Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1995 Aug;15(8):3989–3997. doi: 10.1128/mcb.15.8.3989

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

M L Phelan 1, I Rambaldi 1, M S Featherstone 1
PMCID: PMC230638  PMID: 7623795

Abstract

Homeoprotein products of the Hox/HOM gene family pattern the animal embryo through the transcriptional regulation of target genes. We have previously shown that the labial group protein HOXA-1 has intrinsically weak DNA-binding activity due to residues in the N-terminal arm of its homeodomain (M. L. Phelan, R. Sadoul, and M. S. Featherstone, Mol. Cell. Biol. 14:5066-5075, 1994). This observation, among others, suggests that HOX and HOM proteins require cofactors for stable interactions with DNA. We have demonstrated that a putative HOX cofactor, PBX1A, participates in cooperative DNA binding with HOXA-1 and the Deformed group protein HOXD-4. Three Abdominal-B class HOX proteins failed to cooperate with PBX1A. We mapped the interacting domain of HOXD-4 to the YPWMK pentapeptide motif, a conserved sequence found N terminal to the homeodomain of HOXA-1 and many other homeoproteins but absent from the Abdominal-B class. The naturally occurring fusion of the transcriptional activation domain of E2A with PBX1 creates an oncoprotein implicated in human pre-B-cell leukemias (M. P. Kamps, C. Murre, X.-H. Sun, and D. Baltimore, Cell 60:547-555, 1990; J. Nourse, J. D. Mellentin, N. Galili, J. Wilkinson, E. Starbridge, S. D. Smith, and M. L. Cleary, Cell 60:535-545, 1990). A pentapeptide mutation that abolished cooperative interaction with PBX1A in vitro also abrogated synergistic transcriptional activation with the E2A/PBX oncoprotein. The direct contact of PBX family members by the HOX pentapeptide is likely to play an important role in developmental and oncogenic processes.

Full Text

The Full Text of this article is available as a PDF (495.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aberdam D., Negreanu V., Sachs L., Blatt C. The oncogenic potential of an activated Hox-2.4 homeobox gene in mouse fibroblasts. Mol Cell Biol. 1991 Jan;11(1):554–557. doi: 10.1128/mcb.11.1.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adra C. N., Boer P. H., McBurney M. W. Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene. 1987;60(1):65–74. doi: 10.1016/0378-1119(87)90214-9. [DOI] [PubMed] [Google Scholar]
  3. Affolter M., Percival-Smith A., Müller M., Leupin W., Gehring W. J. DNA binding properties of the purified Antennapedia homeodomain. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4093–4097. doi: 10.1073/pnas.87.11.4093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baron A., Featherstone M. S., Hill R. E., Hall A., Galliot B., Duboule D. Hox-1.6: a mouse homeo-box-containing gene member of the Hox-1 complex. EMBO J. 1987 Oct;6(10):2977–2986. doi: 10.1002/j.1460-2075.1987.tb02603.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bermingham J. R., Jr, Scott M. P. Developmentally regulated alternative splicing of transcripts from the Drosophila homeotic gene Antennapedia can produce four different proteins. EMBO J. 1988 Oct;7(10):3211–3222. doi: 10.1002/j.1460-2075.1988.tb03188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chan S. K., Jaffe L., Capovilla M., Botas J., Mann R. S. The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with extradenticle, another homeoprotein. Cell. 1994 Aug 26;78(4):603–615. doi: 10.1016/0092-8674(94)90525-8. [DOI] [PubMed] [Google Scholar]
