Identification of DNA-damage DNA-binding protein 1 as a conditional essential factor for cytomegalovirus replication in interferon-γ-stimulated cells

PLoS Pathogens

Volumn 7, Issue 6, 2011, Pages

  Trilling, Mirko ^a   Le, Vu Thuy Khanh ^a   Fiedler, Manuela ^a   Zimmermann, Albert ^a   Bleifuß, Elke ^a   Hengel, Hartmut ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA DAMAGE DNA BINDING PROTEIN 1; GAMMA INTERFERON; PM27 VIRUS PROTEIN; SMALL INTERFERING RNA; STAT2 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; DDB1 PROTEIN, MOUSE;

ARTICLE; CELL STIMULATION; CYTOMEGALOVIRUS; IMMUNOPRECIPITATION; PROTEIN BINDING; PROTEIN METABOLISM; VIRAL GENE DELIVERY SYSTEM; VIRUS MUTATION; VIRUS REPLICATION; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL STRAIN 3T3; CYTOMEGALOVIRUS INFECTION; GENETIC TRANSFECTION; GENETICS; HELA CELL; HUMAN; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

CYTOMEGALOVIRUS;

ANIMALS; CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; INTERFERON-GAMMA; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NIH 3T3 CELLS; TRANSFECTION; VIRUS REPLICATION;

EID: 79959814239     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002069     Document Type: Article

References (49)

