Design stars: How small DNA viruses remodel the host nucleus

Future Virology

Volumn 7, Issue 5, 2012, Pages 445-459

  Jiang, Mengxi ^a   Imperiale, Michael J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

adenovirus; chromatin remodeling; DNA damage response; nuclear bodies; nuclear envelope; nucleus; papillomavirus; parvovirus; polyomavirus; tumor suppressor protein

Indexed keywords

DNA; DOUBLE STRANDED DNA; TUMOR SUPPRESSOR PROTEIN; VIRUS DNA;

ADENOVIRUS; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL NUCLEUS; CELL NUCLEUS INCLUSION BODY; CELL NUCLEUS MEMBRANE; CELLULAR PARAMETERS; CHROMATIN; DNA DAMAGE; DNA DAMAGE RESPONSE; DRUG DESIGN; GENE REPLICATION; GENE STRUCTURE; HOST CELL NUCLEUS MEMBRANE REMODELING; HOST CHROMATIN REMODELING; HUMAN; LIFE CYCLE; MERKEL CELL POLYOMAVIRUS; NONHUMAN; NUCLEOLUS; NUCLEOLUS REMODELING; PAPILLOMA VIRUS; PARVOVIRUS; POLYOMA VIRUS; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA NUCLEAR BODY; REVIEW; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS INFECTION; VIRUS PARTICLE; VIRUS TRANSFORMATION;

ADENOVIRIDAE; DNA VIRUSES; PAPILLOMAVIRIDAE; PARVOVIRUS; POLYOMAVIRUS;

EID: 84861322667     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.12.38     Document Type: Review

References (130)

