Escape of herpesviruses from the nucleus

Reviews in Medical Virology

Volumn 20, Issue 4, 2010, Pages 214-230

  Lee, Chung Pei ^a   Chen, Mei Ru ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PHOSPHOTRANSFERASE; NUCLEOCAPSID PROTEIN;

ALPHAHERPESVIRINAE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CYTOPLASM; DNA REPLICATION; DNA VIRUS; GAMMAHERPESVIRINAE; HERPES VIRUS; MACROMOLECULE; NONHUMAN; NUCLEAR LAMINA; NUCLEAR PORE; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; VIRION; VIRUS GENOME; VIRUS NUCLEOCAPSID; ACTIVE TRANSPORT; ANIMAL; GENETICS; HERPES VIRUS INFECTION; HUMAN; METABOLISM; PROTEIN TRANSPORT; VIROLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CYTOPLASM; HERPESVIRIDAE; HERPESVIRIDAE INFECTIONS; HUMANS; NUCLEOCAPSID PROTEINS; PROTEIN TRANSPORT;

EID: 77953302554     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.643     Document Type: Review

References (149)

1. Du MQ, Bacon CM, Isaacson PG. Kaposi sarcomaassociated herpesvirus/human herpesvirus 8 and lymphoproliferative disorders. J Clin Pathol 2007; 60: 1350-1357.
2. Mocarski ES Jr, Shenk T. Pass RF. Cytomegaloviruses. In Fields Virology, 5th edn, Knipe DM, Howley PM (eds). Lippincott Williams & Wilkins: Philadelphia, 2007; 2701-2772.
3. Nahmias AJ, Roizman B. Infection with herpessimplex viruses 1 and 2. 3. N Engl J Med 1973; 289: 781-789.
4. Young LS, Rickinson AB. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004; 4: 757-768.
5. McGeoch DJ, Rixon FJ, Davison AJ. Topics in herpesvirus genomics and evolution. Virus Res 2006; 117: 90-104.
6. Greber UF, Fassati A. Nuclear import of viral DNA genomes. Traffic 2003; 4: 136-143.
7. Whitley RJ. Herpes simplex viruses. In Fields Virology, 4th edn. Knipe DM, Howley PM (eds). Lippincott Williams & Wilkins, Philadelphia, 2001; 2461-2510.
8. Moore PS, Chang Y. Kaposi's sarcoma-associated herpesvirus immunoevasion and tumorigenesis: two sides of the same coin? Annu Rev Microbiol 2003; 57: 609-639.
9. Roizman B, Knipe DM. Herpes simplex viruses and their replication. In Fields Virology, 4th ed., Knipe DM and Howley PM (eds). Lippincott Williams & Wilkins: Philadelphia, 2001; 2399-2459.
10. Lu CC, Chen MR. Lytic replication of Epstein-Barr virus. Future Virology 2006; 1: 435-446.
11. Monier K, Armas JC, Etteldorf S, et al. Annexation of the interchromosomal space during viral infection. Nat Cell Biol 2000; 2: 661-665.
12. Hertel L, Chou S, Mocarski ES. Viral and cell cycleregulated kinases in cytomegalovirus-induced pseudomitosis and replication. PLoS Pathog 2007; 3: e6.
13. Lee CP, Chen JY, Wang JT, et al. Epstein-Barr virus BGLF4 kinase induces premature chromosome condensation through activation of condensin and topoisomerase II. J Virol 2007; 81: 5166-5180.
14. Newcomb WW, Homa FL, Thomsen DR, et al. Assembly of the herpes simplex virus procapsid from purified components and identification of small complexes containing the major capsid and scaffolding proteins. J Virol 1999; 73: 4239-4250.
15. Steven AC, Spear PG. Herpesvirus capsid assembly and envelopment. In Structural Biology of Viruses, Chiu W, Burnett RM, Garcea R (eds). Oxford University Press: New York, 1997; 312-351.
16. Tatman JD, Preston VG, Nicholson P, et al. Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculoviruses. J Gen Virol 1994; 75: 1101-1113.
17. Thomsen DR, Roof LL, Homa FL. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant baculoviruses expressing HSV capsid proteins. J Virol 1994; 68: 2442-2457.
18. Mettenleiter TC, Klupp BG, Granzow H. Herpesvirus assembly: a tale of two membranes. Curr Opin Microbiol 2006; 9: 423-429.
