Herpes simplex virus 1 microRNAs expressed abundantly during latent infection are not essential for latency in mouse trigeminal ganglia

Virology

Volumn 417, Issue 2, 2011, Pages 239-247

  Kramer, Martha F ^a   Jurak, Igor ^a   Pesola, Jean M ^a   Boissel, Sandrine ^a   Knipe, David M ^a   Coen, Donald M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Gene regulation; Herpes simplex virus; Latency; MicroRNAs

Indexed keywords

MICRORNA; MIR H6; PROTEIN ICP4; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; GENE DELETION; GENE EXPRESSION; GENE REPRESSION; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; LAT GENE; LATENT PERIOD; LATENT VIRUS INFECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRIGEMINUS GANGLION; VIRUS GENE;

ANIMALS; CARRIER STATE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; MALE; MICE; MICRORNAS; SEQUENCE DELETION; TRIGEMINAL GANGLION; VIRUS LATENCY;

HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 80052035740     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.06.027     Document Type: Article

References (61)

1. Bartel D.P. MicroRNAs: genomics, biogenesis mechanisms, and function. Cell 2004, 116:281-297.
2. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
3. Beretta J., Morillon A. Pervasive transcription constitutes a new level of eukaryotic genome regulation. EMBO Rep. 2009, 10:973-982.
4. Bohenzky R.A., Papavassiliou A.G., Gelman I.H., Silverstein S. Identification of a promoter mapping within the reiterated sequences that flank the herpes simplex virus type 1 UL region. J. Virol. 1993, 67:632-642.
5. Bohenzky R.A., Lagunoff M., Roizman B., Wagner E.K., Silverstein S. Two overlapping transcription units which extend across the L-S junction of herpes simplex virus type 1. J. Virol. 1995, 69:2889-2897.
6. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
7. Chen S.-H., Kramer M.F., Schaffer P.A., Coen D.M. A viral function represses accumulation of transcripts from productive-cycle genes in mouse ganglia latently infected with herpes simplex virus. J. Virol. 1997, 71:5878-5884.
8. Chen S.-H., Garber D.A., Schaffer P.A., Knipe D.M., Coen D.M. Persistent elevated expression of cytokine transcripts in ganglia latently infected with herpes simplex virus in the absence of ganglionic replication or reactivation. Virology 2000, 278:207-216.
9. Chen S.-H., Lee L.Y., Garber D.A., Schaffer P.A., Knipe D.M., Coen D.M. Neither LAT nor open reading frame P mutations increase expression of spliced or intron-containing ICP0 transcripts in mouse ganglia latently infected with herpes simplex virus. J. Virol. 2002, 76:4764-4772.
10. Chen C., Ridzon D.A., Broomer A.J., Zhou Z., Lee D.H., Nguyen J.T., Barbisin M., Xu N.L., Mahuvakar V.R., Andersen M.R., Lao K.Q., Livak K.J., Guegler K.J. Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 2005, 33:e179.
11. Cliffe A.R., Garber D.A., Knipe D.M. Transcription of the herpes simplex virus latency-associated transcript promotes the formation of facultative heterochromatin on lytic promoters. J. Virol. 2009, 83:8182-8190.
12. Cui C., Griffiths A., Li G., Silva L.M., Kramer M.F., Gaasterland T., Wang X.J., Coen D.M. Prediction and identification of herpes simplex virus 1-encoded microRNAs. J. Virol. 2006, 80:5499-5508.
13. Dobson A.T., Sederati F., Devi-Rao G., Flanagan W.M., Farrell M.J., Stevens J.G., Wagner E.K., Feldman L.T. Identification of the latency-associated transcript promoter by expression of rabbit beta-globin mRNA in mouse sensory nerve ganglia latently infected with a recombinant herpes simplex virus. J. Virol. 1989, 63:3844-3851.
