1887

Abstract

Recently, we have shown that influenza virus budding in MDCK cells is regulated by metabolic inhibitors of ATP and ATP analogues (Hui & Nayak, 290, 329–341, 2001). In this report, we demonstrate that G protein signalling stimulators such as sodium fluoride, aluminium fluoride, compound 48/80 and mastoparan stimulated the budding and release of influenza virus. In contrast, G protein signalling blockers such as suramin and NF023 inhibited virus budding. Furthermore, in filter-grown lysophosphatidylcholine-permeabilized virus-infected MDCK cells, membrane-impermeable GTP analogues, such as guanosine 5’--(3-thiotriphosphate) or 5’-guanylylimidodiphosphate caused an increase in virus budding, which could be competitively inhibited by adding an excess of GTP. These results suggest that the G protein is involved in the regulation of influenza virus budding. We also determined the role of different protein kinases in influenza virus budding. We observed that specific inhibitors or activators of protein kinase A (H-89 and 8-bromoadenosine 3’,5’-cyclic monophosphate) or of protein kinase C (bisindolylmaleimide I and Ro-32-0432) or of phosphatidylinositol 3-kinase (LY294002 and wortmannin) did not affect influenza virus budding. However, the casein kinase 2 (CK2) inhibitor 5,6-dichloro-1-β-D-ribofuranosylbenzimidazole decreased virus budding. We further observed an increase in the CK2 activity during the replication cycle of influenza virus, although Western blot analysis did not reveal any increase in the amount of CK2 protein in virus-infected cells. Also, in digitonin-permeabilized MDCK cells, the introduction of CK2 substrate peptides caused a down-regulation of virus budding. These results suggest that CK2 activity also regulates influenza virus budding.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-12-3055
2002-12-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/12/0833055a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-12-3055&mimeType=html&fmt=ahah

References

  1. Allende J. E., Allende C. C. 1995; Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB Journal 9:313–323
    [Google Scholar]
  2. Almond J. W., Felsenreich V. 1982; Phosphorylation of the nucleoprotein of an avian influenza virus. Journal of General Virology 60:295–305
    [Google Scholar]
  3. Arni S., Keilbaugh S. A., Ostermeyer A. G., Brown D. A. 1998; Association of GAP-43 with detergent-resistant membranes requires two palmitoylated cysteine residues. Journal of Biological Chemistry 273:28478–28485
    [Google Scholar]
  4. Avalos R. T., Zhang Y., Nayak D. P. 1997; Association of influenza virus NP and M1 proteins with cytoskeletal elements in influenza virus-infected cells. Journal of Virology 71:2947–2958
    [Google Scholar]
  5. Barman S., Nayak D. P. 2000; Analysis of the transmembrane domain of influenza virus neuraminidase, a type II transmembrane glycoprotein, for apical sorting and raft association. Journal of Virology 74:6538–6545
    [Google Scholar]
  6. Barman S., Ali A., Hui E. K.-W., Adhikary L., Nayak D. P. 2001; Transport of viral proteins to the apical membranes and interaction of matrix proteins with glycoproteins in the assembly of influenza viruses. Virus Research 77:61–69
    [Google Scholar]
  7. Beindl W., Mitterauer T., Hohenegger M., Ijzerman A. P., Nanoff C., Freissmuth M. 1996; Inhibition of receptor/G protein coupling by suramin analogues. Molecular Pharmacology 50:415–423
    [Google Scholar]
  8. Bigay J., Deterre P., Pfister C., Chabre M. 1985; Fluoroaluminates activate transducin-GDP by mimicking the γ-phosphate of GTP in its binding site. FEBS Letters 191:181–185
    [Google Scholar]
  9. Brewer C. B., Roth M. G. 1995; Polarized exocytosis in MDCK cells is regulated by phosphorylation. Journal of Cell Science 108:789–796
    [Google Scholar]
  10. Bui M., Wills E., Helenius A., Whittaker G. R. 2000; The role of influenza virus M1 in nuclear export of viral RNPs. Journal of Virology 74:1781–1786
    [Google Scholar]
  11. Cavalli V., Corti M., Gruenberg J. 2001; Endocytosis and signaling cascades: a close encounter. FEBS Letters 498:190–196