19. Singer GP, Newcomb WW, Thomsen DR, et al. Identification of a region in the herpes simplex virus scaffolding protein required for interaction with the portal. J Virol 2005; 79: 132-139.
20. Walters JN, Sexton GL, McCaffery JM, et al. Mutation of single hydrophobic residue I27, L35, F39, L58, L65, L67, or L71 in the N terminus of VP5 abolishes interaction with the scaffold protein and prevents closure of herpes simplex virus type 1 capsid shells. J Virol 2003; 77: 4043-4059.
21. Henson BW, Perkins EM, Cothran JE, et al. Selfassembly of Epstein-Barr virus capsids. J Virol 2009; 83: 3877-3890.
22. Perkins EM, Anacker D, Davis A, et al. Small capsid protein pORF65 is essential for assembly of Kaposi's sarcoma-associated herpesvirus capsids. J Virol 2008; 82: 7201-7211.
23. Visalli RJ, van Zeijl M. DNA encapsidation as a target for anti-herpesvirus drug therapy. Antiviral Res 2003; 59: 73-87.
24. Feierbach B, Piccinotti S, Bisher M, et al. Alpha-herpesvirus infection induces the formation of nuclear actin filaments. PLoS Pathog 2006; 2: e85.
25. Forest T, Barnard S, Baines JD. Active intranuclear movement of herpesvirus capsids. Nat Cell Biol 2005; 7: 429-431.
26. Fawcett DW. On the occurrence of a fibrous lamina on the inner aspect of the nuclear envelope in certain cells of vertebrates. Am J Anat 1966; 119: 129-145.
27. Gruenbaum Y, Margalit A, Goldman RD, et al. The nuclear lamina comes of age. Nat Rev Mol Cell Biol 2005; 6: 21-31.
28. Stuurman N, Heins S, Aebi U. Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 1998; 122: 42-66.
29. Fisher DZ, Chaudhary N, Blobel G. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci U S A 1986; 83: 6450-6454.
30. Hoger TH, Zatloukal K, Waizenegger I, et al. Characterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin. Chromosoma 1990; 100: 67-69.
31. Broers JL, Ramaekers FC, Bonne G, et al. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 2006; 86: 967-1008.
32. Hutchison CJ, Alvarez-Reyes M, Vaughan OA. Lamins in disease: why do ubiquitously expressed nuclear envelope proteins give rise to tissue-specific disease phenotypes? J Cell Sci 2001; 114: 9-19.
33. Vlcek S, Foisner R. Lamins and lamin-associated proteins in aging and disease. Curr Opin Cell Biol 2007; 19: 298-304.
34. Reynolds AE, Liang L, Baines JD. Conformational changes in the nuclear lamina induced by herpes simplex virus type 1 require genes U(L)31 and U(L)34. J Virol 2004; 78: 5564-5575.
35. Goldberg MW, Fiserova J, Huttenlauch I, et al. A new model for nuclear lamina organization. Biochem Soc Trans 2008; 36: 1339-1343.
36. McKeon FD, Kirschner MW, Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 1986; 319: 463-468.
37. Moir RD, Spann TP, Goldman RD. The dynamic properties and possible functions of nuclear lamins. Int Rev Cytol 1995; 162B: 141-182.
38. Prokocimer M, Davidovich M, Nissim-Rafinia M, et al. Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med 2009. doi: 10.1111/j.1582-4934.2008.00676.x (published online ahead of print on 4 Feb 2009)
39. Nigg EA. Assembly and cell cycle dynamics of the nuclear lamina. Semin Cell Biol 1992; 3: 245-253.
40. Brodie C and Blumberg PM. Regulation of cell apoptosis by protein kinase c delta. Apoptosis 2003; 8: 19-27.
41. Collas P. Sequential PKC- and Cdc2-mediated phosphorylation events elicit zebrafish nuclear envelope disassembly. J Cell Sci 1999; 112: 977-987.
