Dividing the Archaeal Way: The Ancient Cdv Cell-Division Machinery

Caspi, Yaron; Dekker, Cees

doi:10.3389/fmicb.2018.00174

Cited by 59 publications

(139 citation statements)

References 131 publications

(227 reference statements)

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“…The budding of enveloped viruses from the plasma membrane appears to be an analogous vesiculation process, as the bud neck is again narrow and the ESCRT-III/Vps4 machinery accumulates and is released rapidly (Baumgartel et al 2011, Bleck et al 2014, Feng et al 2013, Jouvenet et al 2011). Other analogous ESCRT-dependent vesiculation processes include ILV budding directly into the vacuole (the yeast equivalent of the lysosome) (Zhu et al 2017, Caspi & Dekker 2018), shedding microvesicle release from the plasma membrane (Choudhuri et al 2014, Matusek et al 2014, Nabhan et al 2012), and possibly also nuclear egress of the Herpes viral core particle (Lee et al 2012) and vesicle secretion at the ciliary transition zone (Diener et al 2015, Wood et al 2013). …”

Section: The Escrt Pathwaymentioning

confidence: 99%

Structures, Functions, and Dynamics of ESCRT-III/Vps4 Membrane Remodeling and Fission Complexes

McCullough

Frost

Sundquist

2018

Annu. Rev. Cell Dev. Biol.

222

272

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The endosomal sorting complexes required for transport (ESCRT) pathway mediates cellular membrane remodeling and fission reactions. The pathway comprises five core complexes: ALIX, ESCRT-I, ESCRT-II, ESCRT-III, and Vps4. These soluble complexes are typically recruited to target membranes by site-specific adaptors that bind one or both of the early-acting ESCRT factors: ALIX and ESCRT-I/ESCRT-II. These factors, in turn, nucleate assembly of ESCRT-III subunits into membrane-bound filaments that recruit the AAA ATPase Vps4. Together, ESCRT-III filaments and Vps4 remodel and sever membranes. Here, we review recent advances in our understanding of the structures, activities, and mechanisms of the ESCRT-III and Vps4 machinery, including the first high-resolution structures of ESCRT-III filaments, the assembled Vps4 enzyme in complex with an ESCRT-III substrate, the discovery that ESCRT-III/Vps4 complexes can promote both inside-out and outside-in membrane fission reactions, and emerging mechanistic models for ESCRT-mediated membrane fission.

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Section: The Escrt Pathwaymentioning

confidence: 99%

Structures, Functions, and Dynamics of ESCRT-III/Vps4 Membrane Remodeling and Fission Complexes

McCullough

Frost

Sundquist

2018

Annu. Rev. Cell Dev. Biol.

222

272

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“…It has been proposed that the archaeal S-layer assists the cell against turgor pressure (1, 9). Compensating for the absence of S-layer by forming a strong barrier at the site of cell division is hypothesized to be one role for Cdv proteins (27). The S-layer is believed to be a receptor for viruses and has been shown to change structure after viral induction and provide a barrier to virus egress during maturation of the SSV viral particle (28).…”

Section: Introductionmentioning

confidence: 99%

Revealing S-layer Functions in the Hyperthermophilic Crenarchaeon Sulfolobus islandicus

