A Ubiquitin-specific Protease Possesses a Decisive Role for Adenovirus Replication and Oncogene-mediated Transformation

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Ching, Wilhelm ^a   Koyuncu, Emre ^a,d   Singh, Sonia ^a   Arbelo Roman, Christina ^b   Hartl, Barbara ^a   Kremmer, Elisabeth ^c   Speiseder, Thomas ^a   Meier, Chris ^b   Dobner, Thomas ^a  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E1B PROTEIN; UBIQUITIN; UBIQUITIN SPECIFIC PROTEINASE 7; UNCLASSIFIED DRUG;

ADENOVIRUS; ARTICLE; BINDING ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE SILENCING; GENETIC TRANSFORMATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; NONHUMAN; ONCOGENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA INTERFERENCE; VIRUS REPLICATION; WESTERN BLOTTING;

ADENOVIRUSES, HUMAN; ANIMALS; BINDING SITES; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; DOWN-REGULATION; ENDOPEPTIDASES; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; RAS PROTEINS; RATS; RNA, SMALL INTERFERING; UBIQUITIN THIOLESTERASE; VIRUS REPLICATION;

ADENOVIRIDAE;

EID: 84875991070     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003273     Document Type: Article

References (73)

1. Shenk T (2001) Adenoviridae: the viruses and their replication. Virology. New York: Lippincott-Raven. pp. 2265-2300.
2. Dingle JH, Langmuir AD, (1968) Epidemiology of acute, respiratory disease in military recruits. Am Rev Respir Dis 97 (Suppl):: 1-65.
3. Jones MS 2nd, Harrach B, Ganac RD, Gozum MMA, Dela Cruz WP, et al. (2007) New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81: 5978-5984.
4. Zhou X, Robinson CM, Rajaiya J, Dehghan S, Seto D, et al. (2012) Analysis of human adenovirus type 19 associated with epidemic keratoconjunctivitis and its reclassification as adenovirus type 64. Invest Ophthalmol Vis Sci 53: 2804-2811.
5. Robinson CM, Shariati F, Gillaspy AF, Dyer DW, Chodosh J, (2008) Genomic and bioinformatics analysis of human adenovirus type 37: new insights into corneal tropism. BMC Genomics 9: 213.
6. Robinson CM, Shariati F, Zaitshik J, Gillaspy AF, Dyer DW, et al. (2009) Human adenovirus type 19: genomic and bioinformatics analysis of a keratoconjunctivitis isolate. Virus Res 139: 122-126.
7. Yolken RH, Lawrence F, Leister F, Takiff HE, Strauss SE, (1982) Gastroenteritis associated with enteric type adenovirus in hospitalized infants. J Pediatr 101: 21-26.
8. Jawetz E, (1959) The story of shipyard eye. Br Med J 1: 873-876.
9. Ginsberg HS, Gold E, Jordan WS Jr, Katz S, Badger GF, et al. (1955) Relation of the new respiratory agents to acute respiratory diseases. Am J Public Health Nations Health 45: 915-922.
10. Abe S, Miyamura K, Oba T, Terakura S, Kasai M, et al. (2003) Oral ribavirin for severe adenovirus infection after allogeneic marrow transplantation. Bone Marrow Transplant 32: 1107-1108.
11. Walls T, Shankar AG, Shingadia D, (2003) Adenovirus: an increasingly important pathogen in paediatric bone marrow transplant patients. Lancet Infect Dis 3: 79-86.
12. Lenaerts L, De Clercq E, Naesens L, (2008) Clinical features and treatment of adenovirus infections. Rev Med Virol 18: 357-374.
13. Naesens L, Lenaerts L, Andrei G, Snoeck R, Van Beers D, et al. (2005) Antiadenovirus activities of several classes of nucleoside and nucleotide analogues. Antimicrob Agents Chemother 49: 1010-1016.
14. Boutell C, Everett RD, (2003) The herpes simplex virus type 1 (HSV-1) regulatory protein ICP0 interacts with and Ubiquitinates p53. J Biol Chem 278: 36596-36602.
