Identification of interaction domains within the UL37 tegument protein of herpes simplex virus type 1

Virology

Volumn 416, Issue 1-2, 2011, Pages 42-53

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

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b University of North Carolina   (United States)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

Assembly; Herpes; Herpesvirus; HSV 1; Tegument; UL36; UL37; VP1 2

Indexed keywords

PROTEIN VP1; PROTEIN VP2; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING COMPETITION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE DELETION; GENETIC TRANSFECTION; HERPES SIMPLEX VIRUS 1; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; VERO CELL;

ANIMALS; ANTIBODIES, VIRAL; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 1, HUMAN; IMMUNOPRECIPITATION; PROTEIN STRUCTURE, TERTIARY; VERO CELLS; VIRAL STRUCTURAL PROTEINS;

HERPES; HERPESVIRIDAE; HUMAN HERPESVIRUS 1;

EID: 79958041282     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.04.018     Document Type: Article

References (67)

1. Albright A.G., Jenkins F.J. The herpes simplex virus UL37 protein is phosphorylated in infected cells. J. Virol. 1993, 67(8):4842-4847.
2. Antinone S.E., Smith G.A. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J. Virol. 2010, 84(3):1504-1512.
3. Bechtel J.T., Shenk T. Human cytomegalovirus UL47 tegument protein functions after entry and before immediate-early gene expression. J. Virol. 2002, 76(3):1043-1050.
4. Boll W., Ohno H., Songyang Z., Rapoport I., Cantley L.C., Bonifacino J.S., Kirchhausen T. Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 1996, 15(21):5789-5795.
5. 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.
6. Coller K.E., Lee J.I., Ueda A., Smith G.A. The capsid and tegument of the alphaherpesviruses are linked by an interaction between the UL25 and VP1/2 proteins. J. Virol. 2007, 81(21):11790-11797.
7. Desai P.J. A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unenveloped DNA-filled capsids in the cytoplasm of infected cells. J. Virol. 2000, 74(24):11608-11618.
8. Desai P., DeLuca N.A., Glorioso J.C., Person S. Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA. J. Virol. 1993, 67(3):1357-1364.
9. Desai P., Sexton G.L., McCaffery J.M., Person S. A null mutation in the gene encoding the herpes simplex virus type 1 UL37 polypeptide abrogates virus maturation. J. Virol. 2001, 75(21):10259-10271.
10. Desai P., Sexton G.L., Huang E., Person S. Localization of herpes simplex virus type 1 UL37 in the Golgi complex requires UL36 but not capsid structures. J. Virol. 2008, 82(22):11354-11361.
11. Fossum E., Friedel C.C., Rajagopala S.V., Titz B., Baiker A., Schmidt T., Kraus T., Stellberger T., Rutenberg C., Suthram S., Bandyopadhyay S., Rose D., von Brunn A., Uhlmann M., Zeretzke C., Dong Y.A., Boulet H., Koegl M., Bailer S.M., Koszinowski U., Ideker T., Uetz P., Zimmer R., Haas J. Evolutionarily conserved herpesviral protein interaction networks. PLoS Pathog. 2009, 5(9):e1000570.
12. Fuchs W., Granzow H., Klupp B.G., Kopp M., Mettenleiter T.C. The UL48 tegument protein of pseudorabies virus is critical for intracytoplasmic assembly of infectious virions. J. Virol. 2002, 76(13):6729-6742.
13. Fuchs W., Klupp B.G., Granzow H., Mettenleiter T.C. Essential function of the pseudorabies virus UL36 gene product is independent of its interaction with the UL37 protein. J. Virol. 2004, 78(21):11879-11889.
14. Gibson W., Roizman B. Proteins specified by herpes simplex virus. 8. Characterization and composition of multiple capsid forms of subtypes 1 and 2. J. Virol. 1972, 10(5):1044-1052.
15. Granzow H., Klupp B.G., Mettenleiter T.C. The pseudorabies virus US3 protein is a component of primary and of mature virions. J. Virol. 2004, 78(3):1314-1323.
16. Grunewald K., Desai P., Winkler D.C., Heymann J.B., Belnap D.M., Baumeister W., Steven A.C. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 2003, 302(5649):1396-1398.
17. 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.
18. Honess R.W., Roizman B. 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. 1973, 12(6):1347-1365.
