{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T01:56:37Z","timestamp":1793325397828,"version":"4.5.0"},"reference-count":86,"publisher":"Springer Science and Business Media LLC","issue":"8","license":[{"start":{"date-parts":[[2025,5,15]],"date-time":"2025-05-15T00:00:00Z","timestamp":1747267200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2025,5,15]],"date-time":"2025-05-15T00:00:00Z","timestamp":1747267200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Struct Mol Biol"],"published-print":{"date-parts":[[2025,8]]},"DOI":"10.1038\/s41594-025-01554-0","type":"journal-article","created":{"date-parts":[[2025,5,15]],"date-time":"2025-05-15T05:02:28Z","timestamp":1747285348000},"page":"1408-1423","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Reciprocal stabilization of CtBP and TRIM28 represses autophagy to promote metastasis"],"prefix":"10.1038","volume":"32","author":[{"given":"Lixin","family":"Tai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongliang","family":"Zhu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ping","family":"Tang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiajia","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junyi","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peipei","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhonghua","family":"Tao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2058-8054","authenticated-orcid":false,"given":"Haipeng","family":"Lei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4832-3354","authenticated-orcid":false,"given":"Kai","family":"Miao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hong-xia","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4782-5320","authenticated-orcid":false,"given":"Shuhai","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Man","family":"Dou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7369-5227","authenticated-orcid":false,"given":"Han-Ming","family":"Shen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8033-3902","authenticated-orcid":false,"given":"Chuxia","family":"Deng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7313-6991","authenticated-orcid":false,"given":"Li-jun","family":"Di","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,5,15]]},"reference":[{"key":"1554_CR1","doi-asserted-by":"publisher","first-page":"4176","DOI":"10.1073\/pnas.1717800115","volume":"115","author":"S Vega-Rubin-de-Celis","year":"2018","unstructured":"Vega-Rubin-de-Celis, S. et al. Increased autophagy blocks HER2-mediated breast tumorigenesis. Proc. Natl Acad. Sci. USA 115, 4176\u20134181 (2018).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1554_CR2","doi-asserted-by":"publisher","first-page":"2036","DOI":"10.4161\/auto.34398","volume":"10","author":"M Cicchini","year":"2014","unstructured":"Cicchini, M. et al. Autophagy regulator BECN1 suppresses mammary tumorigenesis driven by Wnt1 activation and following parity. Autophagy 10, 2036\u20132052 (2014).","journal-title":"Autophagy"},{"key":"1554_CR3","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1038\/45257","volume":"402","author":"XH Liang","year":"1999","unstructured":"Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by Beclin 1. Nature 402, 672\u2013676 (1999).","journal-title":"Nature"},{"key":"1554_CR4","doi-asserted-by":"publisher","first-page":"1809","DOI":"10.1172\/JCI20039","volume":"112","author":"X Qu","year":"2003","unstructured":"Qu, X. et al. Promotion of tumorigenesis by heterozygous disruption of the Beclin 1 autophagy gene. J. Clin. Invest. 112, 1809\u20131820 (2003).","journal-title":"J. Clin. Invest."},{"key":"1554_CR5","doi-asserted-by":"publisher","first-page":"15077","DOI":"10.1073\/pnas.2436255100","volume":"100","author":"Z Yue","year":"2003","unstructured":"Yue, Z., Jin, S., Yang, C., Levine, A. J. & Heintz, N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl Acad. Sci. USA 100, 15077\u201315082 (2003).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1554_CR6","doi-asserted-by":"publisher","first-page":"717","DOI":"10.1101\/gad.2016111","volume":"25","author":"S Yang","year":"2011","unstructured":"Yang, S. et al. Pancreatic cancers require autophagy for tumor growth. Genes Dev. 25, 717\u2013729 (2011).","journal-title":"Genes Dev."},{"key":"1554_CR7","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1101\/gad.2016311","volume":"25","author":"JY Guo","year":"2011","unstructured":"Guo, J. Y. et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 25, 460\u2013470 (2011).","journal-title":"Genes Dev."},{"key":"1554_CR8","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1091\/mbc.e10-06-0500","volume":"22","author":"R Lock","year":"2011","unstructured":"Lock, R. et al. Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation. Mol. Biol. Cell 22, 165\u2013178 (2011).","journal-title":"Mol. Biol. Cell"},{"key":"1554_CR9","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.tcb.2014.09.001","volume":"25","author":"CM Kenific","year":"2015","unstructured":"Kenific, C. M. & Debnath, J. Cellular and metabolic functions for autophagy in cancer cells. Trends Cell Biol. 25, 37\u201345 (2015).","journal-title":"Trends Cell Biol."},{"key":"1554_CR10","doi-asserted-by":"publisher","first-page":"856","DOI":"10.15252\/embj.201490784","volume":"34","author":"L Galluzzi","year":"2015","unstructured":"Galluzzi, L. et al. Autophagy in malignant transformation and cancer progression. EMBO J. 34, 856\u2013880 (2015).","journal-title":"EMBO J."},{"key":"1554_CR11","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1083\/jcb.200804140","volume":"183","author":"PT Caswell","year":"2008","unstructured":"Caswell, P. T. et al. Rab-coupling protein coordinates recycling of \u03b15\u03b21 integrin and EGFR1 to promote cell migration in 3D microenvironments. J. Cell Biol. 183, 143\u2013155 (2008).","journal-title":"J. Cell Biol."},{"key":"1554_CR12","doi-asserted-by":"publisher","first-page":"3317","DOI":"10.4161\/cc.26298","volume":"12","author":"V Tuloup-Minguez","year":"2013","unstructured":"Tuloup-Minguez, V. et al. Autophagy modulates cell migration and \u03b21 integrin membrane recycling. Cell Cycle 12, 3317\u20133328 (2013).","journal-title":"Cell Cycle"},{"key":"1554_CR13","doi-asserted-by":"publisher","first-page":"646","DOI":"10.1158\/0008-5472.CAN-15-3458","volume":"77","author":"CM Dower","year":"2017","unstructured":"Dower, C. M., Bhat, N., Wang, E. W. & Wang, H. G. Selective reversible inhibition of autophagy in hypoxic breast cancer cells promotes pulmonary metastasis. Cancer Res. 77, 646\u2013657 (2017).","journal-title":"Cancer Res."},{"key":"1554_CR14","doi-asserted-by":"publisher","first-page":"e56006","DOI":"10.7554\/eLife.56006","volume":"9","author":"C Bressan","year":"2020","unstructured":"Bressan, C. et al. The dynamic interplay between ATP\/ADP levels and autophagy sustain neuronal migration in vivo. eLife 9, e56006 (2020).","journal-title":"eLife"},{"key":"1554_CR15","doi-asserted-by":"publisher","first-page":"1660","DOI":"10.1016\/j.celrep.2016.04.065","volume":"15","author":"MN Sharifi","year":"2016","unstructured":"Sharifi, M. N. et al. Autophagy promotes focal adhesion disassembly and cell motility of metastatic tumor cells through the direct interaction of paxillin with LC3. Cell Rep. 15, 1660\u20131672 (2016).","journal-title":"Cell Rep."},{"key":"1554_CR16","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1083\/jcb.201503075","volume":"212","author":"CM Kenific","year":"2016","unstructured":"Kenific, C. M. et al. NBR1 enables autophagy-dependent focal adhesion turnover. J. Cell Biol. 212, 577\u2013590 (2016).","journal-title":"J. Cell Biol."},{"key":"1554_CR17","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-17395-y","volume":"11","author":"ZL Li","year":"2020","unstructured":"Li, Z. L. et al. Autophagy deficiency promotes triple-negative breast cancer resistance to T cell-mediated cytotoxicity by blocking tenascin-C degradation. Nat. Commun. 11, 3806 (2020).","journal-title":"Nat. Commun."},{"key":"1554_CR18","doi-asserted-by":"publisher","first-page":"3011","DOI":"10.1080\/15548627.2020.1850609","volume":"17","author":"R Deng","year":"2021","unstructured":"Deng, R. et al. MAPK1\/3 kinase-dependent ULK1 degradation attenuates mitophagy and promotes breast cancer bone metastasis. Autophagy 17, 3011\u20133029 (2021).","journal-title":"Autophagy"},{"key":"1554_CR19","doi-asserted-by":"publisher","first-page":"40","DOI":"10.1038\/s41420-018-0105-y","volume":"4","author":"A Warri","year":"2018","unstructured":"Warri, A. et al. Autophagy and unfolded protein response (UPR) regulate mammary gland involution by restraining apoptosis-driven irreversible changes. Cell Death Discov. 4, 40 (2018).","journal-title":"Cell Death Discov."},{"key":"1554_CR20","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1080\/15548627.2020.1720427","volume":"17","author":"J Elswood","year":"2021","unstructured":"Elswood, J. et al. Autophagy regulates functional differentiation of mammary epithelial cells. Autophagy 17, 420\u2013438 (2021).","journal-title":"Autophagy"},{"key":"1554_CR21","doi-asserted-by":"publisher","first-page":"1593","DOI":"10.1016\/j.biocel.2007.01.025","volume":"39","author":"G Chinnadurai","year":"2007","unstructured":"Chinnadurai, G. Transcriptional regulation by C-terminal binding proteins. Int. J. Biochem. Cell Biol. 39, 1593\u20131607 (2007).","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"1554_CR22","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1080\/15384047.2017.1323586","volume":"18","author":"MM Dcona","year":"2017","unstructured":"Dcona, M. M., Morris, B. L., Ellis, K. C. & Grossman, S. R. CtBP\u2014an emerging oncogene and novel small molecule drug target: advances in the understanding of its oncogenic action and identification of therapeutic inhibitors. Cancer Biol. Ther. 18, 379\u2013391 (2017).","journal-title":"Cancer Biol. Ther."