Heterologous viral promoters incorporated into the human cytomegalovirus genome are silenced during experimental latency

Journal of Virology

Volumn 87, Issue 17, 2013, Pages 9886-9894

  Qin, Qingsong ^a   Penkert, Rhiannon R ^a   Kalejta, Robert F ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; IMMEDIATE EARLY PROTEIN;

ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; FIBROBLAST; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; VIRUS GENOME; VIRUS LATENCY; VIRUS STRAIN;

ANIMALS; ANTIGENS, CD34; CELL LINE; CELLS, CULTURED; CYTOMEGALOVIRUS; GENE SILENCING; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; MICE; MONOCYTES; MYELOID CELLS; PROMOTER REGIONS, GENETIC; RECOMBINATION, GENETIC; SPLEEN FOCUS-FORMING VIRUSES; TERMINAL REPEAT SEQUENCES; VIRAL PROTEINS; VIRUS LATENCY;

EID: 84883283392     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01726-13     Document Type: Article

References (49)

1. Mocarski ES, Jr, Shenk T, Pass RF. 2007. Cytomegalovirus, p 2701-2772. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Kalejta RF. 2008. Functions of human cytomegalovirus tegument proteins prior to immediate early gene expression. Curr. Top. Microbiol. Immunol. 325:101-115.
3. Saffert RT, Kalejta RF. 2006. Inactivating a cellular intrinsic immune defense mediated by Daxx is the mechanism through which the human cytomegalovirus pp71 protein stimulates viral immediate-early gene expression. J. Virol. 80:3863-3871.
4. Sinclair J. 2010. Chromatin structure regulates human cytomegalovirus gene expression during latency, reactivation and lytic infection. Biochim. Biophys. Acta 1799:286-295.
5. Goodrum F, Caviness K, Zagallo P. 2012. Human cytomegalovirus persistence. Cell. Microbiol. 14:644-655.
6. Saffert RT, Kalejta RF. 2007. Human cytomegalovirus gene expression is silenced by Daxx-mediated intrinsic immune defense in model latent infections established in vitro. J. Virol. 81:9109-9120.
7. Saffert RT, Penkert RR, Kalejta RF. 2010. Cellular and viral control over the initial events of human cytomegalovirus experimental latency in CD34+ cells. J. Virol. 84:5594-5604.
8. Penkert RR, Kalejta RF. 2013. Human embryonic stem cell lines model experimental human cytomegalovirus latency. mBio 4(3):e00298-13. doi: 10.1128/mBio.00298-13.
9. Penkert RR, Kalejta RF. 2010. Nuclear localization of tegumentdelivered pp71 in human cytomegalovirus-infected cells is facilitated by one or more factors present in terminally differentiated fibroblasts. J. Virol. 84:9853-9863.
10. Penkert RR, Kalejta RF. 2012. Tale of a tegument transactivator: the past, present and future of human CMV pp71. Future Virol. 7:855-869.
11. Hofmann H, Sindre H, Stamminger T. 2002. Functional interaction between the pp71 protein of human cytomegalovirus and the PMLinteracting protein human Daxx. J. Virol. 76:5769-5783.
12. Ruger B, Klages S, Walla B, Albrecht J, Fleckenstein B, Tomlinson P, Barrell B. 1987. Primary structure and transcription of the genes coding for the two virion phosphoproteins pp65 and pp71 of human cytomegalovirus. J. Virol. 61:446-453.
13. Hensel GM, Meyer HH, Buchmann I, Pommerehne D, Schmolke S, Plachter B, Radsak K, Kern HF. 1996. Intracellular localization and expression of the human cytomegalovirus matrix phosphoprotein pp71 (ppUL82): evidence for its translocation into the nucleus. J. Gen. Virol. 77(Part 12):3087-3097.
