Home LiteratureArticle Details
PMID: 8057441 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Site-specific binding of the human cytomegalovirus IE2 86-kilodalton protein to an early gene promoter.

Journal of virology ·Vol. 68 ·No. 9 ·1994-09-00 ·Pages 5613-22

Schwartz R, Sommer MH, Scully A, Spector DH

Abstract

We have previously demonstrated that the human cytomegalovirus (HCMV) immediate-early region 2 86-kDa protein (the IE2 86 protein) is the major transactivator of the HCMV early promoter for the 2.2-kb class of RNAs (open reading frame UL 112-113). Here we show that specific stimulation of this promoter by IE2 86 in transient-expression assays requires sequences located between nucleotides (nt) -113 and -58 relative to the transcription start site; this is also the major regulatory region for this promoter during HCMV infection. To determine whether IE2 86 can bind to this promoter, a glutathione-S-transferase (GST)-IE2 86 fusion protein was incubated with the 32P-labeled promoter and specific binding was assessed by retention of the protein-DNA complex on glutathione-agarose beads. DNase I footprint analysis was also used to map the sequences involved in the binding. Our results indicate that three regions, located between nt -286 and -257, nt -248 and -218, and nt -148 and -120, bind strongly to the IE2 86 protein and share sequence similarity with the previously identified cis repression signal located near the cap site of the major HCMV IE gene. In addition, there is a weaker binding region between nt -113 and -85, which shares some sequence homology with the cis repression signal element and the strong binding regions of the 2.2-kb RNA promoter but lacks one of the two CG dinucleotides present in all of the high-affinity binding sites. With a set of IE2 86 protein deletion mutants, we also show that the DNA-binding domain spans a large region in the carboxy-terminal half of the protein.

