Pbx Modulation of Hox Homeodomain Amino-Terminal Arms Establishes Different DNA-Binding Specificities across the Hox Locus

REFERENCES

• Acampora, D., M. D’Esposito, A. Faiella, M. Pannese, E. Migliaccio, F. Morelli, A. Stornaiuolo, V. Nitro, A. Simeone, and E. Boncinelli. 1989. The human HOX family. Nucleic Acids Res. 17:10385–10402.
   PubMed Web of Science ®Google Scholar
• Akam, M. 1989. Hox and Hom: homologous gene clusters in insects and vertebrates. Cell 57:347–349.
   PubMedGoogle Scholar
• Beachy, P. A., J. Varkey, K. E. Young, D. P. von Kessler, B. I. Sun, and S. C. Ekker. 1993. Cooperative binding of an Ultrabithorax homeo domain protein to nearby and distant DNA sites. Mol. Cell. Biol. 13:6941–6956.
   PubMedGoogle Scholar
• Benjamin, S., D. A. Hursh, D. Jackson, and P. A. Beachy. 1995. Ultrabithorax protein is necessary but not sufficient for full activation of decapentaplegic expression in the visceral mesoderm. EMBO J. 14:520–535.
   PubMedGoogle Scholar
• Benson, G. V., T.-H. E. Nguyen, and R. L. Mass. 1995. The expression pattern of the murine Hoxa-10 gene and the sequence recognition of its homeodomain reveal specific properties of Abdominal B-like genes. Mol. Cell. Biol. 15:1591–1601.
   PubMedGoogle Scholar
• Billeter, M., Y. Q. Qian, G. Otting, M. Müller, W. Gehring, and K. Wüthrich. 1993. Determination of the NMR solution structure of an Antennapedia homeodomain-DNA complex. J. Mol. Biol. 234:1084–1093.
   PubMedGoogle Scholar
• Blackwell, T. K., and H. Weintraub. 1990. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250:1104–1110.
   PubMed Web of Science ®Google Scholar
• Bürglin, T. R. 1994. A comprehensive classification of homeobox genes, p. 27–41. In D. Duboule (ed.), Guidebook to the homeobox genes. Oxford University Press, Oxford.
   Google Scholar
• Catron, K. M., N. Iler, and C. Abate. 1993. Nucleotides flanking a conserved TAAT core dictate the DNA binding specificity of three murine homeodomain proteins. Mol. Cell. Biol. 13:2354–2365.
   PubMed Web of Science ®Google Scholar
• Chan, K. S., and R. Mann. 1993. The segment identity functions of ultrabithorax are contained within its homeodomain and carboxy-terminal sequences. Genes Dev. 7:796–811.
   PubMedGoogle Scholar
• Chan, S.-K., L. Jaffe, M. Capovilla, J. Botas, and R. S. Mann. 1994. The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with Extradenticle, another homeoprotein. Cell 78:603–615.
   PubMedGoogle Scholar
• Chang, C.-P., and M. L. Cleary. Unpublished observations.
   Google Scholar
• Chang, C.-P., W.-F. Shen, S. Rozenfeld, H. J. Lawrence, C. Largman, and M. L. Cleary. 1995. Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins. Genes Dev. 9:663–674.
   PubMedGoogle Scholar
• Corsetti, J. M., P. Briata, L. Sanseverino, A. Daga, I. Airoldi, A. Simeone, G. Palmisano, C. Angelini, E. Boncinelli, and G. Corte. 1992. Differential DNA binding properties of three human homeodomain proteins. Nucleic Acids Res. 20:4465–4472.
   PubMedGoogle Scholar
• Desplan, C., J. Theis, and P. H. O’Farrell. 1988. The sequence specificity of homeodomain-DNA interaction. Cell 54:1081–1090.
   PubMed Web of Science ®Google Scholar
• Dessain, S., C. T. Gross, M. A. Kuziora, and W. McGinnis. 1992. Antp-like homeodomains have distinct DNA binding specificities that correlate with their different regulatory functions in embryos. EMBO J. 11:991–1002.
   PubMed Web of Science ®Google Scholar
• Ekker, S. C., D. G. Jackson, D. P. von Kessler, B. I. Sun, K. E. Young, and P. A. Beachy. 1994. The degree of variation in DNA sequence recognition among four Drosophila homeotic proteins. EMBO J. 13:3551–3560.