14. Farrell M.J., Dobson A.T., Feldman L.T. Herpes simplex virus latency-associated transcript is a stable intron. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:790-794.
15. Feldman L.T., Ellison A.R., Voytek C.C., Yang L., Krause P., Margolis T.P. Spontaneous molecular reactivation of herpes simplex virus type 1 latency in mice. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:978-983.
16. Garber D.A., Schaffer P.A., Knipe D.M. A LAT-associated function reduces productive-cycle gene expression during acute infection of murine sensory neurons with herpes simplex virus type 1. J. Virol. 1997, 71:5885-5893.
17. Giordani N.V., Neumann D.M., Kwiatkowski D.L., Bhattacharjee P.S., McAnany P.K., Hill J.M., Bloom D.C. During herpes simplex virus type 1 infection of rabbits, the ability to express the latency-associated transcript increases latent-phase transcription of lytic genes. J. Virol. 2008, 82:6056-6060.
18. Holland L.E., Sandri-Goldin R.M., Goldin A.L., Glorioso J.C., Levine M. Transcriptional and genetic analyses of the herpes simplex virus type 1 genome: coordinates 0.29-0.45. J. Virol. 1984, 49l:947-959.
19. Honess R.W., Roizman B. Regulation of herpes virus macromolecular synthesis. I. Cascade regulation and synthesis of three groups of viral proteins. J. Virol. 1974, 14:8-19.
20. Hoshino Y., Pesnicak L., Straus S.E., Cohen J.I. Impairment in reactivation of a latency associated transcript (LAT)-deficient HSV-2 is not solely dependent on the latent viral load or the number of CD8(+) T cells infiltrating the ganglia. Virology 2009, 387:193-199.
21. Jacquier A. The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs. Nat. Rev. Genet. 2009, 10:833-844.
22. Jurak I., Kramer M.F., Mellor J.C., van Lint A.L., Roth F.P., Knipe D.M., Coen D.M. Numerous conserved and divergent microRNAs expressed by herpes simplex viruses 1 and 2. J. Virol. 2010, 84:4659-4672.
23. Knickelbein J.E., Khanna K.M., Yee M.B., Baty C.J., Kinchington P.R., Hendricks R.L. Noncytotoxic lytic granule-mediated CD8+ T cell inhibition of HSV-1 reactivation from neuronal latency. Science 2008, 322:268-271.
24. Kramer M.F., Coen D.M. Quantification of transcripts from the ICP4 and thymidine kinase genes in mouse ganglia latently infected with herpes simplex virus. J. Virol. 1995, 69:1389-1399.
25. Kramer M.F., Chen S.-H., Knipe D.M., Coen D.M. Accumulation of viral transcripts and DNA during establishment of latency by herpes simplex virus. J. Virol. 1998, 72:1177-1185.
26. Kramer M.F., Cook W.J., Roth F.R., Zhu J., Holman H., Knipe D.M., Coen D.M. Latent herpes simplex virus infection of sensory neurons alters neuronal gene expression. J. Virol. 2003, 77:9533-9541.
27. Krause P.R., Croen K.D., Straus S.E., Ostrove J.M. Detection and primary characterization of herpes simplex virus type 1 transcripts in latently infected human trigeminal ganglia. J. Virol. 1988, 62:4819-4823.
28. Krause P.R., Ostrove J.M., Straus S.E. The nucleotide sequence, 5' end, promoter domain, and kinetics of expression of the gene encoding the herpes simplex virus type 2 latency-associated transcript. J. Virol. 1991, 65:5619-5623.
29. Krause P.R., Stanberry L.R., Bourne N., Connelly B., Kurawadwala J.F., Patel A., Straus S.E. Expression of the herpes simplex virus type 2 latency-associated transcript enhances spontaneous reactivation of genital herpes in latently infected guinea pigs. J. Exp. Med. 1995, 181:297-306.
