[{"publisher":"Springer Nature","article_processing_charge":"Yes","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"corr_author":"1","pmid":1,"doi":"10.1038/s41467-025-66409-0","oa":1,"acknowledgement":"We thank de Bono lab members for helpful comments on the manuscript, and the Mass Spec Facility at the Max Perutz Labs, notably WeiQiang Chen and Markus Hartl, for invaluable discussions and comments on mass spec analyses of worm samples. All LC-MS/MS analyses were performed on instruments of the Vienna BioCenter Core Facilities (VBCF). Microscopy was supported by the Scientific Services Units (SSU) of ISTA through resources provided by the Imaging & Optics Facility (IOF). We are grateful to Dr. Geraldine Seydoux (Johns Hopkins University) for worm strains and plasmids, and Dr. Seung-Jae V. Lee (KAIST) for RNAi clones. We are grateful to Ekaterina Lashmanova for designing the daf-16::TbID::mNG::3xFLAG knock-in construct and for her outstanding support in the lab. This work was supported by a Wellcome Investigator Award (209504/A/17/Z) to MdB and an ISTplus Fellowship to MA (Marie Sklodowska-Curie agreement No 754411).","department":[{"_id":"MaDe"}],"month":"12","project":[{"name":"ISTplus - Postdoctoral Fellowships","grant_number":"754411","_id":"260C2330-B435-11E9-9278-68D0E5697425","call_identifier":"H2020"},{"grant_number":"209504/A/17/Z","_id":"23870BE8-32DE-11EA-91FC-C7463DDC885E","name":"Molecular mechanisms of neural circuit function"}],"article_type":"original","volume":16,"author":[{"id":"C407B586-6052-11E9-B3AE-7006E6697425","first_name":"Murat","orcid":"0000-0001-8945-6992","full_name":"Artan, Murat","last_name":"Artan"},{"full_name":"Schön, Hanna","last_name":"Schön","first_name":"Hanna","id":"C8E17EDC-D7AA-11E9-B7B7-45ECE5697425"},{"orcid":"0000-0001-8347-0443","first_name":"Mario","id":"4E3FF80E-F248-11E8-B48F-1D18A9856A87","full_name":"De Bono, Mario","last_name":"De Bono"}],"publication_identifier":{"eissn":["2041-1723"]},"OA_type":"gold","oa_version":"Published Version","date_created":"2026-01-04T23:01:34Z","title":"Proximity labeling of DAF-16 FOXO highlights aging regulatory proteins","publication_status":"published","file":[{"access_level":"open_access","success":1,"content_type":"application/pdf","date_created":"2026-01-05T10:58:28Z","file_size":1642352,"checksum":"748e2e003b878b85b6048d51621d6aae","file_name":"2025_NatureComm_Artan.pdf","relation":"main_file","creator":"dernst","file_id":"20941","date_updated":"2026-01-05T10:58:28Z"}],"status":"public","PlanS_conform":"1","scopus_import":"1","ec_funded":1,"DOAJ_listed":"1","file_date_updated":"2026-01-05T10:58:28Z","acknowledged_ssus":[{"_id":"Bio"}],"publication":"Nature Communications","date_updated":"2026-01-05T11:00:03Z","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","ddc":["570"],"year":"2025","article_number":"11355","intvolume":"        16","OA_place":"publisher","date_published":"2025-12-11T00:00:00Z","quality_controlled":"1","type":"journal_article","external_id":{"pmid":["41381452"]},"_id":"20929","language":[{"iso":"eng"}],"abstract":[{"lang":"eng","text":"Insulin/insulin-like growth factor signaling inhibits FOXO transcription factors to control development, homeostasis, and aging. Here, we use proximity labeling to identify proteins interacting with the C. elegans FOXO DAF-16. We show that in well-fed, unstressed animals harboring active insulin signaling, DAF-16 forms a complex with the PAR-1/MARK serine/threonine kinase, a key regulator of cell polarity. PAR-1 inhibits DAF-16 accumulation and promotes DAF-16 phosphorylation at S249, at a conserved motif that PAR-1/human MARK2 phosphorylates in vitro. DAF-2 insulin-like receptor signaling stimulates DAF-16 S249 phosphorylation, suggesting DAF-2 activates PAR-1. DAF-2 also promotes PAR-1 expression by inhibiting DAF-16. PAR-1 knockdown, or DAF-16 S249A, prolong lifespan, whereas phosphomimetic DAF-16 S249D suppresses the longevity of daf-2 mutants. At low insulin signaling, DAF-16 proximity labeling highlights transcription factors, chromatin regulators, and DNA repair proteins. One interactor, the zinc finger/homeobox protein ZFH-2/ZFHX3, forms a complex with DAF-16 and prolongs lifespan. Our work provides entry points for hypothesis-driven studies of FOXO function and longevity."}],"citation":{"apa":"Artan, M., Schön, H., &#38; de Bono, M. (2025). Proximity labeling of DAF-16 FOXO highlights aging regulatory proteins. