Auto-inhibition and partner proteins, core-binding factor β (CBFβ) and Ets-1, modulate DNA binding by CBFα2 (AML1)

Molecular and Cellular Biology

Volumn 20, Issue 1, 2000, Pages 91-103

  Gu, Ting Lei ^a   Goetz, Tamara L ^b   Graves, Barbara J ^b   Speck, Nancy A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; DIMERIZATION; DNA BINDING; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; QUANTITATIVE ASSAY; REGULATORY MECHANISM;

ANIMALIA; MAMMALIA;

EID: 0033988402     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.1.91-103.2000     Document Type: Article

References (87)

1. Adja, N., T. Stacy, N. A. Speck, and P. P. Liu. 1998. The leukemic protein CBFβ-S.MMHC sequesters CBFα2 into cytoskeletal filaments and aggregates. Mol. Cell. Biol. 18:7432-7443.
2. Albagli, O., A. Klaes, E. Ferreira, D. Leprince, and C. Klambt. 1996. Function of ets genes is conserved between vertebrates and Drosophila. Mech. Dev. 59:29-40.
3. Bae, S.-C., E. Ogawa, M. Maruyama, H. Oka, M. Satake, K. Shigesada, N. A. Jenkins, D. J. Gilbert, N. G. Copeland, and Y. Ito. 1994. PEBP2αB/mouse AML1 consists of multiple isoforms that possess differential transactivation potentials. Mol. Cell. Biol. 14:3242-3252.
4. Bae, S.-C., E. Takahashi, Y. W. Zhang, E. Ogawa, K. Shigesada, Y. Namba, M. Satake, and Y. Ito. 1995. Cloning, mapping and expression of PEBP2αC, a third gene encoding the mammalian Runt domain. Gene 159:245-248.
5. Bae, S. C., Y. Yamaguchi-Iwai, E. Ogawa, M. Maruyama, M. Inuzuka, H. Kagoshima, K. Shigesada, M. Satake, and Y. Ito. 1993. Isolation of PEBP2αB cDNA representing the mouse homolog of human acute myeloid leukemia gene, AML1. Oncogene 8:809-814.
6. Barton, K., N. Muthusamy, C. Fischer, C. N. Ting, T. L. Walunas, L. L. Lanier, and J. M. Leiden. 1998, The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 9:555-563.
7. Ben-David, U., E. B. Giddens, K. Letwin, and A. Bernstein. 1991. Erythroleukemia induction by Friend murine leukemia virus: insertional activation of a new member of the ets gene family, Fli-1, closely linked to c-ets-1. Genes Dev. 5:908-918.
8. Berardi, M., C. Sun, M. Zehr, F. Abildgaard, J. Peng, N. A. Speck, and J. H. Bushweller. 1999. The Ig fold of the core binding factor α Runt domain is a member of a family of structurally and functionally related Ig fold DNA binding domains. Structure 7:1247-1256.
9. Bories, J. C., D. M. Willerford, D. Grevin, L. Davidson, A. Camus, P. Martin, D. Stehelin, and F. W. Alt. 1995. Increased T-cell apoptosis and terminal B-cell differentiation induced by inactivation of the Ets-1 proto-oncogene. Nature 377:635-638.
10. Brass, A. L., E. Kehrli, C. F. Eisenbeis, U. Storb, and H. Singh. 1996. Pip, a lymphoid-restricted IRF, contains a regulatory domain that is important for autoinhibition and ternary complex formation with the ets factor PU. 1. Genes Dev. 10:2335-2347.
11. Brunner, D., K. Ducker, N. Oellers, E. Hafen, H. Scholz, and C. Klambt. 1994. The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370:386-389.
12. Crute, B. E., A. F. Lewis, Z. Wu, J. H. Bushweller, and N. A. Speck. 1996. Biochemical and biophysical properties of the CBFa2 (AML1) DNA-binding domain. J. Biol. Chem. 271:26251-26260.
13. Daga, A., C. A. Karlovich, K. Dumstrei, and U. Banerjee. 1996. Patterning of cells in the Drosophila eye by Lozenge, which shares homologous domains with AML1. Genes Dev. 10:1194-1205.
14. Dalton, S., and R. Treisman. 1992. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell 68:597-612.
15. Dignam, J. D., R. M. Lebowitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
16. Duffy, J. B., and J. P. Gergen. 1991. The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal. Genes Dev. 5:2176-2187.
17. Duffy, J. B., M. A. Kania, and J. P. Gergen. 1991. Expression and function of the Drosophila gene ntnt in early stages of neural development. Development 113:1223-1230.
