Mechanism for Vipp1 spiral formation, ring biogenesis, and membrane repair

Liu, J. et al. Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. Cell 184, 3660–3673 (2021).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Tarrason Risa, G. et al. The proteasome controls ESCRT-III–mediated cell division in an archaeon. Science 369, eaaz2532 (2020).

Votteler, J. & Sundquist, W. I. Virus budding and the ESCRT pathway. Cell Host Microbe 14, 232–241 (2013).

Article  CAS  PubMed  Google Scholar 

Liu, J. et al. Functional assignment of multiple ESCRT‐III homologs in cell division and budding in Sulfolobus islandicus. Mol. Microbiol. 105, 540–553 (2017).

Article  CAS  PubMed  Google Scholar 

Juan, T. & Fürthauer, M. Biogenesis and function of ESCRT-dependent extracellular vesicles. Semin. Cell Dev. Biol. 74, 66–77 (2018).

Article  CAS  PubMed  Google Scholar 

Ellen, A. F. et al. Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles 13, 67–79 (2009).

Article  CAS  PubMed  Google Scholar 

Tang, S. et al. Structural basis for activation, assembly and membrane binding of ESCRT-III Snf7 filaments. eLife 4, e12548 (2015).

Olmos, Y. The ESCRT machinery: remodeling, repairing, and sealing membranes. Membranes 12, 633 (2022).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Junglas, B. et al. PspA adopts an ESCRT-III-like fold and remodels bacterial membranes. Cell 184, 3674–3688 (2021).

Article  CAS  PubMed  Google Scholar 

Brissette, J. L., Russel, M., Weiner, L. & Model, P. Phage shock protein, a stress protein of Escherichia coli. Proc. Natl Acad. Sci. USA 87, 862–866 (1990).

Joly, N. et al. Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol. Rev. 34, 797–827 (2010).

Article  CAS  PubMed  Google Scholar 

Kobayashi, R., Suzuki, T. & Yoshida, M. Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66, 100–109 (2007).

Article  CAS  PubMed  Google Scholar 

McDonald, C., Jovanovic, G., Ces, O. & Buck, M. Membrane stored curvature elastic stress modulates recruitment of maintenance proteins PspA and Vipp1. mBio 6, e01188-15 (2015).

Yamaguchi, S., Gueguen, E., Horstman, N. K. & Darwin, A. J. Membrane association of PspA depends on activation of the phage-shock-protein response in Yersinia enterocolitica. Mol. Microbiol. 78, 429–443 (2010).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Aseeva, E. et al. Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol. Biochem. 45, 119–128 (2007).

Article  CAS  PubMed  Google Scholar 

Fuhrmann, E., Gathmann, S., Rupprecht, E., Golecki, J. & Schneider, D. Thylakoid membrane reduction affects the photosystem stoichiometry in the Cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 149, 735–744 (2009).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Gao, H. & Xu, X. Depletion of Vipp1 in Synechocystis sp. PCC 6803 affects photosynthetic activity before the loss of thylakoid membranes. FEMS Microbiol. Lett. 292, 63–70 (2009).

Article  CAS  PubMed  Google Scholar 

Gutu, A., Chang, F. & O’Shea, E. K. Dynamical localization of a thylakoid membrane binding protein is required for acquisition of photosynthetic competency. Mol. Microbiol. 108, 16–31 (2018).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Nordhues, A. et al. Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell 24, 637–659 (2012).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Kroll, D. et al. VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc. Natl Acad. Sci. USA 98, 4238–4242 (2001).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Lo, S. M. & Theg, S. M. Role of vesicle-inducing protein in plastids 1 in cpTat transport at the thylakoid. Plant J. 71, 656–668 (2012).

Article  CAS  PubMed  Google Scholar 

Walter, B., Hristou, A., Nowaczyk, M. M. & Schünemann, D. In vitro reconstitution of co-translational D1 insertion reveals a role of the cpSec–Alb3 translocase and Vipp1 in photosystem II biogenesis. Biochem. J. 468, 315–324 (2015).

Article  CAS  PubMed  Google Scholar 

Westphal, S., Heins, L., Soll, J. & Vothknecht, U. C. Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proc. Natl Acad. Sci. USA 98, 4243–4248 (2001).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Zhang, L. & Sakamoto, W. Possible function of VIPP1 in maintaining chloroplast membranes. Biochim. Biophys. Acta 1847, 831–837 (2015).

Article  CAS  PubMed  Google Scholar 

McCullough, J., Frost, A. & Sundquist, W. I. Structures, functions, and dynamics of ESCRT-III/Vps4 membrane remodeling and fission complexes. Annu. Rev. Cell Dev. Biol. 34, 85–109 (2018).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Schlösser, L., Sachse, C., Low, H. H. & Schneider, D. Conserved structures of ESCRT-III superfamily members across domains of life. Trends Biochem. Sci. 48, 993–1004 (2023).

Article  PubMed  Google Scholar 

Pfitzner, A.-K., Moser von Filseck, J. & Roux, A. Principles of membrane remodeling by dynamic ESCRT-III polymers. Trends Cell Biol. 31, 856–868 (2021).

Article  CAS  PubMed  Google Scholar 

Buchkovich, N. J., Henne, W. M., Tang, S. & Emr, S. D. Essential N-terminal insertion motif anchors the ESCRT-III filament during MVB vesicle formation. Dev. Cell 27, 201–214 (2013).

Otters, S. et al. The first α-helical domain of the vesicle-inducing protein in plastids 1 promotes oligomerization and lipid binding. Planta 237, 529–540 (2013).

Article  CAS  PubMed  Google Scholar 

Heidrich, J. et al. Organization into higher ordered ring structures counteracts membrane binding of IM30, a protein associated with inner membranes in chloroplasts and cyanobacteria. J. Biol. Chem. 291, 14954–14962 (2016).

Zhang, L., Kondo, H., Kamikubo, H., Kataoka, M. & Sakamoto, W. VIPP1 has a disordered C-terminal tail necessary for protecting photosynthetic membranes against stress. Plant Physiol. 171, 1983–1995 (2016).

Article  PubMed  PubMed Central  Google Scholar 

Hennig, R. et al. The IM30/Vipp1 C-terminus associates with the lipid bilayer and modulates membrane fusion. Biochim. Biophys. Acta 1858, 126–136 (2017).

Article  CAS  Google Scholar 

Hennig, R. et al. IM30 triggers membrane fusion in cyanobacteria and chloroplasts. Nat. Commun. 6, 7018 (2015).

Article  CAS  PubMed  Google Scholar 

McCullough, J. et al. Structure and membrane remodeling activity of ESCRT-III helical polymers. Science 350, 1548–1551 (2015).

Article  CAS  PubMed  PubMed Central  Google Scholar 

Gupta, T. K. et al. Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity. Cell 184, 3643–3659 (2021).

Article  CAS  PubMed  Google Scholar 

Comments (0)

No login
gif