CCAAT-Binding Factor NF-Y and RFX Are Required for In Vivo Assembly of a Nucleoprotein Complex That Spans 250 Base Pairs: the Invariant Chain Promoter as a Model

REFERENCES

• Arents, G., R. W. Burlingame, B.-C. Wang, W. E. Love, and E. N. Moudrianakis. 1991. The nucleosomal core histone octamer at 3.1 Å resolution: a tripartite protein assembly and a left-handed superhelix. Proc. Natl. Acad. Sci. USA 88:10148–10152.
   PubMed Web of Science ®Google Scholar
• Arents, G., and E. N. Moudrianakis. 1995. The histone fold: a ubiquitous architectural motif utilized in DNA compaction and protein dimerization. Proc. Natl. Acad. Sci. USA 92:11170–11174.
   PubMed Web of Science ®Google Scholar
• Barr, C. L., and G. F. Saunders. 1991. Interferon-g-inducible regulation of the human invariant chain gene. J. Biol. Chem. 266:3475–3481.
   PubMed Web of Science ®Google Scholar
• Baxevanis, A. D., G. Arents, E. N. Moudrianakis, and D. Landsman. 1995. A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res. 23:2685–2691.
   PubMed Web of Science ®Google Scholar
• Benoist, C., and D. Mathis. 1990. Regulation of major histocompatibility complex class-II genes: X, Y, and other letters of the alphabet. Annu. Rev. Immunol. 8:681–715.
   PubMed Web of Science ®Google Scholar
• Brickey, J. Unpublished data.
   Google Scholar
• Brown, A. M., C. L. Barr, and J. P.-Y. Ting. 1991. Sequences homologous to class II MHC W, X, and Y elements mediate constitutive and IFN-g-induced expression of human class II-associated invariant chain gene. J. Immunol. 146:3183–3189.
   PubMed Web of Science ®Google Scholar
• Brown, A. M., M. W. Linhoff, B. Stein, K. L. Wright, A. S. Baldwin, P. V. Basta, and J. P.-Y. Ting. 1994. Function of NF-kB/Rel binding sites in the major histocompatibility complex class II invariant chain promoter is dependent on cell-specific binding of different NF-kB/Rel subunits. Mol. Cell. Biol. 14:2926–2935.
   PubMedGoogle Scholar
• Brown, A. M., K. L. Wright, and J. P.-Y. Ting. 1993. Human major histocompatibility complex class II-associated invariant chain gene promoter: functional analysis and in vivo protein/DNA interactions of constitutive and IFN-g-induced expression. J. Biol. Chem. 268:26328–26333.
   PubMedGoogle Scholar
• Bucher, P. 1990. Weight matrix description of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 212:563–578.
   PubMed Web of Science ®Google Scholar
• Cassinotti, P., and M. Weitz. 1994. Increasing the sensitivity of a common CAT assay. BioTechniques 17:36–40.
   PubMedGoogle Scholar
• Chang, C.-H., and R. A. Flavell. 1995. Class II transactivator regulates the expression of multiple genes involved in antigen presentation. J. Exp. Med. 181:765–767.
   PubMed Web of Science ®Google Scholar
• Chin, K.-C., C. Mao, C. Skinner, J. L. Riley, K. L. Wright, C. S. Moreno, G. R. Stark, J. M. Boss, and J. P.-Y. Ting. 1994. Molecular analysis of G1B and G3A IFNG mutants reveals that defects in CIITA or RFX result in defective class II MHC and Ii gene induction. Immunity 1:687–697.
   PubMedGoogle Scholar
• Chodosh, L. A., A. S. Baldwin, R. W. Carthew, and P. A. Sharp. 1988. Human CCAAT-binding proteins have heterologous subunits. Cell 53:11–24.
   PubMed Web of Science ®Google Scholar
• Chodosh, L. A., J. Olesen, S. Hahn, A. S. Baldwin, L. Guarente, and P. A. Sharp. 1988. A yeast and a human CCAAT-binding protein have heterologous subunits that are functionally interchangeable. Cell 53:25–35.
