Home LiteratureArticle Details
PMID: 11044097 Published · ppublish English Journal Article

High-mobility-group protein I can modulate binding of transcription factors to the U5 region of the human immunodeficiency virus type 1 proviral promoter.

Journal of virology ·Vol. 74 ·No. 22 ·2000-11-00 ·Pages 10523-34

Henderson A, Bunce M, Siddon N, Reeves R, Tremethick DJ

Abstract

HMG I/Y appears to be a multifunctional protein that relies on in its ability to interact with DNA in a structure-specific manner and with DNA, binding transcriptional activators via distinct protein-protein interaction surfaces. To investigate the hypothesis that HMG I/Y may have a role in human immunodeficiency virus type 1 (HIV-1) expression, we have analyzed whether HMG I/Y interacts with the 5' long terminal repeat and whether this interaction can modulate transcription factor binding. Using purified recombinant HMG I, we have identified several high-affinity binding sites which overlap important transcription factor binding sites. One of these HMG I binding sites coincides with an important binding site for AP-1 located downstream of the transcriptional start site, in the 5' untranslated region at the boundary of a positioned nucleosome. HMG I binding to this composite site inhibits the binding of recombinant AP-1. Consistent with this observation, using nuclear extracts prepared from Jurkat T cells, we show that HMG I (but not HMG Y) is strongly induced upon phorbol myristate acetate stimulation and this induced HMG I appears to both selectively inhibit the binding of basal DNA-binding proteins and enhance the binding of an inducible AP-1 transcription factor to this AP-1 binding site. We also report the novel finding that a component present in this inducible AP-1 complex is ATF-3. Taken together, these results argue that HMG I may play a fundamental role in HIV-1 expression by determining the nature of transcription factor-promoter interactions.

