Real-time Transcriptional Profiling of Cellular and Viral Gene Expression during Lytic Cytomegalovirus Infection

PLoS Pathogens

Volumn 8, Issue 9, 2012, Pages

  Marcinowski, Lisa ^a   Lidschreiber, Michael ^a   Windhager, Lukas ^a   Rieder, Martina ^a   Bosse, Jens B ^b   Rädle, Bernd ^a   Bonfert, Thomas ^a   Györy, Ildiko ^c   de Graaf, Miranda ^d   da Costa, Olivia Prazeres ^e   Rosenstiel, Philip ^f   Friedel, Caroline C ^a   Zimmer, Ralf ^a   Ruzsics, Zsolt ^a   Dölken, Lars ^a,d  

^a UNIVERSITY OF MUNICH   (Germany)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF PLYMOUTH   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYC PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CYTOMEGALOVIRUS INFECTION; DNA DAMAGE; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS ENTRY; VIRUS LOAD; VIRUS REPLICATION;

CYTOMEGALOVIRUS; HERPESVIRIDAE; MAIZE CHLOROTIC MOTTLE VIRUS; MURID HERPESVIRUS 1;

EID: 84866919768     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002908     Document Type: Article

References (104)

1. Mocarski E, Shenk T, Pass R (2007) Cytomegaloviruses. In: Knipe DM, Howley PM, editors Fields Virology, Vol2, pp 2701-2772 Lippincott Williams & Wilkins: Philadelphia.
2. Yurochko AD, Hwang ES, Rasmussen L, Keay S, Pereira L, et al. (1997) The human cytomegalovirus UL55 (gB) and UL75 (gH) glycoprotein ligands initiate the rapid activation of Sp1 and NF-kappaB during infection. J Virol 71: 5051-5059.
3. Simmen K, Singh J, Luukkonen BG, Lopper M, Bittner A, et al. (2001) Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc Natl Acad Sci U S A 98: 7140-7145.
4. Browne EP, Shenk T, (2003) Human cytomegalovirus UL83-coded pp65 virion protein inhibits antiviral gene expression in infected cells. Proc Natl Acad Sci U S A 100: 11439-11444.
5. Compton T, Feire A (2007) Early events in human cytomegalovirus infection. In: Source Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K, editors. Cambridge: Cambridge University Press. Chapter 16.
6. Zhu H, Cong JP, Mamtora G, Gingeras T, Shenk T, (1998) Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc Natl Acad Sci U S A 95: 14470-14475.
7. Kenzelmann M, Muhlemann K, (2000) Transcriptome analysis of fibroblast cells immediate-early after human cytomegalovirus infection. J Mol Biol 304: 741-751.
8. Browne EP, Wing B, Coleman D, Shenk T, (2001) Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol 75: 12319-12330.
9. Hertel L, Mocarski ES, (2004) Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle gene expression and induction of Pseudomitosis independent of US28 function. J Virol 78: 11988-12011.
10. Challacombe JF, Rechtsteiner A, Gottardo R, Rocha LM, Browne EP, et al. (2004) Evaluation of the host transcriptional response to human cytomegalovirus infection. Physiol Genomics 18: 51-62.
11. Ishov AM, Maul GG, (1996) The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J Cell Biol 134: 815-826.
12. Maul GG, (1998) Nuclear domain 10, the site of DNA virus transcription and replication. BioEssays 20: 660-667.
13. Everett RD, Chelbi-Alix MK, (2007) PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89: 819-830.
14. Wu WS, Vallian S, Seto E, Yang WM, Edmondson D, et al. (2001) The growth suppressor PML represses transcription by functionally and physically interacting with histone deacetylases. Mol Cell Biol 21: 2259-2268.
15. Li H, Chen JD, (2000) PML and the oncogenic nuclear domains in regulating transcriptional repression. Curr Opin Cell Biol 12: 641-644.
16. Hollenbach AD, McPherson CJ, Mientjes EJ, Iyengar R, Grosveld G, (2002) Daxx and histone deacetylase II associate with chromatin through an interaction with core histones and the chromatin-associated protein Dek. J Cell Sci 115: 3319-3330.