14. Tsuji T, Itoh K, Baum C, Ohnishi N, Tomiwa K, Hirano D, Nishimura-Morita Y, Ostertag W, Fujita J. 2000. Retroviral vector-mediated gene expression in human CD34+CD38-cells expanded in vitro: cis elements of FMEV are superior to those of Mo-MuLV. Hum. Gene Ther. 11:271-284.
15. Carter CC, McNamara LA, Onafuwa-Nuga A, Shackleton M, Riddell J, IV, Bixby D, Savona MR, Morrison SJ, Collins KL. 2011. HIV-1 utilizes the CXCR4 chemokine receptor to infect multipotent hematopoietic stem and progenitor cells. Cell Host Microbe 9:223-234.
16. Carter CC, Onafuwa-Nuga A, McNamara LA, Riddell J, IV, Bixby D, Savona MR, Collins KL. 2010. HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat. Med. 16:446-451.
17. Demaison C, Parsley K, Brouns G, Scherr M, Battmer K, Kinnon C, Grez M, Thrasher AJ. 2002. High-level transduction and gene expression in hematopoietic repopulating cells using a human imunodeficiency [sic] virus type 1-based lentiviral vector containing an internal spleen focus forming virus promoter. Hum. Gene Ther. 13:803-813.
18. Yam PY, Li S, Wu J, Hu J, Zaia JA, Yee JK. 2002. Design of HIV vectors for efficient gene delivery into human hematopoietic cells. Mol. Ther. 5:479-484.
19. Baum C, Hegewisch-Becker S, Eckert HG, Stocking C, Ostertag W. 1995. Novel retroviral vectors for efficient expression of the multidrug resistance (mdr-1) gene in early hematopoietic cells. J. Virol. 69:7541-7547.
20. Terhune S, Torigoi E, Moorman N, Silva M, Qian Z, Shenk T, Yu D. 2007. Human cytomegalovirus UL38 protein blocks apoptosis. J. Virol. 81:3109-3123.
21. Wang D, Bresnahan W, Shenk T. 2004. Human cytomegalovirus encodes a highly specific RANTES decoy receptor. Proc. Natl. Acad. Sci. U. S. A. 101:16642-16647.
22. O'Connor CM, Murphy EA. 2012. A myeloid progenitor cell line capable of supporting human cytomegalovirus latency and reactivation, resulting in infectious progeny. J. Virol. 86:9854-9865.
23. Wu C, Lu Y. 2010. High-titre retroviral vector system for efficient gene delivery into human and mouse cells of haematopoietic and lymphocytic lineages. J. Gen. Virol. 91:1909-1918.
24. Tischer BK, von Einem J, Kaufer B, Osterrieder N. 2006. Two-step red-mediated recombination for versatile high-efficiency markerlessDNA manipulation in Escherichia coli. Biotechniques 40:191-197.
25. Qin Q, Hastings C, Miller CL. 2009. Mammalian orthoreovirus particles induce and are recruited into stress granules at early times postinfection. J. Virol. 83:11090-11101.
26. 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.
27. Zhu H, Shen Y, Shenk T. 1995. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J. Virol. 69:7960-7970.
28. Nowak B, Sullivan C, Sarnow P, Thomas R, Bricout F, Nicolas JC, Fleckenstein B, Levine AJ. 1984. Characterization of monoclonal antibodies and polyclonal immune sera directed against human cytomegalovirus virion proteins. Virology 132:325-338.
29. Qin Q, Carroll K, Hastings C, Miller CL. 2011. Mammalian orthoreovirus escape from host translational shutoff correlates with stress granule disruption and is independent of eIF2alpha phosphorylation and PKR. J. Virol. 85:8798-8810.
30. Tischer BK, Smith GA, Osterrieder N. 2010. En passant mutagenesis: a two step markerless red recombination system. Methods Mol. Biol. 634: 421-430.
31. Kalejta RF. 2008. Tegument proteins of human cytomegalovirus. Microbiol. Mol. Biol. Rev. 72:249-265.
32. Gutsch R, Kandemir JD, Pietsch D, Cappello C, Meyer J, Simanowski K, Huber R, Brand K. 2011. CCAAT/enhancer-binding protein beta inhibits proliferation in monocytic cells by affecting the retinoblastoma protein/E2F/cyclin E pathway but is not directly required for macrophage morphology. J. Biol. Chem. 286:22716-22729.
