Nuclear delivery mechanism of herpes simplex virus type 1 genome

Journal of Molecular Recognition

Volumn 24, Issue 3, 2011, Pages 414-421

  Liashkovich, Ivan ^a   Hafezi, Wali ^a   Kühn, Joachim M ^a   Oberleithner, Hans ^a   Shahin, Victor ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

herpes simplex virus type 1 (HSV 1); nuclear delivery of viral genome; nuclear pore complex; viral capsid; viral genome

Indexed keywords

GENETICS; HERPES SIMPLEX VIRUS 1; HUMAN; METABOLISM; NUCLEAR PORE; REVIEW; VIRUS CAPSID; VIRUS GENOME;

CAPSID; GENOME, VIRAL; HERPESVIRUS 1, HUMAN; HUMANS; NUCLEAR PORE;

HUMAN HERPESVIRUS 1; MIRIDAE; SIMPLEXVIRUS;

EID: 79955091009     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.1120     Document Type: Review

References (72)

1. Alber F, Dokudovskaya S, Veenhoff LM, Zhang WH, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Sali A, Rout MP., 2007. The molecular architecture of the nuclear pore complex. Nature 450: 695-701. (Pubitemid 350207701)
2. Banfield BW, Leduc Y, Esford L, Schubert K, Tufaro F., 1995. Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway. J. Virol. 69 (6): 3290-3298.
3. Batterson W, Furlong D, Roizman B., 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 (1): 397-407. (Pubitemid 13166314)
4. Booy FP, Newcomb WW, Trus BL, Brown JC, Baker TS, Steven AC., 1991. Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 64 (5): 1007-1015. (Pubitemid 121001187)
5. Bowman BR, Baker ML, Rixon FJ, Chiu W, Quiocho FA., 2003. Structure of the herpesvirus major capsid protein. EMBO J. 22 (4): 757-765. (Pubitemid 36227778)
6. Bowman BR, Welschhans RL, Jayaram H, Stow ND, Preston VG, Quiocho FA., 2006. Structural characterization of the UL25 DNA-packaging protein from herpes simplex virus type 1. J. Virol. 80 (5): 2309-2317. (Pubitemid 43271536)
7. Cardone G, Winkler DC, Trus BL, Cheng NQ, Heuser JE, Newcomb WW, Brown JC, Steven AC., 2007. Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361 (2): 426-434. (Pubitemid 46574843)
8. Caspar DLD, Klug A., 1962. Physical principlese in construction of regular viruses. Cold Spring Harb. Symp. Quant. Biol. 27: 1-24.
9. Chang JT, Schmid MF, Rixon FJ, Chiu W., 2007. Electron cryotomography reveals the portal in the herpesvirus capsid. J. Virol. 81 (4): 2065-2068. (Pubitemid 46214478)
10. Copeland AM, Newcomb WW, Brown JC., 2009. Herpes simplex virus replication: roles of viral proteins and nucleoporins in capsid-nucleus attachment. J. Virol. 83 (4): 1660-1668.
11. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ., 2002. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 158 (5): 915-927. (Pubitemid 35001082)
12. D'Angelo MA, Hetzer MW., 2006. The role of the nuclear envelope in cellular organization. Cell. Mol. Life Sci. 63 (3): 316-332. (Pubitemid 43202313)
13. Denning DP, Patel SS, Uversky V, Fink AL, Rexach M., 2003. Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc. Natl. Acad. Sci. USA 100 (5): 2450-2455. (Pubitemid 36297519)
14. Desai P, DeLuca NA, Person S., 1998. Herpes simplex virus type 1 VP26 is not essential for replication in cell culture but influences production of infectious virus in the nervous system of infected mice. Virology 247 (1): 115-124. (Pubitemid 28384031)
15. Dohner K, Wolfstein A, Prank U, Echeverri C, Dujardin D, Vallee R, Sodeik B., 2002. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13 (8): 2795-2809.