42. Cross T, Griffiths G, Deacon E, et al. PKC-delta is an apoptotic lamin kinase. Oncogene 2000; 19: 2331-2337.
43. Heald R, McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 1990; 61: 579-589. (Pubitemid 20169014)
44. Peter M, Nakagawa J, Doree M, et al. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 1990; 61: 591-602.
45. Heitlinger E, Peter M, Haner M, et al. Expression of chicken lamin B2 in Escherichia coli: characterization of its structure, assembly, and molecular interactions. J Cell Biol 1991; 113: 485-495. (Pubitemid 21926006)
46. Peter M, Heitlinger E, Haner M, et al. Disassembly of in vitro formed lamin head-to-tail polymers by CDC2 kinase. Embo J 1991; 10: 1535-1544. (Pubitemid 21905618)
47. Alber F, Dokudovskaya S, Veenhoff LM, et al. The molecular architecture of the nuclear pore complex. Nature 2007; 450: 695-701. (Pubitemid 350207701)
48. Bjerke SL, Roller RJ. Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology 2006; 347: 261-276.
49. Hamirally S, Kamil JP, Ndassa-Colday YM, et al. Viral mimicry of Cdc2/cyclin-dependent kinase 1 mediates disruption of nuclear lamina during human cytomegalovirus nuclear egress. PLoS Pathog 2009; 5: e1000275.
50. Lee CP, Huang YH, Lin SF, et al. Epstein-Barr virus BGLF4 kinase induces disassembly of the nuclear lamina to facilitate virion production. J Virol 2008; 82: 11913-11926.
51. Mou F, Forest T, Baines JD. US3 of herpes simplex virus type 1 encodes a promiscuous protein kinase that phosphorylates and alters localization of lamin A/C in infected cells. J Virol 2007; 81: 6459-6470. (Pubitemid 46878051)
52. Park R, Baines JD. Herpes simplex virus type 1 infection induces activation and recruitment of protein kinase C to the nuclear membrane and increased phosphorylation of lamin B. J Virol 2006; 80: 494-504.
53. Scott ES, O'Hare P. Fate of the inner nuclear membrane protein lamin B receptor and nuclear lamins in herpes simplex virus type 1 infection. J Virol 2001; 75: 8818-8830. (Pubitemid 32768985)
54. Nagel CH, Dohner K, Fathollahy M, et al. Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J Virol 2008; 82: 3109-3124.
55. Wild P, Senn C, Manera CL, et al. Exploring the nuclear envelope of herpes simplex virus 1-infected cells by high-resolution microscopy. J Virol 2009; 83: 408-419.
56. Leuzinger H, Ziegler U, Schraner EM, et al. Herpes simplex virus 1 envelopment follows two diverse pathways. J Virol 2005; 79: 13047-13059.
57. Hofemeister H, O'Hare P. Nuclear pore composition and gating in herpes simplex virus-infected cells. J Virol 2008; 82: 8392-8399.
58. Darlington RW, Moss LH, 3rd. Herpesvirus envelopment. J Virol 1968; 2: 48-55.
59. Johnson DC, Spear PG. Monensin inhibits the processing of herpes simplex virus glycoproteins, their transport to the cell surface, and the egress of virions from infected cells. J Virol 1982; 43: 1102-1112.
60. Baines JD, Hsieh CE, Wills E, et al. Electron tomography of nascent herpes simplex virus virions. J Virol 2007; 81: 2726-2735. (Pubitemid 46447037)
61. Granzow H, Klupp BG, Fuchs W, et al. Egress of alphaherpesviruses: comparative ultrastructural study. J Virol 2001; 75: 3675-3684. (Pubitemid 32246377)
62. Mettenleiter TC. Herpesvirus assembly and egress. J Virol 2002; 76: 1537-1547.
63. Remillard-Labrosse G, Guay GLippe R. Reconstitution of herpes simplex virus type 1 nuclear capsid egress in vitro. J Virol 2006; 80: 9741-9753. (Pubitemid 44435648)
64. Skepper JN, Whiteley A, Browne H, et al. Herpes simplex virus nucleocapsids mature to progeny virions by an envelopment - >deenvelopment- > reenvelopment pathway. J Virol 2001; 75: 5697-5702. (Pubitemid 32488165)
65. Smith JD. An additional role for the outer nuclear membrane in the morphogenesis of herpes simplex virus. Intervirology 1980; 13: 312-316.
66. Stackpole CW. Herpes-type virus of the frog renal adenocarcinoma. I. Virus development in tumor transplants maintained at low temperature. J Virol 1969; 4: 75-93.
67. Mettenleiter TC, Minson T. Egress of alphaherpesviruses. J Virol 2006; 80: 1610-1611; author reply 1611-1612.
68. Leach N, Bjerke SL, Christensen DK, et al. Emerin is hyperphosphorylated and redistributed in herpes simplex virus type 1-infected cells in a manner dependent on both UL34 and US3. J Virol 2007; 81: 10792-10803.
