Home LiteratureArticle Details
PMID: 18245380 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes.

Assarsson E, Greenbaum JA, Sundström M, Schaffer L, Hammond JA, Pasquetto V, Oseroff C, Hendrickson RC, Lefkowitz EJ, Tscharke DC, Sidney J, Grey HM, Head SR, Peters B, Sette A

Abstract

Vaccinia virus is the prototypic orthopoxvirus and was the vaccine used to eradicate smallpox, yet the expression profiles of many of its genes remain unknown. Using a genome tiling array approach, we simultaneously measured the expression levels of all 223 annotated vaccinia virus genes during infection and determined their kinetics. For 95% of these genes, significant transcript levels were detected. Most remarkably, classification of the genes by their expression profiles revealed 35 genes exhibiting immediate-early expression. Although a similar kinetic class has been described for other virus families, to our knowledge, this is the first demonstration of its existence in orthopoxviruses. Despite expression levels higher than for genes in the other three kinetic classes, the functions of more than half of these remain unknown. Additionally, genes within each kinetic class were spatially grouped together in the genome. This genome-wide picture of transcription alters our understanding of how orthopoxviruses regulate gene expression.

MeSH Terms
Gene Expression Profiling Genes, Immediate-Early Genes, Viral HeLa Cells Humans Kinetics Multigene Family Open Reading Frames Poxviridae/genetics RNA, Messenger/genetics Reverse Transcriptase Polymerase Chain Reaction Transcription, Genetic
Chemicals
RNA, Messenger
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Assarsson Erika
Division of Vaccine Discovery, La Jolla Institute for Allergy and Immunology, La Jolla, CA 92037, USA.
Greenbaum Jason A
Sundström Magnus
Schaffer Lana
Hammond Jennifer A
Pasquetto Valerie
Oseroff Carla
Hendrickson R Curtis
Lefkowitz Elliot J
Tscharke David C
Sidney John
Grey Howard M
Head Steven R
Peters Bjoern
Sette Alessandro
References (44)
44 references, click to expand
  1. Transcriptional and translational analysis of a strongly expressed early region of the vaccinia virus genome.
    J Virol. 1984 Feb;49(2):459-70 PMID: 6319745
  2. Inhibition of CD1d1-mediated antigen presentation by the vaccinia virus B1R and H5R molecules.
    Eur J Immunol. 2006 Oct;36(10):2595-600 PMID: 16981180
  3. Promoter melting by a stage-specific vaccinia virus transcription factor is independent of the presence of RNA polymerase.
    Cell. 1991 Apr 5;65(1):105-13 PMID: 2013091
  4. Feline immunodeficiency virus OrfA alters gene expression of splicing factors and proteasome-ubiquitination proteins.
    Virology. 2008 Feb 20;371(2):394-404 PMID: 17963812
  5. Characterization and temporal regulation of mRNAs encoded by vaccinia virus intermediate-stage genes.
    J Virol. 1993 Jun;67(6):3515-27 PMID: 8098779
  6. Global identification of human transcribed sequences with genome tiling arrays.
    Science. 2004 Dec 24;306(5705):2242-6 PMID: 15539566
  7. Conserved TAAATG sequence at the transcriptional and translational initiation sites of vaccinia virus late genes deduced by structural and functional analysis of the HindIII H genome fragment.
    J Virol. 1986 Nov;60(2):436-49 PMID: 3021979
  8. MESSENGER RNA IN CELLS INFECTED WITH VACCINIA VIRUS.
    Proc Natl Acad Sci U S A. 1964 Apr;51:577-85 PMID: 14166765
  9. Early transcription factor subunits are encoded by vaccinia virus late genes.
    Proc Natl Acad Sci U S A. 1990 Jun;87(11):4401-5 PMID: 2190222
  10. The immune epitope database and analysis resource: from vision to blueprint.
    PLoS Biol. 2005 Mar;3(3):e91 PMID: 15760272
  11. CD8+ T cell cross-priming via transfer of proteasome substrates.
    Science. 2004 May 28;304(5675):1318-21 PMID: 15166379
  12. N-terminal amino acid sequences of vaccinia virus structural proteins.
    Virology. 1994 Aug 1;202(2):844-52 PMID: 8030247
  13. Induction of cytoplasmic ribonucleic acid (RNA) synthesis in vaccinia-infected LM cells during inhibition of protein synthesis.
    Virology. 1966 Jun;29(2):303-9 PMID: 5949673
  14. Global analysis of herpes simplex virus type 1 transcription using an oligonucleotide-based DNA microarray.
    J Virol. 2000 Nov;74(21):9916-27 PMID: 11024119
  15. Arrangement of late RNAs transcribed from a 7.1-kilobase EcoRI vaccinia virus DNA fragment.
    J Virol. 1984 Feb;49(2):510-20 PMID: 6319750
  16. DNA-dependent ATPase activity associated with vaccinia virus early transcription factor.
    J Biol Chem. 1988 Aug 5;263(22):10761-5 PMID: 2839505
  17. A study of the vaccinia virus interferon-gamma receptor and its contribution to virus virulence.
    J Gen Virol. 2002 Aug;83(Pt 8):1953-1964 PMID: 12124459
