Cell culture-adapted IBDV uses endocytosis for entry in DF-1 chicken embryonic fibroblasts

Virus Research

Volumn 165, Issue 1, 2012, Pages 9-16

  Yip, Chi Wai ^a   Hon, Chung Chau ^a   Zeng, Fanya ^a   Leung, Frederick Chi Ching ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Calcium; Clathrin independent endocytosis; IBDV; Macropinocytosis

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE; BAFILOMYCIN A1; CALCIUM; CLATHRIN; DYNAMIN; EGTAZIC ACID; PROTEIN KINASE P60;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENDOSOME; ENZYME INHIBITION; FIBROBLAST; INFECTIOUS BURSAL DISEASE VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; VIRUS ENTRY; VIRUS UNCOATING;

INFECTIOUS BURSAL DISEASE VIRUS;

EID: 84858864021     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2011.12.016     Document Type: Article

References (65)

1. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., Fukami Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 1987, 262(12):5592-5595.
2. Amstutz B., Gastaldelli M., Kalin S., Imelli N., Boucke K., Wandeler E., Mercer J., Hemmi S., Greber U.F. Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J. 2008, 27(7):956-969.
3. Anderson H.A., Chen Y., Norkin L.C. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell 1996, 7(11):1825-1834.
4. Brenner S.L., Korn E.D. Substoichiometric concentrations of cytochalasin D inhibit actin polymerization. Additional evidence for an F-actin treadmill. J. Biol. Chem. 1979, 254(20):9982-9985.
5. Chemello M.E., Aristimuno O.C., Michelangeli F., Ruiz M.C. Requirement for vacuolar H+-ATPase activity and Ca2+ gradient during entry of rotavirus into MA104 cells. J. Virol. 2002, 76(24):13083-13087.
6. Chen J.Z., Settembre E.C., Aoki S.T., Zhang X., Bellamy A.R., Dormitzer P.R., Harrison S.C., Grigorieff N. Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(26):10644-10648.
7. Christoforidis S., Miaczynska M., Ashman K., Wilm M., Zhao L., Yip S.C., Waterfield M.D., Backer J.M., Zerial M. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1999, 1(4):249-252.
8. Coulibaly F., Chevalier C., Gutsche I., Pous J., Navaza J., Bressanelli S., Delmas B., Rey F.A. The birnavirus crystal structure reveals structural relationships among icosahedral viruses. Cell 2005, 120(6):761-772.
9. Cureton D.K., Massol R.H., Saffarian S., Kirchhausen T.L., Whelan S.P. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 2009, 5(4):e1000394.
10. Da Costa B., Chevalier C., Henry C., Huet J.C., Petit S., Lepault J., Boot H., Delmas B. The capsid of infectious bursal disease virus contains several small peptides arising from the maturation process of pVP2. J. Virol. 2002, 76(5):2393-2402.
11. Damm E.M., Pelkmans L., Kartenbeck J., Mezzacasa A., Kurzchalia T., Helenius A. Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 2005, 168(3):477-488.
12. Delgui L., Ona A., Gutierrez S., Luque D., Navarro A., Caston J.R., Rodriguez J.F. The capsid protein of infectious bursal disease virus contains a functional alpha 4 beta 1 integrin ligand motif. Virology 2009, 386(2):360-372.
13. Diaz-Griffero F., Jackson A.P., Brojatsch J. Cellular uptake of avian leukosis virus subgroup B is mediated by clathrin. Virology 2005, 337(1):45-54.
14. Dormitzer P.R., Nason E.B., Prasad B.V., Harrison S.C. Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 2004, 430(7003):1053-1058.
15. Eash S., Querbes W., Atwood W.J. Infection of vero cells by BK virus is dependent on caveolae. J. Virol. 2004, 78(21):11583-11590.
16. Fittipaldi A., Ferrari A., Zoppé M., Arcangeli C., Pellegrini V., Beltram F., Giacca M. Cell membrane lipid rafts mediate caveolar endocytosis of HIV-1 Tat fusion proteins. J. Biol. Chem. 2003, 278(36):34141-34149.
17. Fra A.M., Williamson E., Simons K., Parton R.G. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 1994, 269(49):30745-30748.
18. Gagliardi S., Gatti P.A., Belfiore P., Zocchetti A., Clarke G.D., Farina C. Synthesis and structure-activity relationships of bafilomycin A1 derivatives as inhibitors of vacuolar H+-ATPase. J. Med. Chem. 1998, 41(11):1883-1893.
19. Galloux M., Libersou S., Morellet N., Bouaziz S., Da Costa B., Ouldali M., Lepault J., Delmas B. Infectious bursal disease virus, a non-enveloped virus, possesses a capsid-associated peptide that deforms and perforates biological membranes. J. Biol. Chem. 2007, 282(28):20774-20784.