19. Jovasevic V., Liang L., Roizman B. Proteolytic cleavage of VP1-2 is required for release of herpes simplex virus 1 DNA into the nucleus. J. Virol. 2008, 82(7):3311-3319.
20. Kattenhorn L.M., Korbel G.A., Kessler B.M., Spooner E., Ploegh H.L. A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol. Cell 2005, 19(4):547-557.
21. Kelly B.J., Fraefel C., Cunningham A.L., Diefenbach R.J. Functional roles of the tegument proteins of herpes simplex virus type 1. Virus Res. 2009, 145(2):173-186.
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. Klupp B.G., Granzow H., Mundt E., Mettenleiter T.C. Pseudorabies virus UL37 gene product is involved in secondary envelopment. J. Virol. 2001, 75(19):8927-8936.
25. Klupp B.G., Fuchs W., Granzow H., Nixdorf R., Mettenleiter T.C. Pseudorabies virus UL36 tegument protein physically interacts with the UL37 protein. J. Virol. 2002, 76(6):3065-3071.
26. Ko D.H., Cunningham A.L., Diefenbach R.J. The major determinant for addition of tegument protein pUL48 (VP16) to capsids in herpes simplex virus type 1 is the presence of the major tegument protein pUL36 (VP1/2). J. Virol. 2010, 84(3):1397-1405.
27. 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.
28. Leege T., Granzow H., Fuchs W., Klupp B.G., Mettenleiter T.C. Phenotypic similarities and differences between UL37-deleted pseudorabies virus and herpes simplex virus type 1. J. Gen. Virol. 2009, 90(Pt 7):1560-1568.
29. Leuzinger H., Ziegler U., Schraner E.M., Fraefel C., Glauser D.L., Heid I., Ackermann M., Mueller M., Wild P. Herpes simplex virus 1 envelopment follows two diverse pathways. J. Virol. 2005, 79(20):13047-13059.
30. Liu X., Fitzgerald K., Kurt-Jones E., Finberg R., Knipe D.M. Herpesvirus tegument protein activates NF-kappaB signaling through the TRAF6 adaptor protein. Proc. Natl Acad. Sci. U. S. A. 2008, 105(32):11335-11339.
31. 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.
32. Luxton G.W., Haverlock S., Coller K.E., Antinone S.E., Pincetic A., Smith G.A. Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl Acad. Sci. U. S. A. 2005, 102(16):5832-5837.
33. Luxton G.W., Lee J.I., Haverlock-Moyns S., Schober J.M., Smith G.A. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J. Virol. 2006, 80(1):201-209.
34. McLauchlan J. The abundance of the herpes simplex virus type 1 UL37 tegument protein in virus particles is closely controlled. J. Gen. Virol. 1997, 78189-78194.
35. McLauchlan J., Liefkens K., Stow N.D. The herpes simplex virus type 1 UL37 gene product is a component of virus particles. J. Gen. Virol. 1994, 75(Pt 8):2047-2052.
36. McNabb D.S., Courtney R.J. Characterization of the large tegument protein (ICP1/2) of herpes simplex virus type 1. Virology 1992, 190(1):221-232.
37. Meckes D.G., Wills J.W. Dynamic interactions of the UL16 tegument protein with the capsid of herpes simplex virus. J. Virol. 2007, 81(23):13028-13036.
38. Meckes D.G., Wills J.W. Structural rearrangement within an enveloped virus upon binding to the host cell. J. Virol. 2008, 82(21):10429-10435.
39. Mettenleiter T.C., Klupp B.G., Granzow H. Herpesvirus assembly: an update. Virus Res. 2009, 143(2):222-234.
40. Mijatov B., Cunningham A.L., Diefenbach R.J. Residues F593 and E596 of HSV-1 tegument protein pUL36 (VP1/2) mediate binding of tegument protein pUL37. Virology 2007, 368(1):26-31.
41. 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.
42. 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.
43. Newcomb W.W., Brown J.C. Time-dependent transformation of the herpesvirus tegument. J. Virol. 2009, 83(16):8082-8089.
44. Newcomb W.W., Brown J.C. Structure and capsid association of the herpesvirus large tegument protein UL36. J. Virol. 2010, 84(18):9408-9414.
45. Padula M.E., Sydnor M.L., Wilson D.W. Isolation and preliminary characterization of herpes simplex virus 1 primary enveloped virions from the perinuclear space. J. Virol. 2009, 83(10):4757-4765.
46. Pasdeloup D., Blondel D., Isidro A.L., Rixon F.J. Herpesvirus capsid association with the nuclear pore complex and viral DNA release involve the nucleoporin CAN/Nup214 and the capsid protein pUL25. J. Virol. 2009, 83(13):6610-6623.