   PubMed Web of Science ®Google Scholar
• Ekker, S. C., K. E. Young, D. P. von Kessler, and P. A. Beachy. 1991. Optimal DNA sequence recognition by the Ultrabithorax homeodomain of Drosophila. EMBO J. 10:1179–1186.
   PubMedGoogle Scholar
• Furukubo-Tokonaga, K., S. Flister, and W. J. Gehring. 1993. Functional specificity of the Antennapedia homeodomain. Proc. Natl. Acad. Sci. USA 90:6360–6364.
   PubMedGoogle Scholar
• Gehring, W. J., Y. Q. Qian, M. Billeter, K. Furukubo-Tokunaga, A. F. Schier, D. Resendez-Perez, M. Affolter, G. Otting, and K. Wüthrich. 1994. Homeodomain-DNA recognition. Cell 78:211–223.
   PubMed Web of Science ®Google Scholar
• Gibson, G., A. Schier, P. LeMotte, and W. J. Gehring. 1990. The specificities of Sexcombs Reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain. Cell 62:1087–1103.
   PubMedGoogle Scholar
• Grueneberg, D. A., S. Natesan, C. Alexander, and M. Z. Gilman. 1992. Human and Drosophila homeodomain proteins that enhance the DNA-binding activity of serum response factor. Science 257:1089–1095.
   PubMed Web of Science ®Google Scholar
• Hanes, S. D., and R. Brent. 1989. DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell 57:1275–1283.
   PubMedGoogle Scholar
• Hayashi, S., and M. P. Scott. 1990. What determines the specificity of action of Drosophila homeodomain proteins? Cell 63:883–894.
   PubMedGoogle Scholar
• Herr, W., and M. A. Cleary. 1995. The POU domain: versatility in transcriptional regulation by a flexible two-in-one DNA-binding domain. Genes Dev. 9:1679–1693.
   PubMed Web of Science ®Google Scholar
• Hoey, T., and M. Levine. 1988. Divergent homeo box proteins recognize similar DNA sequences in Drosophila. Nature (London) 332:858–861.
   PubMedGoogle Scholar
• Hunger, S. P., R. Brown, and M. L. Cleary. 1994. DNA-binding and transcriptional regulatory properties of hepatic leukemia factor (HLF) and the t(17;19) acute lymphoblastic leukemia chimera E2a-HLF. Mol. Cell. Biol. 14:5986–5996.
   PubMed Web of Science ®Google Scholar
• Ingraham, H. A., S. E. Flynn, J. W. Voss, V. R. Albert, M. S. Kapiloff, L. Wilson, and M. G. Rosenfeld. 1990. The POU-specific domain of Pit-1 is essential for sequence-specific, high affinity DNA binding and DNA-depen-dent Pit-1-Pit-1 interactions. Cell 61:1021–1033.
   PubMed Web of Science ®Google Scholar
• Ispisúa-Belmonte, J.-C., H. Falkenstein, P. Dollé, A. Renucci, and D. Deboule. 1991. Murine genes related to the Drosophila AbdB homeotic gene are sequentially expressed during development of the posterior part of the body. EMBO J. 10:2279–2289.
   PubMedGoogle Scholar
• Jacobs, Y., C. Vierra, and C. Nelson. 1993. E2A expression, nuclear localization, and in vivo formation of DNA- and non-DNA-binding species during B-cell development. Mol. Cell. Biol. 13:7321–7333.
   PubMedGoogle Scholar
• Johnson, A. 1992. A combinatorial regulatory circuit in budding yeast, p. 975–1006. In S. L. McKnight and K. R. Yamamoto (ed.), Transcriptional regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Johnson, F. B., E. Parker, and M. A. Krasnow. 1995. extradenticle protein is a selective cofactor for the Drosophila homeotics: role of the homeodomain and YPWM motif in the interaction. Proc. Natl. Acad. Sci. USA 92:739–743.
   PubMedGoogle Scholar
• Kamps, M. P., C. M. Murre, X.-H. Sun, and D. Baltimore. 1990. A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL. Cell 60:547–555.
   PubMed Web of Science ®Google Scholar
• Kiledjian, M., and T. Kadesch. 1990. Analysis of the human liver/bone/kidney alkaline phosphatase promoter in vivo and in vitro. Nucleic Acids Res. 18:957–961.
