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Structure and inhibition mechanisms of Mycobacterium tuberculosis essential transporter efflux protein A

Author

Listed:
  • Nitesh Kumar Khandelwal

    (University of California San Francisco
    Oregon Health & Science University)

  • Meghna Gupta

    (University of California San Francisco
    Oregon Health & Science University)

  • James E. Gomez

    (Broad Institute of MIT and Harvard)

  • Sulyman Barkho

    (Broad Institute of MIT and Harvard)

  • Ziqiang Guan

    (Duke University Medical Center)

  • Ashley Y. Eng

    (Broad Institute of MIT and Harvard)

  • Tomohiko Kawate

    (Broad Institute of MIT and Harvard)

  • Sree Ganesh Balasubramani

    (University of California San Francisco)

  • Andrej Sali

    (University of California San Francisco)

  • Deborah T. Hung

    (Broad Institute of MIT and Harvard
    Harvard Medical School
    Massachusetts General Hospital)

  • Robert M. Stroud

    (University of California San Francisco)

Abstract

A broad chemical genetic screen in Mycobacterium tuberculosis (Mtb) identified compounds (BRD-8000.3 and BRD-9327) that inhibit the essential efflux pump EfpA. To understand the mechanisms of inhibition, we determined the structures of EfpA with these inhibitors bound at 2.7-3.4 Å resolution. Our structures reveal different mechanisms of inhibition by the two inhibitors. BRD-8000.3 binds in a tunnel contacting the lipid bilayer and extending toward the central cavity to displace the fatty acid chain of a lipid molecule bound in the apo structure, suggesting its blocking of an access route for a natural lipidic substrate. Meanwhile, BRD-9327 binds in the outer vestibule without complete blockade of the substrate path to the outside, suggesting its possible inhibition of the movement necessary for alternate access of the transporter. Our results show EfpA as a potential lipid transporter, explain the basis of the synergy of these inhibitors and their potential for combination anti-tuberculosis therapy.

Suggested Citation

  • Nitesh Kumar Khandelwal & Meghna Gupta & James E. Gomez & Sulyman Barkho & Ziqiang Guan & Ashley Y. Eng & Tomohiko Kawate & Sree Ganesh Balasubramani & Andrej Sali & Deborah T. Hung & Robert M. Stroud, 2025. "Structure and inhibition mechanisms of Mycobacterium tuberculosis essential transporter efflux protein A," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58133-6
    DOI: 10.1038/s41467-025-58133-6
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    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. Kien Lam Ung & Mikael Winkler & Lukas Schulz & Martina Kolb & Dorina P. Janacek & Emil Dedic & David L. Stokes & Ulrich Z. Hammes & Bjørn Panyella Pedersen, 2022. "Structures and mechanism of the plant PIN-FORMED auxin transporter," Nature, Nature, vol. 609(7927), pages 605-610, September.
    3. Eachan O. Johnson & Emily LaVerriere & Emma Office & Mary Stanley & Elisabeth Meyer & Tomohiko Kawate & James E. Gomez & Rebecca E. Audette & Nirmalya Bandyopadhyay & Natalia Betancourt & Kayla Delano, 2019. "Large-scale chemical–genetics yields new M. tuberculosis inhibitor classes," Nature, Nature, vol. 571(7763), pages 72-78, July.
    4. Ieva Vasiliauskaité-Brooks & Robert D. Healey & Pascal Rochaix & Julie Saint-Paul & Rémy Sounier & Claire Grison & Thierry Waltrich-Augusto & Mathieu Fortier & François Hoh & Essa M. Saied & Christoph, 2018. "Structure of a human intramembrane ceramidase explains enzymatic dysfunction found in leukodystrophy," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    5. Alexander A. Shcherbakov & Peyton J. Spreacker & Aurelio J. Dregni & Katherine A. Henzler-Wildman & Mei Hong, 2022. "High-pH structure of EmrE reveals the mechanism of proton-coupled substrate transport," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Shuhui Wang & Kun Wang & Kangkang Song & Zon Weng Lai & Pengfei Li & Dongying Li & Yajie Sun & Ye Mei & Chen Xu & Maofu Liao, 2024. "Structures of the Mycobacterium tuberculosis efflux pump EfpA reveal the mechanisms of transport and inhibition," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    7. Silvia Ravera & Juan Pablo Nicola & Glicella Salazar-De Simone & Fred J. Sigworth & Erkan Karakas & L. Mario Amzel & Mario A. Bianchet & Nancy Carrasco, 2022. "Structural insights into the mechanism of the sodium/iodide symporter," Nature, Nature, vol. 612(7941), pages 795-801, December.
    8. 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.
    9. Somnath Mukherjee & Satchal K. Erramilli & Mark Ammirati & Frances J. D. Alvarez & Kimberly F. Fennell & Michael D. Purdy & Blazej M. Skrobek & Katarzyna Radziwon & John Coukos & Yanyong Kang & Przemy, 2020. "Synthetic antibodies against BRIL as universal fiducial marks for single−particle cryoEM structure determination of membrane proteins," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
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