33. Kerry JA, Priddy MA, Staley TL, Jones TR, Stenberg RM. 1997. The role of ATF in regulating the human cytomegalovirus DNA polymerase (UL54) promoter during viral infection. J. Virol. 71:2120-2126.
34. Chambers J, Angulo A, Amaratunga D, Guo H, Jiang Y, Wan JS, Bittner A, Frueh K, Jackson MR, Peterson PA, Erlander MG, Ghazal P. 1999. DNA microarrays of the complex human cytomegalovirus genome: profiling kinetic class with drug sensitivity of viral gene expression. J. Virol. 73:5757-5766.
35. Penkert RR, Kalejta RF. 2011. Tegument protein control of latent herpesvirus establishment and animation. Herpesviridae 2:3. doi:10.1186 /2042-4280-2-3.
36. Budt M, Hristozova T, Hille G, Berger K, Brune W. 2011. Construction of a lytically replicating Kaposi's sarcoma-associated herpesvirus. J. Virol. 85:10415-10420.
37. Thompson RL, Preston CM, Sawtell NM. 2009. De novo synthesis of VP16 coordinates the exit from HSV latency in vivo. PLoS Pathog. 5:e1000352. doi:10.1371/journal.ppat.1000352.
38. Reeves MB. 2011. Chromatin-mediated regulation of cytomegalovirus gene expression. Virus Res. 157:134-143.
39. Smiley JR, Smibert C, Everett RD. 1987. Expression of a cellular gene cloned in herpes simplex virus: rabbit beta-globin is regulated as an early viral gene in infected fibroblasts. J. Virol. 61:2368-2377. 40. Panning B, Smiley JR. 1989. Regulation of cellular genes transduced b y herpes simplex virus. J. Virol. 63:1929-1937.
40. Panning B, Smiley JR. 1989. Regulation of cellular genes transduced b y herpes simplex virus. J. Virol. 63:1929-1937.
41. Roemer K, Johnson PA, Friedmann T. 1995. Transduction of foreign regulatory sequences by a replication-defective herpes simplex virus type 1: the rat neuron-specific enolase promoter. Virus Res. 35:81-89.
42. Warden C, Tang Q, Zhu H. 2011. Herpesvirus BACs: past, present, and future. J. Biomed. Biotechnol. 2011:124595. doi:10.1155/2011/124595.
43. Goodrum FD, Jordan CT, High K, Shenk T. 2002. Human cytomegalovirus gene expression during infection of primary hematopoietic progenitor cells: a model for latency. Proc. Natl. Acad. Sci. U. S. A. 99:16255-16260.
44. Umashankar M, Petrucelli A, Cicchini L, Caposio P, Kreklywich CN, Rak M, Bughio F, Goldman DC, Hamlin KL, Nelson JA, Fleming WH, Streblow DN, Goodrum F. 2011. A novel human cytomegalovirus locus modulates cell type-specific outcomes of infection. PLoS Pathog. 7:e1002444. doi:10.1371/journal.ppat.1002444.
45. Terhune SS, Schroer J, Shenk T. 2004. RNAs are packaged into human cytomegalovirus virions in proportion to their intracellular concentration. J. Virol. 78:10390-10398.
46. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, Whizin N, Oswald K, Shoemaker R, Swanson T, Legasse AW, Chiuchiolo MJ, Parks CL, Axthelm MK, Nelson JA, Jarvis MA, Piatak M, Jr, Lifson JD, Picker LJ. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473:523-527.
47. Kohler CP, Kerry JA, Carter M, Muzithras VP, Jones TR, Stenberg RM. 1994. Use of recombinant virus to assess human cytomegalovirus early and late promoters in the context of the viral genome. J. Virol. 68:6589-6597.
48. Lieu PT, Wagner EK. 2000. The kinetics of VP5 mRNA expression is not critical for viral replication in cultured cells. J. Virol. 74:2770-2776.
49. Albright ER, Kalejta RF. 2013. Myeloblastic cell lines mimic some but not all aspects of human cytomegalovirus experimental latency defined in primary CD34+ cell populations. J. Virol. 87:9802-9812.