   PubMedGoogle Scholar
• Kissinger, C. R., B. Liu, E. Martin-Blanco, T. B. Kornberg, and C. O. Pabo. 1990. Crystal structure of an engrailed homeodomain-DNA complex at 2.8 Å resolution: a framework for understanding homeodomain-DNA interactions. Cell 63:579–590.
   PubMed Web of Science ®Google Scholar
• Knoefler, P. S., and M. P. Kamps. 1995. The pentapeptide motif of Hox proteins is required for cooperative DNA binding with Pbx1, physically contacts Pbx1, and enhances DNA binding by Pbx1. Mol. Cell. Biol. 15:5811–5819.
   PubMedGoogle Scholar
• Krumlauf, R. 1994. Hox genes in vertebrate development. Cell 78:191–201.
   PubMed Web of Science ®Google Scholar
• Kuziora, M. A., and W. McGinnis. 1989. A homeodomain substitution changes the regulatory specificity of the Deformed protein in Drosophila embryos. Cell 59:563–571.
   PubMedGoogle Scholar
• Laughon, A. 1991. DNA binding specificity of homeodomains. Biochemistry 30:11357–11367.
   PubMed Web of Science ®Google Scholar
• Lawrence, H. J., and C. Largman. 1992. Homeobox genes in normal hematopoiesis and leukemia. Blood 80:2445–2453.
   PubMed Web of Science ®Google Scholar
• LeBrun, D. L., and M. L. Cleary. 1994. Fusion with E2A alters the transcriptional properties of the homeodomain protein PBX1 in t(1;19) leukemias. Oncogene 9:1641–1647.
   PubMed Web of Science ®Google Scholar
• Levitt, M. 1983. Protein folding by restrained energy minimization and molecular dynamics. J. Mol. Biol. 170:723–764.
   PubMed Web of Science ®Google Scholar
• Levitt, M. 1992. Accurate modeling of protein conformation by automatic segment matching. J. Mol. Biol. 226:507–533.
   PubMed Web of Science ®Google Scholar
• Lin, L., and W. McGinnis. 1992. Mapping functional specificity in the Dfd and Ubx homeo domains. Genes Dev. 6:1071–1081.
   PubMedGoogle Scholar
• Lu, Q., P. S. Knoepfler, J. Scheele, D. D. Wright, and M. P. Kamps. 1995. Both Pbx1 and E2A-Pbx1 bind the DNA motif ATCAATCAA cooperatively with the products of multiple murine Hox genes, some of which are themselves oncogenes. Mol. Cell. Biol. 15:3786–3795.
   PubMed Web of Science ®Google Scholar
• Lu, Q., D. D. Wright, and M. P. Kamps. 1994. Fusion with E2A converts the Pbx1 homeodomain protein into a constitutive transcriptional activator in human leukemias carrying the t(1;19) translocation. Mol. Cell. Biol. 14:3938–3948.
   PubMedGoogle Scholar
• Malicki, J., L. D. Bogorad, M. M. Martin, F. H. Ruddle, and W. McGinnis. 1993. Functional analysis of the mouse homeobox gene HoxB9 in Drosophila development. Mech. Dev. 42:139–150.
   PubMedGoogle Scholar
• Manak, J., L. Mathies, and M. Scott. 1995. Regulation of a decapentaplegic midgut enhancer by homeotic proteins. Development 120:3605–3619.
   Google Scholar
• Mann, R. S., and D. S. Hogness. 1990. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell 60:597–610.
   PubMedGoogle Scholar
• McGinnis, W., and R. Krumlauf. 1992. Homeobox genes and axial patterning. Cell 68:283–302.
   PubMed Web of Science ®Google Scholar
• Mendel, D. B., P. A. Khavari, P. B. Conley, M. K. Graves, L. P. Hansen, A. Admon, and G. R. Crabtree. 1991. Characterization of a cofactor that regulates dimerization of a mammalian homeodomain protein. Science 254:1762–1767.
   PubMed Web of Science ®Google Scholar
• Monica, K., N. Galili, J. Nourse, D. Saltman, and M. L. Cleary. 1991. PBX2 and PBX3, new homeobox genes with extensive homology to the human proto-oncogene PBX1. Mol. Cell. Biol. 11:6149–6157.
   PubMed Web of Science ®Google Scholar
• Monica, K., D. L. LeBrun, D. A. Dedera, R. Brown, and M. L. Cleary. 1994. Transformation properties of the E2a-Pbx1 chimeric oncoprotein: fusion with E2a is essential but the Pbx1 homeodomain is dispensable. Mol. Cell. Biol. 14:8304–8313.
