TY - JOUR
T1 - Mechanistic studies of mycobacterial glycolipid biosynthesis by the mannosyltransferase PimE
AU - Liu, Yaqi
AU - Brown, Chelsea M.
AU - Borges, Nuno
AU - Nobre, Rodrigo N.
AU - Erramilli, Satchal
AU - Belcher Dufrisne, Meagan
AU - Kloss, Brian
AU - Giacometti, Sabrina
AU - Esteves, Ana M.
AU - Timóteo, Cristina G.
AU - Tokarz, Piotr
AU - Cater, Rosemary J.
AU - Lowary, Todd L.
AU - Morita, Yasu S.
AU - Kossiakoff, Anthony A.
AU - Santos, Helena
AU - Stansfeld, Phillip J.
AU - Nygaard, Rie
AU - Mancia, Filippo
N1 - Funding Information:
This work was supported by R35GM132120 (to F.M.). P.J.S. acknowledges the NIH (R01AI174416 (PI: M. Stephen Trent)), Wellcome (208361/Z/17/Z), MRC, BBSRC, and the Howard Dalton Centre for funding. C.M.B. was supported by an MRC studentship (MR/N014294/1). P.J.S. and C.M.B. acknowledge Sulis at HPC Midlands+, which was funded by the EPSRC on grant EP/T022108/1, and the University of Warwick Scientific Computing Research Technology Platform for computational access. YSM acknowledges the NIH (R21AI168791) for funding. A.A.K. acknowledges support from NIH grant R01GM117372. This project made use of time on ARCHER2 and JADE2 granted via the UK High-End Computing Consortium for Biomolecular Simulation, HECBioSim ( http://www.hecbiosim.ac.uk ), supported by EPSRC (grant no. EP/R029407/1). H.S. acknowledges Funda\u00E7\u00E3o para a Ci\u00EAncia e a Tecnologia (PTDC/BIA-BQM/31031/2017 (Lisboa-01-0145-FEDER-031031), MOSTMICRO-ITQB, UIDB/04612/2020 and UIDP/04612/2020). T.L.L. thanks Academia Sinica for support. We thank Sara Rebelo for major technical assistance.
Publisher Copyright:
© The Author(s) 2025.
PY - 2025/4/29
Y1 - 2025/4/29
N2 - Tuberculosis (TB), a leading cause of death among infectious diseases globally, is caused by Mycobacterium tuberculosis (Mtb). The pathogenicity of Mtb is largely attributed to its complex cell envelope, which includes a class of glycolipids called phosphatidyl-myo-inositol mannosides (PIMs). These glycolipids maintain the integrity of the cell envelope, regulate permeability, and mediate host-pathogen interactions. PIMs comprise a phosphatidyl-myo-inositol core decorated with one to six mannose residues and up to four acyl chains. The mannosyltransferase PimE catalyzes the transfer of the fifth PIM mannose residue from a polyprenyl phosphate-mannose (PPM) donor. This step contributes to the proper assembly and function of the mycobacterial cell envelope; however, the structural basis for substrate recognition and the catalytic mechanism of PimE remain poorly understood. Here, we present the cryo-electron microscopy (cryo-EM) structures of PimE from Mycobacterium abscessus in its apo and product-bound form. The structures reveal a distinctive binding cavity that accommodates both donor and acceptor substrates/products. Key residues involved in substrate coordination and catalysis were identified and validated via in vitro assays and in vivo complementation, while molecular dynamics simulations delineated access pathways and binding dynamics. Our integrated approach provides comprehensive insights into PimE function and informs potential strategies for anti-TB therapeutics.
AB - Tuberculosis (TB), a leading cause of death among infectious diseases globally, is caused by Mycobacterium tuberculosis (Mtb). The pathogenicity of Mtb is largely attributed to its complex cell envelope, which includes a class of glycolipids called phosphatidyl-myo-inositol mannosides (PIMs). These glycolipids maintain the integrity of the cell envelope, regulate permeability, and mediate host-pathogen interactions. PIMs comprise a phosphatidyl-myo-inositol core decorated with one to six mannose residues and up to four acyl chains. The mannosyltransferase PimE catalyzes the transfer of the fifth PIM mannose residue from a polyprenyl phosphate-mannose (PPM) donor. This step contributes to the proper assembly and function of the mycobacterial cell envelope; however, the structural basis for substrate recognition and the catalytic mechanism of PimE remain poorly understood. Here, we present the cryo-electron microscopy (cryo-EM) structures of PimE from Mycobacterium abscessus in its apo and product-bound form. The structures reveal a distinctive binding cavity that accommodates both donor and acceptor substrates/products. Key residues involved in substrate coordination and catalysis were identified and validated via in vitro assays and in vivo complementation, while molecular dynamics simulations delineated access pathways and binding dynamics. Our integrated approach provides comprehensive insights into PimE function and informs potential strategies for anti-TB therapeutics.
UR - https://www.scopus.com/pages/publications/105003841654
U2 - 10.1038/s41467-025-57843-1
DO - 10.1038/s41467-025-57843-1
M3 - Article
C2 - 40301322
AN - SCOPUS:105003841654
SN - 2041-1723
VL - 16
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 3974
ER -