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-025-66409-0\">https://doi.org/10.1038/s41467-025-66409-0</a>","ieee":"M. Artan, H. Schön, and M. de Bono, “Proximity labeling of DAF-16 FOXO highlights aging regulatory proteins,” <i>Nature Communications</i>, vol. 16. Springer Nature, 2025.","short":"M. Artan, H. Schön, M. de Bono, Nature Communications 16 (2025).","mla":"Artan, Murat, et al. “Proximity Labeling of DAF-16 FOXO Highlights Aging Regulatory Proteins.” <i>Nature Communications</i>, vol. 16, 11355, Springer Nature, 2025, doi:<a href=\"https://doi.org/10.1038/s41467-025-66409-0\">10.1038/s41467-025-66409-0</a>.","chicago":"Artan, Murat, Hanna Schön, and Mario de Bono. “Proximity Labeling of DAF-16 FOXO Highlights Aging Regulatory Proteins.” <i>Nature Communications</i>. Springer Nature, 2025. <a href=\"https://doi.org/10.1038/s41467-025-66409-0\">https://doi.org/10.1038/s41467-025-66409-0</a>.","ista":"Artan M, Schön H, de Bono M. 2025. Proximity labeling of DAF-16 FOXO highlights aging regulatory proteins. Nature Communications. 16, 11355.","ama":"Artan M, Schön H, de Bono M. Proximity labeling of DAF-16 FOXO highlights aging regulatory proteins. <i>Nature Communications</i>. 2025;16. doi:<a href=\"https://doi.org/10.1038/s41467-025-66409-0\">10.1038/s41467-025-66409-0</a>"},"day":"11","has_accepted_license":"1"},{"publication":"Behavioral Neurogenetics","date_updated":"2025-04-14T07:43:58Z","page":"277-294","status":"public","ec_funded":1,"editor":[{"full_name":"Yamamoto, Daisuke","last_name":"Yamamoto","first_name":"Daisuke"}],"scopus_import":"1","_id":"11456","language":[{"iso":"eng"}],"abstract":[{"lang":"eng","text":"The proteomes of specialized structures, and the interactomes of proteins of interest, provide entry points to elucidate the functions of molecular machines. Here, we review a proximity-labeling strategy that uses the improved E. coli biotin ligase TurboID to characterize C. elegans protein complexes. Although the focus is on C. elegans neurons, the method is applicable regardless of cell type. We describe detailed extraction procedures that solubilize the bulk of C. elegans proteins and highlight the importance of tagging endogenous genes, to ensure physiological expression levels. We review issues associated with non-specific background noise and the importance of appropriate controls. As proof of principle, we review our analysis of the interactome of a presynaptic active zone protein, ELKS-1. Our aim is to provide a detailed protocol for TurboID-based proximity labeling in C. elegans and to highlight its potential and its limitations to characterize protein complexes and subcellular compartments in this animal."}],"type":"book_chapter","quality_controlled":"1","citation":{"ieee":"M. Artan and M. de Bono, “Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling,” in <i>Behavioral Neurogenetics</i>, vol. 181, D. Yamamoto, Ed. New York: Springer Nature, 2022, pp. 277–294.","short":"M. Artan, M. de Bono, in:, D. Yamamoto (Ed.), Behavioral Neurogenetics, Springer Nature, New York, 2022, pp. 277–294.","mla":"Artan, Murat, and Mario de Bono. “Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling.” <i>Behavioral Neurogenetics</i>, edited by Daisuke Yamamoto, vol. 181, Springer Nature, 2022, pp. 277–94, doi:<a href=\"https://doi.org/10.1007/978-1-0716-2321-3_15\">10.1007/978-1-0716-2321-3_15</a>.","apa":"Artan, M., &#38; de Bono, M. (2022). Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling. In D. Yamamoto (Ed.), <i>Behavioral Neurogenetics</i> (Vol. 181, pp. 277–294). New York: Springer Nature. <a href=\"https://doi.org/10.1007/978-1-0716-2321-3_15\">https://doi.org/10.1007/978-1-0716-2321-3_15</a>","ista":"Artan M, de Bono M. 2022.Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling. In: Behavioral Neurogenetics. Neuromethods, vol. 181, 277–294.","ama":"Artan M, de Bono M. Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling. In: Yamamoto D, ed. <i>Behavioral Neurogenetics</i>. Vol 181. NM. New York: Springer Nature; 2022:277-294. doi:<a href=\"https://doi.org/10.1007/978-1-0716-2321-3_15\">10.1007/978-1-0716-2321-3_15</a>","chicago":"Artan, Murat, and Mario de Bono. “Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling.” In <i>Behavioral Neurogenetics</i>, edited by Daisuke Yamamoto, 181:277–94. NM. New York: Springer Nature, 2022. <a href=\"https://doi.org/10.1007/978-1-0716-2321-3_15\">https://doi.org/10.1007/978-1-0716-2321-3_15</a>."},"day":"04","intvolume":"       181","year":"2022","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","date_published":"2022-06-04T00:00:00Z","acknowledgement":"We thank de Bono lab members for the helpful comments on the manuscript. The biotin-auxotrophic E. coli strain MG1655bioB:kan was a generous gift from J. Cronan (University of Illinois) and was kindly sent to us by Jessica Feldman and Ariana Sanchez (Stanford University). dg398 pEntryslot2_mNeongreen::3XFLAG::stop and dg397 pEntryslot3_mNeongreen::3XFLAG::stop::unc-54 3’UTR entry vector were kindly sent by Dr. Dominique Glauser (University of Fribourg). This work was supported by an Advanced ERC Grant (269058 ACMO) and a Wellcome Investigator Award (209504/Z/17/Z) to MdB and an ISTplus Fellowship to MA (Marie Sklodowska-Curie agreement No 754411).","doi":"10.1007/978-1-0716-2321-3_15","author":[{"last_name":"Artan","full_name":"Artan, Murat","first_name":"Murat","id":"C407B586-6052-11E9-B3AE-7006E6697425","orcid":"0000-0001-8945-6992"},{"full_name":"de