   PubMed Web of Science ®Google Scholar
• Müller, M., M. Affolter, W. Leupin, G. Otting, K. Wüthrich, and W. J. Gehring. 1988. Isolation and sequence-specific DNA binding of the Antennapedia homeodomain. EMBO J. 7:4299–4304.
   PubMedGoogle Scholar
• Neuteboom, S. T. C., L. T. C. Peltenburg, M. A. van Dijk, and C. Murre. 1995. The hexapeptide LFPWMR in Hoxb-8 is required for cooperative DNA binding with Pbx1 and Pbx2 proteins. Proc. Natl. Acad. Sci. USA 92:9166–9170.
   PubMed Web of Science ®Google Scholar
• Nourse, J., J. D. Mellentin, N. Galili, J. Wilkinson, E. Stanbridge, S. D. Smith, and M. L. Cleary. 1990. Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell 60:535–546.
   PubMed Web of Science ®Google Scholar
• Odenwald, W. F., J. Garbern, H. Arnheiter, E. Tournier-Lasserve, and R. A. Lazzarini. 1989. The Hox-1.3 homeo box protein is a sequence-specific DNA-binding phosphoprotein. Genes Dev. 3:158–172.
   PubMedGoogle Scholar
• Otting, G., Y. Q. Qian, M. Billeter, M. Muller, M. Affolter, W. J. Gehring, and K. Wuthrich. 1990. Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J. 9:3085–3092.
   PubMed Web of Science ®Google Scholar
• Peifer, M., and E. Wieschaus. 1990. Mutations in the Drosophila gene extra-denticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev. 4:1209–1223.
   PubMedGoogle Scholar
• Pellerin, I., C. Schnabel, K. M. Catron, and C. Abate. 1994. Hox proteins have different affinities for a consensus DNA site that correlate with the positions of their genes on the hox cluster. Mol. Cell. Biol. 14:4532–4545.
   PubMedGoogle Scholar
• Peverali, F., M. D’Esposito, D. Acampora, G. Bunone, M. Negri, A. Faicella, A. Stornaiuolo, M. Pannese, E. Migliaccio, A. Simeone, G. Della Valle, and E. Boncinelli. 1990. Expression of HOX homeogenes in human neuroblastoma cell culture lines. Differentiation 45:61–69.
   PubMedGoogle Scholar
• Phelan, M. L., I. Rambaldi, and M. S. Featherstone. 1995. Cooperative interactions between HOX and PBX proteins mediated by a conserved peptide motif. Mol. Cell. Biol. 15:3989–3997.
   PubMed Web of Science ®Google Scholar
• Phelan, M. L., R. Sadoul, and M. S. Featherstone. 1994. Functional differences between HOX proteins conferred by two residues in the homeodomain N-terminal arm. Mol. Cell. Biol. 14:5066–5075.
   PubMedGoogle Scholar
• Phillips, C. L., M. R. Stark, A. D. Johnson, and F. W. Dahlquist. 1994. Heterodimerization of the yeast homeodomain transcriptional regulators a2 and a1 induces an interfacial helix in a2. Biochemistry 33:9294–9302.
   PubMedGoogle Scholar
• Popperl, H., M. Bienz, M. Studer, S.-K. Chan, S. Aparicio, S. Brenner, R. S. Mann, and R. Krumlauf. 1995. Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81:1031–1042.
   PubMed Web of Science ®Google Scholar
• Rauskolb, C., M. Peifer, and E. Wieschaus. 1993. extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogene PBX1. Cell 74:1101–1112.
   PubMedGoogle Scholar
• Rauskolb, C., K. M. Smith, M. Peifer, and E. Wieschaus. 1995. extradenticle determines segmental identities throughout Drosophila development. Development 121:3663–3673.
   PubMedGoogle Scholar
• Rauskolb, C., and E. Wieschaus. 1994. Coordinate regulation of downstream genes by extradenticle and the homeotic selector proteins. EMBO J. 13:3561–3569.
   PubMedGoogle Scholar
• Regulski, M., S. Dessain, N. McGinnis, and W. McGinnis. 1991. High-affinity binding sites for the Deformed protein are required for the function of an autoregulatory enhancer of the Deformed gene. Genes Dev. 5:278–286.