17. Hofmann H, Sindre H, Stamminger T, (2002) Functional interaction between the pp71 protein of human cytomegalovirus and the PML-interacting protein human Daxx. J Virol 76: 5769-5783.
18. Ishov AM, Vladimirova OV, Maul GG, (2002) Daxx-mediated accumulation of human cytomegalovirus tegument protein pp71 at ND10 facilitates initiation of viral infection at these nuclear domains. J Virol 76: 7705-7712.
19. Ahn JH, Hayward GS, (1997) The major immediate-early proteins IE1 and IE2 of human cytomegalovirus colocalize with and disrupt PML-associated nuclear bodies at very early times in infected permissive cells. J Virol 71: 4599-4613.
20. Korioth F, Maul GG, Plachter B, Stamminger T, Frey J, (1996) The Nuclear Domain 10 (ND10) Is Disrupted by the Human Cytomegalovirus Gene Product IE1. Exp Cell Res 229: 155-158.
21. Tang Q, Maul GG, (2003) Mouse Cytomegalovirus Immediate-Early Protein 1 Binds with Host Cell Repressors To Relieve Suppressive Effects on Viral Transcription and Replication during Lytic Infection. J Virol 77: 1357-1367.
22. Maul GG, Negorev D, (2008) Differences between mouse and human cytomegalovirus interactions with their respective hosts at immediate early times of the replication cycle. Med Microbiol Immunol 197: 241-249.
23. Marchini A, Liu H, Zhu H, (2001) Human cytomegalovirus with IE-2 (UL122) deleted fails to express early lytic genes. J Virol 75: 1870-1878.
24. Heider JA, Bresnahan WA, Shenk TE, (2002) Construction of a rationally designed human cytomegalovirus variant encoding a temperature-sensitive immediate-early 2 protein. Proc Natl Acad Sci U S A 99: 3141-3146.
25. Anders D, Kerry J (2007) DNA synthesis and late viral gene expression. In: Source Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis. Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K, editors. Cambridge: Cambridge University Press. Chapter 16.
26. Sciortino MT, Suzuki M, Taddeo B, Roizman B, (2001) RNAs Extracted from Herpes Simplex Virus 1 Virions: Apparent Selectivity of Viral but Not Cellular RNAs Packaged in Virions. J Virol 75: 8105-8116.
27. Sarcinella E, Brown M, Tellier R, Petric M, Mazzulli T, (2004) Detection of RNA in purified cytomegalovirus virions. Virus Res 104: 129-137.
28. Terhune SS, Shenk T, (2004) RNAs Are Packaged into Human Cytomegalovirus Virions in Proportion to Their Intracellular Concentration. J Virol 78: 10390-10398.
29. Bechtel J, Grundhoff A, Ganem D, (2005) RNAs in the virion of Kaposi's sarcoma-associated herpesvirus. J Virol 79: 10138-10146.
30. Jochum S, Ruiss R, Moosmann A, Hammerschmidt W, Zeidler R, (2012) RNAs in Epstein-Barr virions control early steps of infection. Proc Natl Acad Sci U S A 109: E1396-404.
31. Groves IJ, Reeves MB, Sinclair JH, (2009) Lytic infection of permissive cells with human cytomegalovirus is regulated by an intrinsic "pre-immediate-early" repression of viral gene expression mediated by histone post-translational modification. J Gen Virol 90: 2364-2374.
32. Cuevas-Bennett C, Shenk T, (2008) Dynamic histone H3 acetylation and methylation at human cytomegalovirus promoters during replication in fibroblasts. J Virol 82: 9525-9536.
33. Nevels M, Paulus C, Shenk T, (2004) Human cytomegalovirus immediate-early 1 protein facilitates viral replication by antagonizing histone deacetylation. Proc Natl Acad Sci U S A 101: 17234-17239.
34. Dölken L, Ruzsics Z, Rädle B, Friedel CC, Zimmer R, et al. (2008) High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14: 1959-1972.
35. Yang E, Van NE, Zavolan M, Rajewsky N, Schroeder M, et al. (2003) Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13: 1863-1872.
36. Friedel CC, Dölken L, (2009) Metabolic tagging and purification of nascent RNA: implications for transcriptomics. Mol Biosyst 5: 1271-1278.