20. Garriga D., Querol-Audi J., Abaitua F., Saugar I., Pous J., Verdaguer N., Caston J.R., Rodriguez J.F. The 2.6-Angstrom structure of infectious bursal disease virus-derived T=1 particles reveals new stabilizing elements of the virus capsid. J. Virol. 2006, 80(14):6895-6905.
21. Gerasimenko J.V., Tepikin A.V., Petersen O.H., Gerasimenko O.V. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 1998, 8(24):1335-1338.
22. Gilbert J.M., Goldberg I.G., Benjamin T.L. Cell penetration and trafficking of polyomavirus. J. Virol. 2003, 77(4):2615-2622.
23. Gold S., Monaghan P., Mertens P., Jackson T. A clathrin independent macropinocytosis-like entry mechanism used by bluetongue virus-1 during infection of BHK cells. PLoS One 2010, 5(6):e11360.
24. Haxhinasto K., Kamath A., Blackwell K., Bodmer J., Van Heukelom J., English A., Bai E.W., Moy A.B. Gene delivery of l-caldesmon protects cytoskeletal cell membrane integrity against adenovirus infection independently of myosin ATPase and actin assembly. Am. J. Physiol. Cell Physiol. 2004, 287(4):C1125-C1138.
25. Ilangumaran S., Hoessli D.C. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 1998, 335(2):433-440.
26. Jeetendra E., Robison C.S., Albritton L.M., Whitt M.A. The membrane-proximal domain of vesicular stomatitis virus G protein functions as a membrane fusion potentiator and can induce hemifusion. J. Virol. 2002, 76(23):12300-12311.
27. Kabayama H., Nakamura T., Takeuchi M., Iwasaki H., Taniguchi M., Tokushige N., Mikoshiba K. Ca2+ induces macropinocytosis via F-actin depolymerization during growth cone collapse. Mol. Cell. Neurosci. 2009, 40(1):27-38.
28. Koivusalo M., Welch C., Hayashi H., Scott C.C., Kim M., Alexander T., Touret N., Hahn K.M., Grinstein S. Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J. Cell Biol. 2010, 188(4):547-563.
29. Kwon H.M., Kim S.J. Sequence analysis of the variable VP2 gene of infectious bursal disease viruses passaged in Vero cells. Virus Genes 2004, 28(3):285-291.
30. Lee C.C., Ko T.P., Chou C.C., Yoshimura M., Doong S.R., Wang M.Y., Wang A.H. Crystal structure of infectious bursal disease virus VP2 subviral particle at 2.6A resolution: implications in virion assembly and immunogenicity. J. Struct. Biol. 2006, 155(1):74-86.
31. Liberali P., Kakkonen E., Turacchio G., Valente C., Spaar A., Perinetti G., Bockmann R.A., Corda D., Colanzi A., Marjomaki V., Luini A. The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J. 2008, 27(7):970-981.
32. Lim B.L., Cao Y., Yu T., Mo C.W. Adaptation of very virulent infectious bursal disease virus to chicken embryonic fibroblasts by site-directed mutagenesis of residues 279 and 284 of viral coat protein VP2. J. Virol. 1999, 73(4):2854-2862.
33. Lin T.W., Lo C.W., Lai S.Y., Fan R.J., Lo C.J., Chou Y.M., Thiruvengadam R., Wang A.H., Wang M.Y. Chicken heat shock protein 90 is a component of the putative cellular receptor complex of infectious bursal disease virus. J. Virol. 2007, 81(16):8730-8741.
34. Liu X., Mayeda A., Tao M., Zheng Z.M. Exonic splicing enhancer-dependent selection of the bovine papillomavirus type 1 nucleotide 3225 3' splice site can be rescued in a cell lacking splicing factor ASF/SF2 through activation of the phosphatidylinositol 3-kinase/Akt pathway. J. Virol. 2003, 77(3):2105-2115.
35. Luo J., Zhang H., Teng M., Fan J.M., You L.M., Xiao Z.J., Yi M.L., Zhi Y.B., Li X.W., Zhang G.P. Surface IgM on DT40 cells may be a component of the putative receptor complex responsible for the binding of infectious bursal disease virus. Avian Pathol. 2010, 39(5):359-365.
36. Macia E., Ehrlich M., Massol R., Boucrot E., Brunner C., Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 2006, 10(6):839-850.
37. Matsushita M., Sano Y., Yokoyama S., Takai T., Inoue H., Mitsui K., Todo K., Ohmori H., Kanazawa H. Loss of calcineurin homologous protein-1 in chicken B lymphoma DT40 cells destabilizes Na+/H+ exchanger isoform-1 protein. Am. J. Physiol. Cell Physiol. 2007, 293(1):C246-C254.
38. Mayor S., Pagano R.E. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 2007, 8(8):603-612.
39. Meier O., Boucke K., Hammer S.V., Keller S., Stidwill R.P., Hemmi S., Greber U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 2002, 158(6):1119-1131.