   PubMedGoogle Scholar
• de Préval, C., M. R. Hadam, and B. Mach. 1988. Regulation of genes for HLA class II antigens in cell lines from patients with severe combined immunodeficiency. N. Engl. J. Med. 318:1295–1300.
   PubMedGoogle Scholar
• Dorn, A., J. Bollekens, A. Staub, C. Benoist, and D. Mathis. 1987. A multiplicity of CCAAT box-binding proteins. Cell 50:863–872.
   PubMed Web of Science ®Google Scholar
• Doyle, C., P. J. Ford, P. D. Ponath, T. Spies, and J. L. Strominger. 1990. Regulation of the class II-associated invariant chain gene in normal and mutant B lymphocytes. Proc. Natl. Acad. Sci. USA 87:4590–4594.
   PubMedGoogle Scholar
• Du, W., D. Thanos, and T. Maniatis. 1993. Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell 74:887–898.
   PubMed Web of Science ®Google Scholar
• Durand, B., M. Kobr, W. Reith, and B. Mach. 1994. Functional complementation of major histocompatibility complex class II regulatory mutants by the purified X-box-binding protein RFX. Mol. Cell. Biol. 14:6839–6847.
   PubMedGoogle Scholar
• Durand, B., P. Sperisen, P. Emery, E. Barras, M. Zufferey, B. Mach, and W. Reith. 1997. RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency. EMBO J. 16:1045–1055.
   PubMedGoogle Scholar
• Echols, H. 1986. Multiple DNA-protein interactions governing high-precision DNA transactions. Science 233:1050–1056.
   PubMed Web of Science ®Google Scholar
• Eickbush, T. H., and E. N. Moudrianakis. 1978. The histone core complex: an octamer assembled by two sets of protein-protein interactions. Biochemistry 17:4955–4964.
   PubMed Web of Science ®Google Scholar
• Falvo, J. V., D. Thanos, and T. Maniatis. 1995. Reversal of intrinsic DNA bends in the IFNb gene enhancer by transcription factors and the architectural protein HMG I(Y). Cell 83:1101–1111.
   PubMed Web of Science ®Google Scholar
• Giese, K., J. Cox, and R. Grosschedl. 1992. The HMG domain of lymphoid enhancer factor-1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69:185–195.
   PubMed Web of Science ®Google Scholar
• Giese, K., C. Kingsley, J. R. Kirshner, and R. Grosschedl. 1995. Assembly and function of a TCRa enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. Genes Dev. 9:995–1008.
   PubMed Web of Science ®Google Scholar
• Glimcher, L. H., and C. J. Kara. 1992. Sequences and factors: a guide to MHC class-II transcription. Annu. Rev. Immunol. 10:13–49.
   PubMed Web of Science ®Google Scholar
• Grosschedl, R. 1995. Higher-order nucleoprotein complexes in transcription: analogies with site-specific recombination. Curr. Opin. Cell Biol. 7:362–370.
   PubMedGoogle Scholar
• Hayes, J. J., D. J. Clark, and A. P. Wolffe. 1991. Histone contributions to the structure of DNA in the nucleosome. Proc. Natl. Acad. Sci. USA 88:6829–6833.
   PubMed Web of Science ®Google Scholar
• Hume, C. R., L. A. Shookster, N. Collins, R. O’Reilly, and J. S. Lee. 1989. Bare lymphocyte syndrome: altered HLA class II expression in B cell lines derived from two patients. Hum. Immunol. 25:1–11.
   PubMedGoogle Scholar
• Kara, C. J., and L. H. Glimcher. 1991. In vivo footprinting of MHC class II genes: bare promoters in the bare lymphocyte syndrome. Science 252:709–712.
   PubMedGoogle Scholar
• Kara, C. J., and L. H. Glimcher. 1993. Promoter accessibility within the environment of the MHC is affected in class II-deficient combined immu-nodeficiency. EMBO J. 12:187–193.
   PubMedGoogle Scholar
• Kara, C. J., and L. H. Glimcher. 1993. Three in vivo promoter phenotypes in MHC class II deficient combined immunodeficiency. Immunogenetics 37:227–230.