MeSH Terms
Base Sequence Binding Sites Cell Line Consensus Sequence Cytomegalovirus/genetics DNA-Binding Proteins/metabolism Gene Expression Regulation, Viral Humans Immediate-Early Proteins/metabolism In Vitro Techniques Membrane Glycoproteins Molecular Sequence Data Oligodeoxyribonucleotides/metabolism Promoter Regions, Genetic Protein Binding RNA, Messenger/genetics Sequence Deletion Structure-Activity Relationship Trans-Activators Transcriptional Activation Viral Envelope Proteins Viral Proteins
Chemicals
DNA-Binding Proteins IE2 protein, Cytomegalovirus Immediate-Early Proteins Membrane Glycoproteins Oligodeoxyribonucleotides RNA, Messenger Trans-Activators UL115 protein, Human herpesvirus 5 Viral Envelope Proteins Viral Proteins glycoprotein H, Cytomegalovirus glycoprotein H, Human cytomegalovirus glycoprotein O, cytomegalovirus
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Schwartz R
Department of Biology, University of California, San Diego, La Jolla 92093-0116.
Sommer M H
Scully A
Spector D H
References (60)
60 references, click to expand
  1. Promoter-specific trans activation and repression by human cytomegalovirus immediate-early proteins involves common and unique protein domains.
    J Virol. 1990 Apr;64(4):1556-65 PMID: 2157043
  2. The human cytomegalovirus 80-kilodalton but not the 72-kilodalton immediate-early protein transactivates heterologous promoters in a TATA box-dependent mechanism and interacts directly with TFIID.
    J Virol. 1992 Jul;66(7):4452-6 PMID: 1318414
  3. Cytomegalovirus activates transcription directed by the long terminal repeat of human immunodeficiency virus type 1.
    J Virol. 1990 Jun;64(6):2932-40 PMID: 2159554
  4. Human cytomegalovirus immediate-early two protein region involved in negative regulation of the major immediate-early promoter.
    J Virol. 1990 Jul;64(7):3532-6 PMID: 2161955
  5. The IE2 gene products of human cytomegalovirus specifically down-regulate expression from the major immediate-early promoter through a target sequence located near the cap site.
    J Virol. 1990 Dec;64(12):6154-65 PMID: 2173785
  6. Human cytomegalovirus ie2 negatively regulates alpha gene expression via a short target sequence near the transcription start site.
    J Virol. 1991 Feb;65(2):887-96 PMID: 1846203
  7. A cis-acting element in the major immediate-early (IE) promoter of human cytomegalovirus is required for negative regulation by IE2.
    J Virol. 1991 Feb;65(2):897-903 PMID: 1846204
  8. The functionally active IE2 immediate-early regulatory protein of human cytomegalovirus is an 80-kilodalton polypeptide that contains two distinct activator domains and a duplicated nuclear localization signal.
    J Virol. 1991 Jul;65(7):3839-52 PMID: 1645794
  9. Sequence requirements for activation of the HIV-1 LTR by human cytomegalovirus.
    Virology. 1991 Jul;183(1):381-5 PMID: 1647074
  10. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  11. Sequence of protein synthesis in cells infected by human cytomegalovirus: early and late virus-induced polypeptides.
    J Virol. 1978 Jun;26(3):686-701 PMID: 209215
  12. Diseases produced by cytomegaloviruses.
    Med Clin North Am. 1978 Sep;62(5):1021-35 PMID: 215855
  13. Sequencing end-labeled DNA with base-specific chemical cleavages.
    Methods Enzymol. 1980;65(1):499-560 PMID: 6246368
  14. Temporal regulation of human cytomegalovirus transcription at immediate early and early times after infection.
    J Virol. 1981 May;38(2):446-59 PMID: 6165834
  15. Human cytomegalovirus DNA: restriction enzyme cleavage maps and map locations for immediate-early, early, and late RNAs.
    Virology. 1981 Oct 15;114(1):23-38 PMID: 6269285
  16. Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection.
    J Virol. 1982 Feb;41(2):462-77 PMID: 6281461
  17. Construction of a cloned library of the EcoRI fragments from the human cytomegalovirus genome (strain AD169).
    J Virol. 1982 May;42(2):547-57 PMID: 6283172
  18. Organization and expression of the immediate early genes of human cytomegalovirus.
    J Virol. 1983 Apr;46(1):1-14 PMID: 6298447
  19. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  20. Transcription in human fibroblasts permissively infected by human cytomegalovirus strain AD169.
    Virology. 1983 Feb;125(1):31-46 PMID: 6187127
  21. Structural analysis of the major immediate early gene of human cytomegalovirus.
    J Virol. 1984 Jan;49(1):190-9 PMID: 6317889
  22. Predominant immediate-early transcripts of human cytomegalovirus AD 169.
    J Virol. 1984 Feb;49(2):363-70 PMID: 6319737
  23. Evidence for a direct role for both the 175,000- and 110,000-molecular-weight immediate-early proteins of herpes simplex virus in the transactivation of delayed-early promoters.
    J Virol. 1985 Mar;53(3):751-60 PMID: 2983086
  24. Transcription of the immediate early genes of human cytomegalovirus strain AD169.
    Virus Res. 1984;1(2):101-6 PMID: 6085199
  25. Identification of immediate early genes from herpes simplex virus that transactivate the virus thymidine kinase gene.
    Proc Natl Acad Sci U S A. 1985 Aug;82(16):5265-9 PMID: 2991915
  26. Multiple spliced and unspliced transcripts from human cytomegalovirus immediate-early region 2 and evidence for a common initiation site within immediate-early region 1.
    J Virol. 1985 Dec;56(3):665-75 PMID: 2999423
  27. Three trans-acting regulatory proteins of herpes simplex virus modulate immediate-early gene expression in a pathway involving positive and negative feedback regulation.
    J Virol. 1985 Dec;56(3):723-33 PMID: 2999428
  28. 2.2-kilobase class of early transcripts encoded by cell-related sequences in human cytomegalovirus strain AD169.
    J Virol. 1986 Feb;57(2):591-602 PMID: 3003391
  29. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4.
    Mol Cell Biol. 1985 Aug;5(8):1997-2008 PMID: 3018543
  30. Association of the herpes simplex virus regulatory protein ICP4 with specific nucleotide sequences in DNA.
    Nucleic Acids Res. 1986 Aug 11;14(15):6067-83 PMID: 3018669
  31. Identification and characterization of the human cytomegalovirus immediate-early region 2 gene that stimulates gene expression from an inducible promoter.
