1887

Abstract

Avian leukosis virus (ALV) is an enveloped and oncogenic retrovirus. Avian leukosis caused by the members of ALV subgroups A, B and J has become one of the major problems challenging the poultry industry in China. However, the cellular factors such as signal transduction pathways involved in ALV infection are not well defined. In this study, our data demonstrated that ALV-J strain NX0101 infection in primary chicken embryo fibroblasts or DF-1 cells was correlated with the activity and phosphorylation of Akt. Akt activation was initiated at a very early stage of infection independently of NX0101 replication. The specific phosphatidylinositol 3-kinase (PI3K) inhibitors LY294002 or wortmannin could suppress Akt phosphorylation, indicating that NX0101-induced Akt phosphorylation is PI3K-dependent. ALV-A strain GD08 or ALV-B strain CD08 infection also demonstrated a similar profile of PI3K/Akt activation. Treatment of DF-1 cells with the drug 5-(N, N-hexamethylene) amiloride that inhibits the activity of chicken Na/H exchanger type 1 significantly reduced Akt activation induced by NX0101, but not by GD08 and CD08. Akt activation triggered by GD08 or CD08 was abolished by clathrin-mediated endocytosis inhibitor chlorpromazine. Receptor-mediated endocytosis inhibitor dansylcadaverine had a negligible effect on all ALV-induced Akt phosphorylation. Moreover, viral replication of ALV was suppressed by LY294002 in a dose-dependent manner, which was due to the inhibition of virus infection by LY294002. These data suggest that the activation of the PI3K/Akt signalling pathway by exogenous ALV infection plays an important role in viral entry, yet the precise mechanism remains under further investigation.

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2011-07-01
2019-10-17
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References

  1. Briand G. , Barbeau B. , Tremblay M. . ( 1997; ). Binding of HIV-1 to its receptor induces tyrosine phosphorylation of several CD4-associated proteins, including the phosphatidylinositol 3-kinase. . Virology 228:, 171–179. [CrossRef].[PubMed].
    [Google Scholar]
  2. Chai N. , Bates P. . ( 2006; ). Na+/H+ exchanger type 1 is a receptor for pathogenic subgroup J avian leukosis virus. . Proc Natl Acad Sci U S A 103:, 5531–5536. [CrossRef].[PubMed].
    [Google Scholar]
  3. Cheng Z. , Liu J. , Cui Z. , Zhang L. . ( 2010; ). Tumors associated with avian leukosis virus subgroup J in layer hens during 2007 to 2009 in China. . J Vet Med Sci 72:, 1027–1033. [CrossRef].[PubMed].
    [Google Scholar]
  4. Chu J. J. , Leong P. W. , Ng M. L. . ( 2006; ). Analysis of the endocytic pathway mediating the infectious entry of mosquito-borne flavivirus West Nile into Aedes albopictus mosquito (C6/36) cells. . Virology 349:, 463–475. [CrossRef].[PubMed].
    [Google Scholar]
  5. Coffin J. M. , Hughes S. H. , Varmus H. E. . ( 1997; ). Retroviruses. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  6. Cooray S. . ( 2004; ). The pivotal role of phosphatidylinositol 3-kinase-Akt signal transduction in virus survival. . J Gen Virol 85:, 1065–1076. [CrossRef].[PubMed].
    [Google Scholar]
  7. Cui Z. , Du Y. , Zhang Z. , Silva R. F. . ( 2003; ). Comparison of Chinese field strains of avian leukosis subgroup J viruses with prototype strain HPRS-103 and United States strains. . Avian Dis 47:, 1321–1330. [CrossRef].[PubMed].
    [Google Scholar]
  8. Diaz-Griffero F. , Hoschander S. A. , Brojatsch J. . ( 2002; ). Endocytosis is a critical step in entry of subgroup B avian leukosis viruses. . J Virol 76:, 12866–12876. [CrossRef].[PubMed].
    [Google Scholar]
  9. Diaz-Griffero F. , Jackson A. P. , Brojatsch J. . ( 2005; ). Cellular uptake of avian leukosis virus subgroup B is mediated by clathrin. . Virology 337:, 45–54. [CrossRef].[PubMed].