16. Douglas MW, Diefenbach RJ, Homa FL, Miranda-Saksena M, Rixon FJ, Vittone V, Byth K, Cunningham AL., 2004. Herpes simplex virus type 1 capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and plays a role in retrograde cellular transport. J. Biol. Chem. 279 (27): 28522-28530. (Pubitemid 38900135)
17. Evilevitch A, Lavelle L, Knobler CM, Raspaud E, Gelbart WM., 2003. Osmotic pressure inhibition of DNA ejection from phage. Proc. Natl. Acad. Sci. USA 100 (16): 9292-9295. (Pubitemid 37033922)
18. Garner JA., 2003. Herpes simplex virion entry into and intracellular transport within mammalian cells. Adv. Drug Delivery Rev. 55 (11): 1497-1513. (Pubitemid 37464575)
19. Grayson P, Han L, Winther T, Phillips R., 2007. Real-time observations of single bacteriophage lambda DNA ejections in vitro. Proc. Natl. Acad. Sci. USA 104: 14652-14657. (Pubitemid 350003198)
20. Gruenbaum Y, Goldman RD, Meyuhas R, Mills E, Margalit A, Fridkin A, Dayani Y, Prokocimer M, Enosh A., 2003. The nuclear lamina and its functions in the nucleus. Int. Rev. Cytol. 226: 1-62. (Pubitemid 36959354)
21. Gruenheid S, Gatzke L, Meadows H, Tufaro F., 1993. Herpes-simplex virus-infection and propagation in a mouse L-cell mutant lacking heparan-sulfate proteoglycans. J. Virol. 67 (1): 93-100. (Pubitemid 23002968)
22. Grunewald K, Desai P, Winkler DC, Heymann JB, Belnap DM, Baumeister W, Steven AC., 2003. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302 (5649): 1396-1398. (Pubitemid 37452181)
23. Holmer L, Worman HJ., 2001. Inner nuclear membrane proteins: functions and targeting. Cell. Mol. Life Sci. 58 (12-13): 1741-1747. (Pubitemid 33108764)
24. Jeembaeva M, Castelnovo M, Larsson F, Evilevitch A., 2008. Osmotic pressure: resisting or promoting DNA ejection from phage ? J. Mol. Biol. 381 (2): 310-323.
25. Jovasevic V, Liang L, Roizman B., 2008. Proteolytic cleavage of VP 1-2 is required for the release of herpes simplex virus 1 DNA into the nucleus. J. Virol. 82 (7): 3311-3319. (Pubitemid 351429909)
26. Kelly BJ, Fraefel C, Cunningham AL, Diefenbach RJ., 2009. Functional roles of the tegument proteins of herpes simplex virus type 1. Virus Res. 145 (2): 173-186.
27. Kramer A, Liashkovich I, Ludwig Y, Shahin V., 2008. Atomic force microscopy visualises a hydrophobic meshwork in the central channel of the nuclear pore. Pflügers Arch. 456 (1): 155-162.
28. Kramer A, Liashkovich I, Oberleithner H, Shahin V., 2010. Caspase-9-dependent decrease of nuclear pore channel hydrophobicity is accompanied by nuclear envelope leakiness. Nanomedicine 6 (5): 605-611.
29. Kramer A, Ludwig Y, Shahin V, Oberleithner H., 2007. A pathway separate from the central channel through the nuclear pore complex for inorganic ions and small macromolecules. J. Biol. Chem. 282 (43): 31437-31443. (Pubitemid 350044878)
30. Lambert O, Letellier L, Gelbart WM, Rigaud JL., 2000. DNA delivery by phage as a strategy for encapsulating toroidal condensates of arbitrary size into liposomes. Proc. Natl. Acad. Sci. USA 97 (13): 7248-7253. (Pubitemid 30431449)
31. Lamberti C, Weller SK., 1996. The Herpes simplex virus type 1 UL6 protein is essential for cleavage and packaging but not for genomic inversion. Virology 226 (2): 403-407. (Pubitemid 27025820)
32. Liashkovich I, Hafezi W, Kuhn JE, Oberleithner H, Kramer A, Shahin V., 2008. Exceptional mechanical and structural stability of HSV-1 unveiled with fluid atomic force microscopy. J. Cell Sci. 121 (14): 2287-2292.