  7. Condie B. G., Capecchi M. R. Mice with targeted disruptions in the paralogous genes hoxa-3 and hoxd-3 reveal synergistic interactions. Nature. 1994 Jul 28;370(6487):304–307. doi: 10.1038/370304a0. [DOI] [PubMed] [Google Scholar]
  8. Corsetti M. T., Briata P., Sanseverino L., Daga A., Airoldi I., Simeone A., Palmisano G., Angelini C., Boncinelli E., Corte G. Differential DNA binding properties of three human homeodomain proteins. Nucleic Acids Res. 1992 Sep 11;20(17):4465–4472. doi: 10.1093/nar/20.17.4465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cribbs D. L., Pultz M. A., Johnson D., Mazzulla M., Kaufman T. C. Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia. EMBO J. 1992 Apr;11(4):1437–1449. doi: 10.1002/j.1460-2075.1992.tb05188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dalton D., Chadwick R., McGinnis W. Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 1989 Dec;3(12A):1940–1956. doi: 10.1101/gad.3.12a.1940. [DOI] [PubMed] [Google Scholar]
  11. Davidson D. R., Crawley A., Hill R. E., Tickle C. Position-dependent expression of two related homeobox genes in developing vertebrate limbs. Nature. 1991 Aug 1;352(6334):429–431. doi: 10.1038/352429a0. [DOI] [PubMed] [Google Scholar]
  12. Dedera D. A., Waller E. K., LeBrun D. P., Sen-Majumdar A., Stevens M. E., Barsh G. S., Cleary M. L. Chimeric homeobox gene E2A-PBX1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell. 1993 Sep 10;74(5):833–843. doi: 10.1016/0092-8674(93)90463-z. [DOI] [PubMed] [Google Scholar]
  13. Dessain S., Gross C. T., Kuziora M. A., McGinnis W. Antp-type homeodomains have distinct DNA binding specificities that correlate with their different regulatory functions in embryos. EMBO J. 1992 Mar;11(3):991–1002. doi: 10.1002/j.1460-2075.1992.tb05138.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dollé P., Duboule D. Two gene members of the murine HOX-5 complex show regional and cell-type specific expression in developing limbs and gonads. EMBO J. 1989 May;8(5):1507–1515. doi: 10.1002/j.1460-2075.1989.tb03535.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dubé I. D., Kamel-Reid S., Yuan C. C., Lu M., Wu X., Corpus G., Raimondi S. C., Crist W. M., Carroll A. J., Minowada J. A novel human homeobox gene lies at the chromosome 10 breakpoint in lymphoid neoplasias with chromosomal translocation t(10;14). Blood. 1991 Dec 1;78(11):2996–3003. [PubMed] [Google Scholar]
  16. Duprey P., Chowdhury K., Dressler G. R., Balling R., Simon D., Guenet J. L., Gruss P. A mouse gene homologous to the Drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev. 1988 Dec;2(12A):1647–1654. doi: 10.1101/gad.2.12a.1647. [DOI] [PubMed] [Google Scholar]
  17. Ekker S. C., Jackson D. G., von Kessler D. P., Sun B. I., Young K. E., Beachy P. A. The degree of variation in DNA sequence recognition among four Drosophila homeotic proteins. EMBO J. 1994 Aug 1;13(15):3551–3560. doi: 10.1002/j.1460-2075.1994.tb06662.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ekker S. C., Young K. E., von Kessler D. P., Beachy P. A. Optimal DNA sequence recognition by the Ultrabithorax homeodomain of Drosophila. EMBO J. 1991 May;10(5):1179–1186. doi: 10.1002/j.1460-2075.1991.tb08058.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ekker S. C., von Kessler D. P., Beachy P. A. Differential DNA sequence recognition is a determinant of specificity in homeotic gene action. EMBO J. 1992 Nov;11(11):4059–4072. doi: 10.1002/j.1460-2075.1992.tb05499.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Erselius J. R., Goulding M. D., Gruss P. Structure and expression pattern of the murine Hox-3.2 gene. Development. 1990 Oct;110(2):629–642. doi: 10.1242/dev.110.2.629. [DOI] [PubMed] [Google Scholar]