    [Google Scholar]
  12. Ceresa B. P., Schmid S. L. 2000; Regulation of signal transduction by endocytosis. Current Opinion in Cell Biology 12:204–210
    [Google Scholar]
  13. Cheng H. C., Kemp B. E., Pearson R. B., Smith A. J., Misconi L., Van Patter S. M., Walsh D. A. 1986; A potent synthetic peptide inhibitor of the camp-dependent protein kinase. Journal of Biological Chemistry 261:989–992
    [Google Scholar]
  14. Cockcroft S., Gomperts B. D. 1985; Role of guanine nucleotide regulatory binding proteins in the activation of polyphosphoinositide phosphodiesterase. Nature 314:534–536
    [Google Scholar]
  15. Dowrick P., Kenworthy P., McCann B., Warn R. 1993; Circular ruffle formation and closure lead to macropinocytosis in hepatocyte growth factor/scatter factor treated cells. European Journal of Cell Biology 61:44–53
    [Google Scholar]
  16. Eker P., Holm P. K., van Deurs B., Sandvig K. 1994; Selective regulation of apical endocytosis in polarized Madin-Darby canine kidney cells by mastoparan and cAMP. Journal of Biological Chemistry 269:18607–18615
    [Google Scholar]
  17. Esparís-Ogando A., Zurzolo C., Rodriguez-Boulan E. 1994; Permeabilization of MDCK cells with cholesterol binding agents: dependence on substratum and confluency. American Journal of Physiology 267:C166–C176
    [Google Scholar]
  18. Faust M., Montenarh M. 2000; Subcellular localization of protein kinase CK2: a key to its function?. Cell and Tissue Research 301:329–340
    [Google Scholar]
  19. Freed E. O. 2002; Viral late domains. Journal of Virology 76:4679–4687
    [Google Scholar]
  20. Freissmuth M., Boehm S., Beindl W., Nickel P., Ijzerman A. P., Hohenegger M., Nanoff C. 1996; Suramin analogues as subtype-selective G protein inhibitors. Molecular Pharmacology 49:602–611
    [Google Scholar]
  21. Garcia J. G. N., Dominguez J., English D. 1991; Sodium fluoride induces phosphoinositide hydrolysis, Ca2+ mobilization and prostacyclin synthesis in cultured human endothelium: further evidence for regulation by a pertussis toxin-insensitive guanine nucleotide-binding protein. American Journal of Respiratory Cell and Molecular Biology 5:113–124
    [Google Scholar]
  22. Geiss G. K., An M. C., Bumgarner R. E., Hammersmark E., Cunningham D., Katze M. G. 2001; Global impact of influenza virus on cellular pathways is mediated by both replication-dependent and -independent events. Journal of Virology 75:4321–4331
    [Google Scholar]
  23. Gómez-Puertas P., Albo C., Pérez-Pastrana E., Vivo A., Portela A. 2000; Influenza virus matrix protein is the major driving force in virus budding. Journal of Virology 74:11538–11547
    [Google Scholar]
  24. Gregoriades A., Christie T., Markarian K. 1984; The membrane (M1) protein of influenza virus occurs in two forms and is a phosphoprotein. Journal of Virology 49:229–235
    [Google Scholar]
  25. Gregoriades A., Guzman G. G., Paoletti E. 1990; The phosphorylation of the integral membrane (M1) protein of influenza virus. Virus Research 16:27–41
    [Google Scholar]
  26. Hansen S. H., Casanova J. E. 1994; Gsα stimulates transcytosis and apical secretion in MDCK cells through cAMP and protein kinase A. Journal of Cell Biology 126:677–687
    [Google Scholar]
  27. Helmreich E. J. M. 2001; Signal transduction pathways through heterotrimeric G proteins: transmission of hormonal and sensory signals. In The Biochemistry of Cell Signalling pp 76–101 Edited by Helmreich E. J. M. Oxford: Oxford University Press;
    [Google Scholar]
  28. Higashijima T., Burnier J., Ross E. M. 1990; Regulation of Gi and Go by mastoparan, related amphiphilic peptides and hydrophobic amines. Journal of Biological Chemistry 265:14176–14186
    [Google Scholar]
  29. Holsinger L. J., Shaughnessy M. A., Micko A., Pinto L. H., Lamb R. A. 1995; Analysis of the posttranslational modifications of the influenza virus M2 protein. Journal of Virology 69:1219–1225
    [Google Scholar]
  30. House C., Kemp B. E. 1987; Protein kinase C contains a pseudosubstrate prototope in its regulatory domain. Science 238:1726–1728
    [Google Scholar]