1. Howley PM, Lowy DR. Papillomaviruses. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA, 2299-2354 (2007).
2. Imperiale MJ, Major EO. Polyomaviruses. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA, 2263-2298 (2007).
3. Berns K, Parrish CR. Parvoviridae. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA, 2299-2349 (2007).
4. Greber UF, Kasamatsu H. Nuclear targeting of SV40 and adenovirus. Trends Cell Biol. 6(5), 189-195 (1996).
5. Greber UF, Suomalainen M, Stidwill RP, Boucke K, Ebersold MW, Helenius A. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J. 16(19), 5998-6007 (1997).
6. Trotman LC, Mosberger N, Fornerod M, Stidwill RP, Greber UF. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol. 3(12), 1092-1100 (2001).
7. Strunze S, Engelke MF, Wang IH et al. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10(3), 210-223 (2011).
8. Butin-Israeli V, Ben-Nun-Shaul O, Kopatz I et al. Simian virus 40 induces lamin A/C fluctuations and nuclear envelope deformation during cell entry. Nucleus 2(4), 320-330 (2011).
9. Okada Y, Suzuki T, Sunden Y et al. Dissociation of heterochromatin protein 1 from lamin B receptor induced by human polyomavirus agnoprotein: role in nuclear egress of viral particles. EMBO Rep. 6(5), 452-457 (2005).
10. Huerfano S, Zila V, Boura E, Spanielova H, Stokrova J, Forstova J. Minor capsid proteins of mouse polyomavirus are inducers of apoptosis when produced individually but are only moderate contributors to cell death during the late phase of viral infection. FEBS J. 277(5), 1270-1283 (2010).
11. Raghava S, Giorda KM, Romano FB, Heuck AP, Hebert DN. The SV40 late protein VP4 is a viroporin that forms pores to disrupt membranes for viral release. PLoS Pathog. 7(6), e1002116 (2011).
12. Giorda KM, Raghava S, Hebert DN. The SV40 late viral protein VP4 disrupts the nuclear envelope for viral release. J. Virol. 86(6), 3180-3192 (2012).
13. Cohen S, Behzad AR, Carroll JB, Pante N. Parvoviral nuclear import: bypassing the host nuclear-transport machinery. J. Gen. Virol. 87(Pt 11), 3209-3213 (2006).
14. Cohen S, Marr AK, Garcin P, Pante N. Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle. J. Virol. 85(10), 4863-4874 (2011).
15. Tattersall P. Replication of the parvovirus MVM. I. Dependence of virus multiplication and plaque formation on cell growth. J. Virol. 10(4), 586-590 (1972).
16. Giacinti C, Giordano A. RB and cell cycle progression. Oncogene 25(38), 5220-5227 (2006).
17. Chellappan S, Kraus VB, Kroger B et al. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl Acad. Sci. USA 89(10), 4549-4553 (1992).
18. Decaprio JA. How the Rb tumor suppressor structure and function was revealed by the study of adenovirus and SV40. Virology 384(2), 274-284 (2009).
19. Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ, Kurdistani SK. Epigenetic reprogramming by adenovirus E1A. Science 321(5892), 1086-1088 (2008
20. Ben-Israel H, Kleinberger T. Adenovirus and cell cycle control. Front. Biosci. 7, d1369-d1395 (2002).
21. Yew PR, Berk AJ. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 357(6373), 82-85 (1992).
22. Querido E, Blanchette P, Yan Q et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15(23), 3104-3117 (2001).
23. Soria C, Estermann FE, Espantman KC, O'Shea CC. Heterochromatin silencing of p53 target genes by a small viral protein. Nature 466(7310), 1076-1081 (2010).
24. Huibregtse JM, Scheffner M, Howley PM. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J. 10(13), 4129-4135 (1991).
25. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75(3), 495-505 (1993).
26. Mietz JA, Unger T, Huibregtse JM, Howley PM. The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein. EMBO J. 11(13), 5013-5020 (1992).
27. Jeon S, Allen-Hoffmann BL, Lambert PF. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J. Virol. 69(5), 2989-2997 (1995).
28. Corden SA, Sant-Cassia LJ, Easton AJ, Morris AG. The integration of HPV-18 DNA in cervical carcinoma. Mol. Pathol. 52(5), 275-282 (1999).
29. Munger K, Baldwin A, Edwards KM et al. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 78(21), 11451-11460 (2004).