   PubMedGoogle Scholar
• Landsberger, N., and A. P. Wolffe. 1995. Role of chromatin and Xenopus laevis heat shock transcription factor in regulation of transcription from the X. laevis hsp70 promoter in vivo. Mol. Cell. Biol. 15:6013–6024.
   PubMedGoogle Scholar
• Love, J. J., X. Li, D. A. Case, K. Giese, R. Grosschedl, and P. E. Wright. 1995. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 376:791–795.
   PubMed Web of Science ®Google Scholar
• Mach, B., V. Steimle, E. Martinez-Soria, and W. Reith. 1996. Regulation of MHC class II genes: lessons from a disease. Annu. Rev. Immunol. 14:301–331.
   PubMed Web of Science ®Google Scholar
• Maity, S. N., P. T. Golumbek, G. Karsenty, and B. de Crombrugghe. 1988. Selective activation of transcription by a novel CCAAT binding factor. Science 241:582–585.
   PubMedGoogle Scholar
• Maity, S. N., S. Sinha, E. C. Ruteshouser, and B. de Crombrugghe. 1992. Three different polypeptides are necessary for DNA binding of the mammalian heteromeric CCAAT binding factor. J. Biol. Chem. 267:16574–16580.
   PubMedGoogle Scholar
• Mao, C., D. Davies, I. M. Kerr, and G. R. Stark. 1993. Mutant human cells defective in induction of major histocompatibility complex class II genes by interferon g. Proc. Natl. Acad. Sci. USA 90:2880–2884.
   PubMedGoogle Scholar
• Moreno, C. S., P. Emery, J. E. West, B. Durand, W. Reith, B. Mach, and J. M. Boss. 1995. Purified X2 binding protein (X2BP) cooperatively binds the class II MHC X box region in the presence of purified RFX, the X box factor deficient in the bare lymphocyte syndrome. J. Immunol. 155:4313–4321.
   PubMedGoogle Scholar
• Mueller, P. R., and B. Wold. 1989. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science 246:780–786.
   PubMed Web of Science ®Google Scholar
• Neumann, J. R., C. A. Morency, and K. O. Russian. 1987. A novel rapid assay for chloramphenicol acetyltransferase gene expression. BioTechniques 5:444–447.
   Web of Science ®Google Scholar
• Pessara, U., and N. Koch. 1990. Tumor necrosis factor a regulates expression of the major histocompatibility complex class II-associated invariant chain by binding of an NF-kB-like factor to a promoter element. Mol. Cell. Biol. 10:4146–4154.
   PubMedGoogle Scholar
• Pfeifer, G. P., R. L. Tanguay, S. D. Steigerwald, and A. D. Riggs. 1990. In vivo footprint and methylation analysis by PCR-aided genomic sequencing: comparison of active and inactive X chromosome DNA at the CpG island and promoter of human PGK-1. Genes Dev. 4:1277–1287.
   PubMed Web of Science ®Google Scholar
• Reith, W., S. Satola, C. Herrero Sanchez, I. Amaldi, B. Lisowska-Grospierre, C. Griscelli, M. R. Hadam, and B. Mach. 1988. Congenital immunodeficiency with a regulatory defect in MHC class II gene expression lacks a specific HLA-DR promoter binding protein, RF-X. Cell 53:897–906.
   PubMed Web of Science ®Google Scholar
• Reith, W., C.-A. Siegrist, B. Durand, E. Barras, and B. Mach. 1994. Function of major histocompatibility complex class II promoters requires cooperative binding between factors RFX and NF-Y. Proc. Natl. Acad. Sci. USA 91:554–558.
   PubMedGoogle Scholar
• Schild, C., F.-X. Claret, W. Wahli, and A. P. Wolffe. 1993. A nucleosomedependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 12:423–433.
   PubMedGoogle Scholar
• Shachar, I., and R. A. Flavell. 1996. Requirement for invariant chain in B cell maturation and function. Science 274:106–108.
   PubMed Web of Science ®Google Scholar
• Sinha, S., I.-S. Kim, K.-Y. Sohn, B. de Crombrugghe, and S. N. Maity. 1996. Three classes of mutations in the A subunit of the CCAAT-binding factor CBF delineate functional domains involved in the three-step assembly of the CBF-DNA complex. Mol. Cell. Biol. 16:328–337.
