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Originally published In Press as doi:10.1074/jbc.M301567200 on March 18, 2003

J. Biol. Chem., Vol. 278, Issue 23, 21232-21239, June 6, 2003
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Structural Requirements for Assembly of the CSL·Intracellular Notch1·Mastermind-like 1 Transcriptional Activation Complex*

Yunsun Nam, Andrew P. Weng, Jon C. Aster and Stephen C. Blacklow {ddagger}

From the Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts 02115

Ligand binding by Notch receptors triggers a series of proteolytic cleavages that liberate the intracellular portion of Notch (ICN) from the cell membrane, permitting it to translocate to the nucleus. Nuclear ICN binds to a highly conserved DNA-binding transcription factor called CSL (also known as RBP-J{kappa}, CBF1, Suppressor of Hairless, and Lag-1) and recruits Mastermind-like transcriptional co-activators to form a transcriptional activation complex. Using bioinformatics tools, we identified a Rel homology region (RHR) within CSL that was used as a guide to determine the minimal protein requirements for ternary complex formation. The RHR of CSL contains both the N- and C-terminal {beta}-sheet domains (RHR-n and RHR-c) of typical Rel transcription factors, as judged by circular dichroism spectra. Binding of monomeric CSL to DNA requires the entire RHR of CSL and an additional 125-residue N-terminal sequence, whereas binding to ICN requires only the RHR-n domain. Although the RAM (RBP-J{kappa} (recombination-signal-sequence-binding protein for J{kappa} genes)-associated molecule) domain of ICN is flexible and relatively unstructured as an isolated polypeptide in solution, it associates stably with CSL on DNA. Recruitment of Mastermind-like 1 (MAML1) to CSL·ICN complexes on DNA requires inclusion of the ankyrin repeat domain of ICN, and N- and C-terminal sequences of CSL extending beyond the DNA-binding region. The requirement for cooperative assembly of the MAML1·ICN·CSL·DNA complex suggests that a primary function of ICN is to render CSL competent for MAML loading. On the basis of our results, we present a working structural model for the organization of the MAML1·ICN·CSL·DNA complex.

Received for publication, February 13, 2003

* This work was supported by National Institutes of Health Grants HL61001 and CA92433 (to S. C. B.) and CA82308 (to J. C. A.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

{ddagger} Pew Scholar in the biomedical sciences and an Established Investigator of the American Heart Association. To whom correspondence should be addressed. Tel.: 617-732-5799; Fax: 617-264-5296; E-mail: sblacklow{at}rics.bwh.harvard.edu.


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