30. Bargonetti J, Reynisdottir I, Friedman PN, Prives C. Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev. 6(10), 1886-1898 (1992).
31. Jiang D, Srinivasan A, Lozano G, Robbins PD. SV40 T antigen abrogates p53-mediated transcriptional activity. Oncogene 8(10), 2805-2812 (1993).
32. Sarnow P, Ho YS, Williams J, Levine AJ. Adenovirus E1b-58kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 kD cellular protein in transformed cells. Cell 28(2), 387-394 (1982).
33. Dey D, Dahl J, Cho S, Benjamin TL. Induction and bypass of p53 during productive infection by polyomavirus. J. Virol. 76(18), 9526-9532 (2002).
34. Dilworth SM. Cell alterations induced by the large T-antigens of SV40 and polyoma virus. Semin. Cancer Biol. 1(6), 407-414 (1990).
35. Lomax M, Fried M. Polyoma virus disrupts ARF signaling to p53. Oncogene 20(36), 4951-4960 (2001).
36. Demetriou SK, Ona-Vu K, Sullivan EM, Dong TK, Hsu SW, Oh DH. Defective DNA repair and cell cycle arrest in cells expressing merkel cell polyomavirus T antigen. Int. J. Cancer doi:10.1002/ ijc.27440 (2012) (Epub ahead of print).
37. Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 408(6811), 433-439 (2000).
38. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85 (2004).
39. Araujo FD, Stracker TH, Carson CT, Lee DV, Weitzman MD. Adenovirus type 5 E4orf3 protein targets the Mre11 complex to cytoplasmic aggresomes. J. Virol. 79(17), 11382-11391 (2005).
40. Stracker TH, Carson CT, Weitzman MD. Adenovirus oncoproteins inactivate the Mre11-Rad50-Nbs1 DNA repair complex. Nature 418(6895), 348-352 (2002).
41. Liu Y, Shevchenko A, Berk AJ. Adenovirus exploits the cellular aggresome response to accelerate inactivation of the MRN complex. J. Virol. 79(22), 14004-14016 (2005).
42. Evans JD, Hearing P. Relocalization of the Mre11-Rad50-Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol. 79(10), 6207-6215 (2005).
43. Carson CT, Orazio NI, Lee DV et al. Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 28(6), 652-662 (2009).
44. Carson CT, Schwartz RA, Stracker TH, Lilley CE, Lee DV, Weitzman MD. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22(24), 6610-6620 (2003).
45. Mathew SS, Bridge E. The cellular Mre11 protein interferes with adenovirus E4 mutant DNA replication. Virology 365(2), 346-355 (2007).
46. Mathew SS, Bridge E. Nbs1-dependent binding of Mre11 to adenovirus E4 mutant viral DNA is important for inhibiting DNA replication. Virology 374(1), 11-22 (2008).
47. Baker A, Rohleder KJ, Hanakahi LA, Ketner G. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol. 81(13), 7034-7040 (2007).
48. Orazio NI, Naeger CM, Karlseder J, Weitzman MD. The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J. Virol. 85(4), 1887-1892 (2011).
49. Forrester NA, Sedgwick GG, Thomas A et al. Serotype-specific inactivation of the cellular DNA damage response during adenovirus infection. J. Virol. 85(5), 2201-2211 (2011).
50. Blackford AN, Patel RN, Forrester NA et al. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc. Natl Acad. Sci. USA 107(27), 12251-12256 (2010).
51. Jayaram S, Gilson T, Ehrlich ES, Yu XF, Ketner G, Hanakahi L. E1B 55k-independent dissociation of the DNA ligase IV/XRCC4 complex by E4 34k during adenovirus infection. Virology 382(2), 163-170 (2008).
52. Boyer J, Rohleder K, Ketner G. Adenovirus E4 34k and E4 11k inhibit double strand break repair and are physically associated with the cellular DNA-dependent protein kinase. Virology 263(2), 307-312 (1999).
53. Moody CA, Laimins LA. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog. 5(10), e1000605 (2009).
54. Fradet-Turcotte A, Bergeron-Labrecque F, Moody CA, Lehoux M, Laimins LA, Archambault J. Nuclear accumulation of the papillomavirus E1 helicase blocks S-phase progression and triggers an ATM-dependent DNA damage response. J. Virol. 85(17), 8996-9012 (2011
55. Sakakibara N, Mitra R, Mcbride AA. The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J. Virol. 85(17), 8981-8995 (2011).
56. King LE, Fisk JC, Dornan ES, Donaldson MM, Melendy T, Morgan IM. Human papillomavirus E1 and E2 mediated DNA replication is not arrested by DNA damage signalling. Virology 406(1), 95-102 (2010).