  31. Huang K.-P., Huang F. L. 1991; Purification and analysis of protein kinase C isozymes. Methods in Enzymology 200:241–252
    [Google Scholar]
  32. Hui E. K.-W. 2002; Virion-associated protein kinases. Cellular and Molecular Life Sciences 59:920–931
    [Google Scholar]
  33. Hui E. K.-W., Nayak D. P. 2001; Role of ATP in influenza virus budding. Virology 290:329–341
    [Google Scholar]
  34. Hui E. K.-W., Yung B. Y.-M. 1992; Protein kinase C activity during sphinganine potentiation of retinoic acid-induced differentiation in a human leukemia cell line (HL-60. Life Sciences 51:415–422
    [Google Scholar]
  35. Ikonen E., Parton R. G., Lafont F., Simons K. 1996; Analysis of the role of p200-containing vesicles in post-Golgi traffic. Molecular Biology of the Cell 7:961–974
    [Google Scholar]
  36. Kistner O., Muller H., Becht H., Scholtissek C. 1985; Phosphopeptide fingerprints of nucleoproteins of various influenza A virus strains grown in different host cells. Journal of General Virology 66:465–472
    [Google Scholar]
  37. Kistner O., Muller K., Scholtissek C. 1989; Differential phosphorylation of the nucleoprotein of influenza A viruses. Journal of General Virology 70:2421–2431
    [Google Scholar]
  38. Koch G., Haberman B., Mohr C., Just I., Aktories K. 1991; Interaction of mastoparan with the low molecular mass GTP-binding proteins rho/rac. FEBS Letters 291:336–340
    [Google Scholar]
  39. Kurokawa M., Ochiai H., Nakajima K., Niwayama S. 1990; Inhibitory effect of protein kinase C inhibitor on the replication of influenza type A virus. Journal of General Virology 71:2149–2155
    [Google Scholar]
  40. Latham T., Galarza J. M. 2001; Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. Journal of Virology 75:6154–6165
    [Google Scholar]
  41. Luban J. 2001; HIV-1 and Ebola virus: the getaway driver nabbed. Nature Medicine 7:1278–1280
    [Google Scholar]
  42. Ludwig S., Pleschka S., Wolff T. 1999; A fatal relationship – influenza virus interactions with the host cell. Viral Immunology 12:175–196
    [Google Scholar]
  43. Marin O., Meggio F., Pinna L. A. 1994; Design and synthesis of two new peptide substrates for the specific and sensitive monitoring of casein kinase-1 and -2. Biochemical and Biophysical Research Communication 198:898–905
    [Google Scholar]
  44. Martin K., Helenius A. 1991; Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67:117–130
    [Google Scholar]
  45. Moffett S., Brown D. A., Linder M. E. 2000; Lipid-dependent targeting of G proteins into rafts. Journal of Biological Chemistry 275:2191–2198
    [Google Scholar]
  46. Mousli M., Bronner C., Landry Y., Bockaert J., Rouot B. 1990; Direct activation of GTP-binding regulatory proteins (G-proteins) by substance P and compound 48/80. FEBS Letters 259:260–262
    [Google Scholar]
  47. Nayak D. P. 1996; A look at assembly and morphogenesis of orthomyxo- and paramyxoviruses. ASM News 62:411–414
    [Google Scholar]
  48. Nayak D. P. 2000; Virus morphology, replication and assembly. In Viral Ecology pp 64–123 Edited by Hurst C. J. London: Academic Press;
    [Google Scholar]
  49. Nayak D. P., Barman S. 2002; Role of lipid rafts in virus assembly and budding. Advances in Virus Research 58:1–28
    [Google Scholar]
  50. Nayak D. P., Hui E. K.-W. 2002; Assembly and morphogenesis of influenza viruses. Recent Research Developments in Virology 4:35–54
    [Google Scholar]
  51. Neumann G., Castrucci M. R., Kawaoka Y. 1997; Nuclear import and export of influenza virus nucleoprotein. Journal of Virology 71:9690–9700
    [Google Scholar]
  52. Patnaik A., Chau V., Wills J. W. 2000; Ubiquitin is part of the retrovirus budding machinery. Proceedings of the National Academy of Sciences, USA 97:13069–13074
    [Google Scholar]
  53. Pears C. J. 1996; Role of the protein kinase C gene family in the regulation of cell function. In Protein Phosphorylation in Cell Growth Regulation pp 111–133 Edited by Clemens M. J. New York & London: Harwood Academic Publishers;
    [Google Scholar]