  21. Featherstone M. S., Baron A., Gaunt S. J., Mattei M. G., Duboule D. Hox-5.1 defines a homeobox-containing gene locus on mouse chromosome 2. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4760–4764. doi: 10.1073/pnas.85.13.4760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fitzpatrick V. D., Percival-Smith A., Ingles C. J., Krause H. M. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature. 1992 Apr 16;356(6370):610–612. doi: 10.1038/356610a0. [DOI] [PubMed] [Google Scholar]
  23. Frankel A. D., Kim P. S. Modular structure of transcription factors: implications for gene regulation. Cell. 1991 May 31;65(5):717–719. doi: 10.1016/0092-8674(91)90378-c. [DOI] [PubMed] [Google Scholar]
  24. Gehring W. J., Qian Y. Q., Billeter M., Furukubo-Tokunaga K., Schier A. F., Resendez-Perez D., Affolter M., Otting G., Wüthrich K. Homeodomain-DNA recognition. Cell. 1994 Jul 29;78(2):211–223. doi: 10.1016/0092-8674(94)90292-5. [DOI] [PubMed] [Google Scholar]
  25. Gibson G., Schier A., LeMotte P., Gehring W. J. The specificities of Sex combs reduced and Antennapedia are defined by a distinct portion of each protein that includes the homeodomain. Cell. 1990 Sep 21;62(6):1087–1103. doi: 10.1016/0092-8674(90)90386-s. [DOI] [PubMed] [Google Scholar]
  26. Green S., Issemann I., Sheer E. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 1988 Jan 11;16(1):369–369. doi: 10.1093/nar/16.1.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hatano M., Roberts C. W., Minden M., Crist W. M., Korsmeyer S. J. Deregulation of a homeobox gene, HOX11, by the t(10;14) in T cell leukemia. Science. 1991 Jul 5;253(5015):79–82. doi: 10.1126/science.1676542. [DOI] [PubMed] [Google Scholar]
  28. Hill R. E., Jones P. F., Rees A. R., Sime C. M., Justice M. J., Copeland N. G., Jenkins N. A., Graham E., Davidson D. R. A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. Genes Dev. 1989 Jan;3(1):26–37. doi: 10.1101/gad.3.1.26. [DOI] [PubMed] [Google Scholar]
  29. Hu Y., Kazenwadel J., James R. Isolation and characterization of the murine homeobox gene Cdx-1. Regulation of expression in intestinal epithelial cells. J Biol Chem. 1993 Dec 25;268(36):27214–27225. [PubMed] [Google Scholar]
  30. Izpisúa-Belmonte J. C., Falkenstein H., Dollé P., Renucci A., Duboule D. Murine genes related to the Drosophila AbdB homeotic genes are sequentially expressed during development of the posterior part of the body. EMBO J. 1991 Aug;10(8):2279–2289. doi: 10.1002/j.1460-2075.1991.tb07764.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. James R., Erler T., Kazenwadel J. Structure of the murine homeobox gene cdx-2. Expression in embryonic and adult intestinal epithelium. J Biol Chem. 1994 May 27;269(21):15229–15237. [PubMed] [Google Scholar]
  32. Johnson F. B., Parker E., Krasnow M. A. Extradenticle protein is a selective cofactor for the Drosophila homeotics: role of the homeodomain and YPWM amino acid motif in the interaction. Proc Natl Acad Sci U S A. 1995 Jan 31;92(3):739–743. doi: 10.1073/pnas.92.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Jonsson J., Carlsson L., Edlund T., Edlund H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature. 1994 Oct 13;371(6498):606–609. doi: 10.1038/371606a0. [DOI] [PubMed] [Google Scholar]
  34. Kamps M. P., Baltimore D. 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. 1993 Jan;13(1):351–357. doi: 10.1128/mcb.13.1.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kamps M. P., Look A. T., Baltimore D. The human t(1;19) translocation in pre-B ALL produces multiple nuclear E2A-Pbx1 fusion proteins with differing transforming potentials. Genes Dev. 1991 Mar;5(3):358–368. doi: 10.1101/gad.5.3.358. [DOI] [PubMed] [Google Scholar]