57. Iftner T, Elbel M, Schopp B et al. Interference of papillomavirus E6 protein with single-strand break repair by interaction with XRCC1. EMBO J. 21(17), 4741-4748 (2002).
58. Chen B, Simpson DA, Zhou Y et al. Human papilloma virus type16 E6 deregulates CHK1 and sensitizes human fibroblasts to environmental carcinogens independently of its effect on p53. Cell Cycle 8(11), 1775-1787 (2009).
59. Day T, Vaziri C. HPV E6 oncoprotein prevents recovery of stalled replication forks independently of p53 degradation. Cell Cycle 8(14), 2138 (2009).
60. Shin KH, Ahn JH, Kang MK et al. HPV-16 E6 oncoprotein impairs the fidelity of DNA end-joining via p53-dependent and -independent pathways. Int. J. Oncol. 28(1), 209-215 (2006).
61. Spardy N, Covella K, Cha E et al. Human papillomavirus 16 E7 oncoprotein attenuates DNA damage checkpoint control by increasing the proteolytic turnover of claspin. Cancer Res. 69(17), 7022-7029 (2009).
62. Santegoets LA, Van Baars R, Terlou A et al. Different DNA damage and cell cycle checkpoint control in low- and high-risk human papillomavirus infections of the vulva. Int. J. Cancer 130(12), 2874-2885 (2012).
63. Hoskins EE, Morris TA, Higginbotham JM et al. Fanconi anemia deficiency stimulates HPV-associated hyperplastic growth in organotypic epithelial raft culture. Oncogene 28(5), 674-685 (2009).
64. Park JW, Pitot HC, Strati K et al. Deficiencies in the Fanconi anemia DNA damage response pathway increase sensitivity to HPV-associated head and neck cancer. Cancer Res. 70(23), 9959-9968 (2010).
65. Dahl J, You J, Benjamin TL. Induction and utilization of an ATM signaling pathway by polyomavirus. J. Virol. 79(20), 13007-13017 (2005).
66. Shi Y, Dodson GE, Shaikh S, Rundell K, Tibbetts RS. Ataxia- telangiectasia-mutated (ATM) is a T-antigen kinase that controls SV40 viral replication in vivo. J. Biol. Chem. 280(48), 40195-40200 (2005).
67. Lees-Miller SP, Chen YR, Anderson CW. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell Biol. 10(12), 6472-6481 (1990).
68. Zhao X, Madden-Fuentes RJ, Lou BX et al. Ataxia telangiectasia-mutated damage-signaling kinase- and proteasome-dependent destruction of Mre11-Rad50-Nbs1 subunits in Simian virus 40-infected primate cells. J. Virol. 82(11), 5316-5328 (2008).
69. Boichuk S, Hu L, Hein J, Gjoerup OV. Multiple DNA damage signaling and repair pathways deregulated by simian virus 40 large T antigen. J. Virol. 84(16), 8007-8020 (2010).
70. Rohaly G, Korf K, Dehde S, Dornreiter I. Simian virus 40 activates ATR-Delta p53 signaling to override cell cycle and DNA replication control. J. Virol. 84(20), 10727-10747 (2010).
71. Hein J, Boichuk S, Wu J et al. Simian virus 40 large T antigen disrupts genome integrity and activates a DNA damage response via Bub1 binding. J. Virol. 83(1), 117-127 (2009).
72. Wu X, Avni D, Chiba T et al. SV40 T antigen interacts with Nbs1 to disrupt DNA replication control. Genes Dev. 18(11), 1305-1316 (2004).
73. Orba Y, Suzuki T, Makino Y et al. Large T antigen promotes JC virus replication in G2-arrested cells by inducing ATM- and ATR-mediated G2 checkpoint signaling. J. Biol. Chem. 285(2), 1544-1554 (2010).
74. Darbinyan A, Siddiqui KM, Slonina D et al. Role of JC virus agnoprotein in DNA repair. J. Virol. 78(16), 8593-8600 (2004).
75. Trojanek J, Croul S, Ho T et al. T-antigen of the human polyomavirus JC attenuates faithful DNA repair by forcing nuclear interaction between IRS-1 and Rad51. J. Cell Physiol. 206(1), 35-46 (2006).
76. Darbinyan A, White MK, Akan S et al. Alterations of DNA damage repair pathways resulting from JCV infection. Virology 364(1), 73-86 (2007).
77. Choi YK, Nash K, Byrne BJ, Muzyczka N, Song S. The effect of DNA-dependent protein kinase on adeno-associated virus replication. PLoS One 5(12), e15073 (2010).
78. Cervelli T, Palacios JA, Zentilin L et al. Processing of recombinant AAV genomes occurs in specific nuclear structures that overlap with foci of DNA-damage-response proteins. J. Cell Sci. 121(Pt 3), 349-357 (2008).
79. Schwartz RA, Palacios JA, Cassell GD, Adam S, Giacca M, Weitzman MD. The Mre11/Rad50/Nbs1 complex limits adeno-associated virus transduction and replication. J. Virol. 81(23), 12936-12945 (2007).
