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Structures of the CcmABCD heme release complex at multiple states

Author

Listed:
  • Jiao Li

    (Nanjing University of Chinese Medicine
    Yale University)

  • Wan Zheng

    (Nanjing University of Chinese Medicine)

  • Ming Gu

    (Nanjing University of Chinese Medicine)

  • Long Han

    (Yale University)

  • Yanmei Luo

    (Nanjing University of Chinese Medicine)

  • Koukou Yu

    (Nanjing University of Chinese Medicine)

  • Mengxin Sun

    (Nanjing University of Chinese Medicine)

  • Yuliang Zong

    (Nanjing University of Chinese Medicine)

  • Xiuxiu Ma

    (Nanjing University of Chinese Medicine)

  • Bing Liu

    (Nanjing University of Chinese Medicine)

  • Ethan P. Lowder

    (Washington University in St. Louis)

  • Deanna L. Mendez

    (Washington University in St. Louis)

  • Robert G. Kranz

    (Washington University in St. Louis)

  • Kai Zhang

    (Yale University)

  • Jiapeng Zhu

    (Nanjing University of Chinese Medicine)

Abstract

Cytochromes c use heme as a cofactor to carry electrons in respiration and photosynthesis. The cytochrome c maturation system I, consisting of eight membrane proteins (CcmABCDEFGH), results in the attachment of heme to cysteine residues of cytochrome c proteins. Since all c-type cytochromes are periplasmic, heme is first transported to a periplasmic heme chaperone, CcmE. A large membrane complex, CcmABCD has been proposed to carry out this transport and linkage to CcmE, yet the structural basis and mechanisms underlying the process are unknown. We describe high resolution cryo-EM structures of CcmABCD in an unbound form, in complex with inhibitor AMP-PNP, and in complex with ATP and heme. We locate the ATP-binding site in CcmA and the heme-binding site in CcmC. Based on our structures combined with functional studies, we propose a hypothetic model of heme trafficking, heme transfer to CcmE, and ATP-dependent release of holoCcmE from CcmABCD. CcmABCD represents an ABC transporter complex using the energy of ATP hydrolysis for the transfer of heme from one binding partner (CcmC) to another (CcmE).

Suggested Citation

  • Jiao Li & Wan Zheng & Ming Gu & Long Han & Yanmei Luo & Koukou Yu & Mengxin Sun & Yuliang Zong & Xiuxiu Ma & Bing Liu & Ethan P. Lowder & Deanna L. Mendez & Robert G. Kranz & Kai Zhang & Jiapeng Zhu, 2022. "Structures of the CcmABCD heme release complex at multiple states," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34136-5
    DOI: 10.1038/s41467-022-34136-5
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    as
    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Svetlana V. Antonyuk & Cong Han & Robert R. Eady & S. Samar Hasnain, 2013. "Structures of protein–protein complexes involved in electron transfer," Nature, Nature, vol. 496(7443), pages 123-126, April.
    3. Mu Gao & Davi Nakajima An & Jerry M. Parks & Jeffrey Skolnick, 2022. "AF2Complex predicts direct physical interactions in multimeric proteins with deep learning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    5. Bianca Hermann & Melanie Kern & Luigi La Pietra & Jörg Simon & Oliver Einsle, 2015. "The octahaem MccA is a haem c–copper sulfite reductase," Nature, Nature, vol. 520(7549), pages 706-709, April.
    6. Susanne Hofmann & Dovile Januliene & Ahmad R. Mehdipour & Christoph Thomas & Erich Stefan & Stefan Brüchert & Benedikt T. Kuhn & Eric R. Geertsma & Gerhard Hummer & Robert Tampé & Arne Moeller, 2019. "Conformation space of a heterodimeric ABC exporter under turnover conditions," Nature, Nature, vol. 571(7766), pages 580-583, July.
    7. Chang Sun & Samir Benlekbir & Padmaja Venkatakrishnan & Yuhang Wang & Sangjin Hong & Jonathan Hosler & Emad Tajkhorshid & John L. Rubinstein & Robert B. Gennis, 2018. "Structure of the alternative complex III in a supercomplex with cytochrome oxidase," Nature, Nature, vol. 557(7703), pages 123-126, May.
    8. S. B. Jennifer Kan & Xiongyi Huang & Yosephine Gumulya & Kai Chen & Frances H. Arnold, 2017. "Genetically programmed chiral organoborane synthesis," Nature, Nature, vol. 552(7683), pages 132-136, December.
    9. Stuti Sharma & Ruoyu Zhou & Li Wan & Shan Feng & KangKang Song & Chen Xu & Yanyan Li & Maofu Liao, 2021. "Mechanism of LolCDE as a molecular extruder of bacterial triacylated lipoproteins," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    10. Joseph A. Lyons & David Aragão & Orla Slattery & Andrei V. Pisliakov & Tewfik Soulimane & Martin Caffrey, 2012. "Structural insights into electron transfer in caa3-type cytochrome oxidase," Nature, Nature, vol. 487(7408), pages 514-518, July.
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    1. Lorena Ilcu & Lukas Denkhaus & Anton Brausemann & Lin Zhang & Oliver Einsle, 2023. "Architecture of the Heme-translocating CcmABCD/E complex required for Cytochrome c maturation," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

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