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Exploring the folding pathways of annexin I, a multidomain protein. II. Hierarchy in domain folding propensities may govern the folding process

Exploring the folding pathways of annexin I, a multidomain protein. II. Hierarchy in domain folding propensities may govern the folding process

Journal of Molecular Biology 279(5): 1177-1185

ISSN/ISBN: 0022-2836

PMID: 9642093

DOI: 10.1006/jmbi.1998.1828

In the context of exploring the relationship between sequence and folding pathways, the multi-domain proteins of the annexin family constitute very attractive models. They are constituted of four approximately 70-residue domains, named D1 to D4, with identical topologies but only limited sequence homology of approximately 30%. The domains are organized in a pseudochiral circular arrangement. Here, we report on the folding propensity of the D1 domain of annexin I obtained from overexpression in Escherichia coli. Unlike the D2 domain, which is only partially folded, the isolated D1 domain exhibits autonomous refolding in pure aqueous solution. Similarly, the D3 domain and D2-D3 module were obtained from expression in E. coli but were found to be largely unfolded. No conclusion could be drawn for the D4 domain because it was not possible to extract it from the bacterial inclusion bodies. The data allow us to propose a plausible scenario for the annexin I folding. This working model states that firstly the D1 domain folds, and the D2 and D3 domains remain partly unfolded, facilitating the docking of the D4 domain to the D1 domain. In a second step, the D1 and D4 domains dock, and D4 may fold if already not folded. The final step starts with the stabilization of the D1-D4 module. This stabilization is crucial for allowing the non-native local interactions inside the still partially unfolded D2 domain to switch to the native long-range interactions involving D4. This switch allows the complete folding of D2 and D3. The model proposes a sequential and hierarchical process for the folding of annexin I and emphasizes the role of both native framework and non-native structures in the process.

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