Bono, Mario","last_name":"de Bono","id":"4E3FF80E-F248-11E8-B48F-1D18A9856A87","first_name":"Mario","orcid":"0000-0001-8347-0443"}],"volume":181,"project":[{"grant_number":"209504/A/17/Z","_id":"23870BE8-32DE-11EA-91FC-C7463DDC885E","name":"Molecular mechanisms of neural circuit function"},{"name":"ISTplus - Postdoctoral Fellowships","call_identifier":"H2020","_id":"260C2330-B435-11E9-9278-68D0E5697425","grant_number":"754411"}],"department":[{"_id":"MaDe"}],"month":"06","corr_author":"1","article_processing_charge":"No","publisher":"Springer Nature","series_title":"NM","publication_status":"published","place":"New York","publication_identifier":{"isbn":["9781071623206"],"eisbn":["9781071623213"],"issn":["0893-2336"],"eissn":["1940-6045"]},"title":"Proteomic Analysis of C. Elegans Neurons Using TurboID-Based Proximity Labeling","date_created":"2022-06-20T08:10:34Z","alternative_title":["Neuromethods"],"oa_version":"None"},{"publication_status":"published","file":[{"access_level":"open_access","file_size":2101656,"date_created":"2022-09-12T08:14:50Z","success":1,"content_type":"application/pdf","file_name":"2022_JBC_Artan.pdf","checksum":"e726c7b9315230e6710e0b1f1d1677e9","creator":"dernst","date_updated":"2022-09-12T08:14:50Z","relation":"main_file","file_id":"12092"}],"publication_identifier":{"issn":["0021-9258"],"eissn":["1083-351X"]},"title":"Depletion of endogenously biotinylated carboxylases enhances the sensitivity of TurboID-mediated proximity labeling in Caenorhabditis elegans","date_created":"2022-09-11T22:01:55Z","oa_version":"Published Version","oa":1,"doi":"10.1016/j.jbc.2022.102343","acknowledgement":"We thank de Bono laboratory members for helpful comments on the article and the Mass Spec Facilities at IST Austria and Max Perutz Labs for invaluable discussions and comments on how to optimize mass spec analyses of worm samples. We are grateful to Ekaterina Lashmanova for designing the degron knock-in constructs and preparing the injection mixes for CRISPR/Cas9-mediated genome editing. All LC–MS/MS analyses were performed on instruments of the Vienna BioCenter Core Facilities instrument pool.\r\nThis work was supported by a Wellcome Investigator Award (grant no.: 209504/Z/17/Z ) to M.d.B. and an ISTplus Fellowship to M.A. (Marie Sklodowska-Curie agreement no.: 754411).","volume":298,"author":[{"full_name":"Artan, Murat","last_name":"Artan","orcid":"0000-0001-8945-6992","first_name":"Murat","id":"C407B586-6052-11E9-B3AE-7006E6697425"},{"full_name":"Hartl, Markus","last_name":"Hartl","first_name":"Markus"},{"first_name":"Weiqiang","full_name":"Chen, Weiqiang","last_name":"Chen"},{"orcid":"0000-0001-8347-0443","id":"4E3FF80E-F248-11E8-B48F-1D18A9856A87","first_name":"Mario","full_name":"De Bono, Mario","last_name":"De Bono"}],"month":"09","department":[{"_id":"MaDe"}],"article_type":"original","project":[{"name":"Molecular mechanisms of neural circuit function","grant_number":"209504/A/17/Z","_id":"23870BE8-32DE-11EA-91FC-C7463DDC885E"},{"name":"ISTplus - Postdoctoral Fellowships","call_identifier":"H2020","_id":"260C2330-B435-11E9-9278-68D0E5697425","grant_number":"754411"}],"article_processing_charge":"No","corr_author":"1","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"publisher":"Elsevier","pmid":1,"external_id":{"isi":["000884241800011"],"pmid":["35933017"]},"language":[{"iso":"eng"}],"_id":"12082","abstract":[{"lang":"eng","text":"Proximity-dependent protein labeling provides a powerful in vivo strategy to characterize the interactomes of specific proteins. We previously optimized a proximity labeling protocol for Caenorhabditis elegans using the highly active biotin ligase TurboID. A significant constraint on the sensitivity of TurboID is the presence of abundant endogenously biotinylated proteins that take up bandwidth in the mass spectrometer, notably carboxylases that use biotin as a cofactor. In C. elegans, these comprise POD-2/acetyl-CoA carboxylase alpha, PCCA-1/propionyl-CoA carboxylase alpha, PYC-1/pyruvate carboxylase, and MCCC-1/methylcrotonyl-CoA carboxylase alpha. Here, we developed ways to remove these carboxylases prior to streptavidin purification and mass spectrometry by engineering their corresponding genes to add a C-terminal His10 tag. This allows us to deplete them from C. elegans lysates using immobilized metal affinity chromatography. To demonstrate the method's efficacy, we use it to expand the interactome map of the presynaptic active zone protein ELKS-1. We identify many known active zone proteins, including UNC-10/RIM, SYD-2/liprin-alpha, SAD-1/BRSK1, CLA-1/CLArinet, C16E9.2/Sentryn, as well as previously uncharacterized potentially synaptic proteins such as the ortholog of human angiomotin, F59C12.3 and the uncharacterized protein R148.3. Our approach provides a quick and inexpensive solution to a common contaminant problem in biotin-dependent proximity labeling. The approach may be applicable to other model organisms and will enable deeper and more complete analysis of interactors for proteins of interest."