18. Erman, B., M. Cortes, N. A. Speck, and R. Sen. 1998. ETS-core binding factor: a common composite motif in antigen receptor gene enhancers. Mol. Cell. Biol. 18:1322-1330.
19. Giese, K., C. Kingsley, J. R. Kirshner, and R. Grosschedl. 1995. Assembly and function of a TCRα enhancer complex is dependent on LEF-1-induced DNA binding and multiple protein-protein interactions. Genes Dev. 9:995-1008.
20. Goetz, T. L., T. L. Gu, N. A. Speck, and B. J. Graves. 1999. Auto-inhibition of Ets-1 is counteracted by DNA binding cooperativity with core-binding factor α2. Mol. Cell. Biol. 20:81-90.
21. Goger, M., V. Gupta, W.-Y. Kim, K. Shigesada, Y. Ito, and M. H. Werner. 1999. Molecular insights into PEBP2/CBFβ-SMMHC associated acute leukemia revealed from the three-dimensional structure of PEBP2/CBFβ. Nat. Struct. Biol. 6:620-623.
22. Golling, G., L.-H. Li, M. Pepling, M. Stebbins, and J. P. Gergen. 1996. Drosophila homologues of proto-oncogene product PEBP2/CBFβ regulate the DNA-binding properties of Runt. Mol. Cell. Biol. 16:932-942.
23. Golub, T. R., G. F. Barker, S. K. Bohlander, S. Hiebert, D. C. Ward, P. Bray-Ward, E. Morgan, S. C. Raimondi, J. D. Rowley, and D. G. Gilliland. 1995. Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 92:4917-4921.
24. Graves, B. J., D. O. Cowley, T. L. Goetz, J. M. Petersen, M. D. Jonsen, and M. E. Gillespie. 1998. Autoinhibition as a transcriptional regulatory mechanism. Cold Spring Harbor Symp. Quant. Biol. 63:621-629.
25. Graves, B. J., and J. M. Peterson. 1998. Specificity within the ets family of transcription factors. Adv. Cancer Res. 75:1-55.
26. Huang, X., B. E. Crute, C. Sun, Y.-Y. Tang, J. J. Kelley III, A. F. Lewis, K. L. Hartman, T. M. Laue, N. A. Speck, and J. H. Bushweller. 1998. Overexpression, purification, and biophysical characterization of the heterodimerization domain of the core-binding factor β subunit. J. Biol. Chem. 273:2480-2487.
27. Huang, X., J. W. Peng, N. A. Speck, and J. H. Bushweller. 1999. Core binding factor β revealed: solution structure and map of the CBFα binding site. Nat. Struct. Biol. 6:624-627.
28. Ingham. P., and P. Gergen. 1988. Interactions between the pair-rule genes runt, hairy, even-skipped and fushi tarazu and the establishment of periodic pattern in the Drosophila embryo. Development 104(Suppl.):51-60.
29. Jonsen, M. D., J. M. Petersen, Q.-P. Xu, and B. J. Graves. 1996. Characterization of cooperative function of inhibitory sequences in Ets-1. Mol. Cell. Biol. 16:2065-2073.
30. Kagoshima, H., Y. Akamatsu, Y. Ito, and K. Shigesada. 1996. Functional dissection of the a and β subunits of the transcription factor PEBP2 and the redox susceptibility of its DNA binding activity. J. Biol. Chem. 271:33074-33082.
31. Kagoshima, H., K. Shigesada, M. Satake, Y. Ito, H. Miyoshi, M. Ohki, M. Pepling, and J. P. Gergen. 1993. The Runt-domain identifies a new family of heteromeric DNA-binding transcriptional regulatory proteins. Trends Genet. 9:338-341.
32. Kanno, T., Y. Kanno, L.-F. Chen, E. Ogawa, W.-Y. Kim, and Y. Ito. 1998. Intrinsic transcriptional activation-inhibition domains of the polyomavirus enhancer binding protein 2/core binding factor a subunit revealed in the presence of the β subunit. Mol. Cell. Biol. 18:2444-2454.
33. Kim, W.-Y., M. Sieweke, E. Ogawa, H.-J. Wee, U. Englmeier, T. Graf, and Y. Ito. 1999. Mutual activation of Ets-1 and AML1 DNA binding by direct interaction of their autoinhibitory domains. EMBO J. 18:1609-1620.
34. Komori, T., H. Yagi, S. Nomura, A. Yamaguchi, K. Sasaki, K. Deguchi, Y. Shimizu, R. T. Bronson, Y.-H. Gao, M. Inada, M. Sato, R. Okamoto, Y. Kitamura, S. Yoshiki, and T. Kishimoto. 1997. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764.
