Virion incorporation of the herpes simplex virus type 1 tegument protein VP22 is facilitated by trans-Golgi network localization and is independent of interaction with glycoprotein E

Virology

Volumn 405, Issue 1, 2010, Pages 176-192

  O'Regan, Kevin J ^a   Brignati, Michael J ^b   Murphy, Michael A ^c   Bucks, Michelle A ^d   Courtney, Richard J ^d  

^a FOX CHASE CANCER CENTER   (United States)

^b Troutman Sanders LLP   (United States)

^c AlphaVax Inc   (United States)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Acidic cluster; GE; HSV 1; Virion Incorporation; Virus assembly; VP16; VP22

Indexed keywords

GLYCOPROTEIN E; PROTEIN VP22;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENE CLUSTER; GENE IDENTIFICATION; HERPES SIMPLEX VIRUS 1; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS; TRANS GOLGI NETWORK; VIRION; VIRUS CELL INTERACTION; VIRUS PARTICLE; WILD TYPE;

HUMAN HERPESVIRUS 1;

EID: 77955515275     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.06.007     Document Type: Article

References (53)

1. Alconada A., Bauer U., Baudoux L., Piette J., Hoflack B. Intracellular transport of the glycoproteins gE and gI of the varicella-zoster virus. gE accelerates the maturation of gI and determines its accumulation in the trans-Golgi network. J. Biol. Chem. 1998, 273(22):13430-13436.
2. Alconada A., Bauer U., Sodeik B., Hoflack B. Intracellular traffic of herpes simplex virus glycoprotein gE: characterization of the sorting signals required for its trans-Golgi network localization. J. Virol. 1999, 73(1):377-387.
3. Bonifacino J.S. The GGA proteins: adaptors on the move. Nat. Rev. Mol. Cell Biol. 2004, 5(1):23-32.
4. Brack A.R., Dijkstra J.M., Granzow H., Klupp B.G., Mettenleiter T.C. Inhibition of virion maturation by simultaneous deletion of glycoproteins E, I, and M of pseudorabies virus. J. Virol. 1999, 73(7):5364-5372.
5. Brack A.R., Klupp B.G., Granzow H., Tirabassi R., Enquist L.W., Mettenleiter T.C. Role of the cytoplasmic tail of pseudorabies virus glycoprotein E in virion formation. J. Virol. 2000, 74(9):4004-4016.
6. Brignati M.J., Loomis J.S., Wills J.W., Courtney R.J. Membrane association of VP22, a herpes simplex virus type 1 tegument protein. J. Virol. 2003, 77(8):4888-4898.
7. Bucks M.A., O'Regan K.J., Murphy M.A., Wills J.W., Courtney R.J. Herpes simplex virus type 1 tegument proteins VP1/2 and UL37 are associated with intranuclear capsids. Virology 2007, 361(2):316-324.
8. Chi J.H., Harley C.A., Mukhopadhyay A., Wilson D.W. The cytoplasmic tail of herpes simplex virus envelope glycoprotein D binds to the tegument protein VP22 and to capsids. J. Gen. Virol. 2005, 86(Pt 2):253-261.
9. Duffy C., Lavail J.H., Tauscher A.N., Wills E.G., Blaho J.A., Baines J.D. Characterization of a UL49-null mutant: VP22 of herpes simplex virus type 1 facilitates viral spread in cultured cells and the mouse cornea. J. Virol. 2006, 80(17):8664-8675.
10. Elliott G., Hafezi W., Whiteley A., Bernard E. Deletion of the herpes simplex virus VP22-encoding gene (UL49) alters the expression, localization, and virion incorporation of ICP0. J. Virol. 2005, 79(15):9735-9745.
11. Elliott G., Mouzakitis G., O'Hare P. VP16 interacts via its activation domain with VP22, a tegument protein of herpes simplex virus, and is relocated to a novel macromolecular assembly in coexpressing cells. J. Virol. 1995, 69(12):7932-7941.
12. Elliott G.D., Meredith D.M. The herpes simplex virus type 1 tegument protein VP22 is encoded by gene UL49. J. Gen. Virol. 1992, 73(Pt 3):723-726.
13. Enquist L.W., Husak P.J., Banfield B.W., Smith G.A. Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 1998, 51:237-347.