}],"quality_controlled":"1","type":"journal_article","citation":{"ama":"Artan M, Hartl M, Chen W, de Bono M. Depletion of endogenously biotinylated carboxylases enhances the sensitivity of TurboID-mediated proximity labeling in Caenorhabditis elegans. <i>Journal of Biological Chemistry</i>. 2022;298(9). doi:<a href=\"https://doi.org/10.1016/j.jbc.2022.102343\">10.1016/j.jbc.2022.102343</a>","ista":"Artan M, Hartl M, Chen W, de Bono M. 2022. Depletion of endogenously biotinylated carboxylases enhances the sensitivity of TurboID-mediated proximity labeling in Caenorhabditis elegans. Journal of Biological Chemistry. 298(9), 102343.","chicago":"Artan, Murat, Markus Hartl, Weiqiang Chen, and Mario de Bono. “Depletion of Endogenously Biotinylated Carboxylases Enhances the Sensitivity of TurboID-Mediated Proximity Labeling in Caenorhabditis Elegans.” <i>Journal of Biological Chemistry</i>. Elsevier, 2022. <a href=\"https://doi.org/10.1016/j.jbc.2022.102343\">https://doi.org/10.1016/j.jbc.2022.102343</a>.","mla":"Artan, Murat, et al. “Depletion of Endogenously Biotinylated Carboxylases Enhances the Sensitivity of TurboID-Mediated Proximity Labeling in Caenorhabditis Elegans.” <i>Journal of Biological Chemistry</i>, vol. 298, no. 9, 102343, Elsevier, 2022, doi:<a href=\"https://doi.org/10.1016/j.jbc.2022.102343\">10.1016/j.jbc.2022.102343</a>.","ieee":"M. Artan, M. Hartl, W. Chen, and M. de Bono, “Depletion of endogenously biotinylated carboxylases enhances the sensitivity of TurboID-mediated proximity labeling in Caenorhabditis elegans,” <i>Journal of Biological Chemistry</i>, vol. 298, no. 9. Elsevier, 2022.","short":"M. Artan, M. Hartl, W. Chen, M. de Bono, Journal of Biological Chemistry 298 (2022).","apa":"Artan, M., Hartl, M., Chen, W., &#38; de Bono, M. (2022). Depletion of endogenously biotinylated carboxylases enhances the sensitivity of TurboID-mediated proximity labeling in Caenorhabditis elegans. <i>Journal of Biological Chemistry</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.jbc.2022.102343\">https://doi.org/10.1016/j.jbc.2022.102343</a>"},"day":"01","has_accepted_license":"1","intvolume":"       298","article_number":"102343","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","ddc":["570"],"year":"2022","date_published":"2022-09-01T00:00:00Z","file_date_updated":"2022-09-12T08:14:50Z","date_updated":"2025-04-14T07:44:00Z","publication":"Journal of Biological Chemistry","isi":1,"acknowledged_ssus":[{"_id":"Bio"}],"status":"public","issue":"9","ec_funded":1,"scopus_import":"1"},{"oa_version":"Published Version","title":"MON-2, a Golgi protein, promotes longevity by upregulating autophagy through mediating inter-organelle communications","date_created":"2022-03-13T23:01:47Z","publication_identifier":{"eissn":["1554-8635"],"issn":["1554-8627"]},"publication_status":"published","pmid":1,"publisher":"Taylor & Francis","article_processing_charge":"No","article_type":"original","department":[{"_id":"MaDe"}],"month":"02","volume":18,"author":[{"full_name":"Artan, Murat","last_name":"Artan","orcid":"0000-0001-8945-6992","id":"C407B586-6052-11E9-B3AE-7006E6697425","first_name":"Murat"},{"full_name":"Sohn, Jooyeon","last_name":"Sohn","first_name":"Jooyeon"},{"last_name":"Lee","full_name":"Lee, Cheolju","first_name":"Cheolju"},{"full_name":"Park, Seung Yeol","last_name":"Park","first_name":"Seung Yeol"},{"last_name":"Lee","full_name":"Lee, Seung Jae V.","first_name":"Seung Jae V."}],"acknowledgement":"This work is funded by National Research Foundation of Korea (NRF) grants NRF-2019R1A3B2067745 from the Korean Government (Ministry of Science and Information and Communications Technology (S-J.V.L.). NRF-2017R1A5A1015366 (S.Y.P, S-J.V.L). Korea Institute of Science and Technology (KIST) intramural grant (C.L).","doi":"10.1080/15548627.2022.2039523","oa":1,"main_file_link":[{"open_access":"1","url":"https://doi.org/10.1080/15548627.2022.2039523"}],"date_published":"2022-02-19T00:00:00Z","year":"2022","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","intvolume":"        18","citation":{"ieee":"M. Artan, J. Sohn, C. Lee, S. Y. Park, and S. J. V. Lee, “MON-2, a Golgi protein, promotes longevity by upregulating autophagy through mediating inter-organelle communications,” <i>Autophagy</i>, vol. 18, no. 5. Taylor &#38; Francis, pp. 1208–1210, 2022.","short":"M. Artan, J. Sohn, C. Lee, S.Y. Park, S.J.V. Lee, Autophagy 18 (2022) 1208–1210.","mla":"Artan, Murat, et al. “MON-2, a Golgi Protein, Promotes Longevity by Upregulating Autophagy through Mediating Inter-Organelle Communications.” <i>Autophagy</i>, vol. 18, no. 5, Taylor &#38; Francis, 2022, pp. 1208–10, doi:<a href=\"https://doi.org/10.1080/15548627.2022.2039523\">10.1080/15548627.2022.2039523</a>.","apa":"Artan, M., Sohn, J., Lee, C., Park, S. Y., &#38; Lee, S. J. V. (2022). MON-2, a Golgi protein, promotes longevity by upregulating autophagy through mediating inter-organelle communications. <i>Autophagy</i>. Taylor &#38; Francis. <a href=\"https://doi.org/10.1080/15548627.2022.2039523\">https://doi.org/10.1080/15548627.2022.2039523</a>","ista":"Artan M, Sohn J, Lee C, Park SY, Lee SJV. 2022. MON-2, a Golgi protein, promotes longevity by upregulating autophagy through mediating inter-organelle communications. Autophagy. 