15. Foster SA, Demers GW, Etscheid BG, Galloway DA, (1994) The ability of human papillomavirus E6 proteins to target p53 for degradation in vivo correlates with their ability to abrogate actinomycin D-induced growth arrest. J Virol 68: 5698-5705.
16. Gardiol D, Banks L, (1998) Comparison of human papillomavirus type 18 (HPV-18) E6-mediated degradation of p53 in vitro and in vivo reveals significant differences based on p53 structure and cell type but little difference with respect to mutants of HPV-18 E6. J Gen Virol 79 (Pt 8):: 1963-1970.
17. Sato Y, Kamura T, Shirata N, Murata T, Kudoh A, et al. (2009) Degradation of phosphorylated p53 by viral protein-ECS E3 ligase complex. PLoS Pathog 5: e1000530.
18. Baker A, Rohleder KJ, Hanakahi LA, Ketner G, (2007) Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J Virol 81: 7034-7040.
19. Dallaire F, Blanchette P, Groitl P, Dobner T, Branton PE, (2009) Identification of integrin alpha3 as a new substrate of the adenovirus E4orf6/E1B 55-kilodalton E3 ubiquitin ligase complex. J Virol 83: 5329-5338.
20. Orazio NI, Naeger CM, Karlseder J, Weitzman MD, (2011) The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J Virol 85: 1887-1892.
21. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, et al. (2001) Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev 15: 3104-3117.
22. Schwartz RA, Lakdawala SS, Eshleman HD, Russell MR, Carson CT, et al. (2008) Distinct requirements of adenovirus E1b55K protein for degradation of cellular substrates. J Virol 82: 9043-9055.
23. Gupta A, Jha S, Engel DA, Ornelles DA, Dutta A, (2012) Tip60 degradation by adenovirus relieves transcriptional repression of viral transcriptional activator EIA. Oncogene Available:http://pubget.com/paper/23178490/Tip60_degradation_by_adenovirus_relieves_transcriptional_repression_of_viral_transcriptional_activator_EIA. Accessed 14 December 2012.
24. Liao T-L, Wu C-Y, Su W-C, Jeng K-S, Lai MMC, (2010) Ubiquitination and deubiquitination of NP protein regulates influenza A virus RNA replication. EMBO J 29: 3879-3890.
25. Perry JW, Ahmed M, Chang K-O, Donato NJ, Showalter HD, et al. (2012) Antiviral Activity of a Small Molecule Deubiquitinase Inhibitor Occurs via Induction of the Unfolded Protein Response. PLoS Pathog 8: e1002783.
26. Meredith M, Orr A, Everett R, (1994) Herpes simplex virus type 1 immediate-early protein Vmw110 binds strongly and specifically to a 135-kDa cellular protein. Virology 200: 457-469.
27. Sivachandran N, Sarkari F, Frappier L, (2008) Epstein-Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog 4: e1000170.
28. Sarkari F, Sanchez-Alcaraz T, Wang S, Holowaty MN, Sheng Y, et al. (2009) EBNA1-mediated recruitment of a histone H2B deubiquitylating complex to the Epstein-Barr virus latent origin of DNA replication. PLoS Pathog 5: e1000624.
29. Jäger W, Santag S, Weidner-Glunde M, Gellermann E, Kati S, et al. (2012) The ubiquitin-specific protease USP7 modulates the replication of Kaposi's sarcoma-associated herpesvirus latent episomal DNA. J Virol 86: 6745-6757.
30. Saridakis V, Sheng Y, Sarkari F, Holowaty MN, Shire K, et al. (2005) Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein-Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol Cell 18: 25-36.
31. Nevels M, Rubenwolf S, Spruss T, Wolf H, Dobner T, (1997) The adenovirus E4orf6 protein can promote E1A/E1B-induced focus formation by interfering with p53 tumor suppressor function. Proc Natl Acad Sci USA 94: 1206-1211.