14. Farnsworth A., Goldsmith K., Johnson D.C. Herpes simplex virus glycoproteins gD and gE/gI serve essential but redundant functions during acquisition of the virion envelope in the cytoplasm. J. Virol. 2003, 77(15):8481-8494.
15. Farnsworth A., Wisner T.W., Johnson D.C. Cytoplasmic residues of herpes simplex virus glycoprotein gE required for secondary envelopment and binding of tegument proteins VP22 and UL11 to gE and gD. J. Virol. 2007, 81(1):319-331.
16. Fuchs W., Klupp B.G., Granzow H., Hengartner C., Brack A., Mundt A., Enquist L.W., Mettenleiter T.C. Physical interaction between envelope glycoproteins E and M of pseudorabies virus and the major tegument protein UL49. J. Virol. 2002, 76(16):8208-8217.
17. Hafezi W., Bernard E., Cook R., Elliott G. Herpes simplex virus tegument protein VP22 contains an internal VP16 interaction domain and a C-terminal domain that are both required for VP22 assembly into the virus particle. J. Virol. 2005, 79(20):13082-13093.
18. Harty R.N., Paragas J., Sudol M., Palese P. A proline-rich motif within the matrix protein of vesicular stomatitis virus and rabies virus interacts with WW domains of cellular proteins: implications for viral budding. J. Virol. 1999, 73(4):2921-2929.
19. Heine J.W., Honess R.W., Cassai E., Roizman B. Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains. J. Virol. 1974, 14(3):640-651.
20. Ilsley J.L., Sudol M., Winder S.J. The WW domain: linking cell signalling to the membrane cytoskeleton. Cell. Signal. 2002, 14(3):183-189.
21. Ingham R.J., Colwill K., Howard C., Dettwiler S., Lim C.S., Yu J., Hersi K., Raaijmakers J., Gish G., Mbamalu G., Taylor L., Yeung B., Vassilovski G., Amin M., Chen F., Matskova L., Winberg G., Ernberg I., Linding R., O'Donnell P., Starostine A., Keller W., Metalnikov P., Stark C., Pawson T. WW domains provide a platform for the assembly of multiprotein networks. Mol. Cell. Biol. 2005, 25(16):7092-7106.
22. Kirchhausen T. Adaptors for clathrin-mediated traffic. Annu. Rev. Cell Dev. Biol. 1999, 15:705-732.
23. Kirchhausen T., Bonifacino J.S., Riezman H. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 1997, 9(4):488-495.
24. Lee J.H., Vittone V., Diefenbach E., Cunningham A.L., Diefenbach R.J. Identification of structural protein-protein interactions of herpes simplex virus type 1. Virology 2008, 378(2):347-354.
25. Leslie J., Rixon F.J., McLauchlan J. Overexpression of the herpes simplex virus type 1 tegument protein VP22 increases its incorporation into virus particles. Virology 1996, 220(1):60-68.
26. Loomis J.S., Bowzard J.B., Courtney R.J., Wills J.W. Intracellular trafficking of the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 2001, 75(24):12209-12219.
27. Loomis J.S., Courtney R.J., Wills J.W. Binding partners for the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 2003, 77(21):11417-11424.
28. Loomis J.S., Courtney R.J., Wills J.W. Packaging determinants in the UL11 tegument protein of herpes simplex virus type 1. J. Virol. 2006, 80(21):10534-10541.
29. Lyman M.G., Demmin G.L., Banfield B.W. The attenuated pseudorabies virus strain Bartha fails to package the tegument proteins Us3 and VP22. J. Virol. 2003, 77(2):1403-1414.
30. McMillan T.N., Johnson D.C. Cytoplasmic domain of herpes simplex virus gE causes accumulation in the trans-Golgi network, a site of virus envelopment and sorting of virions to cell junctions. J. Virol. 2001, 75(4):1928-1940.
31. Mettenleiter T.C. Herpesvirus assembly and egress. J. Virol. 2002, 76(4):1537-1547.
32. Mettenleiter T.C., Klupp B.G., Granzow H. Herpesvirus assembly: an update. Virus Res. 2009, 143(2):222-234.
33. Miranda-Saksena M., Boadle R.A., Armati P., Cunningham A.L. In rat dorsal root ganglion neurons, herpes simplex virus type 1 tegument forms in the cytoplasm of the cell body. J. Virol. 2002, 76(19):9934-9951.
