancer Res. 57:5498-5504.
13. Doxsey, S. J., F. M. Brodsky, G. S. Blank, and A. Helenius. 1987. Inhibition of endocytosis by anti-clathrin antibodies. Cell 50:453-463.
14. Fazioli, F., L. Minichiello, B. Matoskova, W. T. Wong, and P. P. Di Fiore. 1993. eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol. Cell. Biol. 13:5814-5828.
15. Gold, E. S., D. M. Underhill, N. S. Morrissette, J. Guo, M. A. McNiven, and A. Aderem. 1999. Dynamin 2 is required for phagocytosis in macrophages. J. Exp. Med. 190:1849-1856.
16. Guinea, R., and L. Carrasco. 1995. Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J. Virol. 69:2306-2312.
17. Helenius, A., B. Morein, E. Fries, K. Simons, P. Robinson, V. Schirrmacher, C. Terhorst, and J. L. Strominger. 1978. Human (HLA-A and HLA-B) and murine (H-2K and H-2D) histocompatibility antigens are cell surface receptors for Semliki Forest virus. Proc. Natl. Acad. Sci. USA 75:3846-3850.
18. Henley, J. R., E. W. A. Krueger, B. J. Oswald, and M. A. McNiven. 1998. Dynamin-mediated internalization of caveolae. J. Cell Biol. 141:85-99.
19. Hernandez, L. D., L. R. Hoffman, T. G. Wolfsberg, and J. M. White. 1996. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12:627-661.
20. Hinshaw, J. E. 2000. Dynamin and its role in membrane fission. Annu. Rev. Cell Dev. Biol. 16:483-519.
21. Iannolo, G., A. E. Salcini, I. Gaidarov, O. B. Goodman, Jr., J. Baulida, G. Carpenter, P. G. Pelicci, P. P. Di Fiore, and J. H. Keen. 1997. Mapping of the molecular determinants involved in the interaction between eps15 and AP-2. Cancer Res. 57:240-245.
22. Johannes, L., and C. Lamaze. 2002. Clathrin-dependent or not: is it still the question? Traffic 3:443-451.
23. Joki-Korpela, P., V. Marjomaki, C. Krogerus, J. Heino, and T. Hyypia. 2001. Entry of human parechovirus 1. J. Virol. 75:1958-1967.
24. Jones, S. M., K. E. Howell, J. R. Henley, H. Cao, and M. A. McNiven. 1998. Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science 279:573-577.
25. Krizanová, O., F. Ciampor, and P. Verber. 1982. Influence of chlorpromazine on the replication of influenza virus in chick embryo fibroblasts. Acta Virol. 26:209-216.
26. Lamaze, C., A. Dujeancourt, T. Baba, C. G. Lo, A. Benmerah, and A. Dautry-Varsat. 2001. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7:661-671.
27. Larkin, J. M., M. S. Brown, J. L. Goldstein, and R. G. Anderson. 1983. Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell 33:273-285.
28. Madshus, I. H., K. Sandvig, S. Olsnes, and B. van Deurs. 1987. Effect of reduced endocytosis induced by hypotonic shock and potassium depletion on the infection of Hep 2 cells by picornaviruses. J. Cell. Physiol. 131:14-22.
29. Maniak, M. 2001. Macropinocytosis, p. 78-93. In M. Marsh (ed.), Endocytosis. Oxford University Press, Oxford, United Kingdom.
30. Marsh, M., and A. Helenius. 1980. Adsorptive endocytosis of Semliki Forest virus. J. Mol. Biol. 142:439-454.
31. Marsh, M., and A. Helenius. 1989. Virus entry into animal cells. Adv. Virus Res. 36:107-151.
32. Marsh, M., and H. T. McMahon. 1999. The structural era of endocytosis. Science 285:215-220.
33. Matlin, K. S., H. Reggio, A. Helenius, and K. Simons. 1981. Infectious entry pathway of influenza virus in a canine kidney cell line. J. Cell Biol. 91:601-613.
34. Matlin, K. S., H. Reggio, A. Helenius, and K. Simons. 1982. Pathway of vesicular stomatitis virus leading to infection. J. Mol. Biol. 156:609-631.
35. Miller, N., and L. M. Hutt-Fletcher. 1992. Epstein-Barr virus enters B cells and epithelial cells by different routes. J. Virol. 66:3409-3414.