37. Bresnahan WA, Shenk T, (2000) A subset of viral transcripts packaged within human cytomegalovirus particles. Science 288: 2373-2376.
38. Miller MR, Robinson KJ, Cleary MD, Doe CQ, (2009) TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nat Methods 6: 439-441.
39. Miller C, Schwalb B, Maier K, Schulz D, Dümcke S, et al. (2011) Dynamic transcriptome analysis measures rates of mRNA synthesis and decay in yeast. Mol Syst Biol 7: 458.
40. Friedel CC, Dölken L, Ruzsics Z, Koszinowski UH, Zimmer R, (2009) Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res 37: e115.
41. Rabani M, Levin JZ, Fan L, Adiconis X, Raychowdhury R, et al. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat Biotechnol 29: 436-442.
42. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, et al. (2011) Global quantification of mammalian gene expression control. Nature 473: 337-342.
43. Windhager L, Bonfert T, Burger K, Ruzsics Z, Krebs S, et al. (2012) Ultra short and progressive 4sU-tagging reveals key characteristics of RNA processing at nucleotide resolution. Genome Res Epub ahead of print.
44. Munger J, Bajad SU, Coller Ha, Shenk T, Rabinowitz JD, (2006) Dynamics of the cellular metabolome during human cytomegalovirus infection. PLoS Pathog 2: e132.
45. Kenzelmann M, Maertens S, Hergenhahn M, Kueffer S, Hotz-Wagenblatt A, et al. (2007) Microarray analysis of newly synthesized RNA in cells and animals. Proc Natl Acad Sci U S A 104: 6164-6169.
46. Melvin WT, Milne HB, Slater a a, Allen HJ, Keir HM, (1978) Incorporation of 6-thioguanosine and 4-thiouridine into RNA. Application to isolation of newly synthesised RNA by affinity chromatography. Eur J Biochem 92: 373-379.
47. Ghosh S, Karin M, (2002) Missing Pieces in the NF-κB Puzzle. Cell 109: S81-S96.
48. Gribaudo G, (1996) The murine cytomegalovirus immediate-early 1 protein stimulates NF-κ B activity by transactivating the NF-κ B p105/p50 promoter. Virus Res 45: 15-27.
49. Mack C, Sickmann A, Lembo D, Brune W, (2008) Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1-interacting protein. Proc Natl Acad Sci U S A 105: 3094-3099.
50. Fliss PM, Jowers TP, Brinkmann MM, Holstermann B, Mack C, et al. (2012) Viral Mediated Redirection of NEMO/IKKγ to Autophagosomes Curtails the Inflammatory Cascade. PLoS Patho 8: e1002517.
51. Taniguchi T, Ogasawara K, Takaoka A, Tanaka N, (2001) IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19: 623-655.
52. 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.
53. Caposio P, Luganini A, Bronzini M, Landolfo S, Gribaudo G, (2010) The Elk-1 and serum response factor binding sites in the major immediate-early promoter of human cytomegalovirus are required for efficient viral replication in quiescent cells and compensate for inactivation of the NF-kappaB sites in proliferating cells. J Virol 84: 4481-4493.
54. Shi Y, Lee JS, Galvin KM, (1997) Everything you have ever wanted to know about Yin Yang 1. Biochi Biophys Acta 1332: F49-66.
55. Liu R, Baillie J, Sissons JG, Sinclair JH, (1994) The transcription factor YY1 binds to negative regulatory elements in the human cytomegalovirus major immediate early enhancer/promoter and mediates repression in non-permissive cells. Nucleic Acids Res 22: 2453-2459.
56. Liu XF, Yan S, Abecassis M, Hummel M, (2010) Biphasic recruitment of transcriptional repressors to the murine cytomegalovirus major immediate-early promoter during the course of infection in vivo. J Virol 84: 3631-3643.
57. Dang CV, Resar LM, Emison E, Kim S, Li Q, et al. (1999) Function of the c-Myc oncogenic transcription factor. Exp Cell Res 253: 63-77.
58. Hagemeier C, Walker SM, Sissons PJ, Sinclair JH, (1992) The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently trans-activate the c-fos, c-myc and hsp70 promoters via basal promoter elements. J Gen Virol 73: 2385-2393.