    J Virol. 1987 Oct;61(10):3214-21 PMID: 3041043
  32. Four phosphoproteins with common amino termini are encoded by human cytomegalovirus AD169.
    J Virol. 1988 Jan;62(1):331-40 PMID: 2824853
  33. Immediate-early gene region of human cytomegalovirus trans-activates the promoter of human immunodeficiency virus.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8642-6 PMID: 2825201
  34. Participation of two human cytomegalovirus immediate early gene regions in transcriptional activation of adenovirus promoters.
    Virology. 1987 Dec;161(2):276-85 PMID: 2825403
  35. trans-activation and autoregulation of gene expression by the immediate-early region 2 gene products of human cytomegalovirus.
    J Virol. 1988 Apr;62(4):1167-79 PMID: 2831379
  36. A high-efficiency HeLa cell nuclear transcription extract.
    DNA. 1988 Jan-Feb;7(1):47-55 PMID: 3349904
  37. Identification of sequence requirements and trans-acting functions necessary for regulated expression of a human cytomegalovirus early gene.
    J Virol. 1988 Sep;62(9):3463-73 PMID: 2841497
  38. Direct correlation between a negative autoregulatory response element at the cap site of the herpes simplex virus type 1 IE175 (alpha 4) promoter and a specific binding site for the IE175 (ICP4) protein.
    J Virol. 1988 Nov;62(11):4307-20 PMID: 2845144
  39. A human cytomegalovirus early gene has three inducible promoters that are regulated differentially at various times after infection.
    J Virol. 1989 Jan;63(1):281-90 PMID: 2535734
  40. Regulated expression of the human cytomegalovirus pp65 gene: octamer sequence in the promoter is required for activation by viral gene products.
    J Virol. 1989 Mar;63(3):1232-8 PMID: 2536831
  41. Posttranscriptional regulation of a class of human cytomegalovirus phosphoproteins encoded by an early transcription unit.
    J Virol. 1989 Jul;63(7):3117-27 PMID: 2542619
  42. Separation of primary structural components conferring autoregulation, transactivation, and DNA-binding properties to the herpes simplex virus transcriptional regulatory protein ICP4.
    J Virol. 1989 Sep;63(9):3714-28 PMID: 2760981
  43. Sequences in the human cytomegalovirus 2.7-kilobase RNA promoter which mediate its regulation as an early gene.
    J Virol. 1989 Dec;63(12):5334-43 PMID: 2555558
  44. Binding of the herpes simplex virus major regulatory protein to viral DNA.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9808-12 PMID: 2557630
  45. Characterization of DNA-protein complex formation in nuclear extracts with a sequence from the herpes simplex virus thymidine kinase gene.
    J Biol Chem. 1990 Jan 25;265(3):1648-57 PMID: 2153138
  46. Transactivation of a human cytomegalovirus early promoter by gene products from the immediate-early gene IE2 and augmentation by IE1: mutational analysis of the viral proteins.
    J Virol. 1990 Apr;64(4):1498-506 PMID: 2157038
  47. The 86-kilodalton IE-2 protein of human cytomegalovirus is a sequence-specific DNA-binding protein that interacts directly with the negative autoregulatory response element located near the cap site of the IE-1/2 enhancer-promoter.
    J Virol. 1993 Jan;67(1):323-31 PMID: 8380080
  48. An in vitro system for human cytomegalovirus immediate early 2 protein (IE2)-mediated site-dependent repression of transcription and direct binding of IE2 to the major immediate early promoter.
    Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):707-11 PMID: 8380646
  49. In vivo and in vitro analysis of transcriptional activation mediated by the human cytomegalovirus major immediate-early proteins.
    Mol Cell Biol. 1993 Feb;13(2):1238-50 PMID: 8423789
  50. Human cytomegalovirus immediate-early gene 2 protein interacts with itself and with several novel cellular proteins.
    J Virol. 1993 Aug;67(8):4981-91 PMID: 8392623
  51. Direct interaction of the human cytomegalovirus IE86 protein with the cis repression signal does not preclude TBP from binding to the TATA box.
    J Virol. 1993 Sep;67(9):5595-604 PMID: 8394462
  52. Identification and mapping of dimerization and DNA-binding domains in the C terminus of the IE2 regulatory protein of human cytomegalovirus.
    J Virol. 1993 Oct;67(10):6201-14 PMID: 8396676
  53. Human cytomegalovirus IE86 protein interacts with promoter-bound TATA-binding protein via a specific region distinct from the autorepression domain.
    J Virol. 1993 Dec;67(12):7539-46 PMID: 8230473
  54. Site-specific inhibition of RNA polymerase II preinitiation complex assembly by human cytomegalovirus IE86 protein.
    J Virol. 1993 Dec;67(12):7547-55 PMID: 8230474
  55. Modulation of T-cell activation through protein kinase C- or A-dependent signalling pathways synergistically increases human immunodeficiency virus long terminal repeat induction by cytomegalovirus immediate-early proteins.
    J Virol. 1991 Oct;65(10):5477-84 PMID: 1654449
  56. A discrete cis element in the human immunodeficiency virus long terminal repeat mediates synergistic trans activation by cytomegalovirus immediate-early proteins.
    J Virol. 1991 Dec;65(12):6735-42 PMID: 1682509
  57. Human cytomegalovirus US3 and UL36-38 immediate-early proteins regulate gene expression.
    J Virol. 1992 Jan;66(1):95-105 PMID: 1370097
  58. A 10-base-pair element of the human immunodeficiency virus type 1 long terminal repeat (LTR) is an absolute requirement for transactivation by the human cytomegalovirus 72-kilodalton IE1 protein but can be compensated for by other LTR regions in transactivation by the 80-kilodalton IE2 protein.
    J Virol. 1992 Mar;66(3):1543-50 PMID: 1310765
  59. An AP-1 binding site is the predominant cis-acting regulatory element in the 1.2-kilobase early RNA promoter of human cytomegalovirus.
    J Virol. 1992 Apr;66(4):2407-17 PMID: 1312636
  60. Characterization of multiple molecular interactions between human cytomegalovirus (HCMV) and human immunodeficiency virus type 1 (HIV-1).
    Virology. 1990 May;176(1):87-97 PMID: 2158700
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1994-09-00
Pages
5613-22
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC236962
Subset
IM
Grants
NCI NIH HHS · CA 34729 · United States
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: product@genelibs.com