  54. Perales B., Sanz-Ezquerro S., Gastaminza P., Ortega J., Santarén J. F., Ortín J., Nieto A. 2000; The replication activity of influenza virus polymerase is linked to the capacity of the PA subunit to induce proteolysis. Journal of Virology 74:1307–1312
    [Google Scholar]
  55. Perich J. W., Meggio M., Reynolds E. C., Marin O., Pinna L. A. 1992; Role of phosphorylated aminoacyl residues in generating atypical consensus sequences which are recognized by casein kinase-2 but not by casein kinase-1. Biochemistry 31:5893–5897
    [Google Scholar]
  56. Petri T., Dimmock N. J. 1981; Phosphorylation of influenza virus nucleoprotein in vivo. Journal of General Virology 57:185–190
    [Google Scholar]
  57. Petri T., Patterson S., Dimmock N. J. 1982; Polymorphism of the NS1 protein of type A influenza virus. Journal of General Virology 61:217–231
    [Google Scholar]
  58. Pimplikar S. W., Simons K. 1993; Regulation of apical transport in epithelial cells by a Gs class of heterotrimeric G protein. Nature 362:456–458
    [Google Scholar]
  59. Pimplikar S. W., Ikonen E., Simons K. 1994; Basolateral protein transport in streptolysin O-permeabilized MDCK cells. Journal of Cell Biology 125:1025–1035
    [Google Scholar]
  60. Pleschka S., Wolff T., Ehrhardt C., Hobom G., Planz O., Rapp U. R., Ludwig S. 2001; Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nature Cell Biology 3:301–305
    [Google Scholar]
  61. Portela A., Digard P. 2002; The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. Journal of General Virology 83:723–734
    [Google Scholar]
  62. Reinhardt J., Wolff T. 2000; The influenza A virus M1 protein interacts with the cellular receptor of activated C kinase (RACK) 1 and can be phosphorylated by protein kinase C. Veterinary Microbiology 74:87–100
    [Google Scholar]
  63. Richardson J. C., Akkina R. K. 1991; NS2 protein of influenza virus is found in purified virus and phosphorylated in infected cells. Archives of Virology 116:69–80
    [Google Scholar]
  64. Ridley A. J. 1994; Membrane ruffling and signal transduction. BioEssays 16:321–327
    [Google Scholar]
  65. Ridley A. J. 2001; Rho protein, PI 3-kinase and monocyte/macrophage motility. FEBS Letters 498:168–171
    [Google Scholar]
  66. Root C. N., Wills E. G., McNair L. L., Whittaker G. R. 2000; Entry of influenza viruses into cells is inhibited by a highly specific protein kinase C inhibitor. Journal of General Virology 81:2697–2705
    [Google Scholar]
  67. Sanz-Ezquerro J. J., Férnandez Santarén J., Sierra T., Aragón T., Ortega J., Ortín J., Smith G. L., Nieto A. 1998; The PA influenza virus polymerase subunit is a phosphorylated protein. Journal of General Virology 79:471–478
    [Google Scholar]
  68. Scheiffele P., Rietveld A., Wilk T., Simons K. 1999; Influenza viruses select ordered lipid domains during budding from the plasma membrane. Journal of Biological Chemistry 274:2038–2044
    [Google Scholar]
  69. Terry N., van Montagu M., Inze D. 1995; GTP-binding proteins in plant. In Guidebook to Small GTPase pp 32–38 Edited by Zerial M., Huber L. A. Oxford: Oxford University Press;
    [Google Scholar]
  70. Tucker S. P., Penn C. R., McCauley J. W. 1990; Characterisation of the influenza virus associated protein kinase and its resemblance to casein kinase II. Virus Research 18:243–262
    [Google Scholar]
  71. Vogel U., Kunerl M., Scholtissek C. 1994; Influenza A virus late mRNAs are specifically retained in the nucleus in the presence of a methyltransferase or a protein kinase inhibitor. Virology 198:227–233
    [Google Scholar]
  72. Yung B. Y.-M., Hsiao T.-F., Wei L. L.-L., Hui E. K.-W. 1994; Sphinganine potentiation of dimethyl sulfoxide-induced granulocytic differentiation, increase of alkaline phosphatase activity and decrease of protein kinase C activity in a human leukemia cell line (HL-60. Biochemical and Biophysical Research Communications 199:888–896
    [Google Scholar]
  73. Zhang J., Pekosz A., Lamb R. A. 2000; Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. Journal of Virology 74:4635–4644
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-12-3055
Loading
/content/journal/jgv/10.1099/0022-1317-83-12-3055
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error