The High Mobility Group protein HMG I(Y) is required for NF-κB-dependent virus induction of the human IFN-β gene

Abstract In this paper, we show that both NF-κB and the high mobility group protein I(Y) (HMG I(Y)) are required for virus induction of the human interferon-β (IFN-β) gene. NF-κB binds to the terminal regions of a 10 by regulatory sequence through contacts in the major groove, while HMG I(Y) recognizes the central region of the same sequence through contacts in the minor groove. Mutations that interfere with binding of either protein decrease the level of virus induction, and activation of the gene can be blocked by either NF-κB or HMG I(Y) antisense RNA. HMG I(Y) stimulates the binding of NF-κB to the IFN-β promoter, and it may also function as a promoter-specific accessory factor for NF-κB transcriptional activity.

[1]  R. Reeves,et al.  Complete murine cDNA sequence, genomic structure, and tissue expression of the high mobility group protein HMG-I(Y). , 1988, The Journal of biological chemistry.

[2]  M. Horikoshi,et al.  Interaction of TFIID in the minor groove of the TATA element , 1991, Cell.

[3]  M. Solomon,et al.  A mammalian high mobility group protein recognizes any stretch of six A.T base pairs in duplex DNA. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Gary J. Nabel,et al.  Cloning of an NF-κB subunit which stimulates HIV transcription in synergy with p65 , 1991, Nature.

[5]  M. Birnstiel,et al.  Cloning of cDNAs coding for human HMG I and HMG Y proteins: both are capable of binding to the octamer sequence motif. , 1989, Nucleic acids research.

[6]  D. Baltimore,et al.  Immunoglobulin gene transcription is activated by downstream sequence elements , 1983, Cell.

[7]  C. Scheidereit,et al.  Cloning of the DNA-binding subunit of human nuclear factor kappa B: the level of its mRNA is strongly regulated by phorbol ester or tumor necrosis factor alpha. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  W. Greene,et al.  Kappa B-specific DNA binding proteins are differentially inhibited by enhancer mutations and biological oxidation. , 1991, The New biologist.

[9]  C. Caskey,et al.  Construction of plasmids that express E. coli beta-galactosidase in mammalian cells. , 1989, Nucleic acids research.

[10]  S. McKnight,et al.  In situ detection of sequence-specific DNA binding activity specified by a recombinant bacteriophage. , 1988, Genes & development.

[11]  T. Maniatis,et al.  Two different virus‐inducible elements are required for human beta‐interferon gene regulation. , 1989, The EMBO journal.

[12]  H. Yang-Yen,et al.  Purification and characterization of a high-mobility-group-like DNA-binding protein that stimulates rRNA synthesis in vitro , 1988, Molecular and cellular biology.

[13]  R. Roeder,et al.  Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. , 1983, Nucleic acids research.

[14]  A. Varshavsky,et al.  A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome , 1984, Cell.

[15]  T. Taniguchi,et al.  Critical role of a common transcription factor, IRF‐1, in the regulation of IFN‐beta and IFN‐inducible genes. , 1992, The EMBO journal.

[16]  A. Israël,et al.  The DNA binding subunit of NF-κB is identical to factor KBF1 and homologous to the rel oncogene product , 1990, Cell.

[17]  D. Baltimore,et al.  The involvement of NF-κB in β-interferon gene regulation reveals its role as widely inducible mediator of signal transduction , 1989, Cell.

[18]  G. Nabel,et al.  Distinct combinations of NF-kappa B subunits determine the specificity of transcriptional activation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. Grueneberg,et al.  Human and Drosophila Homeodomain Proteins That Enhance the DNA-Binding Activity of Serum Response Factor , 1992, Science.

[20]  P. Baeuerle The inducible transcription activator NF-κB: regulation by distinct protein subunits , 1991 .

[21]  B. Howard,et al.  Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells , 1982, Molecular and cellular biology.

[22]  S. Henikoff Unidirectional digestion with exonuclease III in DNA sequence analysis. , 1987, Methods in enzymology.

[23]  E. Demaeyer,et al.  Interferons and other regulatory cytokines , 1988 .

[24]  M. Nissen,et al.  The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. , 1990, The Journal of biological chemistry.

[25]  U Zabel,et al.  DNA binding of purified transcription factor NF-kappa B. Affinity, specificity, Zn2+ dependence, and differential half-site recognition. , 1991, The Journal of biological chemistry.

[26]  K. Arai,et al.  Comparison of constitutive and inducible transcriptional enhancement mediated by kappa B-related sequences: modulation of activity in B cells by human T-cell leukemia virus type I tax gene. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Vincent Bours,et al.  Cloning of a mitogen-inducible gene encoding a κB DNA-binding protein with homology to the rel oncogene and to cell-cycle motifs , 1990, Nature.