18(5), 1208–1210.","ama":"Artan M, Sohn J, Lee C, Park SY, Lee SJV. MON-2, a Golgi protein, promotes longevity by upregulating autophagy through mediating inter-organelle communications. <i>Autophagy</i>. 2022;18(5):1208-1210. doi:<a href=\"https://doi.org/10.1080/15548627.2022.2039523\">10.1080/15548627.2022.2039523</a>","chicago":"Artan, Murat, Jooyeon Sohn, Cheolju Lee, Seung Yeol Park, and Seung Jae V. Lee. “MON-2, a Golgi Protein, Promotes Longevity by Upregulating Autophagy through Mediating Inter-Organelle Communications.” <i>Autophagy</i>. Taylor &#38; Francis, 2022. <a href=\"https://doi.org/10.1080/15548627.2022.2039523\">https://doi.org/10.1080/15548627.2022.2039523</a>."},"day":"19","type":"journal_article","quality_controlled":"1","language":[{"iso":"eng"}],"_id":"10846","abstract":[{"text":"The Golgi apparatus regulates the process of modification and subcellular localization of macromolecules, including proteins and lipids. Aberrant protein sorting caused by defects in the Golgi leads to various diseases in mammals. However, the role of the Golgi apparatus in organismal longevity remained largely unknown. By employing a quantitative proteomic approach, we demonstrated that MON-2, an evolutionarily conserved Arf-GEF protein implicated in Golgi-to-endosome trafficking, promotes longevity via upregulating macroautophagy/autophagy in C. elegans. Our data using cultured mammalian cells indicate that MON2 translocates from the Golgi to the endosome under starvation conditions, subsequently increasing autophagic flux by binding LGG-1/GABARAPL2. Thus, Golgi-to-endosome trafficking appears to be an evolutionarily conserved process for the upregulation of autophagy, which contributes to organismal longevity.","lang":"eng"}],"external_id":{"pmid":["35188063"],"isi":["000758859600001"]},"scopus_import":"1","issue":"5","status":"public","page":"1208-1210","isi":1,"date_updated":"2023-10-03T10:54:54Z","publication":"Autophagy"},{"type":"journal_article","quality_controlled":"1","_id":"10117","abstract":[{"text":"Proximity labeling provides a powerful in vivo tool to characterize the proteome of subcellular structures and the interactome of specific proteins. The nematode Caenorhabditis elegans is one of the most intensely studied organisms in biology, offering many advantages for biochemistry. Using the highly active biotin ligase TurboID, we optimize here a proximity labeling protocol for C. elegans. An advantage of TurboID is that biotin's high affinity for streptavidin means biotin-labeled proteins can be affinity-purified under harsh denaturing conditions. By combining extensive sonication with aggressive denaturation using SDS and urea, we achieved near-complete solubilization of worm proteins. We then used this protocol to characterize the proteomes of the worm gut, muscle, skin, and nervous system. Neurons are among the smallest C. elegans cells. To probe the method's sensitivity, we expressed TurboID exclusively in the two AFD neurons and showed that the protocol could identify known and previously unknown proteins expressed selectively in AFD. The active zones of synapses are composed of a protein matrix that is difficult to solubilize and purify. To test if our protocol could solubilize active zone proteins, we knocked TurboID into the endogenous elks-1 gene, which encodes a presynaptic active zone protein. We identified many known ELKS-1-interacting active zone proteins, as well as previously uncharacterized synaptic proteins. Versatile vectors and the inherent advantages of using C. elegans, including fast growth and the ability to rapidly make and functionally test knock-ins, make proximity labeling a valuable addition to the armory of this model organism.","lang":"eng"}],"language":[{"iso":"eng"}],"external_id":{"isi":["000706409200006"]},"has_accepted_license":"1","day":"01","citation":{"apa":"Artan, M., Barratt, S., Flynn, S. M., Begum, F., Skehel, M., Nicolas, A., &#38; de Bono, M. (2021). Interactome analysis of Caenorhabditis elegans synapses by TurboID-based proximity labeling. <i>Journal of Biological Chemistry</i>. Elsevier. <a href=\"https://doi.org/10.1016/J.JBC.2021.101094\">https://doi.org/10.1016/J.JBC.2021.101094</a>","ieee":"M. Artan <i>et al.