  18. Vaccinia virus transcription.
    J Gen Virol. 2003 Sep;84(Pt 9):2293-2303 PMID: 12917449
  19. Peculiarities of herpes simplex virus (HSV) transcription: an overview.
    Virus Genes. 2004 Apr;28(3):293-310 PMID: 15266111
  20. Sequence and transcriptional analysis of the vaccinia virus HindIII I fragment.
    J Virol. 1988 Jun;62(6):1889-97 PMID: 2835495
  21. Studies on the mechanisms of vaccinia virus cytopathic effects. II. Early cell rounding is associated with virus polypeptide synthesis.
    J Gen Virol. 1978 Jun;39(3):403-13 PMID: 660161
  22. The vaccinia virus A41L protein is a soluble 30 kDa glycoprotein that affects virus virulence.
    J Gen Virol. 2001 Sep;82(Pt 9):2095-2105 PMID: 11514718
  23. Poxvirus DNA-dependent RNA polymerase.
    Proc Natl Acad Sci U S A. 1967 Jul;58(1):134-41 PMID: 5231593
  24. Vaccinia virus capping enzyme is a transcription initiation factor.
    EMBO J. 1991 Sep;10(9):2553-8 PMID: 1651230
  25. Mapping and insertional mutagenesis of a vaccinia virus gene encoding a 13,800-Da secreted protein.
    Virology. 1989 Aug;171(2):579-87 PMID: 2763467
  26. Organization of RNA transcripts from a vaccinia virus early gene cluster.
    J Virol. 1984 Aug;51(2):283-97 PMID: 6086946
  27. Inhibition of protein synthesis by vaccinia virus. IV. The role of low-molecular-weight viral RNA in the inhibition of protein synthesis.
    Virology. 1981 Jul 15;112(1):13-24 PMID: 7245615
  28. Functional analysis of vaccinia virus B5R protein: essential role in virus envelopment is independent of a large portion of the extracellular domain.
    J Virol. 1998 Jan;72(1):294-302 PMID: 9420227
  29. Expression of mutated glucocerebrosidase alleles in human cells.
    Hum Mol Genet. 1997 Jun;6(6):887-95 PMID: 9175735
  30. Transcriptomal analysis of varicella-zoster virus infection using long oligonucleotide-based microarrays.
    J Gen Virol. 2005 Oct;86(Pt 10):2673-2684 PMID: 16186220
  31. Purification and identification of a vaccinia virus-encoded intermediate stage promoter-specific transcription factor that has homology to eukaryotic transcription factor SII (TFIIS) and an additional role as a viral RNA polymerase subunit.
    J Biol Chem. 1994 May 13;269(19):14260-7 PMID: 8188710
  32. The inhibition of HeLa cell RNA synthesis following infection with vaccinia virus.
    J Gen Virol. 1984 Oct;65 ( Pt 10):1687-97 PMID: 6208316
  33. Vaccinia virus gene encoding a component of the viral early transcription factor.
    J Virol. 1990 Apr;64(4):1523-9 PMID: 2138681
  34. Identification by mass spectroscopy of three major early proteins associated with virosomes in vaccinia virus-infected cells.
    Virus Res. 1999 Jan;59(1):1-12 PMID: 10854161
  35. The Vaccinia virus E8R gene product: a viral membrane protein that is made early in infection and packaged into the virions' core.
    J Virol. 2002 Oct;76(19):9773-86 PMID: 12208956
  36. A cellular factor is required for transcription of vaccinia viral intermediate-stage genes.
    Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3794-8 PMID: 8170989
  37. Regulation of viral transcription elongation and termination during vaccinia virus infection.
    Biochim Biophys Acta. 2002 Sep 13;1577(2):325-36 PMID: 12213661
  38. Expression monitoring by hybridization to high-density oligonucleotide arrays.
    Nat Biotechnol. 1996 Dec;14(13):1675-80 PMID: 9634850
  39. Steroid hormone synthesis by vaccinia virus suppresses the inflammatory response to infection.
    J Exp Med. 2003 May 19;197(10):1269-78 PMID: 12756265
  40. The product of the vaccinia virus L5R gene is a fourth membrane protein encoded by all poxviruses that is required for cell entry and cell-cell fusion.
    J Virol. 2005 Sep;79(17):10988-98 PMID: 16103150
  41. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias.
    Bioinformatics. 2003 Jan 22;19(2):185-93 PMID: 12538238
  42. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling.
    J Biol Chem. 1995 Jul 7;270(27):15974-8 PMID: 7608155
  43. Localization and fine structure of a vaccinia virus gene encoding an envelope antigen.
    J Virol. 1986 Jun;58(3):757-64 PMID: 3701927
  44. Structure and expression of the vaccinia virus gene which prevents virus-induced breakdown of RNA.
    J Virol. 1990 Aug;64(8):3853-63 PMID: 2370683
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2008-02-12
Epub
2008-00-01
Pages
2140-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2542872
Subset
IM
Grants
NIAID NIH HHS · HHSN266200400036C · United States
NIAID NIH HHS · R01 AI056268 · United States
PHS HHS · HHSN266200400124C · United States
NIAID NIH HHS · R0I-AI-56268 · United States
Corrections
ErratumIn
-
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]