69. Morris JB, Hofemeister HO'Hare P. Herpes simplex virus infection induces phosphorylation and delocalization of emerin, a key inner nuclear membrane protein. J Virol 2007; 81: 4429-4437.
70. Reynolds AE, Wills EG, Roller RJ, et al. 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: 8939-8952.
71. Kawaguchi Y, Kato K, Tanaka M, et al. Conserved protein kinases encoded by herpesviruses and cellular protein kinase cdc2 target the same phosphorylation site in eukaryotic elongation factor 1delta. J Virol 2003; 77: 2359-2368. (Pubitemid 36222759)
72. Gershburg E, Pagano JS. Conserved herpesvirus protein kinases. Biochim Biophys Acta 2008; 1784: 203-212.
73. Zhu J, Liao G, Shan L, et al. Protein array identification of substrates of the Epstein-Barr virus protein kinase BGLF4. J Virol 2009; 83: 5219-5231.
74. Prichard MN. Function of human cytomegalovirus UL97 kinase in viral infection and its inhibition by maribavir. Rev Med Virol 2009; 19: 215-229.
75. Kato A, Yamamoto M, Ohno T, et al. Herpes simplex virus 1-encoded protein kinase UL13 phosphorylates viral Us3 protein kinase and regulates nuclear localization of viral envelopment factors UL34 and UL31. J Virol 2006; 80: 1476-1486.
76. Marschall M, Marzi A, aus dem Siepen P, et al. Cellular p32 recruits cytomegalovirus kinase pUL97 to redistribute the nuclear lamina. J Biol Chem 2005; 280: 33357-33367.
77. Gershburg E, Raffa S, Torrisi MR, et al. Epstein-Barr virus-encoded protein kinase (BGLF4) is involved in production of infectious virus. J Virol 2007; 81: 5407-5412.
78. Klupp BG, Granzow H, Mettenleiter TC. Effect of the pseudorabies virus US3 protein on nuclear membrane localization of the UL34 protein and virus egress from the nucleus. J Gen Virol 2001; 82: 2363-2371.
79. Poon AP, Benetti L, Roizman B. U(S)3 and U(S)3.5 protein kinases of herpes simplex virus 1 differ with respect to their functions in blocking apoptosis and in virion maturation and egress. J Virol 2006; 80: 3752-3764.
80. Wagenaar F, Pol JM, Peeters B, et al. The US3-encoded protein kinase from pseudorabies virus affects egress of virions from the nucleus. J Gen Virol 1995; 76: 1851-1859.
81. Farina A, Santarelli R, Gonnella R, et al. The BFRF1 gene of Epstein-Barr virus encodes a novel protein. J Virol 2000; 74: 3235-3244.
82. Gonnella R, Farina A, Santarelli R, et al. Characterization and intracellular localization of the Epstein-Barr virus protein BFLF2: interactions with BFRF1 and with the nuclear lamina. J Virol 2005; 79: 3713-3727.
83. Klupp BG, Granzow H, Mettenleiter TC. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J Virol 2000; 74: 10063-10073.
84. Muranyi W, Haas J, Wagner M, et al. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 2002; 297: 854-857. (Pubitemid 34839639)
85. Reynolds AE, Ryckman BJ, Baines JD, et al. U(L)31 and U(L)34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J Virol 2001; 75: 8803-8817.
86. Santarelli R, Farina A, Granato M, et al. Identification and characterization of the product encoded by ORF69 of Kaposi's sarcoma-associated herpesvirus. J Virol 2008; 82: 4562-4572.
87. Schnee M, Ruzsics Z, Bubeck A, et al. Common and specific properties of herpesvirus UL34/UL31 protein family members revealed by protein complementation assay. J Virol 2006; 80: 11658-11666. (Pubitemid 44788879)
88. Ye GJ, Roizman B. The essential protein encoded by the UL31 gene of herpes simplex virus 1 depends for its stability on the presence of UL34 protein. Proc Natl Acad Sci U S A 2000; 97: 11002-11007.
89. Camozzi D, Pignatelli S, Valvo C, et al. Remodelling of the nuclear lamina during human cytomegalovirus infection: role of the viral proteins pUL50 and pUL53. J Gen Virol 2008; 89: 731-740.