</i>, “Interactome analysis of Caenorhabditis elegans synapses by TurboID-based proximity labeling,” <i>Journal of Biological Chemistry</i>, vol. 297, no. 3. Elsevier, 2021.","short":"M. Artan, S. Barratt, S.M. Flynn, F. Begum, M. Skehel, A. Nicolas, M. de Bono, Journal of Biological Chemistry 297 (2021).","mla":"Artan, Murat, et al. “Interactome Analysis of Caenorhabditis Elegans Synapses by TurboID-Based Proximity Labeling.” <i>Journal of Biological Chemistry</i>, vol. 297, no. 3, 101094, Elsevier, 2021, doi:<a href=\"https://doi.org/10.1016/J.JBC.2021.101094\">10.1016/J.JBC.2021.101094</a>.","chicago":"Artan, Murat, Stephen Barratt, Sean M. Flynn, Farida Begum, Mark Skehel, Armel Nicolas, and Mario de Bono. “Interactome Analysis of Caenorhabditis Elegans Synapses by TurboID-Based Proximity Labeling.” <i>Journal of Biological Chemistry</i>. Elsevier, 2021. <a href=\"https://doi.org/10.1016/J.JBC.2021.101094\">https://doi.org/10.1016/J.JBC.2021.101094</a>.","ista":"Artan M, Barratt S, Flynn SM, Begum F, Skehel M, Nicolas A, de Bono M. 2021. Interactome analysis of Caenorhabditis elegans synapses by TurboID-based proximity labeling. Journal of Biological Chemistry. 297(3), 101094.","ama":"Artan M, Barratt S, Flynn SM, et al. Interactome analysis of Caenorhabditis elegans synapses by TurboID-based proximity labeling. <i>Journal of Biological Chemistry</i>. 2021;297(3). doi:<a href=\"https://doi.org/10.1016/J.JBC.2021.101094\">10.1016/J.JBC.2021.101094</a>"},"year":"2021","ddc":["612"],"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","article_number":"101094","intvolume":"       297","date_published":"2021-09-01T00:00:00Z","file_date_updated":"2021-10-11T12:20:58Z","isi":1,"date_updated":"2025-04-14T07:43:46Z","publication":"Journal of Biological Chemistry","status":"public","scopus_import":"1","ec_funded":1,"issue":"3","publication_status":"published","file":[{"access_level":"open_access","file_size":1680010,"date_created":"2021-10-11T12:20:58Z","success":1,"content_type":"application/pdf","file_name":"2021_JBC_Artan.pdf","checksum":"19e39d36c5b9387c6dc0e89c9ae856ab","file_id":"10121","date_updated":"2021-10-11T12:20:58Z","relation":"main_file","creator":"cchlebak"}],"publication_identifier":{"issn":["0021-9258"],"eissn":["1083-351X"]},"oa_version":"Published Version","date_created":"2021-10-10T22:01:23Z","title":"Interactome analysis of Caenorhabditis elegans synapses by TurboID-based proximity labeling","acknowledgement":"We thank de Bono lab members for helpful comments on the manuscript, IST Austria and University of Vienna Mass Spec Facilities for invaluable discussions and comments for the optimization of mass spec analyses of worm samples. The biotin auxotropic E. coli strain MG1655bioB:kan was gift from John Cronan (University of Illinois) and was kindly sent to us by Jessica Feldman and Ariana Sanchez (Stanford University). dg398 pEntryslot2_mNeongreen::3XFLAG::stop and dg397 pEntryslot3_mNeongreen::3XFLAG::stop::unc-54 3′UTR entry vector were kindly shared by Dr Dominique Glauser (University of Fribourg). Codon-optimized mScarlet vector was a generous gift from Dr Manuel Zimmer (University of Vienna).","doi":"10.1016/J.JBC.2021.101094","oa":1,"article_type":"original","project":[{"_id":"260C2330-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","grant_number":"754411","name":"ISTplus - Postdoctoral Fellowships"}],"department":[{"_id":"MaDe"},{"_id":"LifeSc"}],"month":"09","volume":297,"author":[{"first_name":"Murat","id":"C407B586-6052-11E9-B3AE-7006E6697425","orcid":"0000-0001-8945-6992","last_name":"Artan","full_name":"Artan, Murat"},{"id":"57740d2b-2a88-11ec-97cf-d9e6d1b39677","first_name":"Stephen","full_name":"Barratt, Stephen","last_name":"Barratt"},{"first_name":"Sean M.","full_name":"Flynn, Sean M.","last_name":"Flynn"},{"full_name":"Begum, Farida","last_name":"Begum","first_name":"Farida"},{"full_name":"Skehel, Mark","last_name":"Skehel","first_name":"Mark"},{"id":"2A103192-F248-11E8-B48F-1D18A9856A87","first_name":"Armel","last_name":"Nicolas","full_name":"Nicolas, Armel"},{"last_name":"De Bono","full_name":"De Bono, Mario","id":"4E3FF80E-F248-11E8-B48F-1D18A9856A87","first_name":"Mario","orcid":"0000-0001-8347-0443"}],"publisher":"Elsevier","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"article_processing_charge":"Yes"},{"type":"journal_article","quality_controlled":"1","abstract":[{"lang":"eng","text":"Vaccinia virus–related kinase (VRK) is an evolutionarily conserved nuclear protein kinase. VRK-1, the single Caenorhabditis elegans VRK ortholog, functions in cell division and germline proliferation. However, the role of VRK-1 in postmitotic cells and adult life span remains unknown. Here, we show that VRK-1 increases organismal longevity by activating the cellular energy sensor, AMP-activated protein kinase (AMPK), via direct phosphorylation. We found that overexpression of vrk-1 in the soma of adult C. elegans increased life span and, conversely, inhibition of vrk-1 decreased life span. In addition, vrk-1 was required for longevity conferred by mutations that inhibit C. elegans mitochondrial respiration, which requires AMPK. VRK-1 directly phosphorylated and up-regulated AMPK in both C. elegans and cultured human cells. Thus, our data show that the somatic nuclear kinase, VRK-1, promotes longevity through AMPK activation, and this function appears to be conserved between C. elegans and humans."