Synergy between a cytoplasmic vWFA/VIT protein and a WD40-repeat F-box protein controls development in Dictyostelium
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 s...
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| Published in | Frontiers in cell and developmental biology Vol. 11; p. 1259844 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Media S.A
14.09.2023
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| Subjects | |
| Online Access | Get full text |
| ISSN | 2296-634X 2296-634X |
| DOI | 10.3389/fcell.2023.1259844 |
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| Abstract | 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 O
2
-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. |
|---|---|
| AbstractList | 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. 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 O 2 -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. 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.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. Like most eukaryotes, the pre-metazoan social amoeba depends on the SCF (Skp1/cullin-1/F-box protein) family of E3 ubiquitin ligases to regulate its proteome. In , 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 O -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 -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. |
| Author | Gas-Pascual, Elisabet van der Wel, Hanke West, Christopher M. Kim, Hyun W. Boland, Andrew W. |
| AuthorAffiliation | 1 Department of Biochemistry and Molecular Biology, University of Georgia , Athens , GA , United States 2 Complex Carbohydrate Research Center, University of Georgia , Athens , GA , United States 3 Center for Tropical and Emerging Global Diseases , University of Georgia , Athens , GA , United States |
| AuthorAffiliation_xml | – name: 2 Complex Carbohydrate Research Center, University of Georgia , Athens , GA , United States – name: 3 Center for Tropical and Emerging Global Diseases , University of Georgia , Athens , GA , United States – name: 1 Department of Biochemistry and Molecular Biology, University of Georgia , Athens , GA , United States |
| Author_xml | – sequence: 1 givenname: Andrew W. surname: Boland fullname: Boland, Andrew W. – sequence: 2 givenname: Elisabet surname: Gas-Pascual fullname: Gas-Pascual, Elisabet – sequence: 3 givenname: Hanke surname: van der Wel fullname: van der Wel, Hanke – sequence: 4 givenname: Hyun W. surname: Kim fullname: Kim, Hyun W. – sequence: 5 givenname: Christopher M. surname: West fullname: West, Christopher M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37779900$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1002/pmic.200900516 10.1006/plas.1999.1391 10.1038/s41398-021-01681-4 10.1016/j.mib.2015.04.006 10.1074/jbc.271.22.12814 10.1186/s12864-015-1491-7 10.1093/pcp/pcf151 10.1016/j.canlet.2003.09.011 10.1146/annurev.biochem.78.101807.093809 10.1074/jbc.R300039200 10.1093/nar/gkab301 10.1073/pnas.050005097 10.1038/nrm3582 10.1242/dev.118.2.353 10.1074/jbc.RA119.011916 10.1016/j.celrep.2019.12.059 10.1093/nar/gkv314 10.1016/j.bpj.2017.03.011 10.1038/ncb2755 10.3852/mycologia.97.1.178 10.1002/pmic.200900352 10.1074/mcp.M114.044560 10.1186/gb-2010-11-3-r35 10.1038/ncomms8551 10.3892/ol.2018.7972 10.1016/s0074-7696(02)22016-1 10.1146/annurev-biochem-090120-013613 10.1101/gad.1252404 10.3390/cancers14030488 10.1038/nprot.2016.008 10.1093/nar/gkab1061 10.1038/329219a0 10.1073/pnas.80.22.6750 10.1042/bj1190175 10.1016/j.dnarep.2014.05.003 10.3389/fphys.2019.00390 10.1038/sj.embor.7400851 10.1387/ijdb.190260eb 10.1016/j.ydbio.2010.10.013 10.1093/glycob/12.2.17r 10.1016/0014-4827(71)90107-8 10.1111/j.1600-0854.2009.00992.x 10.1016/j.jbc.2022.102305 10.1074/jbc.M112.355446 10.1074/jbc.M109.022574 10.1242/dev.000893 10.1042/bj3150001 10.1002/iub.1011 10.1074/jbc.M110.190678 10.1016/j.molcel.2005.09.003 10.1093/glycob/cwz049 10.1111/j.1755-148X.2012.01018.x 10.1091/mbc.e02-05-0259 10.1186/1471-213X-12-31 10.3389/fphys.2022.827435 10.1038/s41586-021-03819-2 10.1006/bbrc.2002.6472 10.1387/ijdb.190226pf 10.3389/fcell.2020.00039 10.1016/j.biocel.2007.02.012 10.1074/jbc.273.29.18242 10.1073/pnas.1934602100 10.3390/cells8101187 10.1016/j.bbamcr.2013.05.026 10.1186/s12915-021-01108-y 10.1016/j.celrep.2015.07.039 10.1016/S0960-9822(00)80020-2 10.1007/978-981-15-1025-0_3 10.1146/annurev.immunol.25.022106.141618 10.1101/gad.871101 10.1016/s0092-8674(00)00057-x 10.1099/mic.0.000653 10.1128/EC.05053-11 10.1038/s41598-018-36618-3 10.1016/j.str.2006.10.001 10.1016/j.bbamcr.2004.09.027 10.1074/jbc.M115.703751 |
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| Copyright | Copyright © 2023 Boland, Gas-Pascual, van der Wel, Kim and West. Copyright © 2023 Boland, Gas-Pascual, van der Wel, Kim and West. 2023 Boland, Gas-Pascual, van der Wel, Kim and West |
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| Keywords | VIT RING F-box protein E3(SCF)ubiquitin-ligase von willebrand domain A glycosylation cellular slime mold |
| Language | English |
| License | Copyright © 2023 Boland, Gas-Pascual, van der Wel, Kim and West. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Barbara Pergolizzi, University of Turin, Italy Present address: Andrew W. Boland, Independent Researcher, Watertown, MA, United States Edited by: Pauline Schaap, University of Dundee, United Kingdom Margaret Nelson, Allegheny College, United States |
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Dictyostelium
depends on the SCF (Skp1/cullin-1/F-box protein) family of E3 ubiquitin ligases to regulate... Like most eukaryotes, the pre-metazoan social amoeba depends on the SCF (Skp1/cullin-1/F-box protein) family of E3 ubiquitin ligases to regulate its proteome.... 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... |
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| Title | Synergy between a cytoplasmic vWFA/VIT protein and a WD40-repeat F-box protein controls development in Dictyostelium |
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