IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36048-4.html
   My bibliography  Save this article

Structural insights into the elevator-type transport mechanism of a bacterial ZIP metal transporter

Author

Listed:
  • Yao Zhang

    (Michigan State University)

  • Yuhan Jiang

    (Michigan State University)

  • Kaifu Gao

    (Michigan State University)

  • Dexin Sui

    (Michigan State University)

  • Peixuan Yu

    (Michigan State University)

  • Min Su

    (University of Michigan)

  • Guo-Wei Wei

    (Michigan State University
    Michigan State University)

  • Jian Hu

    (Michigan State University
    Michigan State University)

Abstract

The Zrt-/Irt-like protein (ZIP) family consists of ubiquitously expressed divalent metal transporters critically involved in maintaining systemic and cellular homeostasis of zinc, iron, and manganese. Here, we present a study on a prokaryotic ZIP from Bordetella bronchiseptica (BbZIP) by combining structural biology, evolutionary covariance, computational modeling, and a variety of biochemical assays to tackle the issue of the transport mechanism which has not been established for the ZIP family. The apo state structure in an inward-facing conformation revealed a disassembled transport site, altered inter-helical interactions, and importantly, a rigid body movement of a 4-transmembrane helix (TM) bundle relative to the other TMs. The computationally generated and biochemically validated outward-facing conformation model revealed a slide of the 4-TM bundle, which carries the transport site(s), by approximately 8 Å toward the extracellular side against the static TMs which mediate dimerization. These findings allow us to conclude that BbZIP is an elevator-type transporter.