35. Leprince, D., A. Gegonne, J. Coll, C. de Taisne, A. Schneeberger, C. Lagrou, and D. Stehelin. 1983. A putative second cell-derived oncogene of the avian leukaemia retrovirus E26. Nature 306:395-397.
36. Levanon, D., V. Negreanu, Y. Bernstein, I. Bar-Am, L. Avivi, and Y. Groner. 1994. AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics 23:425-432.
37. Li, L. H., and J. P. Gergen. 1999. Differential interactions between Brother proteins and Runt domain proteins in the Drosophila embryo and eye. Development 126:3313-3322.
38. Ling, Y., J. H. Lakey, C. E. Roberts, and A. D. Sharrocks. 1997. Molecular characterization of the B-box protein-protein interaction motif of the ETS-domain transcription factor Elk-1. EMBO J. 16:2431-2440.
39. Liu, P., S. A. Tarle, A. Hajra, D. F. Claxton, P. Marlton, M. Freedman, M. J. Siciliano, and F. S. Collins. 1993. Fusion between transcription factor CBFβ/PEBP2β and a myosin heavy chain in acute myeloid leukemia. Science 261:1041-1044.
40. Lu, J., M. Maruyama, M. Satake, S.-C. Bae, E. Ogawa, H. Kagoshima, K. Shigesada, and Y. Ito. 1995. Subcellular localization of the α and β subunits of acute myeloid leukemia-linked transcription factor PEBP2/CBF. Mol. Cell. Biol. 15:1651-1661.
41. Mayall, T. P., P. L. Sheridan, M. R. Montminy, and K. A. Jones. 1997. Distinct roles for P-CREB and LEF-1 in TCR enhancer assembly and activation on chromatin templates in vitro. Genes Dev. 11:887-899.
42. McKercher, S. R., B. E. Torbett, K. L. Anderson, G. W. Henkel, D. J. Vestal, H. Baribault, M. Klemsz, A. J. Feeney, G. E. Wu, C. J. Paige, and R. A. Maki. 1996. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15:5647-5658.
43. McLean, T. W., S. Ringold, D. Neuberg, K. Stegmaier, R. Tantravahi, J. Ritz, H. P. Koeffler, S. Takeuchi, J. W. Janssen, T. Seriu, C. R. Bartram, S. E. Sallan, D. G. Gilliland, and T. R. Golub. 1996. TEL/AML-1 dimerizes and is associated with a favorable outcome in childhood acute lymphoblastic leukemia. Blood 88:4252-4258.
44. Melet, F., B. Motro, D. J. Rossi, L. Zhang, and A. Bernstein. 1996. Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia. Mol. Cell. Biol. 16:2708-2718.
45. Meyers, S., J. R. Downing, and S. W. Hiebert. 1993. Identification of AML-1 and the (8;21) translocalion protein (AML-1/ETO) as sequence-specific DNA-binding proteins: the runt homology domain is required for DNA binding and protein-protein interactions. Mol. Cell. Biol. 13:6336-6345.
46. Meyers, S., N. Lenny, and S. W. Hiebert. 1995. The t(8;21) fusion protein interferes with AML1-1B-dependent transcriptional activation. Mol. Cell. Biol. 15:1974-1982.
47. Miyoshi, H., M. Ohira, K. Shimizu, K. Mitani, H. Hirai, T. Imai, K. Yokoyama, E. Soeda, and M. Ohki. 1995. Alternative splicing and genomic structure of the AML1 gene involved in acute myeloid leukemia. Nucleic-Acids Res. 23:2762-2769.
48. Miyoshi, H., K. Shimizu, T. Kozu, N. Maseki, Y. Kaneko, and M. Ohki. 1991. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc. Natl. Acad. Sci. USA 88:10431-10434.
49. Moreau-Gachelin, F., A. Tavitian, and P. Tambourin. 1988. Spi-1 is a putative oncogene in virally induced murine erythroleukaemias. Nature 331:277-280.
50. Muthusaniv, N., K. Barton, and J. M. Leiden. 1995. Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature 377:639-642.
51. Nagata, T., V. Gupta, D. Sorce, W.-Y. Kim, A. Sali, B. T. Chait, K. Shigesada, Y. Ito, and M. H. Werner. 1999. Immunoglobulin motif DNA-binding and heterodimerization for the PEBP2/CBF Runt-domain. Nat. Struct. Biol. 6:615-619.
52. Niki, M., H. Okada, H. Takano, J. Kuno, K. Tani, H. Hibino, S. Asano, Y. Ito, M. Satake, and T. Noda. 1997. Hematopoiesis in the fetal liver is impaired by targeted mutagenesis of a gene encoding a non-DNA binding subunit of the transcription factor, polyomavirus enhancer binding protein 2/core binding factor. Proc. Natl. Acad. Sci. USA 94:5697-5702.
