Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding
Abstract Protein–protein binding enables orderly biological self‐organization and is therefore considered a miracle of nature. Protein‒protein binding is driven by electrostatic forces, hydrogen bonding, van der Waals force, and hydrophobic interactions. Among these physical forces, only hydrophobic...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Wiley
2023-07-01
|
| Series: | Global Challenges |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/gch2.202300022 |
| _version_ | 1827895838617108480 |
|---|---|
| author | Lin Yang Shuai Guo Chenchen Liao Chengyu Hou Shenda Jiang Jiacheng Li Xiaoliang Ma Liping Shi Lin Ye Xiaodong He |
| author_facet | Lin Yang Shuai Guo Chenchen Liao Chengyu Hou Shenda Jiang Jiacheng Li Xiaoliang Ma Liping Shi Lin Ye Xiaodong He |
| author_sort | Lin Yang |
| collection | DOAJ |
| description | Abstract Protein–protein binding enables orderly biological self‐organization and is therefore considered a miracle of nature. Protein‒protein binding is driven by electrostatic forces, hydrogen bonding, van der Waals force, and hydrophobic interactions. Among these physical forces, only hydrophobic interactions can be considered long‐range intermolecular attractions between proteins due to the electrostatic shielding of surrounding water molecules. Low‐entropy hydration shells around proteins drive hydrophobic attraction among them that essentially coordinate protein‒protein binding. Here, an innovative method is developed for identifying low‐entropy regions of hydration shells of proteins by screening off pseudohydrophilic groups on protein surfaces and revealing that large low‐entropy regions of the hydration shells typically cover the binding sites of individual proteins. According to an analysis of determined protein complex structures, shape matching between a large low‐entropy hydration shell region of a protein and that of its partner at the binding sites is revealed as a universal law. Protein‒protein binding is thus found to be mainly guided by hydrophobic collapse between the shape‐matched low‐entropy hydration shells that is verified by bioinformatics analyses of hundreds of structures of protein complexes, which cover four test systems. A simple algorithm is proposed to accurately predict protein binding sites. |
| first_indexed | 2024-03-12T22:26:24Z |
| format | Article |
| id | doaj.art-253fb1a022d245f687abdcba4b2880a0 |
| institution | Directory Open Access Journal |
| issn | 2056-6646 |
| language | English |
| last_indexed | 2024-03-12T22:26:24Z |
| publishDate | 2023-07-01 |
| publisher | Wiley |
| record_format | Article |
| series | Global Challenges |
| spelling | doaj.art-253fb1a022d245f687abdcba4b2880a02023-07-22T04:24:12ZengWileyGlobal Challenges2056-66462023-07-0177n/an/a10.1002/gch2.202300022Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein BindingLin Yang0Shuai Guo1Chenchen Liao2Chengyu Hou3Shenda Jiang4Jiacheng Li5Xiaoliang Ma6Liping Shi7Lin Ye8Xiaodong He9National Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaNational Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaSchool of Electronics and Information Engineering Harbin Institute of Technology Harbin 150080 P. R. ChinaSchool of Electronics and Information Engineering Harbin Institute of Technology Harbin 150080 P. R. ChinaNational Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaNational Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaNational Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaNational Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaSchool of System Design and Intelligent Manufacturing Southern University of Science and Technology Shenzhen 518055 P. R. ChinaNational Key Laboratory of Science and Technology on Advanced Composites in Special Environments Center for Composite Materials and Structures Harbin Institute of Technology Harbin 150080 P. R. ChinaAbstract Protein–protein binding enables orderly biological self‐organization and is therefore considered a miracle of nature. Protein‒protein binding is driven by electrostatic forces, hydrogen bonding, van der Waals force, and hydrophobic interactions. Among these physical forces, only hydrophobic interactions can be considered long‐range intermolecular attractions between proteins due to the electrostatic shielding of surrounding water molecules. Low‐entropy hydration shells around proteins drive hydrophobic attraction among them that essentially coordinate protein‒protein binding. Here, an innovative method is developed for identifying low‐entropy regions of hydration shells of proteins by screening off pseudohydrophilic groups on protein surfaces and revealing that large low‐entropy regions of the hydration shells typically cover the binding sites of individual proteins. According to an analysis of determined protein complex structures, shape matching between a large low‐entropy hydration shell region of a protein and that of its partner at the binding sites is revealed as a universal law. Protein‒protein binding is thus found to be mainly guided by hydrophobic collapse between the shape‐matched low‐entropy hydration shells that is verified by bioinformatics analyses of hundreds of structures of protein complexes, which cover four test systems. A simple algorithm is proposed to accurately predict protein binding sites.https://doi.org/10.1002/gch2.202300022binding siteGibbs free energyhydration shelllow entropyprotein–protein interactions |
| spellingShingle | Lin Yang Shuai Guo Chenchen Liao Chengyu Hou Shenda Jiang Jiacheng Li Xiaoliang Ma Liping Shi Lin Ye Xiaodong He Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding Global Challenges binding site Gibbs free energy hydration shell low entropy protein–protein interactions |
| title | Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding |
| title_full | Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding |
| title_fullStr | Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding |
| title_full_unstemmed | Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding |
| title_short | Spatial Layouts of Low‐Entropy Hydration Shells Guide Protein Binding |
| title_sort | spatial layouts of low entropy hydration shells guide protein binding |
| topic | binding site Gibbs free energy hydration shell low entropy protein–protein interactions |
| url | https://doi.org/10.1002/gch2.202300022 |
| work_keys_str_mv | AT linyang spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT shuaiguo spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT chenchenliao spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT chengyuhou spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT shendajiang spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT jiachengli spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT xiaoliangma spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT lipingshi spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT linye spatiallayoutsoflowentropyhydrationshellsguideproteinbinding AT xiaodonghe spatiallayoutsoflowentropyhydrationshellsguideproteinbinding |