The role of the nuclear pore complex in adenovirus DNA entry

EMBO Journal

Volumn 16, Issue 19, 1997, Pages 5998-6007

  Greber, Urs F ^a   Suomalainen, Maarit ^a   Stidwill, Robert P ^a   Boucke, Karin ^a   Ebersold, Melanie W ^b   Helenius, Ari ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenovirus; Calcium; DNA; Nuclear import; Nuclear pore complex

Indexed keywords

CALCIUM; CARRIER PROTEIN; CELL DNA; GLYCOPROTEIN; IONOPHORE; THAPSIGARGIN; VIRUS DNA;

ADENOVIRUS; ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; VIRUS ADSORPTION; VIRUS CAPSID; VIRUS DNA CELL DNA INTERACTION;

ADENOVIRIDAE; ANTIBODIES; BIOLOGICAL TRANSPORT; CALCIUM; CAPSID; CELL NUCLEUS; DNA, VIRAL; HELA CELLS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; NUCLEAR ENVELOPE; VIRAL STRUCTURAL PROTEINS; WHEAT GERM AGGLUTININS;

ADENOVIRIDAE; MIRIDAE;

EID: 0030875903     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.19.5998     Document Type: Article

References (69)

1. Adam,E.J.H. and Adam,S.A. (1994) Identification of cytosolic factors required for nuclear location sequence-mediated binding to the nuclear envelope. J. Cell Biol., 125, 547-555.
2. Akey,C.W. and Goldfarb,D.S. (1989) Protein import through the nuclear pore complex is a multistep process. J. Cell Biol., 109, 971-982.
3. Bachs,O., Agell,N. and Carafoli,E. (1994) Calmodulin and calmodulin-binding proteins in the nucleus. Cell Calcium, 16, 289-296.
4. Badminton,M.N., Campbell,A.K. and Rembold,C.M. (1996) Differential regulation of nuclear and cytosolic calcium in HeLa cells. J. Biol. Chem., 271, 31210-31214.
5. Baum,S.G., Horwitz,M.S. and Maizel,J.V. (1972) Studies of the mechanism of enhancement of human adenovirus infection in monkey cells by simian virus 40. J. Virol., 10, 211-219.
6. Bergelson,J.M., Cunningham,J.A., Droguett,G., Kurt-Jones,E.A., Krithivas,A., Hong,J.S., Horwitz,M.S., Crowell,R.L. and Finberg,R.W. (1997) Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science, 275, 1320-1323.
7. Berridge,M.J. (1995) Calcium signalling and cell proliferation. BioEssays, 17, 491-500.
8. Brostrom,C.O. and Brostrom,M.A. (1990) Calcium-dependent regulation of protein synthesis in intact mammalian cells. Annu. Rev. Physiol., 52, 577-590.
9. Chao,T.S., Byron,K.L., Lee,K.M., Villereal,M. and Rosner,M.R. (1992) Activation of MAP kinases by calcium-dependent and calcium-independent pathways. Stimulation by thapsigargin and epidermal growth factor. J. Biol. Chem., 267, 19876-19883.
10. Chardonnet,Y. and Dales,S. (1972) Early events in the interaction of adenoviruses with HeLa cells: III. Relationship between an ATPase activity in nuclear envelopes and transfer of core material: a hypothesis. Virology, 48, 342-359.
11. Clapham,D.E. (1995) Intracellular calcium: replenishing the stores. Nature, 375, 634-635.
12. Cotten,M. and Weber,J.M. (1995) The adenovirus protease is required for virus entry into host cells. Virology, 213, 494-502.
13. Davis,L.I. (1995) The nuclear pore complex. Annu. Rev. Biochem., 64, 865-896.
14. Diamond,M.S. and Springer,T.A. (1994) The dynamic regulation of integrin adhesiveness. Curr. Biol., 4, 506-517.
15. Duverger,E., Pellerinmendes,C., Mayer,R., Roche,A.C. and Monsigny,M. (1995) Nuclear import of glycoconjugates is distinct from the classical nls pathway. J. Cell Sci., 108, 1325-1332.
16. Fasolato,C., Innocenti,B. and Pozzan,T. (1994) Receptor activated calcium influx: how many mechanisms for how many channels? Trends Pharmacol Sci., 15, 77-83.
17. Fields,B.N., Knipe,D.M. and Howley,P.M. (1996) Fundamental Virology. Lippincott-Raven, New York.
18. Finlay,D.R., Newmeyer,D.D., Price,T.M. and Forbes,D.J. (1987) Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J. Cell Biol., 104, 189-200.
19. Gallay,P., Stitt,V., Mundy,C., Oettinger,M. and Trono,D. (1996) Role of the karyopherin pathway in human immunodeficiency virus type 1 nuclear import. J. Virol., 70, 1027-1032.