30. Kristie T.M., Vogel J.L., Sears A.E. Nuclear localization of the C1 factor (host cell factor) in sensory neurons correlates with reactivation of herpes simplex virus from latency. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1229-1233.
31. Kwiatkowski D.L., Thompson H.W., Bloom D.C. The polycomb group protein Bmi1 binds to the herpes simplex virus 1 latent genome and maintains repressive histone marks during latency. J. Virol. 2009, 83:8173-8181.
32. Leib D.A., Bogard C.L., Kosz-Vnenchak M., Hicks K.A., Coen D.M., Knipe D.M., Schaffer P.A. A deletion mutant of the latency-associated transcript of herpes simplex virus type 1 reactivates from the latent state with reduced frequency. J. Virol. 1989, 63:2893-2900.
33. Leib D.A., Coen D.M., Bogard C.L., Hicks K.A., Yager D.R., Knipe D.M., Tyler K.L., Schaffer P.A. Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J. Virol. 1989, 63:759-768.
34. Leib D.A., Harrison T.E., Laslo K.M., Machalek M.A., Moorman N.J., Virgin H.W. Interferons regulate the phenotype of wild-type and mutant herpes simplex viruses in vivo. J. Exp. Med. 1999, 189:663-672.
35. Mador N., Goldenberg D., Cohen O., Panet A., Steiner I. Herpes simplex virus type 1 latency-associated transcripts suppress viral replication and reduce immediate-early gene mRNA levels in a neuronal cell line. J. Virol. 1998, 72:5067-5075.
36. Margolis T.P., Elfman F.L., Leib D., Pakpour N., Apakupakul K., Imai Y., Voytek C. Spontaneous reactivation of herpes simplex virus type 1 in latently infected murine sensory ganglia. J. Virol. 2007, 81:11069-11074.
37. Mark K.E., Wald A., Magaret A.S., Selke S., Olin L., Huang M.-L., Corey L. Rapidly cleared episodes of herpes simplex virus reactivation in immunocompetent adults. J. Infect. Dis. 2008, 198:1141-1149.
38. Moens U. Silencing viral microRNA as a novel antiviral therapy. J. Biomed. Biotechnol. 2009, 2009:e419539.
39. Perng G., Dunkel E.C., Geary P.A., Slanina S.M., Ghiasi H., Kaiwar R., Nesburn A.B., Wechsler S.L. The latency-associated transcript gene of herpes simplex virus type 1 (HSV-1) is required for efficient in vivo spontaneous reactivation of HSV-1 from latency. J. Virol. 1994, 68:8045-8055.
40. Pesola J.M., Zhu J., Knipe D.M., Coen D.M. Herpes simplex virus 1 immediate-early and early gene expression during reactivation from latency under conditions that prevent infectious virus production. J. Virol. 2005, 79:14516-14525.
41. Roizman B., Knipe D.M., Whitley R.J. Herpes simplex viruses. Fields Virology 2007, 2502-2601. Lippincott Williams & Wilkins, Philadelphia. Fifth Edition. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, S.E. Straus, M.A. Martin, B. Roizman (Eds.).
42. Schiffer J.T., Abu-Raddad L., Mark K.E., Zhu J., Selke S., Magaret A.S., Wald A., Corey L. Frequent release of low amounts of herpes simplex virus from neurons: results of a mathematical model. Sci. Transl. Med. 2009, 1. (7ra16).
43. Sedarati F., Izumi K.M., Wagner E.K., Stevens J.G. Herpes simplex virus type 1 latency-associated transcription plays no role in establishment or maintenance of a latent infection in murine sensory neurons. J. Virol. 1989, 63:4455-4458.
44. Simmons A., Slobedman B., Speck P., Arthur J., Efstathiou S. Two patterns of persistence of herpes simplex virus DNA sequences in the nervous systems of latently infected mice. J. Gen. Virol. 1992, 73:1287-1291.
45. Singh J., Wagner E.K. Transcriptional analysis of the herpes simplex virus type 1 region containing the TRL/UL junction. Virology 1993, 196:220-231.