   PubMedGoogle Scholar
• Sinha, S., S. N. Maity, J. Lu, and B. de Crombrugghe. 1995. Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc. Natl. Acad. Sci. USA 92:1624–1628.
   PubMed Web of Science ®Google Scholar
• Steimle, V., B. Durand, E. Barras, M. Zufferey, M. R. Hadam, B. Mach, and W. Reith. 1995. A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). Genes Dev. 9:1021–1032.
   PubMedGoogle Scholar
• Steimle, V., L. A. Otten, M. Zufferey, and B. Mach. 1993. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75:135–146.
   PubMed Web of Science ®Google Scholar
• Thanos, D., and T. Maniatis. 1995. Virus induction of human IFNb gene expression requires the assembly of an enhanceosome. Cell 83:1091–1100.
   PubMed Web of Science ®Google Scholar
• Ting, J. P.-Y., and A. S. Baldwin. 1993. Regulation of MHC gene expression. Curr. Opin. Immunol. 5:8–16.
   PubMed Web of Science ®Google Scholar
• Tjian, R., and T. Maniatis. 1994. Transcriptional activation: a complex puzzle with few easy pieces. Cell 77:5–8.
   PubMed Web of Science ®Google Scholar
• Truss, M., J. Bartsch, A. Schelbert, R. J. G. Hache, and M. Beato. 1995. Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. EMBO J. 14:1737–1751.
   PubMedGoogle Scholar
• Vilen, B. J., J. P. Cogswell, and J. P.-Y. Ting. 1991. Stereospecific alignment of the X and Y elements is required for major histocompatibility complex class II DRA promoter function. Mol. Cell. Biol. 11:2406–2415.
   PubMedGoogle Scholar
• Vilen, B. J., J. F. Penta, and J. P.-Y. Ting. 1992. Structural constraints within a trimeric transcriptional regulatory region: constitutive and interferon-g-inducible expression of the HLA-DRA gene. J. Biol. Chem. 267:23728–23734.
   PubMedGoogle Scholar
• Wright, K. L. Submitted for publication.
   Google Scholar
• Wright, K. L., T. L. Moore, B. J. Vilen, A. M. Brown, and J. P.-Y. Ting. 1995. Major histocompatibility complex class II-associated invariant chain gene expression is up-regulated by cooperative interactions of Sp1 and NF-Y. J. Biol. Chem. 270:20978–20986.
   PubMed Web of Science ®Google Scholar
• Wright, K. L., and J. P.-Y. Ting. 1992. In vivo footprint analysis of the HLA-DR promoter: cell-specific interaction at the octamer site and upregulation of X box binding protein by interferon-g. Proc. Natl. Acad. Sci. USA 89:7601–7605.
   PubMedGoogle Scholar
• Wright, K. L., B. J. Vilen, Y. Itoh-Lindstrom, T. L. Moore, G. Li, M. Criscitiello, P. Cogswell, J. Badley Clarke, and J. P.-Y. Ting. 1994. CCAAT box binding protein NF-Y facilitates in vivo recruitment of upstream DNA binding transcription factors. EMBO J. 13:4042–4053.
   PubMedGoogle Scholar
• Xie, X., T. Kokubo, S. L. Cohen, U. A. Mirza, A. Hoffmann, B. T. Chait, R. G. Roeder, Y. Nakatani, and S. K. Burley. 1996. Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nature 380:316–322.
   PubMed Web of Science ®Google Scholar
• Xing, Y., J. D. Fikes, and L. Guarente. 1993. Mutations in yeast HAP2/HAP3 define a hybrid CCAAT box binding domain. EMBO J. 12:4647–4655.
   PubMedGoogle Scholar
• Zeleznik-Le, N. J., J. C. Azizkhan, and J. P.-Y. Ting. 1991. Affinity-purified CCAAT-box-binding protein (YEBP) functionally regulates expression of a human class II major histocompatibility complex gene and the herpes simplex virus thymidine kinase gene. Proc. Natl. Acad. Sci. USA 88:1873–1877.
   PubMedGoogle Scholar