Oxygen-dependent regulation of E3(SCF)ubiquitin ligases and a Skp1-associated JmjD6 homolog in development of the social amoeba Dictyostelium

Boland, Andrew W.; Gas-Pascual, Elisabet; Nottingham, Braxton L.; Wel, Hanke van der; Sheikh, M. Osman; Schafer, Christopher M.; West, Christopher M.

doi:10.1016/j.jbc.2022.102305

Cited by 4 publications

(12 citation statements)

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“… a, Loomis, 1971 ; b, Parikh et al, 2010 ; c, Boland et al, 2022 ; d, Sheikh et al, 2015 ; e, Gruenheit et al, 2021 . …”

Section: Methodsunclassified

“…A strain in which the C-terminus of FbxwD (dictyBase DDB_G0292312) is similarly FLAG 3 -tagged was described previously ( Boland et al, 2022 ). A related strain in which the C-terminus is tagged with FLAG 3 and two ubiquitin-binding domains (UBA 2 ) in tandem was produced as follows.…”

Section: Methodsmentioning

confidence: 99%

“…This process is dependent on concerted transcriptional ( Rosengarten et al, 2015 ; Santhanam et al, 2015 ) and proteomic ( Bakthavatsalam and Gomer, 2010 ; Czarna et al, 2010 ; González-Velasco et al, 2019 ) changes. The significance of proteomic changes is emphasized by the effects on development of mutations in FBPs (e.g., Ennis et al, 2000 ; Mohanty et al, 2001 ) and inhibitors of the ubiquitin-proteasome system ( Pergolizzi et al, 2019 ; Boland et al, 2022 ; Kim et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…Its Skp1 subunit is post-translationally modified by hydroxylation of a proline in an oxygen dependent manner and subsequent glycosylation with a pentasaccharide ( Teng-umnuay et al, 1998 ). Loss of the prolyl hydroxylase responsible for generating the anchor point for the Skp1-glycan modifies the O 2 -setpoint for permitting its transition from the motile slug stage of development to mature fruiting bodies ( West et al, 2007 ), by a mechanism that involves the proteasome ( Boland et al, 2022 ). The addition of the glycan is required for mediating the O 2 -dependence ( Wang et al, 2009 ; Wang et al, 2011 ), and has been shown to increase Skp1’s level of interaction with several F-box proteins, including the WD40 domain containing FBP FbxwD ( Sheikh et al, 2015 ; Boland et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…Loss of the prolyl hydroxylase responsible for generating the anchor point for the Skp1-glycan modifies the O 2 -setpoint for permitting its transition from the motile slug stage of development to mature fruiting bodies ( West et al, 2007 ), by a mechanism that involves the proteasome ( Boland et al, 2022 ). The addition of the glycan is required for mediating the O 2 -dependence ( Wang et al, 2009 ; Wang et al, 2011 ), and has been shown to increase Skp1’s level of interaction with several F-box proteins, including the WD40 domain containing FBP FbxwD ( Sheikh et al, 2015 ; Boland et al, 2022 ). Building from findings in Dictyostelium , the Skp1 modification has been described in the human parasite Toxoplasma gondii ( Xu et al, 2012a ; Rahman et al, 2016 ) and the plant pathogen Pythium ultimum ( van der Wel et al, 2019 ), and the modification genes are evident in many other unicellular organisms including pathogenic fungi ( West and Blader, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

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Synergy between a cytoplasmic vWFA/VIT protein and a WD40-repeat F-box protein controls development in Dictyostelium

Boland,

Gas-Pascual,

van der Wel

et al. 2023

Front. Cell Dev. Biol.

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Like most eukaryotes, the pre-metazoan social amoeba Dictyostelium depends on the SCF (Skp1/cullin-1/F-box protein) family of E3 ubiquitin ligases to regulate its proteome. In Dictyostelium, starvation induces a transition from unicellular feeding to a multicellular slug that responds to external signals to culminate into a fruiting body containing terminally differentiated stalk and spore cells. These transitions are subject to regulation by F-box proteins and O2-dependent posttranslational modifications of Skp1. Here we examine in greater depth the essential role of FbxwD and Vwa1, an intracellular vault protein inter-alpha-trypsin (VIT) and von Willebrand factor-A (vWFA) domain containing protein that was found in the FbxwD interactome by co-immunoprecipitation. Reciprocal co-IPs using gene-tagged strains confirmed the interaction and similar changes in protein levels during multicellular development suggested co-functioning. FbxwD overexpression and proteasome inhibitors did not affect Vwa1 levels suggesting a non-substrate relationship. Forced FbxwD overexpression in slug tip cells where it is normally enriched interfered with terminal cell differentiation by a mechanism that depended on its F-box and RING domains, and on Vwa1 expression itself. Whereas vwa1-disruption alone did not affect development, overexpression of either of its three conserved domains arrested development but the effect depended on Vwa1 expression. Based on structure predictions, we propose that the Vwa1 domains exert their negative effect by artificially activating Vwa1 from an autoinhibited state, which in turn imbalances its synergistic function with FbxwD. Autoinhibition or homodimerization might be relevant to the poorly understood tumor suppressor role of the evolutionarily related VWA5A/BCSC-1 in humans.

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“… a, Loomis, 1971 ; b, Parikh et al, 2010 ; c, Boland et al, 2022 ; d, Sheikh et al, 2015 ; e, Gruenheit et al, 2021 . …”

Section: Methodsunclassified

Section: Methodsmentioning

confidence: 99%