Zhang

et al. 2018

Preprint

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36The crystalline surface layer (S-layer), consisting of two glycoproteins SlaA and SlaB, is 37 considered to be the exclusive component of the cell envelope outside of the cytoplasmic 38 membrane in Sulfolobus species. Although biochemically and structurally characterized, the S-39 layer in vivo functions remain largely elusive in Archaea. Here, we investigate how the S-layer 40 genes contribute to the S-layer architecture and affect cellular physiology in a crenarchaeal 41 model, Sulfolobus islandicus M.16.4. Electron micrographs of mutant cells lacking slaA or both 42 slaA and slaB confirm the absence of the outermost layer (SlaA), whereas cells with intact, 43 partially, or completely detached SlaA are observed for the ΔslaB mutant. Importantly, we 44 identify a novel S-layer-associated protein M164_1049, which does not functionally replace its 45 homolog SlaB but likely assists SlaB to stabilize SlaA. Additionally, we find that mutants 46 deficient in SlaA form large cell aggregates and the individual cell size varies significantly. The 47 slaB gene deletion also causes noticeable cellular aggregation, but the size of those aggregates 48 is smaller when compared to ΔslaA and ΔslaAB mutants. We further show the ΔslaA mutant 49 cells exhibit more sensitivity to hyperosmotic stress but are not reduced to wild-type cell size. 50Finally, we demonstrate that the ΔslaA mutant contains aberrant chromosome copy numbers 51 not seen in wild-type cells where the cell cycle is tightly regulated. Together these data suggest 52 that the lack of slaA results in either cell fusion or irregularities in cell division. Our studies 53 provide novel insights into the physiological and cellular functions of the S-layer in Archaea. 55Significance 56Rediscovery of the ancient evolutionary relationship between archaea and eukaryotes has 57 revitalized interest in archaeal cell biology. Key to understanding the archaeal cell is the S-58 layer which is ubiquitous in Archaea but whose in vivo function is unknown. In this study, we 59 genetically dissect how the two well-known S-layer genes as well as a newly identified S-layer-60 associated-protein-encoding gene contribute to the S-layer architecture in a hyperthermophilic 61 crenarchaeal model S. islandicus. We provide genetic evidence for the first time showing that 62 the slaA gene is a key cell morphology determinant and may play a role in Sulfolobus cell 63 division or cell fusion.64 65 66 67 68 69 70 71 72The primary interface between the cell and its environment is a multi-functional cellular 73 envelope. Comprised in this structure in some bacterial and most archaeal cells is a 74 proteinaceous 2D-crystalline matrix coating the outside of the cell called the surface layer (S-75 layer). Despite its broad distribution in cells from two domains, a generalized function of the 76 S-layer has not been identified. One unifying concept suggests the S-layer functions as an 77 exoskeleton that interacts with other proteins in the cell membrane to coordinate diverse 78 internal and externa...

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“…[89] Though not much is currently known aboutt his particular system, there is as ignificant body of work on the eukaryotic ESCRT system that helps to inform our understanding of the CdvABC system.R econstituting the CdvABC system in al iposome to induce as uccessful division event would mark as ignificant step forward in creatingarobust but simple divisions ystem for aSynCell. [89] Though not much is currently known aboutt his particular system, there is as ignificant body of work on the eukaryotic ESCRT system that helps to inform our understanding of the CdvABC system.R econstituting the CdvABC system in al iposome to induce as uccessful division event would mark as ignificant step forward in creatingarobust but simple divisions ystem for aSynCell.…”

Section: The Eukaryotic Escrt System and The Archaeal Cdvabc Systemmentioning

confidence: 99%

“…[87,88] Cdv proteins are organized into two groups.T he first group is encoded by cdvA, cdvB,a nd cdvC genes organized on one chromosomal locus, and the second group is encoded by three cdvB paralogueso rganized at different locations along the chromosome. [89] Current research suggests that the four CdvB genes are homologues to the eukaryotic ESCRT-III class, [89] and CdvC is ah omologue of Vps4. [90] CdvA can bind to the membrane, so it is often modeled as the recruiter of CdvB to the membrane (Figure 7).…”

Section: The Eukaryotic Escrt System and The Archaeal Cdvabc Systemmentioning

confidence: 99%

“…The CdvABC system is ap romisingc andidate for dividing SynCellsd ue to its simplicity.T he system comprises only of three core proteins and three accessory proteins. [89] Though not much is currently known aboutt his particular system, there is as ignificant body of work on the eukaryotic ESCRT system that helps to inform our understanding of the CdvABC system.R econstituting the CdvABC system in al iposome to induce as uccessful division event would mark as ignificant step forward in creatingarobust but simple divisions ystem for aSynCell.…”

Section: The Eukaryotic Escrt System and The Archaeal Cdvabc Systemmentioning

confidence: 99%

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Lessons from a Minimal Genome: What Are the Essential Organizing Principles of a Cell Built from Scratch?

et al. 2019

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One of the primary challenges facing synthetic biology is reconstituting a living system from its component parts. A particularly difficult landmark is reconstituting a self‐organizing system that can undergo autonomous chromosome compaction, segregation, and cell division. Here, we discuss how the syn3.0 minimal genome can inform us of the core self‐organizing principles of a living cell and how these self‐organizing processes can be built from the bottom up. The review underscores the importance of fundamental biology in rebuilding life from its molecular constituents.

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Dividing the Archaeal Way: The Ancient Cdv Cell-Division Machinery

Cited by 59 publications

References 131 publications

Structures, Functions, and Dynamics of ESCRT-III/Vps4 Membrane Remodeling and Fission Complexes

Structures, Functions, and Dynamics of ESCRT-III/Vps4 Membrane Remodeling and Fission Complexes

Revealing S-layer Functions in the Hyperthermophilic Crenarchaeon Sulfolobus islandicus

Lessons from a Minimal Genome: What Are the Essential Organizing Principles of a Cell Built from Scratch?

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