Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins
In every established species, protein-protein interactions have evolved such that they are fit for purpose. However, the molecular details of the evolution of new protein-protein interactions are poorly understood. We have used nuclear magnetic resonance spectroscopy to investigate the changes in st...
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todo:paper_23752548_v4_n10_p_Jemth2023-10-03T16:41:18Z Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins Jemth, P. Karlsson, E. Vögeli, B. Guzovsky, B. Andersson, E. Hultqvist, G. Dogan, J. Güntert, P. Riek, R. Chi, C.N. Dynamics Magnetic domains Nuclear magnetic resonance spectroscopy Inter-domain interactions Intrinsically disordered proteins Isothermal calorimetry Protein-protein complexes Protein-protein interactions Solvent accessible surface areas Structure and dynamics Transcriptional coregulators Proteins In every established species, protein-protein interactions have evolved such that they are fit for purpose. However, the molecular details of the evolution of new protein-protein interactions are poorly understood. We have used nuclear magnetic resonance spectroscopy to investigate the changes in structure and dynamics during the evolution of a protein-protein interaction involving the intrinsically disordered CREBBP (CREB-binding protein) interaction domain (CID) and nuclear coactivator binding domain (NCBD) from the transcriptional coregulators NCOA (nuclear receptor coactivator) and CREBBP/p300, respectively. The most ancient low-affinity "Cambrian-like" [540 to 600 million years (Ma) ago] CID/NCBD complex contained less secondary structure and was more dynamic than the complexes from an evolutionarily younger "Ordovician-Silurian" fish ancestor (ca. 440 Ma ago) and extant human. The most ancient Cambrian-like CID/NCBD complex lacked one helix and several interdomain interactions, resulting in a larger solvent-accessible surface area. Furthermore, the most ancient complex had a high degree of millisecond-to-microsecond dynamics distributed along the entire sequences of both CID and NCBD. These motions were reduced in the Ordovician-Silurian CID/NCBD complex and further redistributed in the extant human CID/NCBD complex. Isothermal calorimetry experiments show that complex formation is enthalpically favorable and that affinity is modulated by a largely unfavorable entropic contribution to binding. Our data demonstrate how changes in structure and motion conspire to shape affinity during the evolution of a protein-protein complex and provide direct evidence for the role of structural, dynamic, and frustrational plasticity in the evolution of interactions between intrinsically disordered proteins. Copyright © 2018 The Authors, some rights reserved. JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_23752548_v4_n10_p_Jemth |
| institution |
Universidad de Buenos Aires |
| institution_str |
I-28 |
| repository_str |
R-134 |
| collection |
Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA) |
| topic |
Dynamics Magnetic domains Nuclear magnetic resonance spectroscopy Inter-domain interactions Intrinsically disordered proteins Isothermal calorimetry Protein-protein complexes Protein-protein interactions Solvent accessible surface areas Structure and dynamics Transcriptional coregulators Proteins |
| spellingShingle |
Dynamics Magnetic domains Nuclear magnetic resonance spectroscopy Inter-domain interactions Intrinsically disordered proteins Isothermal calorimetry Protein-protein complexes Protein-protein interactions Solvent accessible surface areas Structure and dynamics Transcriptional coregulators Proteins Jemth, P. Karlsson, E. Vögeli, B. Guzovsky, B. Andersson, E. Hultqvist, G. Dogan, J. Güntert, P. Riek, R. Chi, C.N. Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| topic_facet |
Dynamics Magnetic domains Nuclear magnetic resonance spectroscopy Inter-domain interactions Intrinsically disordered proteins Isothermal calorimetry Protein-protein complexes Protein-protein interactions Solvent accessible surface areas Structure and dynamics Transcriptional coregulators Proteins |
| description |
In every established species, protein-protein interactions have evolved such that they are fit for purpose. However, the molecular details of the evolution of new protein-protein interactions are poorly understood. We have used nuclear magnetic resonance spectroscopy to investigate the changes in structure and dynamics during the evolution of a protein-protein interaction involving the intrinsically disordered CREBBP (CREB-binding protein) interaction domain (CID) and nuclear coactivator binding domain (NCBD) from the transcriptional coregulators NCOA (nuclear receptor coactivator) and CREBBP/p300, respectively. The most ancient low-affinity "Cambrian-like" [540 to 600 million years (Ma) ago] CID/NCBD complex contained less secondary structure and was more dynamic than the complexes from an evolutionarily younger "Ordovician-Silurian" fish ancestor (ca. 440 Ma ago) and extant human. The most ancient Cambrian-like CID/NCBD complex lacked one helix and several interdomain interactions, resulting in a larger solvent-accessible surface area. Furthermore, the most ancient complex had a high degree of millisecond-to-microsecond dynamics distributed along the entire sequences of both CID and NCBD. These motions were reduced in the Ordovician-Silurian CID/NCBD complex and further redistributed in the extant human CID/NCBD complex. Isothermal calorimetry experiments show that complex formation is enthalpically favorable and that affinity is modulated by a largely unfavorable entropic contribution to binding. Our data demonstrate how changes in structure and motion conspire to shape affinity during the evolution of a protein-protein complex and provide direct evidence for the role of structural, dynamic, and frustrational plasticity in the evolution of interactions between intrinsically disordered proteins. Copyright © 2018 The Authors, some rights reserved. |
| format |
JOUR |
| author |
Jemth, P. Karlsson, E. Vögeli, B. Guzovsky, B. Andersson, E. Hultqvist, G. Dogan, J. Güntert, P. Riek, R. Chi, C.N. |
| author_facet |
Jemth, P. Karlsson, E. Vögeli, B. Guzovsky, B. Andersson, E. Hultqvist, G. Dogan, J. Güntert, P. Riek, R. Chi, C.N. |
| author_sort |
Jemth, P. |
| title |
Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| title_short |
Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| title_full |
Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| title_fullStr |
Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| title_full_unstemmed |
Structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| title_sort |
structure and dynamics conspire in the evolution of affinity between intrinsically disordered proteins |
| url |
http://hdl.handle.net/20.500.12110/paper_23752548_v4_n10_p_Jemth |
| work_keys_str_mv |
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1807315684225449984 |