Suggested Citation

  • Yao Zhang & Yuhan Jiang & Kaifu Gao & Dexin Sui & Peixuan Yu & Min Su & Guo-Wei Wei & Jian Hu, 2023. "Structural insights into the elevator-type transport mechanism of a bacterial ZIP metal transporter," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36048-4
    DOI: 10.1038/s41467-023-36048-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36048-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36048-4?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. Jian Hu & Yi Xue & Sangwon Lee & Ya Ha, 2011. "The crystal structure of GXGD membrane protease FlaK," Nature, Nature, vol. 475(7357), pages 528-531, July.
    2. Nien-Jen Hu & So Iwata & Alexander D. Cameron & David Drew, 2011. "Crystal structure of a bacterial homologue of the bile acid sodium symporter ASBT," Nature, Nature, vol. 478(7369), pages 408-411, October.
    3. Nurunisa Akyuz & Elka R. Georgieva & Zhou Zhou & Sebastian Stolzenberg & Michel A. Cuendet & George Khelashvili & Roger B. Altman & Daniel S. Terry & Jack H. Freed & Harel Weinstein & Olga Boudker & S, 2015. "Transport domain unlocking sets the uptake rate of an aspartate transporter," Nature, Nature, vol. 518(7537), pages 68-73, February.
    4. Xiaoming Zhou & Elena J. Levin & Yaping Pan & Jason G. McCoy & Ruchika Sharma & Brian Kloss & Renato Bruni & Matthias Quick & Ming Zhou, 2014. "Structural basis of the alternating-access mechanism in a bile acid transporter," Nature, Nature, vol. 505(7484), pages 569-573, January.
    5. Nicolas Reyes & Christopher Ginter & Olga Boudker, 2009. "Transport mechanism of a bacterial homologue of glutamate transporters," Nature, Nature, vol. 462(7275), pages 880-885, December.
    6. Lan Zhao & Eduardo Oliver & Klio Maratou & Santosh S. Atanur & Olivier D. Dubois & Emanuele Cotroneo & Chien-Nien Chen & Lei Wang & Cristina Arce & Pauline L. Chabosseau & Joan Ponsa-Cobas & Maria G. , 2015. "The zinc transporter ZIP12 regulates the pulmonary vascular response to chronic hypoxia," Nature, Nature, vol. 524(7565), pages 356-360, August.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Yao Zhang & Majid Jafari & Tuo Zhang & Dexin Sui & Luca Sagresti & Kenneth M. Merz & Jian Hu, 2024. "Molecular insights into substrate translocation in an elevator-type metal transporter," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    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. Martin F. Peter & Jan A. Ruland & Peer Depping & Niels Schneberger & Emmanuele Severi & Jonas Moecking & Karl Gatterdam & Sarah Tindall & Alexandre Durand & Veronika Heinz & Jan Peter Siebrasse & Paul, 2022. "Structural and mechanistic analysis of a tripartite ATP-independent periplasmic TRAP transporter," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Takafumi Kato & Tsukasa Kusakizako & Chunhuan Jin & Xinyu Zhou & Ryuichi Ohgaki & LiLi Quan & Minhui Xu & Suguru Okuda & Kan Kobayashi & Keitaro Yamashita & Tomohiro Nishizawa & Yoshikatsu Kanai & Osa, 2022. "Structural insights into inhibitory mechanism of human excitatory amino acid transporter EAAT2," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Fuhui Meng & Yang Xiao & Yujia Ji & Ziyi Sun & Xiaoming Zhou, 2022. "An open-like conformation of the sigma-1 receptor reveals its ligand entry pathway," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Benedikt T. Kuhn & Jonathan Zöller & Iwan Zimmermann & Tim Gemeinhardt & Dogukan H. Özkul & Julian D. Langer & Markus A. Seeger & Eric R. Geertsma, 2024. "Interdomain-linkers control conformational transitions in the SLC23 elevator transporter UraA," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Yongzhen Liu & Thomas R. Cafiero & Debby Park & Abhishek Biswas & Benjamin Y. Winer & Cheul H. Cho & Yaron Bram & Vasuretha Chandar & Aoife K. O’ Connell & Hans P. Gertje & Nicholas Crossland & Robert, 2023. "Targeted viral adaptation generates a simian-tropic hepatitis B virus that infects marmoset cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Kaho Shionoya & Jae-Hyun Park & Toru Ekimoto & Junko S. Takeuchi & Junki Mifune & Takeshi Morita & Naito Ishimoto & Haruka Umezawa & Kenichiro Yamamoto & Chisa Kobayashi & Atsuto Kusunoki & Norimichi , 2024. "Structural basis for hepatitis B virus restriction by a viral receptor homologue," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Yao Zhang & Majid Jafari & Tuo Zhang & Dexin Sui & Luca Sagresti & Kenneth M. Merz & Jian Hu, 2024. "Molecular insights into substrate translocation in an elevator-type metal transporter," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. David B. Sauer & Jennifer J. Marden & Joseph C. Sudar & Jinmei Song & Christopher Mulligan & Da-Neng Wang, 2022. "Structural basis of ion – substrate coupling in the Na+-dependent dicarboxylate transporter VcINDY," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    9. Atsushi Yamagata & Yoshiko Murata & Kosuke Namba & Tohru Terada & Shuya Fukai & Mikako Shirouzu, 2022. "Uptake mechanism of iron-phytosiderophore from the soil based on the structure of yellow stripe transporter," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Zhenglai Zhang & Huiwen Chen & Ze Geng & Zhuoya Yu & Hang Li & Yanli Dong & Hongwei Zhang & Zhuo Huang & Juquan Jiang & Yan Zhao, 2022. "Structural basis of ligand binding modes of human EAAT2," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    11. Anna M. Borowska & Maria Gabriella Chiariello & Alisa A. Garaeva & Jan Rheinberger & Siewert J. Marrink & Cristina Paulino & Dirk J. Slotboom, 2024. "Structural basis of the obligatory exchange mode of human neutral amino acid transporter ASCT2," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Changxu Pang & Jin Chai & Ping Zhu & John Shanklin & Qun Liu, 2023. "Structural mechanism of intracellular autoregulation of zinc uptake in ZIP transporters," Nature Communications, Nature, vol. 14(1), pages 1-10, 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:14:y:2023:i:1:d:10.1038_s41467-023-36048-4. 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.