}],"_id":"15057","language":[{"iso":"eng"}],"has_accepted_license":"1","citation":{"ieee":"S. Park <i>et al.</i>, “VRK-1 extends life span by activation of AMPK via phosphorylation,” <i>Science Advances</i>, vol. 6, no. 27. American Association for the Advancement of Science, 2020.","short":"S. Park, M. Artan, S.H. Han, H.-E.H. Park, Y. Jung, A.B. Hwang, W.S. Shin, K.-T. Kim, S.-J.V. Lee, Science Advances 6 (2020).","mla":"Park, Sangsoon, et al. “VRK-1 Extends Life Span by Activation of AMPK via Phosphorylation.” <i>Science Advances</i>, vol. 6, no. 27, aaw7824, American Association for the Advancement of Science, 2020, doi:<a href=\"https://doi.org/10.1126/sciadv.aaw7824\">10.1126/sciadv.aaw7824</a>.","apa":"Park, S., Artan, M., Han, S. H., Park, H.-E. H., Jung, Y., Hwang, A. B., … Lee, S.-J. V. (2020). VRK-1 extends life span by activation of AMPK via phosphorylation. <i>Science Advances</i>. American Association for the Advancement of Science. <a href=\"https://doi.org/10.1126/sciadv.aaw7824\">https://doi.org/10.1126/sciadv.aaw7824</a>","ista":"Park S, Artan M, Han SH, Park H-EH, Jung Y, Hwang AB, Shin WS, Kim K-T, Lee S-JV. 2020. VRK-1 extends life span by activation of AMPK via phosphorylation. Science Advances. 6(27), aaw7824.","ama":"Park S, Artan M, Han SH, et al. VRK-1 extends life span by activation of AMPK via phosphorylation. <i>Science Advances</i>. 2020;6(27). doi:<a href=\"https://doi.org/10.1126/sciadv.aaw7824\">10.1126/sciadv.aaw7824</a>","chicago":"Park, Sangsoon, Murat Artan, Seung Hyun Han, Hae-Eun H. Park, Yoonji Jung, Ara B. Hwang, Won Sik Shin, Kyong-Tai Kim, and Seung-Jae V. Lee. “VRK-1 Extends Life Span by Activation of AMPK via Phosphorylation.” <i>Science Advances</i>. American Association for the Advancement of Science, 2020. <a href=\"https://doi.org/10.1126/sciadv.aaw7824\">https://doi.org/10.1126/sciadv.aaw7824</a>."},"day":"01","year":"2020","ddc":["570"],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","intvolume":"         6","article_number":"aaw7824","date_published":"2020-07-01T00:00:00Z","file_date_updated":"2024-03-04T09:46:41Z","publication":"Science Advances","date_updated":"2024-03-04T09:52:09Z","status":"public","issue":"27","publication_status":"published","file":[{"date_created":"2024-03-04T09:46:41Z","file_size":1864415,"success":1,"content_type":"application/pdf","access_level":"open_access","creator":"dernst","file_id":"15058","relation":"main_file","date_updated":"2024-03-04T09:46:41Z","file_name":"2020_ScienceAdvances_Park.pdf","checksum":"a37157cd0de709dce5fe03f4a31cd0b6"}],"publication_identifier":{"eissn":["2375-2548"]},"oa_version":"Published Version","date_created":"2024-03-04T09:41:57Z","title":"VRK-1 extends life span by activation of AMPK via phosphorylation","acknowledgement":"This research was supported by grants NRF-2019R1A3B2067745 and NRF-2017R1A5A1015366 funded by the Korean Government (MSIT) through the National Research Foundation (NRF) of Korea to S.-J.V.L. and by grant Basic Science Research Program (No. 2019R1A2C2009440) funded by the Korean Government (MSIT) through the NRF of Korea to K.-T.K. ","doi":"10.1126/sciadv.aaw7824","oa":1,"article_type":"original","month":"07","department":[{"_id":"MaDe"}],"volume":6,"author":[{"last_name":"Park","full_name":"Park, Sangsoon","first_name":"Sangsoon"},{"orcid":"0000-0001-8945-6992","first_name":"Murat","id":"C407B586-6052-11E9-B3AE-7006E6697425","full_name":"Artan, Murat","last_name":"Artan"},{"first_name":"Seung Hyun","full_name":"Han, Seung Hyun","last_name":"Han"},{"first_name":"Hae-Eun H.","last_name":"Park","full_name":"Park, Hae-Eun H."},{"full_name":"Jung, Yoonji","last_name":"Jung","first_name":"Yoonji"},{"last_name":"Hwang","full_name":"Hwang, Ara B.","first_name":"Ara B."},{"full_name":"Shin, Won Sik","last_name":"Shin","first_name":"Won Sik"},{"last_name":"Kim","full_name":"Kim, Kyong-Tai","first_name":"Kyong-Tai"},{"first_name":"Seung-Jae V.","last_name":"Lee","full_name":"Lee, Seung-Jae V."