Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins
Abstract Pairing center (PC) on each chromosome of Caenorhabditis elegans is crucial for homolog pairing and initiating synapsis. Within each PC, clusters of 11/12 bp DNA motif recruit one of four paralogous meiosis-specific proteins: ZIM-1, ZIM-2, ZIM-3, or HIM-8. However, the mechanistic basis und...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2024-11-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-54548-9 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850057998170324992 |
|---|---|
| author | Meili Li Chengming Zhu Zheng Xu Mingjing Xu Yan Kuang Xinhao Hou Xinya Huang Mengqi Lv Yongrui Liu Yong Zhang Ziyan Xu Xu Han Suman Wang Yunyu Shi Shouhong Guang Fudong Li |
| author_facet | Meili Li Chengming Zhu Zheng Xu Mingjing Xu Yan Kuang Xinhao Hou Xinya Huang Mengqi Lv Yongrui Liu Yong Zhang Ziyan Xu Xu Han Suman Wang Yunyu Shi Shouhong Guang Fudong Li |
| author_sort | Meili Li |
| collection | DOAJ |
| description | Abstract Pairing center (PC) on each chromosome of Caenorhabditis elegans is crucial for homolog pairing and initiating synapsis. Within each PC, clusters of 11/12 bp DNA motif recruit one of four paralogous meiosis-specific proteins: ZIM-1, ZIM-2, ZIM-3, or HIM-8. However, the mechanistic basis underlying the specificity of ZIM/HIM-8-PC DNA interaction remains elusive. Here, we describe crystal structures of HIM-8, ZIM-1 and ZIM-2 DNA binding domains (ZF1, ZF2 and CTD) in complex with their cognate PC DNA motifs, respectively. These structures demonstrated the ZF1-2-CTD folds as an integrated structural unit crucial for its DNA binding specificity. Base-specific DNA-contacting residues are exclusively distributed on ZF1-2 and highly conserved. Furthermore, the CTD potentially contributes to the conformational diversity of ZF1-2, imparting binding specificity to distinct PC DNA motifs. These findings shed light on the mechanism governing PC DNA motif recognition by ZIM/HIM-8 proteins, suggesting a co-evolution relationship between PC DNA motifs and ZF1-2-CTD in shaping the specific recognition. |
| format | Article |
| id | doaj-art-cec402e2816d4f738b37af3c3858cc3a |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-cec402e2816d4f738b37af3c3858cc3a2025-08-20T02:51:16ZengNature PortfolioNature Communications2041-17232024-11-0115111610.1038/s41467-024-54548-9Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteinsMeili Li0Chengming Zhu1Zheng Xu2Mingjing Xu3Yan Kuang4Xinhao Hou5Xinya Huang6Mengqi Lv7Yongrui Liu8Yong Zhang9Ziyan Xu10Xu Han11Suman Wang12Yunyu Shi13Shouhong Guang14Fudong Li15MOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaDivision of Nephrology and Kidney Research Institute, State Key Laboratory of Biotherapy, West China Hospital, Sichuan UniversityMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaMOE Key Laboratory for Cellular Dynamics, Hefei National Laboratory for Physical Sciences at the Microscale, The First Affiliated Hospital of USTC, Biomedical Sciences and Health Laboratory of Anhui Province, Division of Life Sciences and Medicine, University of Science and Technology of ChinaAbstract Pairing center (PC) on each chromosome of Caenorhabditis elegans is crucial for homolog pairing and initiating synapsis. Within each PC, clusters of 11/12 bp DNA motif recruit one of four paralogous meiosis-specific proteins: ZIM-1, ZIM-2, ZIM-3, or HIM-8. However, the mechanistic basis underlying the specificity of ZIM/HIM-8-PC DNA interaction remains elusive. Here, we describe crystal structures of HIM-8, ZIM-1 and ZIM-2 DNA binding domains (ZF1, ZF2 and CTD) in complex with their cognate PC DNA motifs, respectively. These structures demonstrated the ZF1-2-CTD folds as an integrated structural unit crucial for its DNA binding specificity. Base-specific DNA-contacting residues are exclusively distributed on ZF1-2 and highly conserved. Furthermore, the CTD potentially contributes to the conformational diversity of ZF1-2, imparting binding specificity to distinct PC DNA motifs. These findings shed light on the mechanism governing PC DNA motif recognition by ZIM/HIM-8 proteins, suggesting a co-evolution relationship between PC DNA motifs and ZF1-2-CTD in shaping the specific recognition.https://doi.org/10.1038/s41467-024-54548-9 |
| spellingShingle | Meili Li Chengming Zhu Zheng Xu Mingjing Xu Yan Kuang Xinhao Hou Xinya Huang Mengqi Lv Yongrui Liu Yong Zhang Ziyan Xu Xu Han Suman Wang Yunyu Shi Shouhong Guang Fudong Li Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins Nature Communications |
| title | Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins |
| title_full | Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins |
| title_fullStr | Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins |
| title_full_unstemmed | Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins |
| title_short | Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins |
| title_sort | structural basis for c elegans pairing center dna binding specificity by the zim him 8 family proteins |
| url | https://doi.org/10.1038/s41467-024-54548-9 |
| work_keys_str_mv | AT meilili structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT chengmingzhu structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT zhengxu structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT mingjingxu structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT yankuang structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT xinhaohou structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT xinyahuang structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT mengqilv structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT yongruiliu structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT yongzhang structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT ziyanxu structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT xuhan structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT sumanwang structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT yunyushi structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT shouhongguang structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins AT fudongli structuralbasisforceleganspairingcenterdnabindingspecificitybythezimhim8familyproteins |