36. Neufeld, E. B., A. M. Cooney, J. Pitha, E. A. Dawidowicz, N. K. Dwyer, P. G. Pentchev, and E. J. Blanchette-Mackie. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271:21604-21613.
37. Nichols, B. J., A. K. Kenworthy, R. S. Polishchuk, R. Lodge, T. H. Roberts, K. Hirschberg, R. D. Phair, and J. Lippincott-Schwartz. 2001. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153:529-541.
38. Nichols, B. J., and J. Lippincott-Schwartz. 2001. Endocytosis without clathrin coats. Trends Cell Biol. 11:406-412.
39. Nicoziani, P., F. Vilhardt, A. Llorente, L. Hilout, P. J. Courtoy, K. Sandvig, and B. van Deurs. 2000. Role for dynamin in late endosome dynamics and trafficking of the cation-independent mannose 6-phosphate receptor. Mol. Biol. Cell 11:481-495.
40. Parton, R. G., B. Joggerst, and K. Simons. 1994. Regulated internalization of caveolae. J. Cell Biol. 127:1199-1215.
41. Pelkmans, L., K. J., and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular transport pathway to the ER. Nat. Cell Biol. 3:473-483.
42. Pho, M. T., A. Ashok, and W. J. Atwood. 2000. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J. Virol. 74:2288-2292.
43. Root, C. R., E. G. Wills, L. L. McNair, and G. R. Whittaker. 2000. Entry of influenza viruses into cells is inhibited by a highly specific protein kinase C inhibitor. J. Gen. Virol. 81:2697-2705.
44. Rothberg, K. G., J. E. Heuser, W. C. Donzell, Y. S. Ying, J. R. Glenney, and R. G. Anderson. 1992. Caveolin, a protein component of caveolae membrane coats. Cell 68:673-682.
45. Roy, A.-M. M., J. S. Parker, C. R. Parrish, and G. R. Whittaker. 2000. Early stages of influenza virus entry into Mv-1 lung cells: involvement of dynamin. Virology 267:17-28.
46. Russell, D. G., and M. Marsh. 2001. Endocytosis in pathogen entry and replication, p. 247-280. In M. Marsh (ed.), Endocytosis. Oxford University Press, Oxford, United Kingdom.
47. Salcini, A. E., S. Confalonieri, M. Doria, E. Santolini, E. Tassi, O. Minenkova, G. Cesareni, P. G. Pelicci, and P. P. Di Fiore, 1997. Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev. 11:2239-2249.
48. Scheiffele, P., A. Rietveld, T. Wilk, and K. Simons. 1999. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274:2038-2044.
49. Scheiffele, P., M. G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16:5501-5508.
50. Schmid, S. L., M. A. McNiven, and P. De Camilli. 1998. Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10:504-512.
51. Shin, J. S., and S. N. Abraham. 2001. Caveolae as portals of entry for microbes. Microbes Infect. 3:755-761.
52. Sieczkarski, S. B., and G. R. Whittaker, 2002. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:1535-1545. (First published 28 March 2002; 10.1099/vir.0.18346-0.)
53. Skehel, J. J., T. Bizebard, P. A. Bullough, F. M. Hughson, M. Knossow, D. A. Steinhauer, S. A. Wharton, and D. C. Wiley. 1995. Membrane fusion by influenza virus. Cold Spring Harbor Symp. Quant. Biol. 55:573-580.
54. Skretting, G., M. L. Torgersen, B. van Deurs, and K. Sandvig. 1999. Endocytic mechanisms responsible for uptake of GPI-linked diphtheria toxin receptor. J. Cell Sci. 112:3899-3909.
55. Tebar, F., T. Sorkina, A. Sorkin, M. Ericsson, and T. Kirchhausen. 1996. Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J. Biol. Chem. 271:28727-28730.
56. Wang, K. S., R. J. Kuhn, E. G. Strauss, S. Ou, and J. H. Strauss. 1992. High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J. Virol. 66:4992-5001.
57. Wang, L. H., K. G. Rothberg, and R. G. Anderson. 1993. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 123:1107-1117.
58. White, J., J. Kartenbeck, and A. Helenius. 1982. Membrane fusion activity of influenza virus. EMBO J. 1:217-222.
59. Whittaker, G., I. Kemler, and A. Helenius. 1995. Hyperphosphorylation of mutant influenza virus matrix (MI) protein causes its retention in the nucleus. J. Virol. 69:439-445.