34. Mouzakitis G., McLauchlan J., Barreca C., Kueltzo L., O'Hare P. Characterization of VP22 in herpes simplex virus-infected cells. J. Virol. 2005, 79(19):12185-12198.
35. Mukhopadhyay A., Lee G.E., Wilson D.W. The amino terminus of the herpes simplex virus 1 protein Vhs mediates membrane association and tegument incorporation. J. Virol. 2006, 80(20):10117-10127.
36. Murphy M.A., Bucks M.A., O'Regan K.J., Courtney R.J. The HSV-1 tegument protein pUL46 associates with cellular membranes and viral capsids. Virology 2008, 376(2):279-289.
37. Naldinho-Souto R., Browne H., Minson T. Herpes simplex virus tegument protein VP16 is a component of primary enveloped virions. J. Virol. 2006, 80(5):2582-2584.
38. O'Regan K.J., Bucks M.A., Murphy M.A., Wills J.W., Courtney R.J. A conserved region of the herpes simplex virus type 1 tegument protein VP22 facilitates interaction with the cytoplasmic tail of glycoprotein E (gE). Virology 2007, 358(1):192-200.
39. O'Regan K.J., Murphy M.A., Bucks M.A., Wills J.W., Courtney R.J. Incorporation of the herpes simplex virus type 1 tegument protein VP22 into the virus particle is independent of interaction with VP16. Virology 2007, 369(2):263-280.
40. Pomeranz L.E., Blaho J.A. Assembly of infectious Herpes simplex virus type 1 virions in the absence of full-length VP22. J. Virol. 2000, 74(21):10041-10054.
41. Roizman B., Pellett P.E. The family herpesviridae: a brief introduction. Fields Virology 2001, 2381-2387. Lippincott-Raven, Philadelphia. D.M. Knipe, P.M. Howley (Eds.).
42. Sanchez V., Greis K.D., Sztul E., Britt W.J. Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J. Virol. 2000, 74(2):975-986.
43. Schlegel E.F., Blaho J.A. A conserved carboxy-terminal domain in the major tegument structural protein VP22 facilitates virion packaging of a chimeric protein during productive herpes simplex virus 1 infection. Virology 2009, 387(2):449-458.
44. Skepper J.N., Whiteley A., Browne H., Minson A. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment→deenvelopment→reenvelopment pathway. J. Virol. 2001, 75(12):5697-5702.
45. Smith K.O. Relationship between the envelope and the infectivity of herpes simplex virus. Proc. Soc. Exp. Biol. Med. 1964, 115:814-816.
46. Stylianou J., Maringer K., Cook R., Bernard E., Elliott G. Virion incorporation of the herpes simplex virus type 1 tegument protein VP22 occurs via glycoprotein E-specific recruitment to the late secretory pathway. J. Virol. 2009, 83(10):5204-5218.
47. Tugizov S., Maidji E., Xiao J., Pereira L. An acidic cluster in the cytosolic domain of human cytomegalovirus glycoprotein B is a signal for endocytosis from the plasma membrane. J. Virol. 1999, 73(10):8677-8688.
48. van Genderen I.L., Brandimarti R., Torrisi M.R., Campadelli G., van Meer G. The phospholipid composition of extracellular herpes simplex virions differs from that of host cell nuclei. Virology 1994, 200(2):831-836.
49. Verdecia M.A., Bowman M.E., Lu K.P., Hunter T., Noel J.P. Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat. Struct. Biol. 2000, 7(8):639-643.
50. Vittone V., Diefenbach E., Triffett D., Douglas M.W., Cunningham A.L., Diefenbach R.J. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 2005, 79(15):9566-9571.
51. Wan L., Molloy S.S., Thomas L., Liu G., Xiang Y., Rybak S.L., Thomas G. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 1998, 94(2):205-216.
52. Whealy M.E., Card J.P., Meade R.P., Robbins A.K., Enquist L.W. Effect of brefeldin A on alphaherpesvirus membrane protein glycosylation and virus egress. J. Virol. 1991, 65(3):1066-1081.
53. Whiteley A., Bruun B., Minson T., Browne H. Effects of targeting herpes simplex virus type 1 gD to the endoplasmic reticulum and trans-Golgi network. J. Virol. 1999, 73(11):9515-9520.