Differential infectious entry of human influenza A/NWS/33 virus (H1N1) in mammalian kidney cells

Virus Research

Volumn 155, Issue 1, 2011, Pages 221-230

  De Conto, Flora ^a   Covan, Silvia ^a   Arcangeletti, Maria Cristina ^a   Orlandini, Guido ^a   Gatti, Rita ^a   Dettori, Giuseppe ^a   Chezzi, Carlo ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

Endocytosis; Influenza virus A; Internalization inhibitors; Kidney cells; Nucleoprotein

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; ACTIN; CHLOROQUINE; CHLORPROMAZINE; CLATHRIN; NYSTATIN;

ANIMAL CELL; ARTICLE; CAVEOLA; CELL STRAIN; ENDOCYTOSIS; EXPERIMENTAL DOG; INFECTION SENSITIVITY; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; KIDNEY CELL; NEWBORN; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN; SWINE; VIRUS ENTRY; VIRUS REPLICATION;

ANIMALS; CELL LINE; DOGS; ENDOCYTOSIS; HAPLORHINI; INFLUENZA A VIRUS, H1N1 SUBTYPE; KIDNEY; SWINE; VIRUS INTERNALIZATION;

INFLUENZA A VIRUS; INFLUENZAVIRUS A; MAMMALIA; ORTHOMYXOVIRIDAE; SIMIAE; SUIDAE;

EID: 78650533541     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2010.10.008     Document Type: Article

References (56)