90. Milbradt J, Auerochs S, Marschall M. Cytomegaloviral proteins pUL50 and pUL53 are associated with the nuclear lamina and interact with cellular protein kinase C. J Gen Virol 2007; 88: 2642-2650. (Pubitemid 47555015)
91. Milbradt J, Auerochs S, Sticht H, et al. Cytomegaloviral proteins that associate with the nuclear lamina: components of a postulated nuclear egress complex. J Gen Virol 2009; 90: 579-590.
92. Farina A, Feederle R, Raffa S, et al. BFRF1 of Epstein-Barr virus is essential for efficient primary viral envelopment and egress. J Virol 2005; 79: 3703-3712. (Pubitemid 40327958)
93. Roller RJ, Zhou Y, Schnetzer R, et al. Herpes simplex virus type 1 U(L)34 gene product is required for viral envelopment. J Virol 2000; 74: 117-129.
94. Klupp BG, Granzow H, Fuchs W, et al. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci U S A 2007; 104: 7241-7246. (Pubitemid 47186039)
95. Chang YE, Roizman B. The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J Virol 1993; 67: 6348-6356. (Pubitemid 23309098)
96. Purves FC, Spector D, Roizman B. UL34, the target of the herpes simplex virus U(S)3 protein kinase, is a membrane protein which in its unphosphorylated state associates with novel phosphoproteins. J Virol 1992; 66: 4295-4303.
97. Ryckman BJ, Roller RJ. Herpes simplex virus type 1 primary envelopment: UL34 protein modification and the US3-UL34 catalytic relationship. J Virol 2004; 78: 399-412.
98. Purves FC, Spector D, Roizman B. The herpes simplex virus 1 protein kinase encoded by the US3 gene mediates posttranslational modification of the phosphoprotein encoded by the UL34 gene. J Virol 1991; 65: 5757-5764.
99. Mou F, Wills E, Baines JD. Phosphorylation of the UL31 protein of Herpes simplex virus 1 by the US3 encoded kinase regulates localization of the nuclear envelopment complex and egress of nucleocapsids. J Virol 2009; 83: 5181-5191.
100. Wills E, Mou F, Baines JD. The UL31 and UL34 gene products of Herpes simplex virus 1 are required for optimal localization of viral glycoproteins D and M to the inner nuclear membrane of infected cells. J Virol 2009; 83: 4800-4809.
101. Padula ME, Sydnor ML, Wilson DW. Isolation and preliminary characterization of HSV-1 primary enveloped virions from the perinuclear space. J Virol 2009; 83: 4757-4765.
102. Foster TP, Kousoulas KG. Genetic analysis of the role of herpes simplex virus type 1 glycoprotein K in infectious virus production and egress. J Virol 1999; 73: 8457-8468.
103. Peeters B, de Wind N, Hooisma M, et al. Pseudorabies virus envelope glycoproteins gp50 and gII are essential for virus penetration, but only gII is involved in membrane fusion. J Virol 1992; 66: 894-905.
104. Farnsworth A, Wisner TW, Webb M, et al. Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. Proc Natl Acad Sci U S A 2007; 104: 10187-10192.
105. Klupp B, Altenschmidt J, Granzow H, et al. Glycoproteins required for entry are not necessary for egress of pseudorabies virus. J Virol 2008; 82: 6299-6309.
106. Wisner TW, Wright CC, Kato A, et al. Herpesvirus gB-induced fusion between the virion envelope and outer nuclear membrane during virus egress is regulated by the viral US3 kinase. J Virol 2009; 83: 3115-3126.
107. Granzow H, Klupp BG, Mettenleiter TC. The pseudorabies virus US3 protein is a component of primary and of mature virions. J Virol 2004; 78: 1314-1323.
108. Sam MD, Evans BT, Coen DM, et al. Biochemical, biophysical, and mutational analyses of subunit interactions of the human cytomegalovirus nuclear egress complex. J Virol 2009; 83: 2996-3006.
109. Lake CM, Hutt-Fletcher LM. The Epstein-Barr virus BFRF1 and BFLF2 proteins interact and coexpression alters their cellular localization. Virology 2004; 320: 99-106.
110. Epstein MA, Achong BC. Morphology of the virus and virus-induced cytopathologic changes. In The Epstein-Barr virus, Epstein MA, Achong BC (eds). Springer Verlag: New York, 1979; 23-27.
111. Feederle R, Bannert H, Lips H, et al. The Epstein-Barr virus alkaline exonuclease BGLF5 serves pleiotropic functions in virus replication. J Virol 2009; 83: 4952-4962.