20. Gerace,L. and Foisner,R. (1994) Integral membrane proteins and dynamic organization of the nuclear envelope. Trends Cell Biol., 4, 127-131.
21. Goldberg,M.W. and Allen,T.D. (1995) Structural and functional organization of the nuclear envelope. Curr. Opin. Cell Biol., 7, 301-309.
22. Görlich,D. and Mattaj,.W. (1996) Protein kinesis - nucleocytoplasmic transport. Science, 271, 1513-1518.
23. Greber,U.F. and Gerace,L. (1992) Nuclear protein import is inhibited by an antibody to a lumenal epitope of a nuclear pore complex glycoprotein. J. Cell Biol., 116, 15-30.
24. Greber,U.F. and Gerace,L. (1995) Depletion of calcium from the lumen of the endoplasmic reticulum reversibly inhibits passive diffusion and signal-mediated transport into the nucleus. J. Cell Biol., 128, 5-14.
25. Greber,U.F. and Kasamatsu,H. (1996) Nuclear targeting of adenovirus and simian virus SV40. Trends Cell Biol., 6, 189-195.
26. Greber,U.F., Senior,A. and Gerace,L. (1990) A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large lumenal domain and a small cytoplasmic tail. EMBO J., 9, 1495-1502.
27. Greber,U.F., Willetts,M., Webster,P. and Helenius,A. (1993) Stepwise dismantling of adenovirus 2 during entry into cells. Cell, 75, 477-486.
28. Greber,U.F., Singh,I. and Helenius,A. (1994) Mechanisms of virus uncoating. Trends Microbiol., 2, 52-56.
29. Greber,U.F., Webster,P., Weber,J. and Helenius,A. (1996) The role of the adenovirus protease in virus entry into cells. EMBO J., 15, 1766-1777.
30. Hinshaw,J.E., Carragher,B.O. and Milligan,R.A. (1992) Architecture and design of the nuclear pore complex. Cell, 69, 1133-1141.
31. Hong,S.S., Karayan,L., Tournier,J., Curiel,D.T. and Boulanger,P.A. (1997) Adenovirus type 5 fiber knob binds to MHC class I alpha2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J., 16, 2294-2306.
32. Horne,R.W. (1986) Electron microscopy of crystalline arrays af adenoviruses and their components. In Harris,J.R. and Horne,R.W. (eds). Electron Microscopy of Proteins: Viral Structure. Academic Press, New York, Vol. 5, pp. 71-101.
33. Horwitz,M.S. (1990) Adenoviruses. In Fields,B.N. and Knipe,D.M. (eds), Virology. Raven Press, New York, Vol. 1, pp. 1723-1740.
34. Humbert,J.P., Matter,N., Artault,J.-C, Köppler,P. and Malviya,A.N. (1996) Inositol 1,4.5-trisphosphate receptor is located to the inner nuclear membrane vindicating regulation of nuclear calcium signaling by inositol 1,4,5-trisphosphate. J. Biol. Chem., 271, 478-485.
35. Hynes,R.O. (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell, 69, 11-25.
36. Ishov,A.M. and Maul,G.G. (1996) The periphery of nuclear domain 10 (Nd10) as site of DNA virus deposition. J. Cell Biol., 134, 815-826.
37. Kann,M., Bischof,A. and Gerlich,W.H. (1997) In vitro model for the nuclear transport of the hepadnavirus genome. J. Virol., 71, 1310-1316.
38. Lanini,L., Bachs,O. and Carafoli,E. (1992) The calcium pump of the liver nuclear membrane is identical to that of endoplasmic reticulum. J. Biol. Chem., 267, 11548-11552.
39. Mangel,W.F., McGrath,W.J., Toledo,D.L. and Anderson,C.W. (1993) Viral DNA and a viral peptide can act as cofactors of adenovirus virion proteinase activity. Nature, 361, 274-275.
40. Martin,K. and Helenius,A. (1991) Transport of incoming influenza virus nucleocapsids into the nucleus. J. Virol., 65, 232-244.
41. Melchior,F. and Gerace,L. (1995) Mechanisms of nuclear protein import. Curr. Opin. Cell Biol., 7, 310-318.
42. Miles,B.D., Luftig,R.B., Weatherbee,J.A., Weihing,R.R. and Weber,J. (1980) Quantitation of the interaction between adenovirus types 2 and 5 and microtubules inside infected cells. Virology, 105, 265-269.
43. Miller,L. (1996) Insect viruses. In Fields,B.N., Knipe,D.M. and Howley,P.M. (eds), Fundamental Virology. Lippincott-Raven, New York, pp. 401-424.