    [Google Scholar]
  10. Du Y. , Cui Z. , Qin A. , Silva R. F. , Lee L. F. . ( 2000; ). [Isolation of subgroup J avian leukosis viruses and their partial sequence comparison]. . Chin J Virol 16:, 341–346 (in Chinese).
    [Google Scholar]
  11. Ehrhardt C. , Marjuki H. , Wolff T. , Nürnberg B. , Planz O. , Pleschka S. , Ludwig S. . ( 2006; ). Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. . Cell Microbiol 8:, 1336–1348. [CrossRef].[PubMed].
    [Google Scholar]
  12. François F. , Klotman M. E. . ( 2003; ). Phosphatidylinositol 3-kinase regulates human immunodeficiency virus type 1 replication following viral entry in primary CD4+ T lymphocytes and macrophages. . J Virol 77:, 2539–2549. [CrossRef].[PubMed].
    [Google Scholar]
  13. Franke T. F. , Kaplan D. R. , Cantley L. C. . ( 1997; ). PI3K: downstream AKTion blocks apoptosis. . Cell 88:, 435–437. [CrossRef].[PubMed].
    [Google Scholar]
  14. Fujioka Y. , Tsuda M. , Hattori T. , Sasaki J. , Sasaki T. , Miyazaki T. , Ohba Y. . ( 2011; ). The Ras-PI3K signaling pathway is involved in clathrin-independent endocytosis and the internalization of influenza viruses. . PLoS ONE 6:, e16324. [CrossRef].[PubMed].
    [Google Scholar]
  15. Gong M. , Semus H. L. , Bird K. J. , Stramer B. J. , Ruddell A. . ( 1998; ). Differential selection of cells with proviral c-myc and c-erbB integrations after avian leukosis virus infection. . J Virol 72:, 5517–5525.[PubMed].
    [Google Scholar]
  16. Graf T. , Beug H. . ( 1978; ). Avian leukemia viruses: interaction with their target cells in vivo and in vitro . . Biochim Biophys Acta 516:, 269–299.[PubMed].
    [Google Scholar]
  17. Guntermann C. , Murphy B. J. , Zheng R. , Qureshi A. , Eagles P. A. , Nye K. E. . ( 1999; ). Human immunodeficiency virus-1 infection requires pertussis toxin sensitive G-protein-coupled signalling and mediates cAMP downregulation. . Biochem Biophys Res Commun 256:, 429–435. [CrossRef].[PubMed].
    [Google Scholar]
  18. Hale B. G. , Jackson D. , Chen Y. H. , Lamb R. A. , Randall R. E. . ( 2006; ). Influenza A virus NS1 protein binds p85beta and activates phosphatidylinositol-3-kinase signaling. . Proc Natl Acad Sci U S A 103:, 14194–14199. [CrossRef].[PubMed].
    [Google Scholar]
  19. Hayward W. S. , Neel B. G. , Astrin S. M. . ( 1981; ). Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. . Nature 290:, 475–480. [CrossRef].[PubMed].
    [Google Scholar]
  20. Kolokoltsov A. A. , Davey R. A. . ( 2004; ). Rapid and sensitive detection of retrovirus entry by using a novel luciferase-based content-mixing assay. . J Virol 78:, 5124–5132. [CrossRef].[PubMed].
    [Google Scholar]
  21. Lau C. , Wang X. , Song L. , North M. , Wiehler S. , Proud D. , Chow C. W. . ( 2008; ). Syk associates with clathrin and mediates phosphatidylinositol 3-kinase activation during human rhinovirus internalization. . J Immunol 180:, 870–880.[PubMed].[CrossRef]
    [Google Scholar]
  22. Li G. , D'Souza-Schorey C. , Barbieri M. A. , Roberts R. L. , Klippel A. , Williams L. T. , Stahl P. D. . ( 1995; ). Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. . Proc Natl Acad Sci U S A 92:, 10207–10211. [CrossRef].[PubMed].
    [Google Scholar]
  23. Li E. , Stupack D. , Klemke R. , Cheresh D. A. , Nemerow G. R. . ( 1998; ). Adenovirus endocytosis via alpha(v) integrins requires phosphoinositide-3-OH kinase. . J Virol 72:, 2055–2061.[PubMed].