   PubMedGoogle Scholar
• Rey-Campos, J., T. Chouard, M. Yaniv, and S. Cereghini. 1991. vHNF1 is a homeoprotein that activates transcription and forms heterodimers with HNF1. EMBO J. 10:1445–1457.
   PubMed Web of Science ®Google Scholar
• Rost, B., and C. Sander. 1994. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19:55–72.
   PubMed Web of Science ®Google Scholar
• Sasaki, H., E. Yokoyama, and A. Kuroiwa. 1990. Specific DNA binding of the two chicken Deformed family homeodomain proteins, Chox-1.4 and Chox-a. Nucleic Acids Res. 18:1739–1747.
   PubMedGoogle Scholar
• Sauvageau, G., U. Thorsteinsdottir, C. J. Eaves, H. J. Lawrence, C. Larg-man, P. M. Lansdorp, and R. K. Humphries. 1995. Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev. 9:1753–1765.
   PubMed Web of Science ®Google Scholar
• Shen, W.-F., C.-P. Chang, S. Rozenfeld, G. Sauvageau, R. K. Humphries, M. Lu, H. J. Lawrence, M. L. Cleary, and C. Largman. HOX homeodomain proteins exhibit selective complex stabilities with Pbx and DNA. Nucleic Acids Res., in press.
   Google Scholar
• Stern, S., M. Tanaka, and W. Herr. 1989. The Oct-1 homeodomain directs formation of a multiprotein-DNA complex with the HSV transactivator VP16. Nature (London) 341:624–630.
   PubMed Web of Science ®Google Scholar
• Sun, B., D. A. Hursh, D. Jackson, and P. A. Beachy. 1995. Ultrabithorax protein is necessary but not sufficient for full activation of decapentaplegic expression in the viceral mesoderm. EMBO J. 14:520–535.
   PubMedGoogle Scholar
• Treisman, J., P. Gonczy, M. Vashishtha, E. Harris, and C. Desplan. 1989. A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell 59:553–562.
   PubMedGoogle Scholar
• van Dijk, M. A., and C. Murre. 1994. extradenticle raises the DNA binding specificity of homeotic selector gene products. Cell 78:617–624.
   PubMedGoogle Scholar
• van Dijk, M. A., P. M. Voorhoeve, and C. Murre. 1993. Pbx1 is converted into a transcriptional activator upon acquiring the N-terminal region of E2A in pre-B-cell acute lymphoblastoid leukemia. Proc. Natl. Acad. Sci. USA 90:6061–6065.
   PubMedGoogle Scholar
• Verrijzer, C. P., J. A. W. M. van Oosterhout, and P. C. van der Vliet. 1992. The Oct-1 POU domain mediates interactions between Oct-1 and other POU proteins. Mol. Cell. Biol. 12:542–551.
   PubMedGoogle Scholar
• Voss, J. W., L. Wilson, and M. G. Rosenfeld. 1991. POU-domain proteins Pit-1 and Oct-1 interact to form a heterodimeric complex and can cooperate to induce expression of the prolactin promoter. Genes Dev. 5:1309–1320.
   PubMed Web of Science ®Google Scholar
• Weiner, S. J., P. A. Kollman, D. A. Case, U. C. Singh, C. Ghio, G. Alagona, S. Profeta, Jr., and P. Weiner. 1994. A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 106:765–784.
   Google Scholar
• Weiner, S. J., P. A. Kollman, D. T. Nguyen, and D. A. Case. 1986. An all atom force field for simulation of proteins and nucleic acids. J. Comput. Chem. 7:230–252.
   PubMed Web of Science ®Google Scholar
• Wolberger, C., A. K. Vershon, B. Liu, A. D. Johnson, and C. O. Pabo. 1991. Crystal structure of the MATa2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67:517–528.
   PubMed Web of Science ®Google Scholar
• Xue, D., Y. Tu, and M. Chalfie. 1993. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 261:1324–1328.
   PubMedGoogle Scholar
• Zappavigna, V., D. Sartori, and F. Mavilio. 1994. Specificity of HOX protein function depends on DNA-protein and protein-protein interactions, both mediated by the homeo domain. Genes Dev. 8:732–744.
   PubMedGoogle Scholar
• Zeng, W., D. J. Andrew, L. D. Mathies, M. A. Horner, and M. P. Scott. 1993. Ectopic expression and function of the Antp and Scr homeotic genes: the N terminus of the homeodomain is critical to functional specificity. Development 118:339–352.
   PubMedGoogle Scholar