44. Panté,N. and Aebi,U. (1996a) Sequential binding of import ligands to distinct nucleopore regions during their nuclear import. Science, 273, 1729-1732.
45. Panté,N. and Aebi,U. (1996b) Toward the molecular dissection of protein import into nuclei. Curr. Opin. Cell Biol., 8, 397-406.
46. Perez-Terzic,C., Pyle,J., Jaconi,M., Stehno-Bittel,L. and Clapham,D.E. (1996) Conformational states of the nuclear pore complex induced by depletion of nuclear calcium stores. Science, 273, 1875-1877.
47. Perry,R.P. and Kelley,D.E. (1970) Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species. J. Cell Physiol., 76, 127-139.
48. Pettersson,U. and Sambrook,J. (1973) Amount of viral DNA in the genome of cells transformed with adenovirus type 2. J. Mol. Biol., 73, 125-130.
49. Pollard,V.W., Michael,W.M., Nakielny,S., Siomi,M.C., Wang,F. and Dreyfuss,G. (1996) A novel receptor-mediated nuclear protein import pathway. Cell, 86, 985-994.
50. Pozzan,T., Rizzuto,R., Volpe,P. and Meldolesi,J. (1994) Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev., 74, 595-636.
51. Prchla,E., Plank,C., Wagner,E., Blaas,D. and Fuchs,R. (1995) Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2. J. Cell Biol., 131, 111-123.
52. Pruschy,M., Ju,Y., Spitz,L., Carafoli,E. and Goldfarb,D.S. (1994) Facilitated nuclear transport of calmodulin in tissue culture cells. J. Cell Biol., 127, 1527-1536.
53. Rexach,M. and Blobel,G. (1995) Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell, 83, 683-692.
54. Roizman,B. and Sears,A.E. (1996) Herpes viruses and their replication. In Fields,B.N., Knipe,D.M. and Howley,P.M. (eds), Fundamental Virology. Lippincott-Raven, New York, pp. 1043-1107.
55. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Shenk,T. (1996) Adenoviridae: the viruses and their replication. In Fields,B.N., Knipe,D.M. and Howley,P.M. (eds), Fundamental Virology. Lippincott-Raven, New York, pp. 979-1016.
57. Sodeik,B., Ebersold,M.W. and Helenius,A. (1997) Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol., 136, 1007-1021.
58. Snow,C.M., Senior,A. and Gerace,L. (1987) Monoclonal antibodies identify a group of nuclear pore complex glycoproteins. J. Cell Biol., 104, 1143-1156.
59. Stehno-Bittel,L., Perez-Terzic,C. and Clapham,D.E. (1995) Diffusion across the nuclear envelope inhibited by depletion of the nuclear envelope calcium store. Science, 270, 1835-1838.
60. Stevenson,M. (1996) Portals of entry: uncovering HIV nuclear transport pathways. Trends Cell Biol., 6, 9-15.
61. Stewart,P.L., Fuller,S.D. and Burnett,R.M. (1993) Difference imaging of adenovirus: bridging the resolution gap between X-ray crystallography and electron microscopy. EMBO J., 12, 2589-2599.
62. Svensson,U. and Persson,R. (1984) Entry of adenovirus 2 into HeLa cells. J. Virol., 51, 687-694.
63. Sweitzer,T.D. and Hanover,J.A. (1996) Calmodulin activates nuclear protein import - a link between signal transduction and nuclear transport. Proc. Natl Acad. Sci. USA, 93, 14574-14579.
64. 2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc. Natl Acad. Sci. USA, 87, 2466-2470.
65. Tomko,R.P., Xu,R. and Philipson,L. (1997) HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl Acad. Sci. USA, 94, 3352-3356.
66. van Oostrum,J. and Burnett,R.M. (1985) Molecular composition of the adenovirus type 2 virion. J. Virol., 56, 439-448.
67. Whittaker,G., Bui,M. and Helenius,A. (1996) The role of nuclear import and export in influenza virus infection. Trends Cell Biol., 6, 67-71.
68. Wickham,T.J., Mathias,P., Cheresh,D.A. and Nemerow,G.R. (1993) Integrin-alpha-v-beta-3 and integrin-alpha-v-beta-5 promote adenovirus internalization but not virus attachment. Cell, 73, 309-319.
69. Wickham,T.J., Filardo,E.J., Cheresh,D.A. and Nemerow,G.R. (1994) Integrin ανβ5 selectively promotes adenovirus mediated cell membrane permeabilization. J. Cell Biol., 127, 257-264.