1. Arcangeletti M.C., De Conto F., Ferraglia F., Pinardi F., Gatti R., Orlandini G., Covan S., Motta F., Rodighiero I., Dettori G., Chezzi C. Host-cell-dependent role of actin cytoskeleton during the replication of a human strain of influenza A virus. Arch. Virol. 2008, 153:1209-1221.
2. Armstrong R.T., Kushnir A.S., White J.M. The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J. Cell Biol. 2000, 151:425-437.
3. Avalos R.T., Yu Z., Nayak D.P. Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells. J. Virol. 1997, 71:2947-2958.
4. Barman S., Nayak D.P. Lipid raft disruption by cholesterol depletion enhances influenza A virus budding from MDCK cells. J. Virol. 2007, 81:12169-12178.
5. Brügger B., Krautkrämer E., Tibroni N., Munte C.E., Rauch S., Leibrecht I., Glass B., Breuer S., Geyer M., Kräusslich H.G., Kalbitzer H.R., Wieland F.T., Fackler O.T. Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains. Retrovirology 2007, 4:70.
6. Chatterjee P.K., Eng C.H., Kielian M. Novel mutations that control the sphingolipid and cholesterol dependence of the Semliki forest virus fusion protein. J. Virol. 2002, 76:12712-12722.
7. Chernomordik L.V., Frolov V.A., Leikina E., Bronk P., Zimmerberg J. The pathway of membrane fusion catalyzed by influenza hemagglutinin: restriction of lipids, hemifusion, and lipidic fusion pore formation. J. Cell Biol. 1998, 140:1369-1382.
8. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
9. Couet J., Li S., Okamoto T., Ikezu T., Lisanti M.P. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 1997, 272:6525-6533.
10. Couet J., Belanger M.M., Roussel E., Drolet M.C. Cell biology of caveolae and caveolin. Adv. Drug Deliv. Rev. 2001, 49:223-235.
11. Coyne C.B., Kim K.S., Bergelson J.M. Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. EMBO J. 2007, 26:4016-4028.
12. Damke H., Baba T., van der Bliek A.M., Schmid S.L. Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol. 1995, 131:69-80.
13. Ehrhardt C., Marjuki H., Wolff T., Nurnberg B., Planz O., Pleschka S., Ludwig S. Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell. Microbiol. 2006, 8:1336-1348.
14. Francis S.A., Kelly J.M., McCormack J., Rogers R.A., Lai J., Schneeberger E.E., Lynch R.D. Rapid reduction of MDCK cell cholesterol by methyl-beta-cyclodextrin alters steady state transepithelial electrical resistance. Eur. J. Cell Biol. 1999, 78:473-484.
15. Fujimoto L.M., Roth R., Heuser J.E., Schmid S.L. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 2000, 1:161-171.
16. Gujuluva C.N., Kundu A., Murti K.G., Nayak D.P. Abortive replication of influenza virus A/WSN/33 in HeLa229 cells: defective viral entry and budding processes. Virology 1994, 204:491-505.
17. Hambleton S., Steinberg S.P., Gershon M.D., Gershon A.A. Cholesterol dependence of varicella-zoster virion entry into target cells. J. Virol. 2007, 81:7548-7558.
18. Imhoff H., von Messling V., Herrler G., Haas L. Canine distemper virus infection requires cholesterol in the viral envelope. J. Virol. 2007, 81:4158-4165.
19. Jafri M., Donnelly B., McNeal M., Ward R., Tiao G. MAPK signaling contributes to rotaviral-induced cholangiocyte injury and viral replication. Surgery 2007, 142:192-201.
20. Jones A.T. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J. Cell. Mol. Med. 2007, 11:670-684.
21. 2+ induces macropinocytosis via F-actin depolymerization during growth cone collapse. Mol. Cell Neurosci. 2009, 40:27-38.
22. König R., Stertz S., Zhou Y., Inoue A., Hoffmann H.H., Bhattacharyya S., Alamares J.G., Tscherne D.M., Ortigoza M.B., Liang Y., Gao Q., Andrews S.E., Bandyopadhyay, De Jesus P., Tu B.P., Pache L., Shih C., Orth A., Bonamy G., Miraglia L., Ideker T., García-Sastre A., Young J.A., Palese P., Shaw M.L., Chanda S.K. Human host factors required for influenza virus replication. Nature 2010, 463:813-817.
23. Lakadamyali M., Rust M.J., Zhuang X. Endocytosis of influenza viruses. Microbes Infect. 2004, 6:929-936.
24. Landlinger C., Salzer U., Prohaska R. Myristoylation of human LanC-like protein 2 (LANCL2) is essential for the interaction with the plasma membrane and the increase in cellular sensitivity to adriamycin. Biochim. Biophys. Acta 2006, 1758:1759-1767.
25. Leser G.P., Lamb R.A. Influenza virus assembly and budding in raft-derived microdomains: a quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 2005, 342:215-227.
26. Lu Y.E., Cassese T., Kielian M. The cholesterol requirement for sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J. Virol. 1999, 73:4272-4278.