80. Sanlioglu S, Benson P, Engelhardt JF. Loss of ATM function enhances recombinant adeno-associated virus transduction and integration through pathways similar to UV irradiation. Virology 268(1), 68-78 (2000).
81. Luo Y, Chen AY, Qiu J. Bocavirus infection induces a DNA damage response that facilitates viral DNA replication and mediates cell death. J. Virol. 85(1), 133-145 (2011).
82. Adeyemi RO, Landry S, Davis ME, Weitzman MD, Pintel DJ. Parvovirus minute virus of mice induces a DNA damage response that facilitates viral replication. PLoS Pathog. 6(10), e1001141 (2010).
83. Jurvansuu J, Raj K, Stasiak A, Beard P. Viral transport of DNA damage that mimics a stalled replication fork. J. Virol. 79(1), 569-580 (2005).
84. Berthet C, Raj K, Saudan P, Beard P. How adeno-associated virus Rep78 protein arrests cells completely in S phase. Proc. Natl Acad. Sci. USA 102(38), 13634-13639 (2005).
85. Schwartz RA, Carson CT, Schuberth C, Weitzman MD. Adeno-associated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase. J. Virol. 83(12), 6269-6278 (2009).
86. Vogel R, Seyffert M, Strasser R et al. Adeno-associated virus type 2 modulates the host DNA damage response induced by herpes simplex virus 1 during coinfection. J. Virol. 86(1), 143-155 (2012).
87. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair (Amst.) 3(8-9), 959-967 (2004).
88. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J. Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20(5), 801-809 (2005).
89. Lilley CE, Chaurushiya MS, Weitzman MD. Chromatin at the intersection of viral infection and DNA damage. Biochim. Biophys. Acta 1799(3-4), 319-327 (2010).
90. Nichols GJ, Schaack J, Ornelles DA. Widespread phosphorylation of histone H2AX by species C adenovirus infection requires viral DNA replication. J. Virol. 83(12), 5987-5998 (2009
91. Fragkos M, Breuleux M, Clement N, Beard P. Recombinant adeno-associated viral vectors are deficient in provoking a DNA damage response. J. Virol. 82(15), 7379-7387 (2008).
92. Lang SE, Hearing P. The adenovirus E1A oncoprotein recruits the cellular TRRAP/GCN5 histone acetyltransferase complex. Oncogene 22(18), 2836-2841 (2003).
93. Horwitz GA, Zhang K, McBrian MA, Grunstein M, Kurdistani SK, Berk AJ. Adenovirus small E1A alters global patterns of histone modification. Science 321(5892), 1084-1085 (2008).
94. Thomas MC, Chiang CM. E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Mol. Cell 17(2), 251-264 (2005).
95. Duensing S, Munger K. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62(23), 7075-7082 (2002).
96. Zhang B, Laribee RN, Klemsz MJ, Roman A. Human papillomavirus type 16 E7 protein increases acetylation of histone H3 in human foreskin keratinocytes. Virology 329(1), 189-198 (2004).
97. Lee D, Lim C, Seo T, Kwon H, Min H, Choe J. The viral oncogene human papillomavirus E7 deregulates transcriptional silencing by Brm-related gene 1 via molecular interactions. J. Biol. Chem. 277(50), 48842-48848 (2002).
98. Guillaud M, Adler-Storthz K, Malpica A et al. Subvisual chromatin changes in cervical epithelium measured by texture image analysis and correlated with HPV. Gynecol. Oncol. 99(3 Suppl. 1), S16-S23 (2005).
99. Bernardi R, Pandolfi PP. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 8(12), 1006-1016 (2007).
100. Everett RD, Chelbi-Alix MK. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89(6-7), 819-830 (2007).
101. Tavalai N, Stamminger T. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta 1783(11), 2207-2221 (2008).
102. Geoffroy MC, Chelbi-Alix MK. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 31(1), 145-158 (2011).
103. Ishov AM, Sotnikov AG, Negorev D et al. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147(2), 221-234 (1999).
104. Carvalho T, Seeler JS, Ohman K et al. Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. J. Cell Biol. 131(1), 45-56 (1995).
105. Doucas V, Ishov AM, Romo A et al. Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev. 10(2), 196-207 (1996).
106. Ullman AJ, Hearing P. Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. J. Virol. 82(15), 7325-7335 (2008).
107. Ullman AJ, Reich NC, Hearing P. Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. J. Virol. 81(9), 4744-4752 (2007).