53. North, T. E., T.-L. Gu, T. Stacy, Q. Wang, L. Howard, M. Binder, M. Marin-Padilla, and N. A. Speck. 1999. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 126:2563-2575.
54. Nunn, M. F., P. H. Seeberg, C. Moscovici, and P. H. Duesberg. 1983. Tripartite structure of the avian erythroblastosis virus E26 transforming gene. Nature 306:391-395.
55. Nye, J. A., J. M. Petersen, C. V. Gunther, M. D. Jonsen, and B. J. Graves. 1992. Interaction of murine Ets-1 with GGA-binding sites establishes the ETS domain as a new DNA-binding motif. Genes Dev. 6:975-990.
56. Ogawa, E., M. Inuzuka, M. Maruyama, M. Satake, M. Naito-Fujimoto, Y. Ito, and K. Shigesada. 1993. Molecular cloning and characterization of PEBP2β, the heterodimeric partner of a novel Drosophila runt-related DNA binding protein PEBP2α. Virology 194:314-331.
57. Ogawa, E., M. Maruyama, H. Kagoshima, M. Inuzuka, J. Lu, M. Satake, K. Shigesada, and Y. Ito. 1993. PEBP2/PEA2 represents a new family of transcription factor homologous to the products of the Drosophila runt and the human AML1 gene. Proc. Natl. Acad. Sci. USA 90:6859-6863.
58. Okuda, T., J. van Deursen, S. W. Hiebert, G. Grosveld, and J. R. Downing. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321-330.
59. O'Neill, E. M., I. Rebay, R. Tjian, and G. M. Rubin. 1994. The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78:137-147.
60. Otto, F., A. P. Thornell, T. Crompton, A. Denzel, K. C. Gilmour, I. R. Rosewell, G. W. H. Stamp, R. S. P. Beddington, S. Mundlos, B. R. Olsen, P. B. Selby, and M. J. Owen. 1997. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osleoblast differentiation and bone development. Cell 89:765-772.
61. Petersen, J. M., J. J. Skalicky, L. W. Donaldson, L. P. McIntosh, T. Alber, and B. J. Graves. 1995. Modulation of transcription factor Ets-1 DNA binding: DNA-induced unfolding of an alpha helix. Science 269:1866-1869.
62. Petrovick, M. S., S. W. Hiebert, A. D. Friedman, C. J. Hetherington, T. G. Tenen, and D.-E. Zhang. 1998. Multiple functional domains of AML1: PU.1 and C/EBPα synergize with different regions of AML1. Mol. Cell. Biol. 18:3915-3925.
63. Rabbitts, T. H. 1994. Chromosomal translocations in human cancer. Nature 372:143-149.
64. Rizki, T. M., R. M. Rizki, and R. Bellotti. 1985. Genetics of a Drosophila phenoloxidase. Mol. Gen. Genet. 201:7-13.
65. Romana, S. P., M. Mauchauffe, M. Le Coniat, I. Chumakow, D. Le Paslier, R. Berger, and O. A. Bernard. 1995. The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85:3662-3670.
66. Romana, S. P., H. Poirel, M. Leconiat, M.-A. Flexor, M. Mauchauffé, P. Jonveaux, E. A. Macintyre, R. Berger, and O. A. Bernard. 1995. High frequency of t(12;21) in childhood B-lineage acute lymphoblastic leukemia. Blood 86:4263-4269.
67. Sanchez, L., and R. Nothiger. 1983. Sex determination and dosage compensation in Drosophila melanogaster, production of male clones in XX females. EMBO J. 2:485-491.
68. Sasaki, K., H. Yagi, R. T. Bronson, K. Tominaga, T. Matsunashi, K. Deguchi, Y. Tani, T. Kishimoto, and T. Komori. 1996 Absence of fetal liver hematopoiesis in transcriptional co-activator, core binding factor β (Cbfb) deficient mice. Proc. Natl. Acad. Sci. USA 93:12359-12363.
69. Sato, M., E. Morii, T. Komori, H. Kawahata, M. Sugimoto, K. Terai, H. Shimizu, Y. Yasui, H. Ogihara, N. Yasui, T. Ochi, Y. Kitamura, Y. Ito, and S. Nomura. 1998. Transcriptional regulation of osteopontin gene in vivo by PEBP2αA;CBFA1 and ETS1 in the skeletal tissues. Oncogene 17:1517-1525.
70. Scott, E. W., M. C. Simon, J. Anastasi, and H. Singh. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265:1573-1577.