MeSH Terms
5' Untranslated Regions/genetics,metabolism Activating Transcription Factor 3 Base Sequence Binding Sites DNA-Binding Proteins/metabolism Gene Expression Regulation, Viral HIV-1/genetics,physiology HMGA1a Protein High Mobility Group Proteins/genetics,metabolism Humans Lymphocyte Activation Molecular Sequence Data Promoter Regions, Genetic Proviruses/genetics Tetradecanoylphorbol Acetate/pharmacology Transcription Factor AP-1/chemistry,genetics,metabolism Transcription Factors/chemistry,genetics,metabolism
Chemicals
5' Untranslated Regions Activating Transcription Factor 3 DNA-Binding Proteins High Mobility Group Proteins Transcription Factor AP-1 Transcription Factors HMGA1a Protein Tetradecanoylphorbol Acetate
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Henderson A
The John Curtin School of Medical Research, the Australian National University, Canberra, Australian Capital Territory 2601, Australia.
Bunce M
Siddon N
Reeves R
Tremethick D J
References (51)
51 references, click to expand
  1. 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
  2. ATF3 and stress responses.
    Gene Expr. 1999;7(4-6):321-35 PMID: 10440233
  3. Complete murine cDNA sequence, genomic structure, and tissue expression of the high mobility group protein HMG-I(Y).
    J Biol Chem. 1988 Dec 5;263(34):18338-42 PMID: 3192537
  4. Existence of different Fos/Jun complexes during the G0-to-G1 transition and during exponential growth in mouse fibroblasts: differential role of Fos proteins.
    Mol Cell Biol. 1992 Nov;12(11):5015-23 PMID: 1406676
  5. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene.
    Cell. 1992 Nov 27;71(5):777-89 PMID: 1330326
  6. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation.
    EMBO J. 1993 Aug;12(8):3249-59 PMID: 8344262
  7. Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements.
    Cell. 1993 Sep 10;74(5):887-98 PMID: 8374955
  8. Short peptide fragments derived from HMG-I/Y proteins bind specifically to the minor groove of DNA.
    Biochemistry. 1994 May 3;33(17):5347-55 PMID: 8172908
  9. Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly.
    J Cell Biol. 1994 Aug;126(3):591-601 PMID: 8045925
  10. Cooperativity between two NF-kappa B complexes, mediated by high-mobility-group protein I(Y), is essential for cytokine-induced expression of the E-selectin promoter.
    Mol Cell Biol. 1994 Sep;14(9):5701-9 PMID: 7520524
  11. The high mobility group protein HMG I(Y) can stimulate or inhibit DNA binding of distinct transcription factor ATF-2 isoforms.
    Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11318-22 PMID: 7972056
  12. Regulation of cell-type-specific interleukin-2 receptor alpha-chain gene expression: potential role of physical interactions between Elf-1, HMG-I(Y), and NF-kappa B family proteins.
    Mol Cell Biol. 1995 Mar;15(3):1786-96 PMID: 7862168
  13. Functional interaction between the POU domain protein Tst-1/Oct-6 and the high-mobility-group protein HMG-I/Y.
    Mol Cell Biol. 1995 Jul;15(7):3738-47 PMID: 7791781
  14. Functional roles of the transcription factor Oct-2A and the high mobility group protein I/Y in HLA-DRA gene expression.
    J Exp Med. 1995 Aug 1;182(2):487-500 PMID: 7629508
  15. Virus induction of human IFN beta gene expression requires the assembly of an enhanceosome.
    Cell. 1995 Dec 29;83(7):1091-100 PMID: 8548797
  16. Reversal of intrinsic DNA bends in the IFN beta gene enhancer by transcription factors and the architectural protein HMG I(Y).
    Cell. 1995 Dec 29;83(7):1101-11 PMID: 8548798
  17. ATF3 gene. Genomic organization, promoter, and regulation.
    J Biol Chem. 1996 Jan 19;271(3):1695-701 PMID: 8576171
  18. Substrate structure influences binding of the non-histone protein HMG-I(Y) to free nucleosomal DNA.
    Biochemistry. 1996 Apr 16;35(15):5063-74 PMID: 8664299
  19. High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function.
    Prog Nucleic Acid Res Mol Biol. 1996;54:35-100 PMID: 8768072
  20. Genomic footprinting of HTLV type I and HIV type 1 in human T cell lines.
    AIDS Res Hum Retroviruses. 1996 Jun 10;12(9):829-32 PMID: 8738435
  21. Involvement of a high-mobility-group protein in the transcriptional activity of herpes simplex virus latency-active promoter 2.
    Mol Cell Biol. 1996 Oct;16(10):5393-9 PMID: 8816451
  22. Activating protein-1 cooperates with phorbol ester activation signals to increase HIV-1 expression.
    AIDS. 1996 Jul;10(8):819-26 PMID: 8828738
  23. In vitro assembly of enhancer complexes.
    Methods Enzymol. 1996;274:162-73 PMID: 8902803
  24. High mobility group protein I(Y) is required for function and for c-Rel binding to CD28 response elements within the GM-CSF and IL-2 promoters.
    Immunity. 1996 Nov;5(5):479-89 PMID: 8934574
  25. High level expression of the HMGI (Y) gene during embryonic development.
    Oncogene. 1996 Dec 5;13(11):2439-46 PMID: 8957086
  26. HMG I(Y) interferes with the DNA binding of NF-AT factors and the induction of the interleukin 4 promoter in T cells.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15311-6 PMID: 8986808
  27. Changes in superhelicity are introduced into closed circular DNA by binding of high mobility group protein I/Y.
    J Biol Chem. 1995 Mar 3;270(9):4355-60 PMID: 7876198
  28. HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro.
    Cell. 1997 Feb 21;88(4):483-92 PMID: 9038339
  29. SWI2/SNF2 and related proteins: ATP-driven motors that disrupt protein-DNA interactions?
    Cell. 1997 Mar 21;88(6):737-40 PMID: 9118215
  30. The binding of a Fos/Jun heterodimer can completely disrupt the structure of a nucleosome.
    EMBO J. 1997 Apr 15;16(8):2072-85 PMID: 9155033
  31. Intra- and intermolecular cooperative binding of high-mobility-group protein I(Y) to the beta-interferon promoter.
    Mol Cell Biol. 1997 Jul;17(7):3649-62 PMID: 9199299
  32. U5 region of the human immunodeficiency virus type 1 long terminal repeat contains TRE-like cAMP-responsive elements that bind both AP-1 and CREB/ATF proteins.
    Virology. 1997 Jun 23;233(1):235-45 PMID: 9201233
  33. Transcription factor binding sites downstream of the human immunodeficiency virus type 1 transcription start site are important for virus infectivity.
    J Virol. 1997 Aug;71(8):6113-27 PMID: 9223506
  34. Competition between HMG-I(Y), HMG-1 and histone H1 on four-way junction DNA.
    Nucleic Acids Res. 1997 Sep 1;25(17):3523-31 PMID: 9254714
  35. TNFalpha cooperates with the protein kinase A pathway to synergistically increase HIV-1 LTR transcription via downstream TRE-like cAMP response elements.
    Virology. 1997 Oct 27;237(2):422-9 PMID: 9356353
  36. High mobility group I proteins interfere with the homeodomains binding to DNA.
    J Biol Chem. 1997 Nov 21;272(47):29904-10 PMID: 9368066
  37. Functional interaction between the DNA binding subunit trimerization domain of NF-Y and the high mobility group protein HMG-I(Y).
    J Biol Chem. 1997 Dec 5;272(49):30880-8 PMID: 9388234
  38. Enhancement of serum-response factor-dependent transcription and DNA binding by the architectural transcription factor HMG-I(Y).
    J Biol Chem. 1998 Apr 17;273(16):9755-60 PMID: 9545312
  39. Tumor promoter induces high mobility group HMG-Y protein expression in transformation-sensitive but not -resistant cells.
    Oncogene. 1998 Jul 2;16(26):3387-96 PMID: 9692546
  40. Nucleosomes and regulation of gene expression. Structure of the HIV-1 5'LTR.
    Acta Biochim Pol. 1998;45(1):209-19 PMID: 9701513
  41. Roles of histone acetyltransferases and deacetylases in gene regulation.
    Bioessays. 1998 Aug;20(8):615-26 PMID: 9780836
  42. Acetylation of HMG I(Y) by CBP turns off IFN beta expression by disrupting the enhanceosome.
    Mol Cell. 1998 Oct;2(4):457-67 PMID: 9809067
  43. Human immunodeficiency virus type-1 transcription: role of the 5'-untranslated leader region (review).
    Int J Mol Med. 1998 May;1(5):875-81 PMID: 9852310
  44. Chromatin disruption and modification.
    Nucleic Acids Res. 1999 Feb 1;27(3):711-20 PMID: 9889264
  45. HMG protein family members stimulate human immunodeficiency virus type 1 and avian sarcoma virus concerted DNA integration in vitro.
    J Virol. 1999 Apr;73(4):2994-3003 PMID: 10074149
  46. High mobility group-I(Y) protein facilitates nuclear factor-kappaB binding and transactivation of the inducible nitric-oxide synthase promoter/enhancer.
    J Biol Chem. 1999 Mar 26;274(13):9045-52 PMID: 10085153
  47. The HMG-I(Y) A.T-hook peptide motif confers DNA-binding specificity to a structured chimeric protein.
    J Biol Chem. 1999 Jun 4;274(23):16536-44 PMID: 10347218
  48. The role of HMG I(Y) in the assembly and function of the IFN-beta enhanceosome.
    EMBO J. 1999 Jun 1;18(11):3074-89 PMID: 10357819
  49. Purification and assays for high mobility group HMG-I(Y) protein function.
    Methods Enzymol. 1999;304:155-88 PMID: 10372360
  50. A small region in HMG I(Y) is critical for cooperation with NF-kappaB on DNA.
    J Biol Chem. 1999 Jul 16;274(29):20235-43 PMID: 10400641
  51. Elevated levels of a specific class of nuclear phosphoproteins in cells transformed with v-ras and v-mos oncogenes and by cotransfection with c-myc and polyoma middle T genes.
    EMBO J. 1987 Jul;6(7):1981-7 PMID: 2820715
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2000-11-00
Pages
10523-34
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC110927
Subset
IM
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