Herpes simplex virus type 1 entry into host cells: Reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro

Molecular and Cellular Biology

Volumn 20, Issue 13, 2000, Pages 4922-4931

  Ojala, Päivi M ^a,c   Sodeik, Beate ^a,d   Ebersold, Melanie W ^a   Kutay, Ulrike ^b   Helenius, Ari ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; KARYOPHERIN; VIRUS DNA; VIRUS PROTEIN; WHEAT GERM AGGLUTININ;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL STRAIN BHK; CERCOPITHECIDAE; CONTROLLED STUDY; CYTOSOL; HERPES SIMPLEX VIRUS 1; HOST CELL; INTERNALIZATION; NONHUMAN; PRIORITY JOURNAL; RAT; VIRUS CAPSID; VIRUS GENOME;

ANIMALS; CAPSID; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; DNA, VIRAL; GTP-BINDING PROTEINS; HERPESVIRUS 1, HUMAN; KARYOPHERINS; NUCLEAR PROTEINS; RAN GTP-BINDING PROTEIN; RATS; TRYPSIN; VERO CELLS;

EID: 0034091334     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.13.4922-4931.2000     Document Type: Article

References (52)

1. Batterson, W., D. Furlong, and B. Roizman. 1983. Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J. Virol. 45:397-407.
2. Blobel, G., and V. R. Potter. 1966. Nuclei from rat liver: isolation method that combines purity with high yield. Science 154:1662-1665.
3. Burkham, J., D. M. Coen, and S. K. Weller. 1998. ND10 protein PML is recruited to herpes simplex virus type 1 prereplicative sites and replication compartments in the presence of viral DNA polymerase. J. Virol. 72:10100-10107.
4. Church, G. A., and D. W. Wilson. 1997. Study of herpes simplex virus maturation during a synchronous wave of assembly. J. Virol. 71:3603-3612.
5. Davis, L. I., and G. Blobel. 1986. Identification and characterization of a nuclear pore complex protein. Cell 45:699-709.
6. Enquist, L. W., P. J. Husak, B. W. Banfield, and G. A. Smith. 1998. Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 51:237-347.
7. Finlay, D. R., D. D. Newmeyer, T. M. Price, and D. J. Forbes. 1987. Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J. Cell Biol. 104:189-200.
8. Geraghty, R. J., C. Krummenacher, G. H. Cohen, R. J. Eisenberg, and P. G. Spear. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618-1620.
9. Gorlich, D., M. Dabrowski, F. R. Bischoff, U. Kutay, P. Bork, E. Hartmann, S. Prehn, and E. Izaurralde. 1997. A novel class of RanGTP binding proteins. J. Cell Biol. 138:65-80.
10. Gorlich, D., N. Pante, U. Kutay, L. Aebi, and F. R. Bischoff. 1996. Identification of different roles for RanGDP and RanGTP in nuclear protein import. EMBO J. 15:5584-5594.
11. Gorlich, D., S. Prehn, R. A. Laskey, and E. Hartmann. 1994. Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79:767-778.
12. Granzow, H., F. Weiland, A. Jons, B. G. Klupp, A. Karger, and T. C. Mettenleiter. 1997. Ultrastructural analysis of the replication cycle of pseudorabies virus in cell culture: a reassessment. J. Virol. 71:2072-2082.
13. Greber, U. F., I. Singh, and A. Helenius. 1994. Mechanisms of virus uncoating. Trends Microbiol. 2:52-56.
14. Greber, U. F., M. Suomalainen, R. P. Stidwill, K. Boucke, M. W. Ebersold, and A. Helenius. 1997. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16:5998-6007.
15. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
16. Helenius, A., J. Kartenbeck, K. Simons, and E. Fries. 1980. On the entry of Semliki Forest virus into BHK-21 cells. J. Cell Biol. 84:404-420.
17. Honess, R. W., and B. Roizman. 1973. Proteins specified by herpes simplex virus. XI. Identification and relative molar rates of synthesis of structural and nonstructural herpes virus polypeptides in the infected cell. J. Virol. 12: 1347-1365.
18. Klebe, C., H. Prinz, A. Wittinghofer, and R. S. Goody. 1995. The kinetic mechanism of Ran - nucleotide exchange catalyzed by RCC1. Biochemistry 34:12543-12552.
19. Krummenacher, C., A. V. Nicola, J. C. Whitbeck, H. Lou, W. Hou, J. D. Lambris, R. J. Geraghty, P. G. Spear, G. H. Cohen, and R. J. Eisenberg. 1998. Herpes simplex virus glycoprotein D can bind to poliovirus receptor-related protein 1 or herpesvirus entry mediator, two structurally unrelated mediators of virus entry. J. Virol. 72:7064-7074.
20. Kutay, U., E. Izaurralde, F. R. Bischoff, I. W. Mattaj, and D. Gorlich. 1997. Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex. EMBO J. 16:1153-1163.
21. Lukonis, C. J., J. Burkham, and S. K. Weller. 1997. Herpes simplex virus type 1 prereplicative sites are a heterogeneous population: only a subset are likely to be precursors to replication compartments. J. Virol. 71:4771-4781.
22. Maul, G. G., H. H. Guldner, and J. G. Spivack. 1993. Modification of discrete nuclear domains induced by herpes simplex virus type 1 immediate early gene 1 product (ICP0). J. Gen Virol. 74:2679-2690.