112. Torrisi MR, Cirone M, Pavan A, et al. Localization of Epstein-Barr virus envelope glycoproteins on the inner nuclear membrane of virus-producing cells. J Virol 1989; 63: 828-832.
113. Granato M, Feederle R, Farina A, et al. Deletion of Epstein-Barr virus BFLF2 leads to impaired viral DNA packaging and primary egress as well as to the production of defective viral particles. J Virol 2008; 82: 4042-4051.
114. Mettenleiter TC. Budding events in herpesvirus morphogenesis. Virus Res 2004; 106: 167-180.
115. Mettenleiter TC, Klupp BG, Granzow H. Herpesvirus assembly: an update. Virus Res 2009; 143: 222-234.
116. Houben F, Ramaekers FC, Snoeckx LH, et al. Role of nuclear lamina-cytoskeleton interactions in the maintenance of cellular strength. Biochim Biophys Acta 2007; 1773: 675-686.
117. Luxton GW, Lee JI, Haverlock-Moyns S, et al. The pseudorabies virus VP1/2 tegument protein is required for intracellular capsid transport. J Virol 2006; 80: 201-209.
118. Sathish N, Zhu FX, Yuan Y. Kaposi's sarcoma-associated herpesvirus ORF45 interacts with kinesin-2 transporting viral capsid-tegument complexes along microtubules. PLoS Pathog 2009; 5: e1000332.
119. Shanda SK, Wilson DW. UL36p is required for efficient transport of membrane-associated herpes simplex virus type 1 along microtubules. J Virol 2008; 82: 7388-7394.
120. Fuchs W, Klupp BG, Granzow H, et al. The interacting UL31 and UL34 gene products of pseudorabies virus are involved in egress from the host-cell nucleus and represent components of primary enveloped but not mature virions. J Virol 2002; 76: 364-378.
121. Asai R, Ohno T, Kato A, et al. Identification of proteins directly phosphorylated by UL13 protein kinase from herpes simplex virus 1. Microbes Infect 2007; 9: 1434-1438.
122. Bruni R, Fineschi B, Ogle WO, et al. A novel cellular protein, p60, interacting with both herpes simplex virus 1 regulatory proteins ICP22 and ICP0 is modified in a cell-type-specific manner and Is recruited to the nucleus after infection. J Virol 1999; 73: 3810-3817.
123. Coulter LJ, Moss HW, Lang J, et al. A mutant of herpes simplex virus type 1 in which the UL13 protein kinase gene is disrupted. J Gen Virol 1993; 74: 387-395.
124. Kawaguchi Y, Van Sant C, Roizman B. Eukaryotic elongation factor 1delta is hyperphosphorylated by the protein kinase encoded by the U(L)13 gene of herpes simplex virus 1. J Virol 1998; 72: 1731-1736.
125. Long MC, Leong V, Schaffer PA, et al. ICP22 and the UL13 protein kinase are both required for herpes simplex virus-induced modification of the large subunit of RNA polymerase II. J Virol 1999; 73: 5593-5604.
126. Ng TI, Ogle WO, Roizman B. UL13 protein kinase of herpes simplex virus 1 complexes with glycoprotein E and mediates the phosphorylation of the viral Fc receptor: glycoproteins E and I. Virology 1998; 241: 37-48.
127. Ogle WO, Ng TI, Carter KL, et al. The UL13 protein kinase and the infected cell type are determinants of posttranslational modification of ICP0. Virology 1997; 235: 406-413.
128. Ogle WO, Roizman B. Functional anatomy of herpes simplex virus 1 overlapping genes encoding infected-cell protein 22 and US1.5 protein. J Virol 1999; 73: 4305-4315. (Pubitemid 29189878)
129. Romaker D, Schregel V, Maurer K, et al. Analysis of the structure-activity relationship of four herpesviral UL97 subfamily protein kinases reveals partial but not full functional conservation. J Med Chem 2006; 49: 7044-7053. (Pubitemid 44885992)
130. Smith-Donald BA, Roizman B. The interaction of herpes simplex virus 1 regulatory protein ICP22 with the cdc25C phosphatase is enabled in vitro by viral protein kinases US3 and UL13. J Virol 2008; 82: 4533-4543. (Pubitemid 351563690)
131. Baek MC, Krosky PM, Pearson A, et al. Phosphorylation of the RNA polymerase II carboxyl-terminal domain in human cytomegalovirus-infected cells and in vitro by the viral UL97 protein kinase. Virology 2004; 324: 184-193. (Pubitemid 38737410)
132. Hume AJ, Finkel JS, Kamil JP, et al. Phosphorylation of retinoblastoma protein by viral protein with cyclin-dependent kinase function. Science 2008; 320: 797-799.
