The Hox cooperativity motif of the chimeric oncoprotein E2a-Pbx1 is necessary and sufficient for oncogenesis

Molecular and Cellular Biology

Volumn 17, Issue 1, 1997, Pages 81-88

  Chang, Ching Pin ^a   De Vivo, Immaculata ^a   Cleary, Michael L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; DNA; HYBRID PROTEIN; ONCOPROTEIN;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL STRAIN 3T3; CONTROLLED STUDY; COOPERATION; DELETION MUTANT; DNA BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; SITE DIRECTED MUTAGENESIS;

ANIMALIA;

EID: 0031031879     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.1.81     Document Type: Article

References (41)

1. Ananthan, J., R. Baler, D. Morrissey, J. Zuo, Y. Lan, M. Weir, and R. Voellmy. 1993. Synergistic activation of transcription is mediated by the N-terminal domain of Drosophila fushi tarazu homeoprotein and can occur without DNA binding by the protein. Mol. Cell. Biol. 13:1599-1609.
2. Borrow, J., A. M. Shearman, V. P. Stanton Jr., R. Becher, T. Collins, A. J. Williams, I. Dube, F. Katz, Y. L. Kwong, C. Morris, K. Ohyashiki, K. Toyama, J. Rowley, and D. E. Housman. 1996. The t(7;11)(p15;p15) translocalion in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat. Genet. 12:159-167.
3. Bürglin, T. R., and G. Ruvkun. 1992. New motif in PBX genes. Nat. Genet. 1:319-320.
4. 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.
5. Chang, C.-P., L. Brocchieri, W.-F. Shen, C. Largman, and M. L. Cleary. 1996. Pbx modulation of Hox homeodomain amino-terminal arms establishes different DNA-binding specificities across the Hox locus. Mol. Cell. Biol. 16:1734-1745.
6. Chang, C.-P., W-F. Shen, S. Ruzenfeld, 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.
7. Chang, C.-P. and M. L. Cleary. Unpublished observations.
8. Corsetti, M. T., G. Levi, F. Lancia, L. Sanseverino, S. Ferrini, E. Boncinelli, and G. Corte. 1995. Nucleolar localisation of three homeoproteins. J. Cell Sci. 108:187-193.
9. Dedera, D. A., E. K. Waller, D. P. LeBrun, A. Sen-Majumbar, M. E. Stevens, G. S. Barsh, and M. L. Cleary. 1993. Chimeric homeohox gene E2a-Pbx1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell 74:833-843.
10. Fibi, M., B. Zink, M. Kessel, A. M. Colberg-Poley, S. Labeit, H. Lehrach, and P. Gruss. 1988. Coding sequence and expression of the homeohox gene Hox1.3. Development 102:349-359.
11. 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.
12. Jacobs, Y. and M. L. Cleary. Unpublished observations.
13. 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.
14. Kamps, M. P., C. M. Murre, X.-H. Sun, and D. Baltimore. 1990. A new homeohox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL. Cell 60:547-555.
15. Kamps, M. P., and D. Baltimore. 1993. E2A-Pbx1, the t(1;19) translocation protein of human pre-B-eell acute lymphoblastic leukemia, causes acute myeloid leukemia in mice. Mol. Cell. Biol. 13:351-357.
16. Kamps, M. P., T. Look, and D. Baltimore. 1991. The human t(1;19) translocation in pre-B cell ALL produces multiple nuclear E2A-Pbx1 fusion proteins with differing transforming potentials. Genes Dev. 5:358-368.
17. Kamps, M. P., D. D. Wright, and Q. Lu. 1996. DNA-binding by oncoprotein E2A-Pbx1 is important for blocking differentiation but dispensible for fibroblast transformation. Oncogene 12:19-30.
18. Kessel, M., F. Schulze, M. Fibi, and P. Gruss. 1987. Primary structure and nuclear localization of a murine homeodomain protein. Proc. Natl. Acad. Sci. USA 84:5306-5310.
19. Kildjian, 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.
20. 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.
21. 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.
22. Lu, Q., and M. P. Kamps. 1996. Structural determinants within Pbx1 that mediate cooperative DNA binding with pentapeptide-containing Hox proteins: proposal for a model of a Pbx1-Hox-DNA complex. Mol. Cell. Biol. 16:1632-1640.
23. 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
24. 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.
25. 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.
26. 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.
27. Nakamura, T., D. A. Largaespada, M. P. Lee, L. A. Johnson, K. Ohyashiki, K. Toyama, S. J. Chen, C. L. Willman, I.-M. Chen, A. P. Feinberg, N. A. Jenkins, N. G. Copeland, and J. D. Shaughnessy. 1996. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15; p15) in human myeloid leukemias. Nat. Genet. 12:154-158.
28. Neuteboom, S. T. C., L. T. C. Peltenburg, M. A. vanDijk, 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.
29. 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.
30. Numata, S., K. Kato, and K. Horibe. 1993. New E2A/PBX1 fusion transcript in a patient with t(1;19)(q23;p13) acute lymphoblastic leukemia. Leukemia 7:1441-1444.
31. Pear, W. S., M. L. Scott, and G. P. Nolan. Methods for generating high titer, helper-free retroviruses by transient transfection. In P. Robbins (ed.), Gene therapy protocols, in press. Humana Press, Inc., Totowa, N.J.
32. Peers, B., S. Sharma, T. Johnson, M. Kamps, and M. Montminy. 1995. The pancreatic islet factor STF-1 binds cooperatively with Pbx to a regulatory element in the somatostatin promoter: importance of the FPWMK motif and of the homeodomain. Mol. Cell. Biol. 15:7091-7097.
33. Peifer, M. and E. Weischaus. 1990. Mutations in the Drosophila gene extradenticle affect the way specific homeodomain proteins regulate segmental identity. Genes Dev. 4:1209-1223.
34. 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.
35. Pöpperl, 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 hy a highly conserved autoregulatory loop dependent upon exd/pbx. Cell 81: 1031-1042.
36. Rauskolb, C., M. Peifer, and E. Weischaus. 1993. extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogcne PBX1. Cell 74:1101-1112.
37. Schulze, F., K. Chowdhury, A. Zimmer, U. Drescher, and P. Gruss. 1987. The murine homeobox gene product, Hox1.1 protein, is growth-controlled and associated with chromatin. Differentiation 36:130-137.
38. Shen, W.-F., C.-P. Chang, S. Rozenfeld, G. Sauvageau, R. K. Humphries, M. Lu, H. J. Lawrence, M. L. Cleary, and C. Largman. 1996 HOX homeodomain proteins exhibit selective complex stabilities with Pbx and DNA. Nucleic Acids Res. 24:898-906.
39. Smith, K. S., Y. Jacobs, C.-P. Chang, and M. L. Cleary. Chimeric oncoprotein E2a-Pbx1 induces apoptosis of hematopoietic cells by a p53-independent mechanism that is suppressed by Bcl-2. Submitted for publication.
40. van Dijk, M. A., and C. Murre. 1994. extradenticle raises the DNA binding specificity of homeotic selector gene products. Cell 78:617-624.
41. 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.