    [Google Scholar]
  24. Linero F. N. , Scolaro L. A. . ( 2009; ). Participation of the phosphatidylinositol 3-kinase/Akt pathway in Junín virus replication in vitro . . Virus Res 145:, 166–170. [CrossRef].[PubMed].
    [Google Scholar]
  25. Livak K. J. , Schmittgen T. D. . ( 2001; ). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. . Methods 25:, 402–408. [CrossRef].[PubMed].
    [Google Scholar]
  26. Maas R. , van Zoelen D. , Oei H. , Claassen I. . ( 2006; ). Replacement of primary chicken embryonic fibroblasts (CEF) by the DF-1 cell line for detection of avian leucosis viruses. . Biologicals 34:, 177–181. [CrossRef].[PubMed].
    [Google Scholar]
  27. Mothes W. , Boerger A. L. , Narayan S. , Cunningham J. M. , Young J. A. . ( 2000; ). Retroviral entry mediated by receptor priming and low pH triggering of an envelope glycoprotein. . Cell 103:, 679–689. [CrossRef].[PubMed].
    [Google Scholar]
  28. Narayan S. , Barnard R. J. , Young J. A. . ( 2003; ). Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. . J Virol 77:, 1977–1983. [CrossRef].[PubMed].
    [Google Scholar]
  29. Orlowski J. , Grinstein S. . ( 2004; ). Diversity of the mammalian sodium/proton exchanger SLC9 gene family. . Pflugers Arch 447:, 549–565. [CrossRef].[PubMed].
    [Google Scholar]
  30. Putney L. K. , Barber D. L. . ( 2004; ). Expression profile of genes regulated by activity of the Na-H exchanger NHE1. . BMC Genomics 5:, 46. [CrossRef].[PubMed].
    [Google Scholar]
  31. Qin A. , Lee L. F. , Fadly A. , Hunt H. , Cui Z. . ( 2001; ). Development and characterization of monoclonal antibodies to subgroup J avian leukosis virus. . Avian Dis 45:, 938–945. [CrossRef].[PubMed].
    [Google Scholar]
  32. Rasheed S. . ( 1995; ). Retroviruses and oncogenes. . In The Retoviridae, pp. 293–408. Edited by Levy J. A. . . New York:: Plenum Press;.[CrossRef]
    [Google Scholar]
  33. Reed L. J. , Muench H. . ( 1938; ). A simple method of estimating fifty percent endpoints. . Am J Hyg 27:, 493–497.
    [Google Scholar]
  34. Saeed M. F. , Kolokoltsov A. A. , Freiberg A. N. , Holbrook M. R. , Davey R. A. . ( 2008; ). Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. . PLoS Pathog 4:, e1000141.[PubMed].[CrossRef]
    [Google Scholar]
  35. Schelling J. R. , Abu Jawdeh B. G. . ( 2008; ). Regulation of cell survival by Na+/H+ exchanger-1. . Am J Physiol Renal Physiol 295:, F625–F632. [CrossRef].[PubMed].
    [Google Scholar]
  36. Shin Y. K. , Liu Q. , Tikoo S. K. , Babiuk L. A. , Zhou Y. . ( 2007; a). Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenza A virus propagation. . J Gen Virol 88:, 942–950. [CrossRef].[PubMed].
    [Google Scholar]
  37. Shin Y. K. , Liu Q. , Tikoo S. K. , Babiuk L. A. , Zhou Y. . ( 2007; b). Influenza A virus NS1 protein activates the phosphatidylinositol 3-kinase (PI3K)/Akt pathway by direct interaction with the p85 subunit of PI3K. . J Gen Virol 88:, 13–18. [CrossRef].[PubMed].
    [Google Scholar]
  38. Skolnik E. Y. , Margolis B. , Mohammadi M. , Lowenstein E. , Fischer R. , Drepps A. , Ullrich A. , Schlessinger J. . ( 1991; ). Cloning of PI3 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases. . Cell 65:, 83–90. [CrossRef].[PubMed].
    [Google Scholar]
  39. Soares J. A. , Leite F. G. , Andrade L. G. , Torres A. A. , De Sousa L. P. , Barcelos L. S. , Teixeira M. M. , Ferreira P. C. , Kroon E. G. et al. ( 2009; ). Activation of the PI3K/Akt pathway early during vaccinia and cowpox virus infections is required for both host survival and viral replication. . J Virol 83:, 6883–6899. [CrossRef].[PubMed].