33. Loret S, Guay G, Lippe R., 2008. Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J. Virol. 82 (17): 8605-8618.
34. Maurer UE, Sodeik B, Grunewald K., 2008. Native 3D intermediates of membrane fusion in herpes simplex virus 1 entry. Proc. Natl. Acad. Sci. USA 105 (30): 10559-10564.
35. McNab AR, Desai P, Person S, Roof LL, Thomsen DR, Newcomb WW, Brown JC, Homa FL., 1998. The product of the herpes simplex virus type 1 UL25 gene is required for encapsidation but not for cleavage of replicated viral DNA. J. Virol. 72 (2): 1060-1070. (Pubitemid 28116885)
36. Mohr D, Frey S, Fischer T, Guttler T, Gorlich D., 2009. Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 28 (17): 2541-2553.
37. Molineux LJ., 2001. No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol. Microbiol. 40 (1): 1-8.
38. Naim B, Zbaida D, Dagan S, Kapon R, Reich Z., 2009. Cargo surface hydrophobicity is sufficient to overcome the nuclear pore complex selectivity barrier. EMBO J. 28 (18): 2697-2705.
39. Newcomb WW, Booy FP, Brown JC., 2007. Uncoating the herpes simplex virus genome. J. Mol. Biol. 370 (4): 633-642. (Pubitemid 46879779)
40. Newcomb WW, Brown JC., 1994. Induced Extrusion of DNA from the capsid of herpes-simplex virus type-1. J. Virol. 68 (1): 433-440.
41. Newcomb WW, Cockrell SK, Homa FL, Brown JC., 2009. Polarized DNA Ejection from the Herpesvirus Capsid. J. Mol. Biol. 392 (4): 885-894.
42. Newcomb WW, Juhas RM, Thomsen DR, Homa FL, Burch AD, Weller SK, Brown JC., 2001. The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol. 75 (22): 10923-10932. (Pubitemid 33031559)
43. Ogasawara M, Suzutani T, Yoshida I, Azuma M., 2001. Role of the UL25 gene product in packaging DNA into the herpes simplex virus capsid: location of UL25 product in the capsid and demonstration that it binds DNA. J. Virol. 75 (3): 1427-1436. (Pubitemid 32094701)
44. Ojala PM, Sodeik B, Ebersold MW, Kutay U, Helenius A., 2000. Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol. Cell. Biol. 20 (13): 4922-4931. (Pubitemid 30396138)
45. Paine PL, Moore LC, Horowitz SB., 1975. Nuclear envelope permeability. Nature 254: 109-L 114.
46. Pasdeloup D, Blondel D, Isidro AL, Rixon FJ., 2009. Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J. Virol. 83 (13): 6610-6623.
47. Patel SS, Belmont BJ, Sante JM, Rexach MF., 2007. Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129 (1): 83-96. (Pubitemid 46507580)
48. Peleg O, Lim RYH., 2010. Converging on the function of intrinsically disordered nucleoporins in the nuclear pore complex. Biol. Chem. 391 (7): 719-730.
49. Petrov AS, Harvey SC., 2007. Structural and thermodynamic principles of viral packaging. Structure 15 (1): 21-27. (Pubitemid 46073774)
50. Preston VG, Murray J, Preston CM, McDougall IM, Stow ND., 2008. The UL25 gene product of herpes simplex virus type 1 is involved in uncoating of the viral genome. J. Virol. 82 (13): 6654-6666. (Pubitemid 351875142)
51. Qie L, Marcellino D, Herold BC., 1999. Herpes simplex virus entry is associated with tyrosine phosphorylation of cellular proteins. Virology 256 (2): 220-227. (Pubitemid 29393357)
52. Rajcani J, Andrea V, Ingeborg R., 2004. Peculiarities of herpes simplex virus (HSV) transcription: an overview. Virus Genes 28 (3): 293-310. (Pubitemid 39012131)