}],"publisher":"American Association for the Advancement of Science","tmp":{"image":"/images/cc_by_nc.png","short":"CC BY-NC (4.0)","name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode"},"article_processing_charge":"No"},{"file_date_updated":"2020-07-14T12:48:03Z","publication":"Nature Communications","date_updated":"2026-04-03T09:27:08Z","isi":1,"status":"public","scopus_import":"1","_id":"7804","language":[{"iso":"eng"}],"abstract":[{"lang":"eng","text":"Besides pro-inflammatory roles, the ancient cytokine interleukin-17 (IL-17) modulates neural circuit function. We investigate IL-17 signaling in neurons, and the extent it can alter organismal phenotypes. We combine immunoprecipitation and mass spectrometry to biochemically characterize endogenous signaling complexes that function downstream of IL-17 receptors in C. elegans neurons. We identify the paracaspase MALT-1 as a critical output of the pathway. MALT1 mediates signaling from many immune receptors in mammals, but was not previously implicated in IL-17 signaling or nervous system function. C. elegans MALT-1 forms a complex with homologs of Act1 and IRAK and appears to function both as a scaffold and a protease. MALT-1 is expressed broadly in the C. elegans nervous system, and neuronal IL-17–MALT-1 signaling regulates multiple phenotypes, including escape behavior, associative learning, immunity and longevity. Our data suggest MALT1 has an ancient role modulating neural circuit function downstream of IL-17 to remodel physiology and behavior."}],"external_id":{"pmid":["32350248"],"isi":["000531855500029"]},"type":"journal_article","quality_controlled":"1","has_accepted_license":"1","citation":{"mla":"Flynn, Sean M., et al. “MALT-1 Mediates IL-17 Neural Signaling to Regulate C. Elegans Behavior, Immunity and Longevity.” <i>Nature Communications</i>, vol. 11, 2099, Springer Nature, 2020, doi:<a href=\"https://doi.org/10.1038/s41467-020-15872-y\">10.1038/s41467-020-15872-y</a>.","short":"S.M. Flynn, C. Chen, M. Artan, S. Barratt, A. Crisp, G.M. Nelson, S.Y. Peak-Chew, F. Begum, M. Skehel, M. de Bono, Nature Communications 11 (2020).","ieee":"S. M. Flynn <i>et al.</i>, “MALT-1 mediates IL-17 neural signaling to regulate C. elegans behavior, immunity and longevity,” <i>Nature Communications</i>, vol. 11. Springer Nature, 2020.","apa":"Flynn, S. M., Chen, C., Artan, M., Barratt, S., Crisp, A., Nelson, G. M., … de Bono, M. (2020). MALT-1 mediates IL-17 neural signaling to regulate C. elegans behavior, immunity and longevity. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-020-15872-y\">https://doi.org/10.1038/s41467-020-15872-y</a>","ama":"Flynn SM, Chen C, Artan M, et al. MALT-1 mediates IL-17 neural signaling to regulate C. elegans behavior, immunity and longevity. <i>Nature Communications</i>. 2020;11. doi:<a href=\"https://doi.org/10.1038/s41467-020-15872-y\">10.1038/s41467-020-15872-y</a>","ista":"Flynn SM, Chen C, Artan M, Barratt S, Crisp A, Nelson GM, Peak-Chew SY, Begum F, Skehel M, de Bono M. 2020. MALT-1 mediates IL-17 neural signaling to regulate C. elegans behavior, immunity and longevity. Nature Communications. 11, 2099.","chicago":"Flynn, Sean M., Changchun Chen, Murat Artan, Stephen Barratt, Alastair Crisp, Geoffrey M. Nelson, Sew Yeu Peak-Chew, Farida Begum, Mark Skehel, and Mario de Bono. “MALT-1 Mediates IL-17 Neural Signaling to Regulate C. Elegans Behavior, Immunity and Longevity.” <i>Nature Communications</i>. Springer Nature, 2020. <a href=\"https://doi.org/10.1038/s41467-020-15872-y\">https://doi.org/10.1038/s41467-020-15872-y</a>."},"day":"29","intvolume":"        11","article_number":"2099","year":"2020","ddc":["570"],"user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","date_published":"2020-04-29T00:00:00Z","oa":1,"doi":"10.1038/s41467-020-15872-y","volume":11,"author":[{"first_name":"Sean M.","last_name":"Flynn","full_name":"Flynn, Sean M."},{"first_name":"Changchun","last_name":"Chen","full_name":"Chen, Changchun"},{"full_name":"Artan, Murat","last_name":"Artan","orcid":"0000-0001-8945-6992","id":"C407B586-6052-11E9-B3AE-7006E6697425","first_name":"Murat"},{"last_name":"Barratt","full_name":"Barratt, Stephen","first_name":"Stephen"},{"first_name":"Alastair","full_name":"Crisp, Alastair","last_name":"Crisp"},{"first_name":"Geoffrey M.","full_name":"Nelson, Geoffrey M.","last_name":"Nelson"},{"first_name":"Sew Yeu","last_name":"Peak-Chew","full_name":"Peak-Chew, Sew Yeu"},{"first_name":"Farida","full_name":"Begum, Farida","last_name":"Begum"},{"first_name":"Mark","full_name":"Skehel, Mark","last_name":"Skehel"},{"full_name":"De Bono, Mario","last_name":"De Bono","id":"4E3FF80E-F248-11E8-B48F-1D18A9856A87","first_name":"Mario","orcid":"0000-0001-8347-0443"}],"article_type":"original","month":"04","department":[{"_id":"MaDe"}],"tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"corr_author":"1","article_processing_charge":"No","publisher":"Springer Nature","pmid":1,"publication_status":"published","file":[{"access_level":"open_access","date_created":"2020-05-11T10:36:33Z","file_size":4609120,"content_type":"application/pdf","file_name":"2020_NatureComm_Flynn.pdf","checksum":"dce367abf2c1a1d15f58fe6f7de82893","relation":"main_file","file_id":"7817","creator":"dernst","date_updated":"2020-07-14T12:48:03Z"}],"publication_identifier":{"eissn":["2041-1723"]},"date_created":"2020-05-10T22:00:47Z","title":"MALT-1 mediates IL-17 neural signaling to regulate C. elegans behavior, immunity and longevity","oa_version":"Published Version"}]