32. Nevels M, Täuber B, Spruss T, Wolf H, Dobner T, (2001) "Hit-and-run" transformation by adenovirus oncogenes. J Virol 75: 3089-3094.
33. Blackford AN, Grand RJA, (2009) Adenovirus E1B 55-kilodalton protein: multiple roles in viral infection and cell transformation. J Virol 83: 4000-4012.
34. Holowaty MN, Sheng Y, Nguyen T, Arrowsmith C, Frappier L, (2003) Protein interaction domains of the ubiquitin-specific protease, USP7/HAUSP. J Biol Chem 278: 47753-47761.
35. Hu M, Gu L, Li M, Jeffrey PD, Gu W, et al. (2006) Structural basis of competitive recognition of p53 and MDM2 by HAUSP/USP7: implications for the regulation of the p53-MDM2 pathway. PLoS Biol 4: e27.
36. Faesen AC, Dirac AMG, Shanmugham A, Ovaa H, Perrakis A, et al. (2011) Mechanism of USP7/HAUSP activation by its C-terminal ubiquitin-like domain and allosteric regulation by GMP-synthetase. Mol Cell 44: 147-159.
37. Banning C, Votteler J, Hoffmann D, Koppensteiner H, Warmer M, et al. (2010) A flow cytometry-based FRET assay to identify and analyse protein-protein interactions in living cells. PLoS ONE 5: e9344.
38. Doucas V, Ishov AM, Romo A, Juguilon H, Weitzman MD, et al. (1996) Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev 10: 196-207.
39. Kindsmüller K, Groitl P, Härtl B, Blanchette P, Hauber J, et al. (2007) Intranuclear targeting and nuclear export of the adenovirus E1B-55K protein are regulated by SUMO1 conjugation. Proc Natl Acad Sci USA 104: 6684-6689.
40. Ornelles DA, Shenk T, (1991) Localization of the adenovirus early region 1B 55-kilodalton protein during lytic infection: association with nuclear viral inclusions requires the early region 4 34-kilodalton protein. J Virol 65: 424-429.
41. König C, Roth J, Dobbelstein M, (1999) Adenovirus type 5 E4orf3 protein relieves p53 inhibition by E1B-55-kilodalton protein. J Virol 73: 2253-2262.
42. Weitzman MD, Fisher KJ, Wilson JM, (1996) Recruitment of wild-type and recombinant adeno-associated virus into adenovirus replication centers. J Virol 70: 1845-1854.
43. Evans JD, Hearing P, (2003) Distinct Roles of the Adenovirus E4 ORF3 Protein in Viral DNA Replication and Inhibition of Genome Concatenation. J Virol 77: 5295-5304.
44. Orazio NI, Naeger CM, Karlseder J, Weitzman MD, (2011) The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J Virol 85: 1887-1892.
45. Blackford AN, Bruton RK, Dirlik O, Stewart GS, Taylor AMR, et al. (2008) A role for E1B-AP5 in ATR signaling pathways during adenovirus infection. J Virol 82: 7640-7652.
46. Forrester NA, Sedgwick GG, Thomas A, Blackford AN, Speiseder T, et al. (2011) Serotype-specific inactivation of the cellular DNA damage response during adenovirus infection. J Virol 85: 2201-2211.
47. Popp FD, (1972) Synthesis of potential antineoplastic agents. XXI. Compounds related to ellipticine (1) J Heterocyclic Chem 9: 1399-1401.
48. Colland F, Formstecher E, Jacq X, Reverdy C, Planquette C, et al. (2009) Small-molecule inhibitor of USP7/HAUSP ubiquitin protease stabilizes and activates p53 in cells. Mol Cancer Ther 8: 2286-2295.
49. Cummins JM, Vogelstein B, (2004) HAUSP is required for p53 destabilization. Cell Cycle 3: 689-692.
50. Chauhan D, Tian Z, Nicholson B, Kumar KGS, Zhou B, et al. (2012) A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer Cell 22: 345-358.
51. Edelmann MJ, Nicholson B, Kessler BM, (2011) Pharmacological targets in the ubiquitin system offer new ways of treating cancer, neurodegenerative disorders and infectious diseases. Expert Rev Mol Med 13: e35.
52. Nicholson B, Suresh Kumar KG, (2011) The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem Biophys 60: 61-68.
