Cooperative interactions between HOX and PBX proteins mediated by a conserved peptide motif

Molecular and Cellular Biology

Volumn 15, Issue 8, 1995, Pages 3989-3997

  Phelan, Michael L ^a,b   Rambaldi, Isabel ^a   Featherstone, Mark S ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c Fonds de la Rech en S du Quebec ^*

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; ONCOPROTEIN; PENTAPEPTIDE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; DNA BINDING; EMBRYONAL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; TRANSACTIVATION;

ANIMALIA;

EID: 0029008293     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.15.8.3989     Document Type: Article

References (83)

1. Aberdam, D., V. Negreanu, L. Sachs, and C. Blatt. 1991. The oncogenic potential of an activated Hox-2.4 homeobox gene in mouse fibroblasts. Mol. Cell. Biol. 11:554-557.
2. Adra, C. N., P. H. Boer, and M. W. McBurney. 1987. Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene 60:65-74.
3. Affolter, M., A. Percival-Smith, M. Müller, W. Leupin, and W. J. Gehring. 1990. DNA binding properties of the purified Antennapedia homeodomain. Proc. Natl. Acad. Sci. USA 87:4093-4097.
4. Baron, A., M. S. Featherstone, R. E. Hill, A. Hall, B. Galliot, and D. Duboule. 1987. Hox-1.6: a mouse homeobox-containing gene member of the Hox-1 complex. EMBO J. 6:2977-2986.
5. Bermingham, J. R., and M. P. Scott. 1988. Developmentally regulated alternative splicing of transcripts from the Drosophila homeotic gene Antennapedia can produce four different proteins. EMBO J. 7:3211-3222.
6. 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.
7. Condie, B. G., and M. R. Capecchi. 1994. Mice with targeted disruptions in the paralogous genes Hoxa-3 and Hoxd-3 reveal synergistic interactions. Nature (London) 370:304-307.
8. Corsetti, M. T., 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.
9. Cribbs, D. L., M. A. Pultz, D. Johnson, M. Mazzulla, and T. C. Kaufman. 1992. Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia. EMBO J. 11:1437-1449.
10. Dalton, D., R. Chadwick, and W. McGinnis. 1989. Expression and embryonic function of empty spiracles: a Drosophila homeobox gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 3:1940-1956.
11. Davidson, D. R., A. Crawley, R. E. Hill, and C. Tickle. 1991. Position-dependent expression of two related homeobox genes in developing vertebrate limbs. Nature (London) 352:429-431.
12. Dedera, D. A., E. K. Waller, D. P. LeBrun, A. Sen-Majumdar, M. E. Stevens, G. S. Barsh, and M. L. Cleary. 1993. Chimeric homeobox gene E2A-PBX1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell 74:833-843.
13. Dessain, S., C. T. Gross, M. A. Kuziora, and W. McGinnis. 1992. Antp-type homeodomains have distinct DNA binding specificities that correlate with their different regulatory functions in embryos. EMBO J. 11:991-1002.
14. Dollé, P., and D. Duboule. 1989. Two gene members of the murine HOX-5 complex show regional and cell-type specific expression in developing limbs and gonads. EMBO J. 8:1507-1515.
15. Dube, I. D., R. S. Kamel, C. C. Yuan, M. Lu, X. Wu, G. Corpus, S. C. Raimondi, W. M. Crist, A. J. Carroll, J. Minowada, and J. B. Baker. 1991. A novel human homeobox gene lies at the chromosome 10 breakpoint in lymphoid neoplasias with chromosomal translocation t(10;14). Blood 78: 2996-3003.
16. Duprey, P., K. Chowdhury, G. R. Dressler, R. Balling, D. Simon, J.-L. Guenet, and P. Gruss. 1988. A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev. 2:1647-1654.
17. Ekker, S. C., D. G. Jackson, K. D. von, 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.
18. Ekker, S. C., D. P. von Kessler, and P. A. Beachy. 1992. Differential DNA sequence recognition is a determinant of specificity in homeotic gene action. EMBO J. 11:4059-4072.
19. Ekker, S. C., K. E. 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.
20. Erselius, J. R., M. D. Goulding, and P. Gruss. 1990. Structure and expression pattern of the murine Hox-3.2 gene. Development 110:629-642.
21. Featherstone, M. S., A. Baron, S. J. Gaunt, M.-G. Mattel, and D. Duboule. 1988. Hox-5.1 defines a homeobox-containing gene locus on mouse chromosome 2. Proc. Natl. Acad. Sci. USA 85:4760-4764.
22. Fermi, G., and M. Perutz. 1981. Hemoglobin and myoglobin. In D. C. Phillips and F. M. Richards (ed.), Atlas of molecular structures in biology. Clarendon Press, Oxford.
23. Fitzpatrick, V. D., A. Percival-Smith, C. J. Ingles, and H. M. Krause. 1992. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature (London) 356:610-612.