47. Pasdeloup D., Beilstein F., Roberts A.P., McElwee M., McNab D., Rixon F.J. Inner tegument protein pUL37 of herpes simplex virus type 1 is involved in directing capsids to the trans-Golgi network for envelopment. J. Gen. Virol. 2010, 91(Pt 9):2145-2151.
48. Radtke K., Kieneke D., Wolfstein A., Michael K., Steffen W., Scholz T., Karger A., Sodeik B. Plus- and minus-end directed microtubule motors bind simultaneously to herpes simplex virus capsids using different inner tegument structures. PLoS Pathog. 2010, 6(7):e1000991.
49. Read G.S., Patterson M. Packaging of the virion host shutoff (Vhs) protein of herpes simplex virus: two forms of the Vhs polypeptide are associated with intranuclear B and C capsids, but only one is associated with enveloped virions. J. Virol. 2007, 81(3):1148-1161.
50. Reynolds A.E., Wills E.G., Roller R.J., Ryckman B.J., Baines J.D. Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J. Virol. 2002, 76(17):8939-8952.
51. Roberts A.P., Abaitua F., O'Hare P., McNab D., Rixon F.J., Pasdeloup D. Differing roles of inner tegument proteins pUL36 and pUL37 during entry of herpes simplex virus type 1. J. Virol. 2009, 83(1):105-116.
52. Roizman B., Knipe D.M., Whitley R.J. Herpes simplex viruses. Fields Virology 2007, 2501-2601. Lippincott, Williams and Wilkins, Philadelphia, Pa. D.M. Knipe, P.M. Howley (Eds.).
53. Rozen R., Sathish N., Li Y., Yuan Y. Virion-wide protein interactions of Kaposi's sarcoma-associated herpesvirus. J. Virol. 2008, 82(10):4742-4750.
54. Schlieker C., Korbel G.A., Kattenhorn L.M., Ploegh H.L. A deubiquitinating activity is conserved in the large tegument protein of the herpesviridae. J. Virol. 2005, 79(24):15582-15585.
55. Schmitz J.B., Albright A.G., Kinchington P.R., Jenkins F.J. The UL37 protein of herpes simplex virus type 1 is associated with the tegument of purified virions. Virology 1995, 206(2):1055-1065.
56. Shelton L.S., Pensiero M.N., Jenkins F.J. Identification and characterization of the herpes simplex virus type 1 protein encoded by the UL37 open reading frame. J. Virol. 1990, 64(12):6101-6109.
57. Smith K.O. Relationship between the envelope and the infectivity of herpes simplex virus. Proc. Soc. Exp. Biol. Med. 1964, 115814-115816.
58. Spear P.G., Roizman B. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion. J. Virol. 1972, 9(1):143-159.
59. Trus B.L., Newcomb W.W., Cheng N., Cardone G., Marekov L., Homa F.L., Brown J.C., Steven A.C. Allosteric signaling and a nuclear exit strategy: binding of UL25/UL17 heterodimers to DNA-Filled HSV-1 capsids. Mol. Cell 2007, 26(4):479-489.
60. Uetz P., Dong Y.A., Zeretzke C., Atzler C., Baiker A., Berger B., Rajagopala S.V., Roupelieva M., Rose D., Fossum E., Haas J. Herpesviral protein networks and their interaction with the human proteome. Science 2006, 311(5758):239-242.
61. 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.
62. 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.
63. Watanabe D., Ushijima Y., Goshima F., Takakuwa H., Tomita Y., Nishiyama Y. Identification of nuclear export signal in UL37 protein of herpes simplex virus type 2. Biochem. Biophys. Res. Commun. 2000, 276(3):1248-1254.
64. Wild P., Engels M., Senn C., Tobler K., Ziegler U., Schraner E.M., Loepfe E., Ackermann M., Mueller M., Walther P. Impairment of nuclear pores in bovine herpesvirus 1-infected MDBK cells. J. Virol. 2005, 79(2):1071-1083.
65. Wolfstein A., Nagel C.H., Radtke K., Dohner K., Allan V.J., Sodeik B. The inner tegument promotes herpes simplex virus capsid motility along microtubules in vitro. Traffic 2006, 7(2):227-237.
66. Xia D., Srinivas S., Sato H., Pesnicak L., Straus S.E., Cohen J.I. Varicella-zoster virus open reading frame 21, which is expressed during latency, is essential for virus replication but dispensable for establishment of latency. J. Virol. 2003, 77(2):1211-1218.
67. Zhou Z.H., Chen D.H., Jakana J., Rixon F.J., Chiu W. Visualization of tegument-capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol. 1999, 73(4):3210-3218.