IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-54548-9.html
   My bibliography  Save this article

Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins

Author

Listed:
  • Meili Li

    (University of Science and Technology of China)

  • Chengming Zhu

    (University of Science and Technology of China)

  • Zheng Xu

    (Sichuan University)

  • Mingjing Xu

    (University of Science and Technology of China)

  • Yan Kuang

    (University of Science and Technology of China)

  • Xinhao Hou

    (University of Science and Technology of China)

  • Xinya Huang

    (University of Science and Technology of China)

  • Mengqi Lv

    (University of Science and Technology of China)

  • Yongrui Liu

    (University of Science and Technology of China)

  • Yong Zhang

    (University of Science and Technology of China)

  • Ziyan Xu

    (University of Science and Technology of China)

  • Xu Han

    (University of Science and Technology of China)

  • Suman Wang

    (University of Science and Technology of China)

  • Yunyu Shi

    (University of Science and Technology of China)

  • Shouhong Guang

    (University of Science and Technology of China)

  • Fudong Li

    (University of Science and Technology of China)

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.

Suggested Citation

  • 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 L, 2024. "Structural basis for C. elegans pairing center DNA binding specificity by the ZIM/HIM-8 family proteins," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54548-9
    DOI: 10.1038/s41467-024-54548-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-54548-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-54548-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yan Wang & Yanyan Chen & Juan Chen & Lijun Wang & Leitong Nie & Juanjuan Long & Haishuang Chang & Jian Wu & Chenhui Huang & Ming Lei, 2019. "The meiotic TERB1-TERB2-MAJIN complex tethers telomeres to the nuclear envelope," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
    2. Josh Abramson & Jonas Adler & Jack Dunger & Richard Evans & Tim Green & Alexander Pritzel & Olaf Ronneberger & Lindsay Willmore & Andrew J. Ballard & Joshua Bambrick & Sebastian W. Bodenstein & David , 2024. "Accurate structure prediction of biomolecular interactions with AlphaFold 3," Nature, Nature, vol. 630(8016), pages 493-500, June.
    3. Xinhao Hou & Mingjing Xu & Chengming Zhu & Jianing Gao & Meili Li & Xiangyang Chen & Cheng Sun & Björn Nashan & Jianye Zang & Ying Zhou & Shouhong Guang & Xuezhu Feng, 2023. "Systematic characterization of chromodomain proteins reveals an H3K9me1/2 reader regulating aging in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Qianqian Ming & Daniel Antfolk & David A. Price & Anna Manturova & Elliot Medina & Srishti Singh & Charlotte Mason & Timothy H. Tran & Keiran S. M. Smalley & Daisy W. Leung & Vincent C. Luca, 2024. "Structural basis for mouse LAG3 interactions with the MHC class II molecule I-Ab," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Itxaso Anso & Samira Zouhir & Thibault Géry Sana & Petya Violinova Krasteva, 2024. "Structural basis for synthase activation and cellulose modification in the E. coli Type II Bcs secretion system," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Paloma García Casas & Michela Rossini & Linnea Påvénius & Mezida Saeed & Nikita Arnst & Sonia Sonda & Tânia Fernandes & Irene D’Arsiè & Matteo Bruzzone & Valeria Berno & Andrea Raimondi & Maria Livia , 2024. "Simultaneous detection of membrane contact dynamics and associated Ca2+ signals by reversible chemogenetic reporters," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    4. Cornelia Sala & Martin Würtz & Enrico Salvatore Atorino & Annett Neuner & Patrick Partscht & Thomas Hoffmann & Sebastian Eustermann & Elmar Schiebel, 2024. "An interaction network of inner centriole proteins organised by POC1A-POC1B heterodimer crosslinks ensures centriolar integrity," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Yannick Weyer & Sinead I. Schwabl & Xuechen Tang & Astha Purwar & Konstantin Siegmann & Angela Ruepp & Theresia Dunzendorfer-Matt & Michael A. Widerin & Veronika Niedrist & Noa J. M. Mutsters & Maria , 2024. "The Dsc ubiquitin ligase complex identifies transmembrane degrons to degrade orphaned proteins at the Golgi," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. Huiyu