59. Jung P, Menssen A, Mayr D, Hermeking H, (2008) AP4 encodes a c-MYC-inducible repressor of p21. Proc Natl Acad Sci U S A 105: 15046-15051.
60. Hromas R, Davis B, Rauscher FJ, Klemsz M, Tenen D, et al. (1996) Hematopoietic transcriptional regulation by the myeloid zinc finger gene, MZF-1. Curr Top Microbiol Immunol 211: 159-164.
61. Gaboli M, Kotsi PA, Gurrieri C, Cattoretti G, Ronchetti S, et al. (2001) Mzf1 controls cell proliferation and tumorigenesis. Genes Dev 15: 1625-1630.
62. Hilger-Eversheim K, Moser M, Schorle H, Buettner R, (2000) Regulatory roles of AP-2 transcription factors in vertebrate development, apoptosis and cell-cycle control. Gene 260: 1-12.
63. Bell LA, Ryan KM, (2004) Life and death decisions by E2F-1. Cell Death Differ 11: 137-142.
64. Song YJ, Stinski MF, (2002) Effect of the human cytomegalovirus IE86 protein on expression of E2F-responsive genes: a DNA microarray analysis. Proc Natl Acad Sci U S A 99: 2836-2841.
65. Wang G-L, Shi X, Salisbury E, Timchenko NA, (2008) Regulation of apoptotic and growth inhibitory activities of C/EBPalpha in different cell lines. Exp Cell Res 314: 1626-1639.
66. Wang H, Iakova P, Wilde M, Welm A, Goode T, et al. (2001) C/EBPalpha arrests cell proliferation through direct inhibition of Cdk2 and Cdk4. Mol Cell 8: 817-828.
67. Slomiany BA, D'Arigo KL, Kelly MM, Kurtz DT, (2000) C/EBPalpha Inhibits Cell Growth via Direct Repression of E2F-DP-Mediated Transcription. Mol Cell Biol 20: 5986-5997.
68. Kobelt D, Aumann J, Fichtner I, Stein U, Schlag PM, et al. (2010) Activation of the CMV-IE promoter by hyperthermia in vitro and in vivo: biphasic heat induction of cytosine deaminase suicide gene expression. Mol Biotechnol 46: 197-205.
69. Gilmore TD, (2006) Introduction to NF-kappaB: players, pathways, perspectives. Oncogene 25: 6680-6684.
70. Grandori C, Cowley SM, James LP, Eisenman RN, (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol 16: 653-699.
71. Gupta S, Seth A, Davis RJ, (1993) Transactivation of gene expression by Myc is inhibited by mutation at the phosphorylation sites Thr-58 and Ser-62. Proc Natl Acad Sci U S A 90: 3216-3220.
72. 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.
73. Hollander MC, Alamo I, Jackman J, Wang MG, McBride OW, et al. (1993) Analysis of the mammalian gadd45 gene and its response to DNA damage. J Biol Chem 268: 24385-24393.
74. Castillo JP, Frame FM, Rogoff HA, Pickering MT, Yurochko AD, et al. (2005) Human cytomegalovirus IE1-72 activates ataxia telangiectasia mutated kinase and a p53/p21-mediated growth arrest response. J Virol 79: 11467-11475.
75. Kokame K, Agarwala KL, Kato H, Miyata T, (2000) Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress. J Biol Chem 275: 32846-32853.
76. Qian Z, Xuan B, Gualberto N, Yu D, (2011) HCMV protein pUL38 suppresses ER stress-mediated cell death independent of its ability to induce mTORC1 activation. J Virol 85: 9103-9113.
77. Timpl R, Brown JC, (1994) The laminins. Matrix Biol 14: 275-281.
78. Wang JC, (1996) DNA topoisomerases. Annu Rev Biochem 65: 635-692.
79. MacDonald MR, Burney MW, Resnick SB, Virgin HW IV, (1999) Spliced mRNA encoding the murine cytomegalovirus chemokine homolog predicts a beta chemokine of novel structure. J Virol 73: 3682-3691.
80. Maninger S, Bosse JB, Lemnitzer F, Pogoda M, Mohr CA, et al. (2011) M94 is essential for the secondary envelopment of murine cytomegalovirus. J Virol 85: 9254-9267.