71. Sharrocks, A. D., A. L. Brown, Y. Ling, and P. R. Yates. 1998. The Ets-domain transcription factor family. Internat. J. Biochem. 29:1371-1387.
72. Shurtleff, S. A., A. Buijs, F. G. Behm, J. E. Rubnitz, S. C. Raimondi, M. L. Hancock, G. C.-F. Chan, C.-H. Pui, G. Grosveld, and J. R. Downing. 1995. TEL/AML1 fusion resulting from a cryptic t(12;21) is the most common genetic lesion in pediatric ALL and defines a subgroup of patients with an excellent prognosis. Leukemia 9:1985-1989.
73. Skalicky, J. J., L. W. Donaldson, J. M. Petersen, B. J. Graves, and L. P. McIntosh. 1996. Structural coupling of the inhibitory regions flanking the ETS domain of murine Ets-1. Protein Sci. 5:296-309.
74. Speck, N. A., and D. Baltimore. 1987. Six distinct nuclear factors interact with the 75-base-pair repeat of the Moloney murine leukemia virus enhancer. Mol. Cell. Biol. 7:1101-1110.
75. Speck, N. A., and T. Stacy. 1995. A new transcription factor family associated with human leukemias. Crit. Rev. Eukaryotic Gene Expr. 5:337-364.
76. Stewart, M., A. Terry, M. Hu, M. O'Hara, K. Blyth, E. Baxter, E. Cameron, D. E. Onions, and J. C. Neil. 1997. Proviral insertions induce the expression of bone-specific isoforms of PEBP2αA (CBFA1): evidence for a new myc collaborating oncogene. Proc. Natl. Acad. Sci. USA 94:8646-8651.
77. 3, a Drosophila mutant lacking basiconic antennal sensilla. Dev. Biol. 127:12-27.
78. Sun, W., B. J. Graves, and N. A. Speck. 1995. Transactivation of the Moloney murine leukemia virus and T-cell receptor β-chain enhancers by cbf/and ets requires intact binding sites for both proteins. J. Virol. 69:4941-4949.
79. Tanaka, K., T. Tanaka, M. Kurokawa, Y. Imai, S. Ogawa, K. Mitani, Y. Yazaki, and H. Hirai. 1998. The AML/ETO(MTG8) and AML1/Evi-1 leukemia-associated chimeric oncoproteins accumulate PEBP2β(CBFβ) in the nucleus more efficiently than wild-type AML1. Blood 91:1688-1699.
80. Thirunavukkarasu, K., M. Mahajan, K. W. McLarren, S. Stifani, and G. Karsenty. 1998. Two domains unique to osteoblast-specific transcription factor Osf2/Cbfa1 contribute to its transactivation function and its inability to heterodimerize with Cbfβ. Mol. Cell. Biol. 18:4197-4208.
81. Thornell, A., B. Hallberg, and T. Grundstrom. 1991. Binding of SL3-3 enhancer factor 1 transcriptional activators to viral and chromosomal enhancer sequences. J. Virol. 65:42-50.
82. Wang, Q., T. Stacy, M. Binder, M. Marín-Padilla, A. H. Sharpe, and N. A. Speck. 1996. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. USA 93:3444-3449.
83. Wang, Q., T. Stacy, J. D. Miller, A. F. Lewis, X. Huang, J.-C. Bories, J. H. Bushweller, F. W. Alt, M. Binder, M. Marin-Padilla, A. Sharpe, and N. A. Speck. 1996. The CBFβ subunit is essential for CBFα2 (AML1) function in vivo. Cell 87:697-708.
84. Wang, S., and N. A. Speck. 1992. Purification of core-binding factor, a protein that binds the conserved core site in murine leukemia virus enhancers. Mol. Cell. Biol. 12:89-102.
85. Wang, S., Q. Wang, B. E. Crute, I. N. Melnikova, S. R. Keller, and N. A. Speck. 1993. Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol. Cell. Biol. 13:3324-3339.
86. Wotton, D., J. Ghysdael, S. Wang, N. A. Speck, and M. J. Owen. 1994. Cooperative binding of Ets-1 and core binding factor to DNA. Mol. Cell. Biol. 14:840-850.
87. Zeng, C., A. J. Van Wignen, J. L. Stein, S. Meyers, W. Sun, L. Shopland, J. B. Lawrence, S. Penman, J. B. Lian, G. S. Stein, and S. W. Hiebert. 1997. Identification of a nuclear matrix targeting signal in the leukemia and bone-related AML/CBF-α transcription factors. Proc. Natl. Acad. Sci. USA 94: 6746-6751.