40. Mercer J., Helenius A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320(5875):531-535.
41. Mercer J., Helenius A. Virus entry by macropinocytosis. Nat. Cell Biol. 2009, 11(5):510-520.
42. Metherall J.E., Waugh K., Li H. Progesterone inhibits cholesterol biosynthesis in cultured cells. Accumulation of cholesterol precursors. J. Biol. Chem. 1996, 271(5):2627-2633.
43. Misinzo G., Delputte P.L., Nauwynck H.J. Inhibition of endosome-lysosome system acidification enhances porcine circovirus 2 infection of porcine epithelial cells. J. Virol. 2008, 82(3):1128-1135.
44. Muller H., Lange H., Becht H. Formation, characterization and interfering capacity of a small plaque mutant and of incomplete virus particles of infectious bursal disease virus. Virus Res. 1986, 4(3):297-309.
45. Mundt E. Tissue culture infectivity of different strains of infectious bursal disease virus is determined by distinct amino acids in VP2. J. Gen. Virol. 1999, 80(Pt 8):2067-2076.
46. Nitschke M., Korte T., Tielesch C., Ter-Avetisyan G., Tunnemann G., Cardoso M.C., Veit M., Herrmann A. Equine arteritis virus is delivered to an acidic compartment of host cells via clathrin-dependent endocytosis. Virology 2008, 377(2):248-254.
47. O'Donnell V., Larocco M., Baxt B. Heparan sulfate-binding foot-and-mouth disease virus enters cells via caveola-mediated endocytosis. J. Virol. 2008, 82(18):9075-9085.
48. Ogawa M., Yamaguchi T., Setiyono A., Ho T., Matsuda H., Furusawa S., Fukushi H., Hirai K. Some characteristics of a cellular receptor for virulent infectious bursal disease virus by using flow cytometry. Arch. Virol. 1998, 143(12):2327-2341.
49. Pelkmans L. Secrets of caveolae- and lipid raft-mediated endocytosis revealed by mammalian viruses. Biochim. Biophys. Acta 2005, 1746(3):295-304.
50. Pelkmans L., Burli T., Zerial M., Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 2004, 118(6):767-780.
51. Pelkmans L., Puntener D., Helenius A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002, 296(5567):535-539.
52. Pu Y., Zhang X. Mouse hepatitis virus type 2 enters cells through a clathrin-mediated endocytic pathway independent of Eps15. J. Virol. 2008, 82(16):8112-8123.
53. Racoosin E.L., Swanson J.A. Macropinosome maturation and fusion with tubular lysosomes in macrophages. J. Cell Biol. 1993, 121(5):1011-1020.
54. Rappoport J.Z. Focusing on clathrin-mediated endocytosis. Biochem. J. 2008, 412(3):415-423.
55. Richards A.A., Stang E., Pepperkok R., Parton R.G. Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol. Biol. Cell 2002, 13(5):1750-1764.
56. Sanchez-San Martin C., Lopez T., Arias C.F., Lopez S. Characterization of rotavirus cell entry. J. Virol. 2004, 78(5):2310-2318.
57. Schlegel R., Willingham M.C., Pastan I.H. Saturable binding sites for vesicular stomatitis virus on the surface of Vero cells. J. Virol. 1982, 43(3):871-875.
58. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1(1):31-39.
59. Superti F., Seganti L., Ruggeri F.M., Tinari A., Donelli G., Orsi N. Entry pathway of vesicular stomatitis virus into different host cells. J. Gen. Virol. 1987, 68(Pt 2):387-399.
60. Wang L.H., Rothberg K.G., Anderson R.G. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 1993, 123(5):1107-1117.
61. Wong R.T., Hon C.C., Zeng F., Leung F.C. Screening of differentially expressed transcripts in infectious bursal disease virus-induced apoptotic chicken embryonic fibroblasts by using cDNA microarrays. J. Gen. Virol. 2007, 88(Pt 6):1785-1796.
62. Yamaguchi T., Kondo T., Inoshima Y., Ogawa M., Miyoshi M., Yanai T., Masegi T., Fukushi H., Hirai K. In vitro attenuation of highly virulent infectious bursal disease virus: some characteristics of attenuated strains. Avian Dis. 1996, 40(3):501-509.
63. Yano H., Nakanishi S., Kimura K., Hanai N., Saitoh Y., Fukui Y., Nonomura Y., Matsuda Y. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 1993, 268(34):25846-25856.
64. Yip C.W., Yeung Y.S., Ma C.M., Lam P.Y., Hon C.C., Zeng F., Leung F.C. Demonstration of receptor binding properties of VP2 of very virulent strain infectious bursal disease virus on Vero cells. Virus Res. 2007, 123(1):50-56.
65. Zhu Y.Z., Cao M.M., Wang W.B., Wang W., Ren H., Zhao P., Qi Z.T. The association of heat shock protein 70 with lipid rafts is required for Japanese encephalitis virus infection in Huh7 cells. J. Gen. Virol. 2012, 93(Pt 1):61-67.