53. Canning M, Boutell C, Parkinson J, Everett RD, (2004) A RING finger ubiquitin ligase is protected from autocatalyzed ubiquitination and degradation by binding to ubiquitin-specific protease USP7. J Biol Chem 279: 38160-38168.
54. Cummins JM, Rago C, Kohli M, Kinzler KW, Lengauer C, et al. (2004) Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature 428: 1 p following 486.
55. Debbas M, White E, (1993) Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev 7: 546-554.
56. Liu H, Naismith JH, Hay RT, (2003) Adenovirus DNA replication. Curr Top Microbiol Immunol 272: 131-164.
57. Hussain S, Zhang Y, Galardy PJ, (2009) DUBs and cancer: the role of deubiquitinating enzymes as oncogenes, non-oncogenes and tumor suppressors. Cell Cycle 8: 1688-1697.
58. Frappier L, Verrijzer CP, (2011) Gene expression control by protein deubiquitinases. Curr Opin Genet Dev 21: 207-213.
59. Giberson AN, Davidson AR, Parks RJ, (2012) Chromatin structure of adenovirus DNA throughout infection. Nucleic Acids Res 40: 2369-2376.
60. Maertens GN, El Messaoudi-Aubert S, Elderkin S, Hiom K, Peters G, (2010) Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor. EMBO J 29: 2553-2565.
61. Schmid M, Kindsmüller K, Wimmer P, Groitl P, Gonzalez RA, et al. (2011) The E3 ubiquitin ligase activity associated with the adenoviral E1B-55K-E4orf6 complex does not require CRM1-dependent export. J Virol 85: 7081-7094.
62. Babiss LE, Ginsberg HS, Darnell JE Jr, (1985) Adenovirus E1B proteins are required for accumulation of late viral mRNA and for effects on cellular mRNA translation and transport. Mol Cell Biol 5: 2552-2558.
63. Bridge E, Ketner G, (1990) Interaction of adenoviral E4 and E1b products in late gene expression. Virology 174: 345-353.
64. Halbert DN, Cutt JR, Shenk T, (1985) Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J Virol 56: 250-257.
65. Leppard KN, Shenk T, (1989) The adenovirus E1B 55 kd protein influences mRNA transport via an intranuclear effect on RNA metabolism. EMBO J 8: 2329-2336.
66. Pilder S, Moore M, Logan J, Shenk T, (1986) The adenovirus E1B-55K transforming polypeptide modulates transport or cytoplasmic stabilization of viral and host cell mRNAs. Mol Cell Biol 6: 470-476.
67. Fessler SP, Young CS, (1998) Control of adenovirus early gene expression during the late phase of infection. J Virol 72: 4049-4056.
68. Van Breukelen B, Brenkman AB, Holthuizen PE, Van der Vliet PC, (2003) Adenovirus type 5 DNA binding protein stimulates binding of DNA polymerase to the replication origin. J Virol 77: 915-922.
69. Sarkari F, Wang X, Nguyen T, Frappier L, (2011) The herpesvirus associated ubiquitin specific protease, USP7, is a negative regulator of PML proteins and PML nuclear bodies. PLoS ONE 6: e16598.
70. Ching W, Dobner T, Koyuncu E, (2012) The Human Adenovirus Type 5 E1B 55-Kilodalton Protein Is Phosphorylated by Protein Kinase CK2. J Virol 86: 2400-2415.
71. Koppensteiner H, Banning C, Schneider C, Hohenberg H, Schindler M, (2012) Macrophage Internal HIV-1 Is Protected from Neutralizing Antibodies. J Virol 86: 2826-2836.
72. Wimmer P, Blanchette P, Schreiner S, Ching W, Groitl P, et al. (2012) Cross-talk between phosphorylation and SUMOylation regulates transforming activities of an adenoviral oncoprotein. Oncogene Available:http://www.ncbi.nlm.nih.gov/pubmed/22614022. Accessed 8 August 2012.
73. Schreiner S, Wimmer P, Groitl P, Chen S-Y, Blanchette P, et al. (2011) 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: 8752-8765.