81. Fleming P, Davis-Poynter N, Degli-Esposti M, Densley E, Papadimitriou J, et al. (1999) The murine cytomegalovirus chemokine homolog, m131/129, is a determinant of viral pathogenicity. J Virol 73: 6800-6809.
82. Akter P, Cunningham C, McSharry BP, Dolan A, Addison C, et al. (2003) Two novel spliced genes in human cytomegalovirus. J Gen Virol 84: 1117-1122.
83. Babić M, Krmpotić A, Jonjić S, (2011) All is fair in virus-host interactions: NK cells and cytomegalovirus. Trends Mol Med 17: 677-685.
84. Dimova DK, Dyson NJ, (2005) The E2F transcriptional network: old acquaintances with new faces. Oncogene 24: 2810-2826.
85. Attwooll C, Lazzerini Denchi E, Helin K, (2004) The E2F family: specific functions and overlapping interests. EMBO J 23: 4709-4716.
86. Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, et al. (2007) LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6: 1903-1913.
87. Knight AS, Notaridou M, Watson RJ, (2009) A Lin-9 complex is recruited by B-Myb to activate transcription of G2/M genes in undifferentiated embryonal carcinoma cells. Oncogene 28: 1737-1747.
88. Kalejta RF, Bechtel JT, Shenk T, (2003) Human cytomegalovirus pp71 stimulates cell cycle progression by inducing the proteasome-dependent degradation of the retinoblastoma family of tumor suppressors. Mol Cell Biol 23: 1885-1895.
89. Kalejta RF, Shenk T, (2003) Proteasome-dependent, ubiquitin-independent degradation of the Rb family of tumor suppressors by the human cytomegalovirus pp71 protein. Proc Natl Acad Sci U S A 100: 3263-3268.
90. 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.
91. Wathen MW, Stinski MF, (1982) Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection. J Virol 41: 462-477.
92. Geballe AP, Mocarski ES, (1988) Translational control of cytomegalovirus gene expression is mediated by upstream AUG codons. J virol 62: 3334-3340.
93. Geballe AP, Spaete RR, Mocarski ES, (1986) A cis-acting element within the 5′ leader of a cytomegalovirus beta transcript determines kinetic class. Cell 46: 865-872.
94. Sinclair J, (2010) Chromatin structure regulates human cytomegalovirus gene expression during latency, reactivation and lytic infection. Biochim Biophys Acta 1799: 286-295.
95. Woodhall DL, Groves IJ, Reeves MB, Wilkinson G, Sinclair JH, (2006) Human Daxx-mediated repression of human cytomegalovirus gene expression correlates with a repressive chromatin structure around the major immediate early promoter. J Biol Chem 281: 37652-37660.
96. Netterwald J, Yang S, Wang W, Ghanny S, Cody M, et al. (2005) Two gamma interferon-activated site-like elements in the human cytomegalovirus major immediate-early promoter/enhancer are important for viral replication. J Virol 79: 5035-5046.
97. Meier JL, Stinski MF (2006) Major immediate-early enhancer and its gene products. In: Cytomegaloviruses: Molecular Biology and Immunology. Reddehase, M J, editor. Norfolk, UK: Caister Academic Press. pp 151-166.
98. Rupp B, Ruzsics Z, Sacher T, Koszinowski UH, (2005) Conditional cytomegalovirus replication in vitro and in vivo. J Virol 79: 486-494.
99. R Development Core Team (2007) A language and environment for statistical computing. ISBN 3-900051-07-0 http://wwwR-project org 2007.
100. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Series B Stat Methodol 57: 289-300.
101. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
102. Defrance M, Touzet H, (2006) Predicting transcription factor binding sites using local over-representation and comparative genomics. BMC Bioinformatics 7: 396.
103. Scrivano L, Esterlechner J, Mühlbach H, Ettischer N, Hagen C, et al. (2010) The m74 gene product of murine cytomegalovirus (MCMV) is a functional homolog of human CMV gO and determines the entry pathway of MCMV. J Virol 84: 4469-4480.
104. Popa M, Ruzsics Z, Lötzerich M, Dölken L, Buser C, et al. (2010) Dominant negative mutants of the murine cytomegalovirus M53 gene block nuclear egress and inhibit capsid maturation. J Virol 84: 9035-9046.