46. Spivack J.G., Fraser N.W. Detection of herpes simplex virus type 1 transcripts during latent infection in mice. J. Virol. 1987, 61:3841-3847.
47. Spivack J.G., Fraser N.W. Expression of herpes simplex virus type 1 (HSV-1) latency-associated transcripts and transcripts affected by the deletion in avirulent mutant HFEM: evidence for a new class of HSV-1 genes. J. Virol. 1988, 62:3281-3287.
48. Steiner I., Spivack J.G., Lirette R.P., Brown S.M., MacLean A.R., Subak-Sharpe J.H., Fraser N.W. Herpes simplex virus type 1 latency-associated transcripts are evidently not essential for latent infection. EMBO J. 1989, 8:505-511.
49. Tang S., Bertke A.S., Patel A., Wang K., Cohen J.I., Krause P.R. An acutely and latently expressed herpes simplex virus 2 viral microRNA inhibits expression of ICP34.5, a viral neurovirulence factor. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:10931-10936.
50. Tang S., Patel A., Krause P.R. Novel less-abundant viral microRNAs encoded by herpes simplex virus 2 latency-associated transcript and their roles in regulating ICP34.5 and ICP0 mRNAs. J. Virol. 2009, 83:1433-1442.
51. Tang S., Bertke A.S., Patel A., Margolis T.P., Krause P.R. Herpes simplex virus 2 microRNA miR-H6 is a novel latency-associated transcript-associated microRNA, but reduction of its expression does not influence the establishment of viral latency or the recurrence phenotype. J. Virol. 2011, 85:4501-4509.
52. Thompson R.L., Sawtell N.M. The herpes simplex virus type 1 latency-associated transcript gene regulates the establishment of latency. J. Virol. 1997, 71:5432-5440.
53. Thompson R.L., Sawtell N.M. Herpes simplex virus type 1 latency-associated transcript gene promotes neuronal survival. J. Virol. 2001, 75:6660-6675.
54. Umbach J.L., Kramer M.F., Jurak I., Karnowski H.W., Coen D.M., Cullen B.R. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008, 454:780-783.
55. Umbach J.L., Nagel M.A., Cohrs R.J., Gilden D.H., Cullen B.R. Analysis of human alphaherpesvirus microRNA expression in latently infected human trigeminal ganglia. J. Virol. 2009, 83:10677-10683.
56. Umbach J.L., Wang K., Tang S., Krause P.R., Mont E.K., Cohen J.I., Cullen B.R. Identification of viral microRNAs expressed in human sacral ganglia latently infected with herpes simplex virus 2. J. Virol. 2010, 84:1189-1192.
57. Wang Q.Y., Zhou C., Johnson K.E., Colgrove R.C., Coen D.M., Knipe D.M. Herpesviral latency-associated transcript gene promotes assembly of heterochromatin on viral lytic-gene promoters in latent infection. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16055-16059.
58. Weinheimer S.P., McKnight S.L. Transcriptional and post-transcriptional controls establish the cascade of herpes simplex virus protein synthesis. J. Mol. Biol. 1987, 195:819-833.
59. Wu Z., Zhu Y., Bisaro D.M., Parris D.S. Herpes simplex virus type 1 suppresses RNA-induced gene silencing in mammalian cells. J. Virol. 2009, 83:6652-6663.
60. Yeh L., Schaffer P.A. A novel class of transcripts expressed with late kinetics in the absence of ICP4 spans the junction between the long and short segments of the herpes simplex virus type 1 genome. J. Virol. 1993, 67:7373-7382.
61. Zhu J., Kang W., Marquart M.E., Hill J.M., Zheng X., Block T.M., Fraser N.W. Identification of a novel 0.7-kb polyadenylated transcript in the LAT promoter region of HSV-1 that is strain specific and may contribute to virulence. Virology 1999, 265:296-307.