24. Frankel, A. D., and P. S. Kim. 1991. Modular structure of transcription factors: implications for gene regulation. Cell 65:717-719.
25. 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.
26. Gibson, G., A. Schier, P. LeMotte, and W. J. Gehring. 1990. The specificities of sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain. Cell 62:1087-1103.
27. Green, S., I. Issemann, and E. Sheer. 1988. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 16:369.
28. Hatano, M., C. W. Roberts, M. Minden, W. M. Crist, and S. J. Korsmeyer. 1991. Deregulation of a homeobox gene, HOX11, by the t(10;14) in T cell leukemia. Science 253:79-82.
29. Hill, R. E., P. F. Jones, A. R. Rees, C. M. Sime, M. J. Justice, N. G. Copeland, N. A. Jenkins, E. Graham, and D. R. Davidson. 1989. A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. Genes Dev. 3:26-37.
30. Horan, G. S. B., E. Nagy Kovàcs, R. R. Behringer, and M. S. Featherstone. Mutations in paralogous Hox genes give overlapping homeotic transformations of the axial skeleton: Evidence for unique and redundant functions. Dev. Biol., in press.
31. Hu, Y., J. Kazenwadel, and R. James. 1993. Isolation and characterization of the murine homeobox gene Cdx-1. Regulation of expression in intestinal epithelial cells. J. Biol. Chem. 268:27214-27225.
32. Izpisua-Belmonte, J. C., H. Falkenstein, P. Dollé, A. Renucci, and D. Duboule. 1991. Murine genes related to the Drosophila Abd-B homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 10:2279-2289.
33. James, R., T. Erler, and J. Kazenwadel. 1994. Structure of the murine homeobox gene cdx-2. Expression in embryonic and adult intestinal epithelium. J. Biol. Chem. 269:15229-15237.
34. 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.
35. Jonsson, J., L. Carlsson, T. Edlund, and H. Edlund. 1994. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature (London) 371:606-609.
36. Kamps, M. P., and D. Baltimore. 1993. E2A-Pbx1, the t(1;19) translocation protein of human pre-B-cell acute lymphocytic leukemia, causes acute myeloid leukemia in mice. Mol. Cell. Biol. 13:351-357.
37. Kamps, M. P., A. T. Look, and D. Baltimore. 1991. The human t(1;19) translocation in pre-B ALL produces multiple nuclear E2A-Pbx1 fusion proteins with differing transformation potentials. Genes Dev. 5:358-368.
38. Kamps, M. P., C. 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.
39. Kappen, C., K. Schughart, and F. H. Ruddle. 1993. Early evolutionary origin of major homeodomain sequence classes. Genomics 18:54-70.
40. Kennedy, M. A., S. R. Gonzalez, U. R. Kees, F. Lampert, N. Dear, T. Boehm, and T. H. Rabbitts. 1991. HOX11, a homeobox-containing T-cell oncogene on human chromosome 10q24. Proc. Natl. Acad. Sci. USA 88:8900-8904.
41. Kornfield, K., R. B. Saint, P. A. Beachy, P. J. Harte, D. A. Peattie, and D. S. Hogness. 1989. Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev. 3:243-258.
42. Krumlauf, R. 1993. Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet. 9:106-112.
43. Kuziora, M. A., and W. McGinnis. 1991. Altering the regulatory targets of the Deformed protein in Drosophila embryos by substituting the Abdominal-B homeodomain. Mech. Dev. 33:83-94.
44. LaRosa, G. J., and L. J. Gudas. 1988. Early retinoic acid-induced F9 teratocarcinoma stem cell gene ERA-1: alternate splicing creates transcripts for a homeobox-containing protein and one lacking the homeobox. Mol. Cell. Biol. 8:3906-3917.
45. Lawrence, H. J., and C. Largman. 1992. Homeobox genes in normal hematopoiesis and leukemia. Blood 80:2445-2453.
46. LeBrun, D. P., 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.
47. Li, P., X. He, M. R. Gerrero, M. Mok, A. Aggarwal, and M. G. Rosenfeld. 1993. Spacing and orientation of bipartite DNA-binding motifs as potential determinants for POU domain factors. Genes Dev. 7:2483-2496.
48. Lin, L., and W. McGinnis. 1992. Mapping functional specificity in the Dfd and Ubx homeo domains. Genes Dev. 6:1071-1081.
49. Lu, Q., D. D. Wright, and M. A. Kamps. 1994. Fusion with E2A converts the Pbxl homeodomain protein into a constitutive transcriptional activator in human leukemias carrying the t(1;19) translocation. Mol. Cell. Biol. 14: 3938-3948.
50. Mann, R. S., and D. S. Hogness. 1990. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell 60:597-610.
51. Maulbecker, C. C, and P. Gruss. 1993. The oncogenic potential of deregulated homeobox genes. Cell Growth Differ. 4:431-441.
52. Mavilio, F., A. Simeone, A. Giampaolo, A. Faiella, V. Zappavigna, D. Acampora, G. Poiana, G. Russo, C. Peschle, and E. Boncinelli. 1986. Differential and stage-related expression in embryonic tissues of a new human homoeobox gene. Nature (London) 324:664-668.