53. Ribbeck K, Gorlich D., 2002. The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J. 21 (11): 2664-2671. (Pubitemid 34619382)
54. Salman H, Zbaida D, Rabin Y, Chatenay D, Elbaum M., 2001. Kinetics and mechanism of DNA uptake into the cell nucleus. Proc. Natl. Acad. Sci.USA 98 (13): 7247-7252. (Pubitemid 32567934)
55. Schaffer PA, Aron GM, Biswal N, Benyeshm M., 1973. Temperature-sensitive mutants of herpes-simplex virus type 1-isolation, complementation and partial characterization. Virology 52 (1): 57-71.
56. Shahin V., 2006. The nuclear barrier is structurally and functionally highly responsive to glucocorticoids. Bioessays 28 (9): 935-942. (Pubitemid 44433756)
57. Shahin V, Hafezi W, Oberleithner H, Ludwig Y, Windoffer B, Schillers H, Kuhn JE., 2006. The genome of HSV-1 translocates through the nuclear pore as a condensed rod-like structure. J. Cell Sci. 119 (1): 23-30. (Pubitemid 43169295)
58. Shieh MT, Wudunn D, Montgomery RI, Esko JD, Spear PG., 1992. Cell-surface receptors for herpes-simplex virus are heparan-sulfate proteoglycans. J. Cell biol. 116 (5): 1273-1281.
59. Smith DE, Tans SJ, Smith SB, Grimes S, Anderson DL, Bustamante C., 2001. The bacteriophage phi 29 portal motor can package DNA against a large internal force. Nature 413 (6857): 748-752. (Pubitemid 33009954)
60. Sodeik B., 2000. Mechanisms of viral transport in the cytoplasm. Trends Microbiol. 8 (10): 465-472.
61. Sodeik B, Ebersold MW, Helenius A., 1997. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J. Cell biol. 136 (5): 1007-1021. (Pubitemid 27131733)
62. Spear PG., 1993. Entry of alphaherpesviruses into cells. Virology 4 (3): 167-180.
63. Spear PG, Eisenberg RJ, Cohen GH., 2000. Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275 (1): 1-8.
64. Stow ND., 2001. Packaging of genomic and amplicon DNA by the herpes simplex virus type 1 UL25-null mutant KUL25NS. J. Virol. 75 (22): 10755-10765. (Pubitemid 33031545)
65. Trus BL, Chen NQ, Newcomb WW, Homa FL, Brown JC, Steven AC., 2004. Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 78 (22): 12668-12671. (Pubitemid 39458785)
66. Trus BL, Newcomb WW, Cheng NQ, Cardone G, Marekov L, Horna FL, Brown JC, Steven AC., 2007. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-filled HSV-1 capsids. Mol. Cell 26 (4): 479-489. (Pubitemid 46765180)
67. Wadsworth S, Hayward GS, Roizman B., 1976. Anatomy of herpes simplex virus DNA.V. Terminally repetitive sequences. J. Virol. 17 (2): 503-512.
68. Walde S, Kehlenbach RH., 2010. The part and the whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol. 20 (8): 461-469.
69. Weller SK, Carmichael EP, Aschman DP, Goldstein DJ, Schaffer PA., 1987. Genetic and phenotypic characterization of mutants in 4 essential genes that map to the left half of HSV-1 UL DNA. Virology 161 (1): 198-210. (Pubitemid 17161556)
70. White CA, Stow ND, Patel AH, Hughes M, Preston VG., 2003. Herpes simplex virus type 1 portal protein UL6 interacts with the putative terminase subunits UL15 and UL28. J. Virol. 77 (11): 6351-6358. (Pubitemid 36588405)
71. Wolfstein A, Nagel CH, Radtke K, Dohner K, Allan VJ, Sodeik B., 2006. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 7 (2): 227-237.
72. Yang K, Homa F, Baines JD., 2007. Putative terminase subunits of herpes simplex virus 1 form a complex in the cytoplasm and interact with portal protein in the nucleus. J. Virol. 81 (12): 6419-6433. (Pubitemid 46878048)