DOI: 10.1073/pnas.94.16.8732. MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukemia with a t(11;16)(q23;p13.3)

MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukemia with a t(11;16)(q23;p13.3)

10.1073/pnas.94.16.8732

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The recurring translocation t(11;16)(q23;p13.3) has been documented only in cases of acute leukemia or myelodysplasia secondary to therapy with drugs targeting DNA topoisomerase II. We show that the MLL gene is fused to the gene that codes for CBP (CREB-binding protein), the protein that binds specifically to the DNA-binding protein CREB (cAMP response element-binding protein) in this translocation. MLL is fused in-frame to a different exon of CBP in two patients producing chimeric proteins containing the AT-hooks, methyltransferase homology domain, and transcriptional repression domain of MLL fused to the CREB binding domain or to the bromodomain of CBP. Both fusion products retain the histone acetyltransferase domain of CBP and may lead to leukemia by promoting histone acetylation of genomic regions targeted by the MLL AT-hooks, leading to transcriptional deregulation via aberrant chromatin organization. CBP is the first partner gene of MLL containing well defined structural and functional motifs that provide unique insights into the potential mechanisms by which these translocations contribute to leukemogenesis.

Bibliography

Sobulo, O. M., Borrow, J., Tomek, R., Reshmi, S., Harden, A., Schlegelberger, B., Housman, D., Doggett, N. A., Rowley, J. D., & Zeleznik-Le, N. J. (1997). MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukemia with aât(11;16)(q23;p13.3). Proceedings of the National Academy of Sciences, 94(16), 8732â8737.

Authors 10

Olatoyosi M. Sobulo (first)
Julian Borrow (additional)
Ronald Tomek (additional)
Shalini Reshmi (additional)
Alanna Harden (additional)
Brigitte Schlegelberger (additional)
David Housman (additional)
Norman A. Doggett (additional)
Janet D. Rowley (additional)
Nancy J. Zeleznik-Le (additional)

References 54 Referenced 260

J D Rowley, S Reshmi, O Sobulo, T Musvee, J Anastasi, S Raimondi, N R Schneider, J C Barredo, B Schlegelberger, F Behm, N A Doggett, J Borrow, N Zeleznik-Le Blood 90, 535–541 (1997). / Blood by Rowley J D (1997)
10.1073/pnas.88.23.10735
G Cimino, D T Moir, O Canaani, K Williams, W M Crist, S Katzav, L Cannizzaro, B Lange, P C Nowell, C M Croce, E Canaani Cancer Res 51, 6712–6714 (1991). / Cancer Res by Cimino G (1991)
10.1038/ng1092-113
10.1016/0092-8674(92)90602-9
10.1016/0092-8674(92)90603-A
J D Rowley Seminars in Cancer Biology, ed T H Rabbitts (Academic, London), pp. 377–385 (1993). / Seminars in Cancer Biology by Rowley J D (1993)
10.1056/NEJM199309233291302
10.1002/gcc.2870130202
10.1182/blood.V81.12.3197.3197
10.1182/blood.V82.12.3705.3705
C A Felix, B J Lange, M R Hosler, J Fertala, M A Bjornsti Cancer Res 55, 4287–4292 (1995). / Cancer Res by Felix C A (1995)
P H Domer, D R Head, N Renganathan, S C Raimondi, E Yang, M Atlas Leukemia 9, 1305–1312 (1995). / Leukemia by Domer P H (1995)
10.1182/blood.V83.10.2780.2780
10.1016/S0021-9258(19)38926-4
10.1073/pnas.90.16.7884
10.1073/pnas.90.13.6350
10.1073/pnas.91.22.10610
10.1073/pnas.92.26.12160
10.1046/j.1365-313X.1993.04010137.x
10.1073/pnas.92.21.9737
10.1038/378505a0
K L Wydner, S Bhattacharya, R Eckner, J B Lawrence, D M Livingstone Genomics 30, 395–396 (1995). / Genomics by Wydner K L (1995)
10.1038/376348a0
10.1038/ng0996-33
10.1038/370223a0
10.1038/370226a0
A J Bannister, T Oehler, D Wilhelm, P Angel, T Kouzarides Oncogene 11, 2509–2514 (1995). / Oncogene by Bannister A J (1995)
10.1101/gad.10.5.528
10.1126/science.275.5299.523
10.1038/382319a0
10.1016/S0092-8674(00)82001-2
10.1038/384641a0
10.1001/archpedi.1963.02080040590010
10.1002/ajmg.1320560125
10.3109/10428199209053586
10.1200/JCO.1993.11.12.2370
Doggett N. A. Coogwin L. A. Tesmer J. G. Meincke L. J. Bruce D. C. Clark L. M. Altherr M. R. Ford A. A. Chi H. C. & Murrone B. L. (1995) Nature (London) Suppl. 377 335–365.
10.1073/pnas.87.23.9358
10.1182/blood.V86.9.3613.bloodjournal8693613
10.1056/NEJM199602293340916
10.1089/dna.1995.14.475
10.1038/365855a0
10.1073/pnas.89.24.11794
10.1182/blood.V87.7.2649.bloodjournal8772649
Strissel P. L. Hart C. Harden A. Rowley J. D. & Zeleznik-Le N. J. (1996) Blood Suppl. 1 250 (abstr.).
10.1016/S0092-8674(00)81063-6
10.1093/nar/20.10.2603
10.1016/0092-8674(92)90191-E
10.1016/S0092-8674(00)81269-6
10.1126/science.271.5257.1873
10.1182/blood.V89.11.3945
Satake N. Ishida Y. Otoh Y. Hinohara S. Kobayashi H. Sakashita A. Maseki N. & Kaneko Y. (1997) Genes Chromosomes Cancer in press.
10.1006/geno.1997.4699

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 10:35 a.m.)
Deposited	3 years, 2 months ago (June 6, 2022, 5:28 p.m.)
Indexed	1 week, 2 days ago (Aug. 19, 2025, 6:01 a.m.)
Issued	28 years ago (Aug. 5, 1997)
Published	28 years ago (Aug. 5, 1997)
Published Online	28 years ago (Aug. 5, 1997)
Published Print	28 years ago (Aug. 5, 1997)

Funders 0

None

BibTeX

@article{Sobulo_1997, title={MLL is fused to CBP, a histone acetyltransferase, in therapy-related acute myeloid leukemia with a t(11;16)(q23;p13.3)}, volume={94}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.94.16.8732}, DOI={10.1073/pnas.94.16.8732}, number={16}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Sobulo, Olatoyosi M. and Borrow, Julian and Tomek, Ronald and Reshmi, Shalini and Harden, Alanna and Schlegelberger, Brigitte and Housman, David and Doggett, Norman A. and Rowley, Janet D. and Zeleznik-Le, Nancy J.}, year={1997}, month=aug, pages={8732–8737} }

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