Cai & Zuobai Zhang & Mingkai Wang & Bozitao Zhong & Quanxiao Li & Yuxuan Zhong & Yanling Wu & Tianlei Ying & Jian Tang, 2024. "Pretrainable geometric graph neural network for antibody affinity maturation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Anete Romanauska & Edvinas Stankunas & Maya Schuldiner & Alwin Köhler, 2024. "Seipin governs phosphatidic acid homeostasis at the inner nuclear membrane," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Timothy K. Soh & Sofia Ognibene & Saskia Sanders & Robin Schäper & Benedikt B. Kaufer & Jens B. Bosse, 2024. "A proteome-wide structural systems approach reveals insights into protein families of all human herpesviruses," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Nathalie Béchon & Nitzan Tal & Avigail Stokar-Avihail & Alon Savidor & Meital Kupervaser & Sarah Melamed & Gil Amitai & Rotem Sorek, 2024. "Diversification of molecular pattern recognition in bacterial NLR-like proteins," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Amika Singla & Daniel J. Boesch & Ho Yee Joyce Fung & Chigozie Ngoka & Avery S. Enriquez & Ran Song & Daniel A. Kramer & Yan Han & Esther Banarer & Andrew Lemoff & Puneet Juneja & Daniel D. Billadeau , 2024. "Structural basis for Retriever-SNX17 assembly and endosomal sorting," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Sanghyeon Choi & Youngjin Lee & Shinhye Park & Song Yee Jang & Jongbin Park & Do Won Oh & Su-Man Kim & Tae-Hwan Kim & Ga Seul Lee & Changyi Cho & Byoung Sik Kim & Donghan Lee & Eun-Hee Kim & Hae-Kap C, 2024. "Dissemination of pathogenic bacteria is reinforced by a MARTX toxin effector duet," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    12. Yida Jiang & Xinghe Zhang & Honggang Nie & Jianxiong Fan & Shuangshuang Di & Hui Fu & Xiu Zhang & Lijuan Wang & Chun Tang, 2024. "Dissecting diazirine photo-reaction mechanism for protein residue-specific cross-linking and distance mapping," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    13. Xiaoting Shan & Ying Cai & Binyu Zhu & Lingli Zhou & Xujie Sun & Xiaoxuan Xu & Qi Yin & Dangge Wang & Yaping Li, 2024. "Rational strategies for improving the efficiency of design and discovery of nanomedicines," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    14. Yinghui Chen & Yunxin Xu & Di Liu & Yaoguang Xing & Haipeng Gong, 2024. "An end-to-end framework for the prediction of protein structure and fitness from single sequence," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Yijia Cheng & Mark A. B. Kreutzberger & Jianting Han & Edward H. Egelman & Qin Cao, 2024. "Molecular architecture of the assembly of Bacillus spore coat protein GerQ revealed by cryo-EM," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    16. Leishu Lin & Jiayuan Dong & Shun Xu & Jinman Xiao & Cong Yu & Fengfeng Niu & Zhiyi Wei, 2024. "Autoinhibition and relief mechanisms for MICAL monooxygenases in F-actin disassembly," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    17. Xibing Xu & Roland Barriot & Bertille Voisin & Tom J. Arrowsmith & Ben Usher & Claude Gutierrez & Xue Han & Carine Pagès & Peter Redder & Tim R. Blower & Olivier Neyrolles & Pierre Genevaux, 2024. "Nucleotidyltransferase toxin MenT extends aminoacyl acceptor ends of serine tRNAs to control Mycobacterium tuberculosis growth," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    18. Kehan Wu & Yingce Xia & Pan Deng & Renhe Liu & Yuan Zhang & Han Guo & Yumeng Cui & Qizhi Pei & Lijun Wu & Shufang Xie & Si Chen & Xi Lu & Song Hu & Jinzhi Wu & Chi-Kin Chan & Shawn Chen & Liangliang Z, 2024. "TamGen: drug design with target-aware molecule generation through a chemical language model," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    19. Michael Kugler & Felix J. Metzner & Gregor Witte & Karl-Peter Hopfner & Katja Lammens, 2024. "Phosphorylation-mediated conformational change regulates human SLFN11," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    20. Maxime Zamba-Campero & Daniel Soliman & Huaxin Yu & Amanda G. Lasseter & Yuen-Yan Chang & Julia L. Silberman & Jun Liu & L. Aravind & Mollie W. Jewett & Gisela Storz & Philip P. Adams, 2024. "Broadly conserved FlgV controls flagellar assembly and Borrelia burgdorferi dissemination in mice," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54548-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.