133. Kamil JP, Coen DM. Human cytomegalovirus protein kinase UL97 forms a complex with the tegument phosphoprotein pp65. J Virol 2007; 81: 10659-10668.
134. Kawaguchi Y, Matsumura T, Roizman B, et al. Cellular elongation factor 1delta is modified in cells infected with representative alpha-, beta-, or gammaherpesviruses. J Virol 1999; 73: 4456-4460.
135. Krosky PM, Baek MC, Jahng WJ, et al. The human cytomegalovirus UL44 protein is a substrate for the UL97 protein kinase. J Virol 2003; 77: 7720-7727.
136. Marschall M, Freitag M, Suchy P, et al. The protein kinase pUL97 of human cytomegalovirus interacts with and phosphorylates the DNA polymerase processivity factor pUL44. Virology 2003; 311: 60-71.
137. Sanchez V, Angeletti PC, Engler JA, et al. Localization of human cytomegalovirus structural proteins to the nuclear matrix of infected human fibroblasts. J Virol 1998; 72: 3321-3329.
138. Asai R, Kato A, Kato K, et al. Epstein-Barr virus protein kinase BGLF4 is a virion tegument protein that dissociates from virions in a phosphorylationdependent process and phosphorylates the viral immediate-early protein BZLF1. J Virol 2006; 80: 5125-5134.
139. Asai R, Kato A, Kawaguchi Y. Epstein-Barr virus protein kinase BGLF4 interacts with viral transactivator BZLF1 and regulates its transactivation activity. J Gen Virol 2009; 90: 1575-1581.
140. Chen MR, Chang SJ, Huang H, et al. A protein kinase activity associated with Epstein-Barr virus BGLF4 phosphorylates the viral early antigen EAD in vitro. J Virol 2000; 74: 3093-3104.
141. Iwahori S, Murata T, Kudoh A, et al. Phosphorylation of p27Kip1 by Epstein-Barr virus protein kinase induces its degradation through SCFSkp2 ubiquitin ligase actions during viral lytic replication. J Biol Chem 2009; 284: 18923-18931.
142. Kato K, Kawaguchi Y, Tanaka M, et al. Epstein-Barr virus-encoded protein kinase BGLF4 mediates hyperphosphorylation of cellular elongation factor 1delta (EF-1delta): EF-1delta is universally modified by conserved protein kinases of herpesviruses in mammalian cells. J Gen Virol 2001; 82: 1457-1463.
143. Kato K, Yokoyama A, Tohya Y, et al. Identification of protein kinases responsible for phosphorylation of Epstein-Barr virus nuclear antigen leader protein at serine-35, which regulates its coactivator function. J Gen Virol 2003; 84: 3381-3392.
144. Kudoh A, Daikoku T, Ishimi Y, et al. Phosphorylation of MCM4 at sites inactivating DNA helicase activity of the MCM4-MCM6-MCM7 complex during Epstein-Barr virus productive replication. J Virol 2006; 80: 10064-10072.
145. Wang JT, Doong SL, Teng SC, et al. Epstein-Barr virus BGLF4 kinase suppresses the interferon regulatory factor 3 signaling pathway. J Virol 2009; 83: 1856-1869.
146. Yang PW, Chang SS, Tsai CH, et al. Effect of phosphorylation on the transactivation activity of Epstein-Barr virus BMRF1, a major target of the viral BGLF4 kinase. J Gen Virol 2008; 89: 884-895.
147. Yue W, Gershburg E, Pagano JS. Hyperphosphorylation of EBNA2 by Epstein-Barr virus protein kinase suppresses transactivation of the LMP1 promoter. J Virol 2005; 79: 5880-5885.
148. Hamza MS, Reyes RA, Izumiya Y, et al. ORF36 protein kinase of Kaposi's sarcoma herpesvirus activates the c-Jun N-terminal kinase signaling pathway. J Biol Chem 2004; 279: 38325-38330.
149. Izumiya Y, Izumiya C, Van Geelen A, et al. Kaposi's sarcoma-associated herpesvirus-encoded protein kinase and its interaction with K-bZIP. J Virol 2007; 81: 1072-1082.