23. Maul, G. G., A. M. Ishov, and R. D. Everett. 1996. Nuclear domain 10 as preexisting potential replication start sites of herpes simplex virus type-I. Virology 217:67-75.
24. McClain, D. S., and A. O. Fuller. 1994. Cell-specific kinetics and efficiency of HSV-1 entry are determined by two distinct phases of attachment. Virology 198:690-702.
25. McEwen, C. R. 1967. Tables for estimating sedimentation through linear concentration gradients of sucrose solution. Anal. Biochem. 20:114-149.
26. McNabb, D. S., and R. J. Courtney. 1992. Characterization of the large tegument protein (ICP1/2) of herpes simplex virus type 1. Virology 190:221-232.
27. Melchior, F., B. Paschal, J. Evans, and L. Gerace. 1993. Inhibition of nuclear protein import by nonhydrolyzable analogues of GTP and identification of the small GTPase Ran/TC4 as an essential transport factor. J. Cell Biol. 123:1649-1659.
28. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/ NGF receptor family. Cell 87:427-436.
29. Moore, M. S., and G. Blobel. 1993. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 365:661-663.
30. Morrison, E. E., A. J. Stevenson, Y. F. Wang, and D. M. Meredith. 1998. Differences in the intracellular localization and fate of herpes simplex virus tegument proteins early in the infection of Vero cells. J. Gen. Virol. 79: 2517-2528.
31. Newcomb, W. W., and J. C. Brown. 1994. Induced extrusion of DNA from the capsid of herpes simplex virus type 1. J. Virol. 68:433-440.
32. Newcomb, W. W., and J. C. Brown. 1991. Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids. J. Virol. 65:613-620.
33. Newcomb, W. W., B. L. Trus, F. P. Booy, A. C. Steven, J. S. Wall, and J. C. Brown. 1993. Structure of the HSv capsid - molecular composition of the pentons and the triplexes. J. Mol. Biol. 232:499-511.
34. Ohno, M., M. Fornerod, and I. W. Mattaj. 1998. Nucleocytoplasmic transport: the last 200 nanometers. Cell 92:327-336.
35. Palmeri, D., and M. H. Malim. 1999. Importin beta can mediate the nuclear import of an arginine-rich nuclear localization signal in the absence of importin alpha. Mol. Cell. Biol. 19:1218-1225.
36. Reynolds, E. S. 1963. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Histochem. Cytochem. 26:163-169.
37. Roizman, B., and A. E. Sears. 1993. Herpes simplex viruses and their replication, p. 11-68. In B. Roizman, R. J. Whitley, and C. Lopez (ed.), The human herpesviruses. Raven Press, Ltd., New York, N. Y.
38. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
39. Snow, C. M., A. Senior, and L. Gerace. 1987. Monoclonal antibodies identify a group of nuclear pore complex glycoproteins. J. Cell Biol. 104:1143-1156.
40. Sodeik, B., M. W. Ebersold, and A. Helenius. 1997. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell Biol. 136:1007-1021.
41. Spear, P. 1993. Entry of alphaherpesviruses into cells. Semin. Virol. 4:167-180.
42. Spear, P. G. 1993. Membrane fusion induced by HSV, p. 201-232. In J. Bentz (ed.), Viral fusion mechanism. CRC Press, Inc., Boca Raton, Fla.
43. Spear, P. G., and B. Roizman. 1972. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpes virion. J. Virol. 9:143-159.
44. Steven, A., and P. Spear. 1997. Herpesvirus capsid assembly and envelopment. Oxford University Press, New York, N.Y.
45. Takizawa, C. G., K. Weis, and D. O. Morgan. 1999. Ran-independent nuclear import of cyclin B1-Cdc2 by importin beta. Proc. Natl. Acad. Sci. USA 96:7938-7943.
46. Tognon, M., D. Furlong, A. J. Conley, and B. Roizman. 1981. Molecular genetics of herpes simplex virus. V. Characterization of a mutant defective in ability to form plaques at low temperatures and in a viral function which prevents accumulation of coreless capsids at nuclear pores late in infection. J. Virol. 40:870-880.
47. Truant, R., and B. R. Cullen. 1999. The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin beta-dependent nuclear localization signals. Mol. Cell. Biol. 19:1210-1217.
48. Warner, M. S., R. J. Geraghty, W. M. Martinez, R. I. Montgomery, J. C. Whitbeck, R. Xu, R. J. Eisenberg, G. H. Cohen, and P. G. Spear. 1998. A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2, and pseudorabies virus. Virology 246:179-189.
49. Weis, K., C. Dingwall, and A. Lamond. 1996. Characterization of the nuclear protein import mechanism using Ran mutants with altered nucleotide binding specificities. EMBO J. 15:7120-7128.
50. Whittaker, G. R., and A. Helenius. 1998. Nuclear import and export of viruses and virus genomes. Virology 246:1-23.
51. Yamada, M., and H. Kasamatsu. 1993. Role of nuclear pore complex in simian virus 40 nuclear targeting. J. Virol. 67:119-130.
52. Zhou, Z. H., D. H. Chen, J. Jakana, F. J. Rixon, and W. Chiu. 1999. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol. 73:3210-3218.