108. Stracker TH, Lee DV, Carson CT, Araujo FD, Ornelles DA, Weitzman MD. Serotype-specific reorganization of the Mre11 complex by adenoviral E4orf3 proteins. J. Virol. 79(11), 6664-6673 (2005).
109. Hoppe A, Beech SJ, Dimmock J, Leppard KN. Interaction of the adenovirus type 5 E4 Orf3 protein with promyelocytic leukemia protein isoform II is required for ND10 disruption. J. Virol. 80(6), 3042-3049 (2006).
110. Rosa-Calatrava M, Grave L, Puvion- Dutilleul F, Chatton B, Kedinger C. Functional analysis of adenovirus protein IX identifies domains involved in capsid stability, transcriptional activity, and nuclear reorganization. J. Virol. 75(15), 7131-7141 (2001).
111. Schreiner S, Wimmer P, Sirma H et al. Proteasome-dependent degradation of Daxx by the viral E1B-55K protein in human adenovirus-infected cells. J. Virol. 84(14), 7029-7038 (2010).
112. Schreiner S, Wimmer P, Groitl P et al. Adenovirus type 5 early region 1B 55K oncoprotein-dependent degradation of cellular factor Daxx is required for efficient transformation of primary rodent cells. J. Virol. 85(17), 8752-8765 (2011).
113. Day PM, Roden RB, Lowy DR, Schiller JT. The papillomavirus minor capsid protein, L2, induces localization of the major capsid protein, L1, and the viral transcription/replication protein, E2, to PML oncogenic domains. J. Virol. 72(1), 142-150 (1998).
114. Florin L, Schafer F, Sotlar K, Streeck RE, Sapp M. Reorganization of nuclear domain 10 induced by papillomavirus capsid protein l2. Virology 295(1), 97-107 (2002).
115. Kieback E, Muller M. Factors influencing subcellular localization of the human papillomavirus L2 minor structural protein. Virology 345(1), 199-208 (2006).
116. Roberts S, Hillman ML, Knight GL, Gallimore PH. The ND10 component promyelocytic leukemia protein relocates to human papillomavirus type 1 E4 intranuclear inclusion bodies in cultured keratinocytes and in warts. J. Virol. 77(1), 673-684 (2003).
117. Day PM, Baker CC, Lowy DR, Schiller JT. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc. Natl Acad. Sci. USA 101(39), 14252-14257 (2004).
118. Nakahara T, Lambert PF. Induction of promyelocytic leukemia (PML) oncogenic domains (PODs) by papillomavirus. Virology 366(2), 316-329 (2007).
119. Ishov AM, Maul GG. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol. 134(4), 815-826 (1996).
120. Tang Q, Bell P, Tegtmeyer P, Maul GG. Replication but not transcription of simian virus 40 DNA is dependent on nuclear domain 10. J. Virol. 74(20), 9694-9700 (2000).
121. Gasparovic ML, Maginnis MS, O'Hara BA, Dugan AS, Atwood WJ. Modulation of PML protein expression regulates JCV infection. Virology 390(2), 279-288 (2009).
122. Jiang M, Entezami P, Gamez M, Stamminger T, Imperiale MJ. Functional reorganization of promyelocytic leukemia nuclear bodies during BK virus infection. mBio 2(1), e00281-e00210 (2011).
123. Young PJ, Jensen KT, Burger LR, Pintel DJ, Lorson CL. Minute virus of mice NS1 interacts with the SMN protein, and they colocalize in novel nuclear bodies induced by parvovirus infection. J. Virol. 76(8), 3892-3904 (2002).
124. Cziepluch C, Lampel S, Grewenig A, Grund C, Lichter P, Rommelaere J. H-1 parvovirus-associated replication bodies: a distinct virus-induced nuclear structure. J. Virol. 74(10), 4807-4815 (2000).
125. Greco A. Involvement of the nucleolus in replication of human viruses. Rev. Med. Virol. 19(4), 201-214 (2009).
126. Lam YW, Evans VC, Heesom KJ, Lamond AI, Matthews DA. Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol. Cell Proteomics 9(1), 117-130 (2010).
127. Castiglia CL, Flint SJ. Effects of adenovirus infection on rRNA synthesis and maturation in HeLa cells. Mol. Cell Biol. 3(4), 662-671 (1983).
128. Grinstein E, Wernet P, Snijders PJ et al. Nucleolin as activator of human papillomavirus type 18 oncogene transcription in cervical cancer. J. Exp. Med. 196(8), 1067-1078 (2002).
129. Wong JM, Kusdra L, Collins K. Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat. Cell Biol. 4(9), 731-736 (2002).
130. Jiang H, Alonso MM, Gomez-Manzano C, Piao Y, Fueyo J. Oncolytic viruses and DNA-repair machinery: overcoming chemoresistance of gliomas. Expert Rev. Anticancer Ther. 6(11), 1585-1592 (2006)