Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity

Gupta, Tilak Kumar; Klumpe, Sven; Gries, Karin; Heinz, Steffen; Wietrzyñski, Wojciech; Ohnishi, Norikazu; Niemeyer, Justus; Spaniol, Benjamin; Schaffer, Miroslava; Rast, Anna; Ostermeier, Matthias; Strauß, Michael; Plitzko, Jürgen M.; Baumeister, Wolfgang; Rudack, Till; Sakamoto, Wataru; Nickelsen, Jörg; Schuller, Jan M.; Schroda, Michael; Engel, Benjamin D.

doi:10.1016/j.cell.2021.05.011

Cited by 100 publications

(135 citation statements)

References 127 publications

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“…The N. punctiforme Vipp1 C11-C17 models (Figure 2) are broadly consistent with concurrently reported Synechocystis Vipp1 and PspA structures (Gupta et al, 2021;Junglas et al, 2021, this issue of Cell). Future cryo-EM studies using N. punctiforme Vipp1 may facilitate higher resolution maps to be resolved with improved accuracy of main chain position and showing side chain detail.…”

Section: Limitations Of the Studysupporting

confidence: 87%

“…In this study, we use cryo-EM to show that Vipp1 and PspA form ESCRT-III-like filaments and provide a mechanism for Vipp1-mediated membrane remodeling. This is in line with parallel work carried out by other groups (Gupta et al, 2021;Junglas et al, 2021, this issue of Cell). Collectively, our data show that the wider ESCRT-III family of polymers, which includes Vipp1 and PspA, arose prior to the divergence of bacteria and archaea over 3 billion years ago and play common, conserved roles in membrane remodeling and repair across all domains of life.…”

Section: Introductionsupporting

confidence: 90%

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Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Liu

Tassinari

Souza

et al. 2021

Cell

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Section: Limitations Of the Studysupporting

confidence: 87%

Section: Introductionsupporting

confidence: 90%

Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Liu

Tassinari

Souza

et al. 2021

Cell

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“…Homologues of ESCRT-III and Vps4 are coded by the genomes of many archaeal species [55][56][57][58][59][60] , and shown to function in archaeal membrane remodelling during cytokinesis and virus release. More recently, PspA and Vipp1 have been recognized as bacterial ESCRT-III related proteins [61][62][63] . These observations suggest that a subset of ESCRT components have more ancient evolutionary origins.…”

Section: Introductionmentioning

confidence: 99%

Characterisation of the Ubiquitin-ESCRT pathway in Asgard archaea sheds new light on origins of membrane trafficking in eukaryotes

Hatano

Palani

Papatziamou

et al. 2021

Preprint

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The ESCRT machinery performs a critical role in membrane remodelling events in all eukaryotic cells, including in membrane trafficking, membrane repair, cytokinetic abscission, in viral egress, and in the generation of extracellular vesicles. While the machinery is complex in modern day eukaryotes, where it comprises dozens of proteins, the system has simpler and more ancient origins. Indeed, homologues of ESCRT-III and the Vps4 ATPase, the proteins that execute the final membrane scission reaction, play analogous roles in cytokinesis and potentially in extracellular vesicle formation in TACK archaea where ESCRT-I and II homologues seem to be absent. Here, we explore the phylogeny, structure, and biochemistry of homologues of the ESCRT machinery and the associated ubiquitylation system found in genome assemblies of the recently discovered Asgard archaea. In these closest living prokaryotic relatives of eukaryotes, we provide evidence for the ESCRT-I and II sub-complexes being involved in the ubiquitin-directed recruitment of ESCRT-III, as it is in eukaryotes. This analysis suggests a pre-eukaryotic origin for the Ub-coupled ESCRT system and a likely path of ESCRT evolution via a series of gene duplication and diversification events.

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“…Presumed to be the first membrane remodeling machinery to have evolved 1,2 , ESCRT-III acts on virtually all cellular membranes to promote membrane fission from within membrane necks, a process that is essential for many cellular functions such as formation of intralumenal vesicles (ILVs) from endosomal membranes, cytokinetic abscission of the plasma membrane, reformation of the nuclear envelope, and closure of autophagosomes [3][4][5] . Moreover, ESCRT-III catalyzes budding of various virions in eukaryotes and archaea [6][7][8][9][10][11] and functions in repairing lipid membranes, as shown for the eukaryotic and bacterial plasma, lysosomal, nuclear and plastid membranes 2,[12][13][14][15][16][17][18] , a function that is essential to sustain vacuolar confinement of pathogens during certain infections 19,20 . Unlike other membrane remodeling machineries, ESCRT-III can also function with a reverse orientation promoting membrane fission from the outside of membrane necks during release of peroxisomes, recycling of endosomes and lipid droplet formation [21][22][23] .…”

Section: Introductionmentioning

confidence: 99%

Vps60 initiates formation of alternative membrane-bound ESCRT-III filaments

Pfitzner

Zivkovic

Humbert

et al. 2022

Preprint

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Endosomal sorting complex required for transport-III (ESCRT-III)-driven membrane remodeling participates in many crucial cellular functions, from cell division to endosome maturation, and occurs on essentially all cellular organelles. In eukaryotes, ESCRT-III displays a remarkable molecular diversity in its subunits which may have been acquired through evolution to perform novel cellular functions. Here, we describe and characterize a novel ESCRT-III polymer initiated by the subunit Vps60. Membrane-bound Vps60 polymers recruit ESCRT-III subunits Vps2, Vps24, Did2 and Ist1, and undergo polymer turnover powered by the ATPase Vps4. Snf7- and Vps60 filaments can coexist on membranes without interacting. Their nucleation, polymerization and recruitment of downstream subunits remains unaffected by the presence of the respective other polymer. Taken together, our results suggest Vps60 and Snf7 form distinct ESCRT-III polymers, which overall, supports the notion of evolutionary diversification of ESCRT-III assemblies to perform specific cellular functions.

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Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity

Cited by 100 publications

References 127 publications

Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily

Characterisation of the Ubiquitin-ESCRT pathway in Asgard archaea sheds new light on origins of membrane trafficking in eukaryotes

Vps60 initiates formation of alternative membrane-bound ESCRT-III filaments

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