1. Ludwig A, Hengel H, (2009) Epidemiological impact and disease burden of congenital cytomegalovirus infection in Europe. Euro Surveill 14: 26-32.
2. Mocarski ES, Shenk T, Pass RF, (2007) Cytomegaloviruses. In: Knipe DK, Howley PM, editors. Field's Virology Philadelphia Lippincott, Williams & Wilkins pp. 2701-2772.
3. Polic B, Hengel H, Krmpotic A, Trgovcich J, Pavic I, et al. (1998) Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J Exp Med 188: 1047-1054.
4. Crozat K, Georgel P, Rutschmann S, Mann N, Du X, et al. (2006) Analysis of the MCMV resistome by ENU mutagenesis. Mamm Genome 17: 398-406.
5. Gil MP, Bohn E, O'Guin AK, Ramana CV, Levine B, et al. (2001) Biologic consequences of Stat1-independent IFN signaling. Proc Natl Acad Sci U S A 98: 6680-6685.
6. Presti RM, Pollock JL, Dal Canto AJ, O'Guin AK, Virgin HW, (1998) Interferon gamma regulates acute and latent murine cytomegalovirus infection and chronic disease of the great vessels. J Exp Med 188: 577-588.
7. Presti RM, Popkin DL, Connick M, Paetzold S, Virgin HW, (2001) Novel cell type-specific antiviral mechanism of interferon gamma action in macrophages. J Exp Med 193: 483-496.
8. Strobl B, Bubic I, Bruns U, Steinborn R, Lajko R, et al. (2005) Novel functions of tyrosine kinase 2 in the antiviral defense against murine cytomegalovirus. J Immunol 175: 4000-4008.
9. Tabeta K, Georgel P, Janssen E, Du X, Hoebe K, et al. (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci U S A 101: 3516-3521.
10. Hengel H, Koszinowski UH, Conzelmann KK, (2005) Viruses know it all: new insights into IFN networks. Trends Immunol 26: 396-401.
11. Zimmermann A, Trilling M, Wagner M, Wilborn M, Bubic I, et al. (2005) A cytomegaloviral protein reveals a dual role for STAT2 in IFN-{gamma} signaling and antiviral responses. J Exp Med 201: 1543-1553.
12. Abenes G, Lee M, Haghjoo E, Tong T, Zhan X, et al. (2001) Murine cytomegalovirus open reading frame M27 plays an important role in growth and virulence in mice. J Virol 75: 1697-1707.
13. Khan S, Zimmermann A, Basler M, Groettrup M, Hengel H, (2004) A cytomegalovirus inhibitor of gamma interferon signaling controls immunoproteasome induction. J Virol 78: 1831-1842.
14. Le VT, Trilling M, Zimmermann A, Hengel H, (2008) Mouse cytomegalovirus inhibits beta interferon (IFN-beta) gene expression and controls activation pathways of the IFN-beta enhanceosome. J Gen Virol 89: 1131-1141.
15. Park C, Li S, Cha E, Schindler C, (2000) Immune response in Stat2 knockout mice. Immunity 13: 795-804.
16. Haga IR, Bowie AG, (2005) Evasion of innate immunity by vaccinia virus. Parasitology 130: S11-S25.
17. Trilling M, Le VT, Zimmermann A, Ludwig H, Pfeffer K, et al. (2009) Gamma interferon-induced interferon regulatory factor 1-dependent antiviral response inhibits vaccinia virus replication in mouse but not human fibroblasts. J Virol 83: 3684-3695.
18. Stancato LF, David M, Carter-Su C, Larner AC, Pratt WB, (1996) Preassociation of STAT1 with STAT2 and STAT3 in separate signalling complexes prior to cytokine stimulation. J Biol Chem 271: 4134-4137.
19. Lee CK, Bluyssen HA, Levy DE, (1997) Regulation of interferon-alpha responsiveness by the duration of Janus kinase activity. J Biol Chem 272: 21872-21877.
20. Kaspari M, Tavalai N, Stamminger T, Zimmermann A, Schilf R, et al. (2008) Proteasome inhibitor MG132 blocks viral DNA replication and assembly of human cytomegalovirus. FEBS Lett 582: 666-672.
21. Satheshkumar PS, Anton LC, Sanz P, Moss B, (2009) Inhibition of the ubiquitin-proteasome system prevents vaccinia virus DNA replication and expression of intermediate and late genes. J Virol 83: 2469-2479.
22. Andrejeva J, Poole E, Young DF, Goodbourn S, Randall RE, (2002) The p127 subunit (DDB1) of the UV-DNA damage repair binding protein is essential for the targeted degradation of STAT1 by the V protein of the paramyxovirus simian virus 5. J Virol 76: 11379-11386.
23. Precious B, Childs K, Fitzpatrick-Swallow V, Goodbourn S, Randall RE, (2005) Simian virus 5 V protein acts as an adaptor, linking DDB1 to STAT2, to facilitate the ubiquitination of STAT1. J Virol 79: 13434-13441.
24. Ulane CM, Horvath CM, (2002) Paramyxoviruses SV5 and HPIV2 assemble STAT protein ubiquitin ligase complexes from cellular components. Virology 304: 160-166.
25. Ulane CM, Rodriguez JJ, Parisien JP, Horvath CM, (2003) STAT3 ubiquitylation and degradation by mumps virus suppress cytokine and oncogene signaling. J Virol 77: 6385-6393.
26. Hu J, McCall CM, Ohta T, Xiong Y, (2004) Targeted ubiquitination of CDT1 by the DDB1-CUL4A-ROC1 ligase in response to DNA damage. Nat Cell Biol 6: 1003-1009.
27. Liu W, Nichols AF, Graham JA, Dualan R, Abbas A, et al. (2000) Nuclear transport of human DDB protein induced by ultraviolet light. J Biol Chem 275: 21429-21434.
28. Hwang BJ, Toering S, Francke U, Chu G, (1998) p48 Activates a UV-damaged-DNA binding factor and is defective in xeroderma pigmentosum group E cells that lack binding activity. Mol Cell Biol 18: 4391-4399.
29. Angers S, Li T, Yi X, MacCoss MJ, Moon RT, et al. (2006) Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443: 590-593.
30. Jin J, Arias EE, Chen J, Harper JW, Walter JC, (2006) A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol Cell 23: 709-721.
31. Nichols AF, Itoh T, Graham JA, Liu W, Yamaizumi M, et al. (2000) Human damage-specific DNA-binding protein p48. Characterization of XPE mutations and regulation following UV irradiation. J Biol Chem 275: 21422-21428.
32. Lin GY, Paterson RG, Richardson CD, Lamb RA, (1998) The V protein of the paramyxovirus SV5 interacts with damage-specific DNA binding protein. Virology 249: 189-200.
33. Li T, Chen X, Garbutt KC, Zhou P, Zheng N, (2006) Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124: 105-117.
34. Le VT, Trilling M, Wilborn M, Hengel H, Zimmermann A, (2008) Human cytomegalovirus interferes with signal transducer and activator of transcription (STAT) 2 protein stability and tyrosine phosphorylation. J Gen Virol 89: 2416-2426.
35. Cang Y, Zhang J, Nicholas SA, Bastien J, Li B, et al. (2006) Deletion of DDB1 in mouse brain and lens leads to p53-dependent elimination of proliferating cells. Cell 127: 929-940.
36. Wakasugi M, Matsuura K, Nagasawa A, Fu D, Shimizu H, et al. (2007) DDB1 gene disruption causes a severe growth defect and apoptosis in chicken DT40 cells. Biochem Biophys Res Commun 364: 771-777.
37. Karlas A, Machuy N, Shin Y, Pleissner KP, Artarini A, et al. (2010) Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463: 818-822.
38. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, et al. (2008) Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135: 49-60.
39. Konig R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, et al. (2010) Human host factors required for influenza virus replication. Nature 463: 813-817.
40. Fukumoto Y, Dohmae N, Hanaoka F, (2008) Schizosaccharomyces pombe Ddb1 recruits substrate-specific adaptor proteins through a novel protein motif, the DDB-box. Mol Cell Biol 28: 6746-6756.
41. Parisien JP, Lau JF, Horvath CM, (2002) STAT2 acts as a host range determinant for species-specific paramyxovirus interferon antagonism and simian virus 5 replication. J Virol 76: 6435-6441.
42. Parisien JP, Lau JF, Rodriguez JJ, Ulane CM, Horvath CM, (2002) Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha/beta interferon signal transduction. J Virol 76: 4190-4198.
43. Childs KS, Andrejeva J, Randall RE, Goodbourn S, (2009) Mechanism of mda-5 Inhibition by paramyxovirus V proteins. J Virol 83: 1465-1473.
44. Poole E, He B, Lamb RA, Randall RE, Goodbourn S, (2002) The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon-beta. Virology 303: 33-46.
45. Andrejeva J, Young DF, Goodbourn S, Randall RE, (2002) Degradation of STAT1 and STAT2 by the V proteins of simian virus 5 and human parainfluenza virus type 2, respectively: consequences for virus replication in the presence of alpha/beta and gamma interferons. J Virol 76: 2159-2167.
46. Wiebusch L, Neuwirth A, Grabenhenrich L, Voigt S, Hagemeier C, (2008) Cell cycle-independent expression of immediate-early gene 3 results in G1 and G2 arrest in murine cytomegalovirus-infected cells. J Virol 82: 10188-10198.
47. Durbin JE, Hackenmiller R, Simon MC, Levy DE, (1996) Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84: 443-450.
48. Brune W, Hengel H, Koszinowski UH, (2001) A mouse model for cytomegalovirus infection. Curr Protoc Immunol Chapter 19: Unit.
49. Navarro L, Mowen K, Rodems S, Weaver B, Reich N, et al. (1998) Cytomegalovirus activates interferon immediate-early response gene expression and an interferon regulatory factor 3-containing interferon-stimulated response element-binding complex. Mol Cell Biol 18: 3796-3802.