  36. Kamps M. P., Murre C., Sun X. H., Baltimore D. A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL. Cell. 1990 Feb 23;60(4):547–555. doi: 10.1016/0092-8674(90)90658-2. [DOI] [PubMed] [Google Scholar]
  37. Kappen C., Schughart K., Ruddle F. H. Early evolutionary origin of major homeodomain sequence classes. Genomics. 1993 Oct;18(1):54–70. doi: 10.1006/geno.1993.1426. [DOI] [PubMed] [Google Scholar]
  38. Kennedy M. A., Gonzalez-Sarmiento R., Kees U. R., Lampert F., Dear N., Boehm T., Rabbitts T. H. HOX11, a homeobox-containing T-cell oncogene on human chromosome 10q24. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8900–8904. doi: 10.1073/pnas.88.20.8900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kornfeld K., Saint R. B., Beachy P. A., Harte P. J., Peattie D. A., Hogness D. S. Structure and expression of a family of Ultrabithorax mRNAs generated by alternative splicing and polyadenylation in Drosophila. Genes Dev. 1989 Feb;3(2):243–258. doi: 10.1101/gad.3.2.243. [DOI] [PubMed] [Google Scholar]
  40. Krumlauf R. Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet. 1993 Apr;9(4):106–112. doi: 10.1016/0168-9525(93)90203-t. [DOI] [PubMed] [Google Scholar]
  41. Kuziora M. A., McGinnis W. Altering the regulatory targets of the Deformed protein in Drosophila embryos by substituting the Abdominal-B homeodomain. Mech Dev. 1990 Dec;33(1):83–93. doi: 10.1016/0925-4773(90)90137-b. [DOI] [PubMed] [Google Scholar]
  42. LaRosa G. J., Gudas L. J. 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. 1988 Sep;8(9):3906–3917. doi: 10.1128/mcb.8.9.3906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lawrence H. J., Largman C. Homeobox genes in normal hematopoiesis and leukemia. Blood. 1992 Nov 15;80(10):2445–2453. [PubMed] [Google Scholar]
  44. LeBrun D. P., Cleary M. L. Fusion with E2A alters the transcriptional properties of the homeodomain protein PBX1 in t(1;19) leukemias. Oncogene. 1994 Jun;9(6):1641–1647. [PubMed] [Google Scholar]
  45. Li P., He X., Gerrero M. R., Mok M., Aggarwal A., Rosenfeld M. G. Spacing and orientation of bipartite DNA-binding motifs as potential functional determinants for POU domain factors. Genes Dev. 1993 Dec;7(12B):2483–2496. doi: 10.1101/gad.7.12b.2483. [DOI] [PubMed] [Google Scholar]
  46. Lin L., McGinnis W. Mapping functional specificity in the Dfd and Ubx homeo domains. Genes Dev. 1992 Jun;6(6):1071–1081. doi: 10.1101/gad.6.6.1071. [DOI] [PubMed] [Google Scholar]
  47. Lu Q., Wright D. D., Kamps M. P. 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. 1994 Jun;14(6):3938–3948. doi: 10.1128/mcb.14.6.3938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mann R. S., Hogness D. S. Functional dissection of Ultrabithorax proteins in D. melanogaster. Cell. 1990 Feb 23;60(4):597–610. doi: 10.1016/0092-8674(90)90663-y. [DOI] [PubMed] [Google Scholar]
  49. Maulbecker C. C., Gruss P. The oncogenic potential of deregulated homeobox genes. Cell Growth Differ. 1993 May;4(5):431–441. [PubMed] [Google Scholar]
  50. Mavilio F., Simeone A., Giampaolo A., Faiella A., Zappavigna V., Acampora D., Poiana G., Russo G., Peschle C., Boncinelli E. Differential and stage-related expression in embryonic tissues of a new human homoeobox gene. Nature. 1986 Dec 18;324(6098):664–668. doi: 10.1038/324664a0. [DOI] [PubMed] [Google Scholar]
  51. Mlodzik M., Gehring W. J. Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell. 1987 Feb 13;48(3):465–478. doi: 10.1016/0092-8674(87)90197-8. [DOI] [PubMed] [Google Scholar]