53. Mlodzik, M., and W. J. Gehring. 1987. Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell 48:465-478.
54. Monaghan, A. P., D. R. Davidson, C. Sime, E. Graham, R. Baldock, S. S. Bhattacharya, and R. E. Hill. 1991. The Msh-like homeobox genes define domains in the developing vertebrate eye. Development 112:1053-1061.
55. 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.
56. Monica, K., D. P. 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 dispensible. Mol. Cell. Biol. 14:8304-8314.
57. Nourse, J., J. D. Mellentin, N. Galili, J. Wilkinson, E. Starbridge, 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 60:535-545.
58. O'Connor, M. B., R. Binari, L. A. Perkins, and W. Bender. 1988. Alternative RNA products from the Ultrabithorax domain of the bithorax complex. EMBO J. 7:435-445.
59. Ohisson, H., K. Karlsson, and T. Edlund. 1993. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J. 12:4251-4259.
60. Peifer, M., and E. Wieschaus. 1990. Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev. 4:1209-1223.
61. 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.
62. Perkins, A., K. Kongsuwan, J. Visvader, J. M. Adams, and S. Cory. 1990. Homeobox gene expression plus autocrine growth factor production elicits myeloid leukemia. Proc. Natl. Acad. Sci. USA 87:8398-8402.
63. 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.
64. Phillips, C. L., M. R. Stark, A. D. Johnson, and F. W. Dahlquist. 1994. Heterodimerization of the yeast homeodomain transcriptional regulators alpha 2 and a1 induces an interfacial helix in alpha 2. Biochemistry 33:9294-9302.
65. Pöpperl, H., and M. S. Featherstone. 1992. An autoregulatory element of the murine Hox-4.2 gene. EMBO J. 11:3673-80.
66. Qian, Y. Q., G. Otting, K. Furukubo-Tokunaga, M. Affolter, W. J. Gehring, and K. Wüthrich. 1992. NMR structure determination reveals that the homeodomain is connected through a flexible linker to the main body in the Drosophila Antennapedia protein. Proc. Natl. Acad. Sci. USA 89:10738-10742.
67. Rambaldi, I., E. N. Kovacs, and M. S. Featherstone. 1994. A proline-rich transcriptional activation domain in murine HOXD-4 (HOX-4.2). Nucleic Acids Res. 22:376-382.
68. 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.
69. Rauskolb, C., and E. Wieschaus. 1994. Coordinate regulation of downstream genes by extradenticle and the homeotic selector proteins. EMBO J. 13: 3561-3569.
70. Robert, B., D. Sassoon, B. Jacq, W. Gehring, and M. Buckingham. 1989. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J. 8:91-100.
71. Roberts, C. W., J. R. Shutter, and S. J. Korsmeyer. 1994. Hox11 controls the genesis of the spleen. Nature (London) 368:747-749.
72. Rosenberg, A. H., B. N. Lade, D. S. Chui, S. W. Lin, J. J. Dunn, and F. W. Studier. 1987. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene 56:125-135.
73. Sasaki, H., E. Yokoyama, and A. Kuroiwa. 1990. Specific DNA binding of the two chicken Deformed family homeoproteins, Chox-1.4 and Chox-a. Nucleic Acids Res. 18:1739-1747.
74. Satokata, I., and R. Maas. 1994. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6:348-355.
75. Simeone, A., M. Gulisano, D. Acampora, A. Stornaiuolo, M. Rambaldi, and E. Boncinelli. 1992. Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 11:2541-2550.
76. Slack, J. M. W., P. W. H. Holland, and C. F. Graham. 1993. The zootype and the phylotypic stage. Nature (London) 361:490-492.
77. Smith, D. L., and A. D. Johnson. 1992. A molecular mechanism for combinatorial control in yeast: MCM1 protein sets the spacing and orientation of the homeodomains of an α2 dimer. Cell 68:133-142.
78. Suh, E., L. Chen, J. Taylor, and P. G. Traber. 1994. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol. Cell. Biol. 14:7340-7351.
79. van Dijk, M. A., and C. Murre. 1994. extradenticle raises the DNA binding specificity of homeotic selector gene products. Cell 78:617-624.
80. 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.
81. Vershon, A. K., Y. S. Jin, and A. D. Johnson. 1995. A homeo domain protein lacking specific side chains of helix 3 can still bind DNA and direct transcriptional repression. Genes Dev. 9:182-192.
82. Vershon, A. K., and A. D. Johnson. 1993. A short, disordered protein region mediates interactions between the homeodomain of the yeast alpha-2 protein and the MCM1 protein. Cell 72:105-112.
83. Wolberger, C., A. K. Vershon, B. Liu, A. D. Johnson, and C. O. Pabo. 1991. Crystal structure of a MATα2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell 67:517-528.