27. Mannová P., Fang R., Wang H., Deng B., McIntosh M.W., Hanash S.M., Beretta L. Modification of host lipid raft proteome upon hepatitis C virus replication. Mol. Cell Proteomics 2006, 5:2319-2325.
28. Marjuki H., Yen H.L., Franks J., Webster R.G., Pleschka S., Hoffmann E. Higher polymerase activity of a human influenza virus enhances activation of the hemagglutinin-induced Raf/MEK/ERK signal cascade. J. Virol. 2007, 4:134.
29. Marsh M., Helenius A. Virus entry: open sesame. Cell 2006, 4:729-740.
30. Mayor S., Pagano R.E. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell. Biol. 2007, 8:603-612.
31. Melikyan G.B., Brener S.A., Ok D.C., Cohen F.S. Inner but not outer membrane leaflets control the transition from glycosylphosphatidylinositol-anchored influenza hemagglutinin-induced hemifusion to full fusion. J. Cell Biol. 1997, 136:995-1005.
32. Melikyan G.B., Markosyan R.M., Roth M.G., Cohen F.S. A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol. Biol. Cell. 2000, 11:3765-3775.
33. Mercer J., Helenius A. Virus entry by macropinocytosis. Nat. Cell Biol. 2009, 11:510-520.
34. Mercer J., Schelhaas M., Helenius A. Virus entry by endocytosis. Annu. Rev. Biochem. 2010, 79:803-833.
35. Nayak D.P., Hui E.K.W., Barman S. Assembly and budding of influenza virus. Virus Res. 2004, 106:147-165.
36. Nayak D.P., Balogun R.A., Yamada H., Zhou Z.H., Barman S. Influenza virus morphogenesis and budding. Virus Res. 2009, 143:147-161.
37. Nunes-Correia I., Eulálio A., Nir S., Pedroso de Lima M.C. Caveolae as an additional route for influenza virus endocytosis in MDCK cells. Cell. Mol. Biol. Lett. 2004, 9:47-60.
38. Ono A., Freed E.O. Role of lipid rafts in virus replication. Adv. Virus Res. 2005, 64:311-358.
39. Pelkmans L. Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim. Biophys. Acta 2005, 1746:295-304.
40. Pelkmans L. Viruses as probes for systems analysis of cellular signalling, cytoskeleton reorganization and endocytosis. Curr. Opin. Microbiol. 2005, 8:331-337.
41. Qiao H., Armstrong R.T., Melikyan G.B., Cohen F.S., White J.M. A specific point mutant at position 1 of the influenza hemagglutinin fusion peptide displays a hemifusion phenotype. Mol. Biol. Cell. 1999, 10:2759-2769.
42. Razani B., Lisanti M.P. Caveolins and caveolae: molecular and functional relationships. Exp. Cell Res. 2001, 271:36-44.
43. Roberts P.C., Compans R.W. Host cell dependence of viral morphology. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5746-5751.
44. Scheiffele P., Rietveld A., Wilk T., Simons K. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 1999, 274:2038-2044.
45. Sieczkarski S.B., Whittaker G.R. Influenza virus can enter and infect cells in the absence of clathrin-mediated endocytosis. J. Virol. 2002, 76:10455-10564.
46. Simpson-Holley M., Ellis D., Fisher D., Elton D., McCauley J., Digard P. A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 2002, 301:212-225.
47. Stray S.J., Cummings R.D., Air G.M. Influenza virus infection of desialylated cells. Glycobiology 2000, 10:649-658.
48. Stray S.J., Air G.M. Apoptosis by influenza viruses correlates with efficiency of viral mRNA synthesis. Virus Res. 2001, 77:3-17.
49. Sun X., Whittaker G.R. Role for influenza virus envelope cholesterol in virus entry and infection. J. Virol. 2003, 77:12543-12551.
50. Sun X., Whittaker G.R. Role of the actin cytoskeleton during influenza virus internalization into polarized epithelial cells. Cell. Microbiol. 2007, 9:1672-1682.
51. Tsai H.I., Tsai L.H., Chen M.Y., Chou Y.C. Cholesterol deficiency perturbs actin signaling and glutamate homeostasis in hippocampal astrocytes. Brain Res. 2006, 1104:27-38.
52. Verkade P., Harder T., Lafont F., Simons K. Induction of caveolae in the apical plasma membrane of Madin-Darby canine kidney cells. J. Cell. Biol. 2000, 148:727-739. (Erratum in: J. Cell. Biol. 2003. 163, 675).
53. Wang H., Jiang C. Influenza A virus H5N1 entry into host cells is through clathrin-dependent endocytosis. Sci. China C: Life Sci. 2009, 52:464-469.
54. Werden S.J., McFadden G. The role of cell signaling in poxvirus tropism: the case of the M-T5 host range protein of myxoma virus. Biochim. Biophys. Acta 2008, 1784:228-237.
55. Wielgosz M.M., Rauch D.A., Jones K.S., Ruscetti F.W., Ratner L. Cholesterol dependence of HTLV-I infection. AIDS Res. Hum. Retroviruses 2005, 21:43-50.
56. Yarar D., Waterman-Storer C.M., Schmid S.L. A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol. Biol. Cell. 2005, 16:964-975.