  52. Monaghan A. P., Davidson D. R., Sime C., Graham E., Baldock R., Bhattacharya S. S., Hill R. E. The Msh-like homeobox genes define domains in the developing vertebrate eye. Development. 1991 Aug;112(4):1053–1061. doi: 10.1242/dev.112.4.1053. [DOI] [PubMed] [Google Scholar]
  53. Monica K., Galili N., Nourse J., Saltman D., Cleary M. L. PBX2 and PBX3, new homeobox genes with extensive homology to the human proto-oncogene PBX1. Mol Cell Biol. 1991 Dec;11(12):6149–6157. doi: 10.1128/mcb.11.12.6149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Monica K., LeBrun D. P., Dedera D. A., Brown R., Cleary M. L. Transformation properties of the E2a-Pbx1 chimeric oncoprotein: fusion with E2a is essential, but the Pbx1 homeodomain is dispensable. Mol Cell Biol. 1994 Dec;14(12):8304–8314. doi: 10.1128/mcb.14.12.8304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Nourse J., Mellentin J. D., Galili N., Wilkinson J., Stanbridge E., Smith S. D., Cleary M. L. Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell. 1990 Feb 23;60(4):535–545. doi: 10.1016/0092-8674(90)90657-z. [DOI] [PubMed] [Google Scholar]
  56. O'Connor M. B., Binari R., Perkins L. A., Bender W. Alternative RNA products from the Ultrabithorax domain of the bithorax complex. EMBO J. 1988 Feb;7(2):435–445. doi: 10.1002/j.1460-2075.1988.tb02831.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ohlsson H., Karlsson K., Edlund T. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J. 1993 Nov;12(11):4251–4259. doi: 10.1002/j.1460-2075.1993.tb06109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Peifer M., Wieschaus E. Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev. 1990 Jul;4(7):1209–1223. doi: 10.1101/gad.4.7.1209. [DOI] [PubMed] [Google Scholar]
  59. Pellerin I., Schnabel C., Catron K. M., Abate C. 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. 1994 Jul;14(7):4532–4545. doi: 10.1128/mcb.14.7.4532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Perkins A., Kongsuwan K., Visvader J., Adams J. M., Cory S. Homeobox gene expression plus autocrine growth factor production elicits myeloid leukemia. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8398–8402. doi: 10.1073/pnas.87.21.8398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Phelan M. L., Sadoul R., Featherstone M. S. Functional differences between HOX proteins conferred by two residues in the homeodomain N-terminal arm. Mol Cell Biol. 1994 Aug;14(8):5066–5075. doi: 10.1128/mcb.14.8.5066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Phillips C. L., Stark M. R., Johnson A. D., Dahlquist F. W. Heterodimerization of the yeast homeodomain transcriptional regulators alpha 2 and a1 induces an interfacial helix in alpha 2. Biochemistry. 1994 Aug 9;33(31):9294–9302. doi: 10.1021/bi00197a033. [DOI] [PubMed] [Google Scholar]
  63. Pöpperl H., Featherstone M. S. An autoregulatory element of the murine Hox-4.2 gene. EMBO J. 1992 Oct;11(10):3673–3680. doi: 10.1002/j.1460-2075.1992.tb05452.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Qian Y. Q., Otting G., Furukubo-Tokunaga K., Affolter M., Gehring W. J., Wüthrich K. 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 U S A. 1992 Nov 15;89(22):10738–10742. doi: 10.1073/pnas.89.22.10738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rambaldi I., Kovàcs E. N., Featherstone M. S. A proline-rich transcriptional activation domain in murine HOXD-4 (HOX-4.2). Nucleic Acids Res. 1994 Feb 11;22(3):376–382. doi: 10.1093/nar/22.3.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Rauskolb C., Peifer M., Wieschaus E. extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogene pbx1. Cell. 1993 Sep 24;74(6):1101–1112. doi: 10.1016/0092-8674(93)90731-5. [DOI] [PubMed] [Google Scholar]