[28]  D. Friedman,et al.  Integration host factor: A protein for all reasons , 1988, Cell.

[29]  Rudolf Grosschedl,et al.  The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures , 1992, Cell.

[30]  T. Maniatis,et al.  Identification and characterization of a novel repressor of beta-interferon gene expression. , 1991, Genes & development.

[31]  D. Lilley HMG has DNA wrapped up , 1992, Nature.

[32]  G. Nolan,et al.  Independent modes of transcriptional activation by the p50 and p65 subunits of NF-kappa B. , 1992, Genes & development.

[33]  R. Reeves,et al.  A conformational study of the sequence specific binding of HMG-I (Y) with the bovine interleukin-2 cDNA. , 1988, Biochemistry international.

[34]  D. Landsman,et al.  Structural features of the HMG chromosomal proteins and their genes. , 1990, Biochimica et biophysica acta.

[35]  P. Baeuerle,et al.  The p65 subunit is responsible for the strong transcription activating potential of NF‐kappa B. , 1991, The EMBO journal.

[36]  R. Reeves,et al.  A poly(dA-dT) upstream activating sequence binds high-mobility group I protein and contributes to lymphotoxin (tumor necrosis factor-beta) gene regulation , 1992, Molecular and cellular biology.

[37]  R. Reeves,et al.  Alternative processing of mRNAs encoding mammalian chromosomal high-mobility-group proteins HMG-I and HMG-Y , 1989, Molecular and cellular biology.

[38]  T. Maniatis,et al.  Human β-interferon gene expression is regulated by an inducible enhancer element , 1985, Cell.

[39]  E. Winnacker,et al.  The NF-ϰB transcription factor induces DNA bending which is modulated by its 65-kD subunit , 1990 .

[40]  L Cohen,et al.  Synergism between distinct enhanson domains in viral induction of the human beta interferon gene , 1990, Molecular and cellular biology.

[41]  F. Studier,et al.  Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. , 1986, Journal of molecular biology.

[42]  Takashi Miyata,et al.  Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes , 1989, Cell.

[43]  T. Taniguchi,et al.  Involvement of a cis-element that binds an H2TF-1/NF kappa B like factor(s) in the virus-induced interferon-beta gene expression. , 1989, Nucleic acids research.

[44]  P. Baeuerle,et al.  NF‐kappa B contacts DNA by a heterodimer of the p50 and p65 subunit. , 1991, The EMBO journal.

[45]  V. Bours,et al.  A novel mitogen-inducible gene product related to p50/p105-NF-kappa B participates in transactivation through a kappa B site , 1992, Molecular and cellular biology.

[46]  S. Goodbourn,et al.  Double‐stranded RNA activates binding of NF‐kappa B to an inducible element in the human beta‐interferon promoter. , 1989, The EMBO journal.

[47]  S. Ruben,et al.  Isolation of a rel-related human cDNA that potentially encodes the 65-kD subunit of NF-kappa B. , 1991, Science.

[48]  H. Okayama,et al.  Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. , 1988, BioTechniques.

[49]  J. Wienberg,et al.  Cis-acting sequences from mouse rDNA promote plasmid DNA amplification and persistence in mouse cells: implication of HMG-I in their function. , 1989, Nucleic acids research.

[50]  D. Smith,et al.  Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. , 1988, Gene.

[51]  I. Tanaka,et al.  A protein structural motif that bends DNA , 1989, Proteins.

[52]  H. Nash,et al.  Bending and supercoiling of DNA at the attachment site of bacteriophage lambda. , 1990, Trends in biochemical sciences.

[53]  D. K. Hawley,et al.  TFIID binds in the minor groove of the TATA box , 1991, Cell.

[54]  J. LeBlanc,et al.  Induction of human interferon gene expression is associated with a nuclear factor that interacts with the NF-kappa B site of the human immunodeficiency virus enhancer , 1989, Journal of virology.

[55]  T. Taniguchi,et al.  Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-β gene regulatory elements , 1988, Cell.

[56]  T. Taniguchi,et al.  Interferon-β gene regulation: Tandemly repeated sequences of a synthetic 6 bp oligomer function as a virus-inducible enhancer , 1987, Cell.

[57]  M. Grilli,et al.  NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. , 1993, International review of cytology.

[58]  T. Maniatis,et al.  Generation of p50 subunit of NF-kB by processing of p105 through an ATP-dependent pathway , 1991, Nature.