    [Google Scholar]
  40. Stoyanov B. , Volinia S. , Hanck T. , Rubio I. , Loubtchenkov M. , Malek D. , Stoyanova S. , Vanhaesebroeck B. , Dhand R. et al. ( 1995; ). Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. . Science 269:, 690–693. [CrossRef].[PubMed].
    [Google Scholar]
  41. Street A. , Macdonald A. , Crowder K. , Harris M. . ( 2004; ). The hepatitis C virus NS5A protein activates a phosphoinositide 3-kinase-dependent survival signaling cascade. . J Biol Chem 279:, 12232–12241. [CrossRef].[PubMed].
    [Google Scholar]
  42. Sun S. H. , Cui Z. Z. . ( 2007; ). Epidemiological and pathological studies of subgroup J avian leukosis virus infections in Chinese local “yellow” chickens. . Avian Pathol 36:, 221–226. [CrossRef].[PubMed].
    [Google Scholar]
  43. Sun M. , Fuentes S. M. , Timani K. , Sun D. , Murphy C. , Lin Y. , August A. , Teng M. N. , He B. . ( 2008; ). Akt plays a critical role in replication of nonsegmented negative-stranded RNA viruses. . J Virol 82:, 105–114. [CrossRef].[PubMed].
    [Google Scholar]
  44. Tiwari V. , Shukla D. . ( 2010; ). Phosphoinositide 3 kinase signalling may affect multiple steps during herpes simplex virus type-1 entry. . J Gen Virol 91:, 3002–3009. [CrossRef].[PubMed].
    [Google Scholar]
  45. Weiss R. A. . ( 1992; ). Cellular receptors and viral glycoproteins involved in retrovirus entry. . In The Retroviridae, pp. 1–72. Edited by Levy J. A. . . New York:: Plenum Press;.
    [Google Scholar]
  46. Wong W. R. , Chen Y. Y. , Yang S. M. , Chen Y. L. , Horng J. T. . ( 2005; ). Phosphorylation of PI3K/Akt and MAPK/ERK in an early entry step of enterovirus 71. . Life Sci 78:, 82–90. [CrossRef].[PubMed].
    [Google Scholar]
  47. Xu B. , Dong W. , Yu C. , He Z. , Lv Y. , Sun Y. , Feng X. , Li N. , Lee L. F. , Li M. . ( 2004; ). Occurrence of avian leukosis virus subgroup J in commercial layer flocks in China. . Avian Pathol 33:, 13–17. [CrossRef].[PubMed].
    [Google Scholar]
  48. Yang F. , Xian R. R. , Li Y. , Polony T. S. , Beemon K. L. . ( 2007; ). Telomerase reverse transcriptase expression elevated by avian leukosis virus integration in B cell lymphomas. . Proc Natl Acad Sci U S A 104:, 18952–18957. [CrossRef].[PubMed].
    [Google Scholar]
  49. Young J. A. . ( 1998; ). Avian leukosis virus-receptor interactions. . Avian Pathol 27:, S21–S25. [CrossRef]
    [Google Scholar]
  50. Zhang X. , Lai H. , Zhang H. , Xu C. , Liao M. , Xin C. , Cao W. . ( 2009; ). [Isolation and identification of CD08 strain of avian leukosis virus associated with hemangioma]. . Chin J Vet Med 45:, 8–10 (in Chinese).
    [Google Scholar]
  51. Zhang Q. C. , Zhao D. M. , Guo H. J. , Cui Z. Z. . ( 2010; ). Isolation and identification of a subgroup A avian leukosis virus from imported meat-type grand-parent chickens. . Virol Sin 25:, 130–136. [CrossRef].[PubMed].
    [Google Scholar]
  52. Zhou H. , Xu M. , Huang Q. , Gates A. T. , Zhang X. D. , Castle J. C. , Stec E. , Ferrer M. , Strulovici B. , Hazuda D. . ( 2008; ). Genome-scale RNAi screen for host factors required for HIV replication. . Cell Host Microbe 4:, 495–504. [CrossRef].[PubMed].
    [Google Scholar]
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vol. , part 7, pp. 1688 - 1697

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