  67. Rauskolb C., Wieschaus E. Coordinate regulation of downstream genes by extradenticle and the homeotic selector proteins. EMBO J. 1994 Aug 1;13(15):3561–3569. doi: 10.1002/j.1460-2075.1994.tb06663.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Robert B., Sassoon D., Jacq B., Gehring W., Buckingham M. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J. 1989 Jan;8(1):91–100. doi: 10.1002/j.1460-2075.1989.tb03352.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Roberts C. W., Shutter J. R., Korsmeyer S. J. Hox11 controls the genesis of the spleen. Nature. 1994 Apr 21;368(6473):747–749. doi: 10.1038/368747a0. [DOI] [PubMed] [Google Scholar]
  70. Rosenberg A. H., Lade B. N., Chui D. S., Lin S. W., Dunn J. J., Studier F. W. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 1987;56(1):125–135. doi: 10.1016/0378-1119(87)90165-x. [DOI] [PubMed] [Google Scholar]
  71. Sasaki H., Yokoyama E., Kuroiwa A. Specific DNA binding of the two chicken Deformed family homeodomain proteins, Chox-1.4 and Chox-a. Nucleic Acids Res. 1990 Apr 11;18(7):1739–1747. doi: 10.1093/nar/18.7.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Satokata I., Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet. 1994 Apr;6(4):348–356. doi: 10.1038/ng0494-348. [DOI] [PubMed] [Google Scholar]
  73. Simeone A., Gulisano M., Acampora D., Stornaiuolo A., Rambaldi M., Boncinelli E. Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 1992 Jul;11(7):2541–2550. doi: 10.1002/j.1460-2075.1992.tb05319.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Slack J. M., Holland P. W., Graham C. F. The zootype and the phylotypic stage. Nature. 1993 Feb 11;361(6412):490–492. doi: 10.1038/361490a0. [DOI] [PubMed] [Google Scholar]
  75. Smith D. L., Johnson A. D. A molecular mechanism for combinatorial control in yeast: MCM1 protein sets the spacing and orientation of the homeodomains of an alpha 2 dimer. Cell. 1992 Jan 10;68(1):133–142. doi: 10.1016/0092-8674(92)90212-u. [DOI] [PubMed] [Google Scholar]
  76. Suh E., Chen L., Taylor J., Traber P. G. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol. 1994 Nov;14(11):7340–7351. doi: 10.1128/mcb.14.11.7340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Van Dijk M. A., Voorhoeve P. M., Murre C. 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 U S A. 1993 Jul 1;90(13):6061–6065. doi: 10.1073/pnas.90.13.6061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Vershon A. K., Jin Y., Johnson A. D. A homeo domain protein lacking specific side chains of helix 3 can still bind DNA and direct transcriptional repression. Genes Dev. 1995 Jan 15;9(2):182–192. doi: 10.1101/gad.9.2.182. [DOI] [PubMed] [Google Scholar]
  79. Vershon A. K., Johnson A. D. A short, disordered protein region mediates interactions between the homeodomain of the yeast alpha 2 protein and the MCM1 protein. Cell. 1993 Jan 15;72(1):105–112. doi: 10.1016/0092-8674(93)90054-t. [DOI] [PubMed] [Google Scholar]
  80. Wolberger C., Vershon A. K., Liu B., Johnson A. D., Pabo C. O. Crystal structure of a MAT alpha 2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell. 1991 Nov 1;67(3):517–528. doi: 10.1016/0092-8674(91)90526-5. [DOI] [PubMed] [Google Scholar]
  81. van Dijk M. A., Murre C. extradenticle raises the DNA binding specificity of homeotic selector gene products. Cell. 1994 Aug 26;78(4):617–624. doi: 10.1016/0092-8674(94)90526-6. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES