Variable episomal silencing of a recombinant herpesvirus renders its encoded GFP an unreliable marker of infection in primary cells

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Ellison, Thomas J ^a   Kedes, Dean H ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; VALPROIC ACID; CHROMATIN; HISTONE; LATENCY-ASSOCIATED NUCLEAR ANTIGEN; NUCLEAR PROTEIN; VIRUS ANTIGEN;

ANIMAL CELL; ARTICLE; CELL ASSAY; CELL IMMORTALIZATION; CHROMATIN; CONTROLLED STUDY; EPIGENETICS; EPISOME; FLOW CYTOMETRY; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION; GENE SILENCING; HERPES VIRUS INFECTION; MARKER GENE; MESENCHYME CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; VARIABLE EPISOMAL SILENCING; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS LATENCY; VIRUS RECOMBINANT; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DRUG EFFECTS; GENE VECTOR; GENETIC EPIGENESIS; GENETIC TRANSDUCTION; GENETICS; HERPESVIRIDAE; HUMAN; HUMAN HERPESVIRUS 8; MESENCHYMAL STROMA CELL; METABOLISM; PLASMID; PRIMARY CELL CULTURE; REPORTER GENE; VIROLOGY;

HERPESVIRIDAE;

ANIMALS; ANTIGENS, VIRAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; GENE EXPRESSION; GENE SILENCING; GENES, REPORTER; GENETIC VECTORS; HERPESVIRIDAE; HERPESVIRUS 8, HUMAN; HISTONES; HUMANS; MESENCHYMAL STROMAL CELLS; NUCLEAR PROTEINS; PLASMIDS; PRIMARY CELL CULTURE; RATS; TRANSDUCTION, GENETIC; VALPROIC ACID;

EID: 84913556448     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111502     Document Type: Article

References (30)

1. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated kaposi's sarcoma. Science 266 (5192):1865-1869.
2. Nador RG, Cesarman E, Chadburn A, Dawson DB, Ansari MQ, et al. (1996) Primary effusion lymphoma: A distinct clinicopathologic entity associated with the kaposi's sarcoma-associated herpes virus. Blood 88 (2):645-656.
3. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric castleman's disease. Blood 86 (4):1276-1280.
4. Vieira J, O'Hearn PM (2004) Use of the red fluorescent protein as a marker of kaposi's sarcoma-associated herpesvirus lytic gene expression. Virology 325 (2):225-240. doi: 10.1016/j.virol.2004.03.049.
5. Johnson AS, Maronian N, Vieira J (2005) Activation of kaposi's sarcomaassociated herpesvirus lytic gene expression during epithelial differentiation. J Virol 79 (21):13769-13777. doi: 10.1128/JVI.79.21.13769-13777.2005.
6. Seifi A, Weaver EM, Whipple ME, Ikoma M, Farrenberg J, et al. (2011) The lytic activation of KSHV during keratinocyte differentiation is dependent upon a suprabasal position, the loss of integrin engagement, and calcium, but not the interaction of cadherins. Virology 410 (1):17-29. doi: 10.1016/j.virol.2010.10.023.
7. Wu W, Vieira J, Fiore N, Banerjee P, Sieburg M, et al. (2006) KSHV/HHV-8 infection of human hematopoietic progenitor (CD34+) cells: Persistence of infection during hematopoiesis in vitro and in vivo. Blood 108 (1):141-151. doi: 10.1182/blood-2005-04-1697.
8. Jeffery HC, Wheat RL, Blackbourn DJ, Nash GB, Butler LM (2013) Infection and transmission dynamics of rKSHV.219 in primary endothelial cells. J Virol Methods 193 (1):251-259. doi: 10.1016/j.jviromet.2013.06.001.
9. Myoung J, Ganem D (2011) Infection of lymphoblastoid cell lines by kaposi's sarcoma-associated herpesvirus: Critical role of cell-associated virus. J Virol 85 (19):9767-9777. doi: 10.1128/JVI.05136-11.
10. Myoung J, Ganem D (2010) Infection of primary human tonsillar lymphoid cells by KSHV reveals frequent but abortive infection of T cells. Virology 413 (1):1- 11. doi: 10.1016/j.virol.2010.12.036.
11. Jones T, Ye F, Bedolla R, Huang Y, Meng J, et al. (2012) Direct and efficient cellular transformation of primary rat mesenchymal precursor cells by KSHV. J Clin Invest 122 (3):1076-1081. doi: 10.1172/JCI58530.
12. Ashlock BM, Ma Q, Issac B, Mesri EA (2014) Productively infected murine kaposi's sarcoma-like tumors define new animal models for studying and targeting KSHV oncogenesis and replication. PLoS One 9 (1): e87324. doi: 10.1371/journal. pone.0087324.
13. Gunther T, Grundhoff A (2010) The epigenetic landscape of latent kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog 6 (6): e1000935.
14. Toth Z, Maglinte DT, Lee SH, Lee HR, Wong LY, et al. (2010) Epigenetic analysis of KSHV latent and lytic genomes. PLoS Pathog 6 (7): e1001013.
15. Chang PC, Fitzgerald LD, Van Geelen A, Izumiya Y, Ellison TJ, et al. (2009) Kruppel-associated box domain-associated protein-1 as a latency regulator for kaposi's sarcoma-associated herpesvirus and its modulation by the viral protein kinase. Cancer Res 69 (14):5681-5689. doi: 10.1158/0008-5472.CAN-08-4570.
16. Toth Z, Brulois K, Lee HR, Izumiya Y, Tepper C, et al. (2013) Biphasic euchromatin-to-heterochromatin transition on the KSHV genome following de novo infection. PLoS Pathog 9 (12): e1003813. doi: 10.1371/journal. ppat.1003813.
17. Krishnan HH, Naranatt PP, Smith MS, Zeng L, Bloomer C, et al. (2004) Concurrent expression of latent and a limited number of lytic genes with immune modulation and antiapoptotic function by kaposi's sarcoma-associated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J Virol 78(7):3601-3620.
18. Grundhoff A, Ganem D (2004) Inefficient establishment of KSHV latency suggests an additional role for continued lytic replication in kaposi sarcoma pathogenesis. J Clin Invest 113 (1):124-136. doi: 10.1172/JCI17803.
19. Myoung J, Ganem D (2011) Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: Maintenance of tight latency with efficient reactivation upon induction. J Virol Methods 174 (1-2):12-21. doi: 10.1016/j. jviromet.2011.03.012.
20. Adang LA, Parsons CH, Kedes DH (2006) Asynchronous progression through the lytic cascade and variations in intracellular viral loads revealed by highthroughput single-cell analysis of kaposi's sarcoma-associated herpesvirus infection. J Virol 80 (20):10073-10082.
21. Nichols LA, Adang LA, Kedes DH (2011) Rapamycin blocks production of KSHV/HHV8: Insights into the anti-tumor activity of an immunosuppressant drug. PLoS One 6 (1): e14535. doi: 10.1371/journal. pone.0014535.
22. Borah S, Nichols LA, Hassman LM, Kedes DH, Steitz JA (2012) Tracking expression and subcellular localization of RNA and protein species using highthroughput single cell imaging flow cytometry. RNA 18 (8):1573-1579. doi: 10.1261/rna.033126.112.
23. Ballestas ME, Chatis PA, Kaye KM (1999) Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284 (5414):641-644.
24. Ballestas ME, Kaye KM (2001) Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mediates episome persistence through cisacting terminal repeat (TR) sequence and specifically binds TR DNA. J Virol 75 (7):3250-3258. doi: 10.1128/JVI.75.7.3250-3258.2001.
25. Shin HJ, DeCotiis J, Giron M, Palmeri D, Lukac DM (2014) Histone deacetylase classes I and II regulate kaposi's sarcoma-associated herpesvirus reactivation. J Virol 88 (2):1281-1292. doi: 10.1128/JVI.02665-13.
26. Gurvich N, Tsygankova OM, Meinkoth JL, Klein PS (2004) Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res.2004; 64 (3):1079-1086.
27. Collins CM, Boss JM, Speck SH (2009) Identification of infected B-cell populations by using a recombinant murine gammaherpesvirus 68 expressing a fluorescent protein. J Virol 83 (13):6484-6493. doi: 10.1128/JVI.00297-09 [doi].
28. Collins CM, Speck SH (2012) Tracking murine gammaherpesvirus 68 infection of germinal center B cells in vivo. PLoS One 7 (3): e33230. doi: 10.1371/journal. pone.0033230 [doi].
29. Dollery SJ, Santiago-Crespo RJ, Kardava L, Moir S, Berger EA (2014) Efficient infection of a human B cell line with cell-free kaposi's sarcoma-associated herpesvirus. J Virol 88 (3):1748-1757. doi: 10.1128/JVI.03063-13.
30. Brulois KF, Chang H, Lee AS, Ensser A, Wong LY, et al. (2012) Construction and manipulation of a new kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J Virol 86 (18):9708-9720. doi: 10.1128/JVI.01019-12 [doi].