},{"key":"1554_CR23","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.1110\/ps.062115406","volume":"15","author":"M Nardini","year":"2006","unstructured":"Nardini, M. et al. The C-terminal domain of the transcriptional corepressor CtBP is intrinsically unstructured. Protein Sci. 15, 1042\u20131050 (2006).","journal-title":"Protein Sci."},{"key":"1554_CR24","doi-asserted-by":"publisher","first-page":"msad003","DOI":"10.1093\/molbev\/msad003","volume":"40","author":"AM Raicu","year":"2023","unstructured":"Raicu, A. M. et al. The cynosure of CtBP: evolution of a bilaterian transcriptional corepressor. Mol. Biol. Evol. 40, msad003 (2023).","journal-title":"Mol. Biol. Evol."},{"key":"1554_CR25","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1016\/S1097-2765(02)00443-4","volume":"9","author":"G Chinnadurai","year":"2002","unstructured":"Chinnadurai, G. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol. Cell 9, 213\u2013224 (2002).","journal-title":"Mol. Cell"},{"key":"1554_CR26","doi-asserted-by":"publisher","first-page":"10348","DOI":"10.1128\/JVI.00786-13","volume":"87","author":"MJ Cohen","year":"2013","unstructured":"Cohen, M. J. et al. Dissection of the C-terminal region of E1A redefines the roles of CtBP and other cellular targets in oncogenic transformation. J. Virol. 87, 10348\u201310355 (2013).","journal-title":"J. Virol."},{"key":"1554_CR27","doi-asserted-by":"publisher","DOI":"10.1038\/s41389-019-0163-x","volume":"8","author":"AT Chawla","year":"2019","unstructured":"Chawla, A. T. et al. CtBP\u2014a targetable dependency for tumor-initiating cell activity and metastasis in pancreatic adenocarcinoma. Oncogenesis 8, 55 (2019).","journal-title":"Oncogenesis"},{"key":"1554_CR28","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1136\/gutjnl-2015-310838","volume":"66","author":"O de Barrios","year":"2017","unstructured":"de Barrios, O. et al. ZEB1-induced tumourigenesis requires senescence inhibition via activation of DKK1\/mutant p53\/Mdm2\/CtBP and repression of macroH2A1. Gut 66, 666\u2013682 (2017).","journal-title":"Gut"},{"key":"1554_CR29","doi-asserted-by":"publisher","first-page":"2076","DOI":"10.1038\/s41388-018-0570-z","volume":"38","author":"Z Zhao","year":"2019","unstructured":"Zhao, Z. et al. CtBP promotes metastasis of breast cancer through repressing cholesterol and activating TGF-\u03b2 signaling. Oncogene 38, 2076\u20132091 (2019).","journal-title":"Oncogene"},{"key":"1554_CR30","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.molcel.2015.01.023","volume":"58","author":"K Ichikawa","year":"2015","unstructured":"Ichikawa, K. et al. MCRIP1, an ERK substrate, mediates ERK-induced gene silencing during epithelial-mesenchymal transition by regulating the co-repressor CtBP. Mol. Cell 58, 35\u201346 (2015).","journal-title":"Mol. Cell"},{"key":"1554_CR31","doi-asserted-by":"publisher","first-page":"eaau9529","DOI":"10.1126\/scisignal.aau9529","volume":"13","author":"CN Birts","year":"2020","unstructured":"Birts, C. N. et al. p53 is regulated by aerobic glycolysis in cancer cells by the CtBP family of NADH-dependent transcriptional regulators. Sci. Signal 13, eaau9529 (2020).","journal-title":"Sci. Signal"},{"key":"1554_CR32","first-page":"E819","volume":"112","author":"Q Zhang","year":"2015","unstructured":"Zhang, Q. et al. Retraction for Zhang et al., Metabolic regulation of SIRT1 transcription via a HIC1:CtBP corepressor complex. Proc. Natl Acad. Sci. USA 112, E819 (2015).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1554_CR33","doi-asserted-by":"publisher","first-page":"1382","DOI":"10.1038\/nn1791","volume":"9","author":"M Garriga-Canut","year":"2006","unstructured":"Garriga-Canut, M. et al. 2-Deoxy-d-glucose reduces epilepsy progression by NRSF\u2013CtBP-dependent metabolic regulation of chromatin structure. Nat. Neurosci. 9, 1382\u20131387 (2006).","journal-title":"Nat. Neurosci."},{"key":"1554_CR34","doi-asserted-by":"publisher","DOI":"10.1038\/cddis.2014.587","volume":"6","author":"L Wang","year":"2015","unstructured":"Wang, L., Zhou, H., Wang, Y., Cui, G. & Di, L. J. CtBP maintains cancer cell growth and metabolic homeostasis via regulating SIRT4. Cell Death Dis. 6, e1620 (2015).","journal-title":"Cell Death Dis."},{"key":"1554_CR35","doi-asserted-by":"publisher","DOI":"10.1038\/s41389-018-0036-8","volume":"7","author":"L Wang","year":"2018","unstructured":"Wang, L. et al. Molecular link between glucose and glutamine consumption in cancer cells mediated by CtBP and SIRT4. Oncogenesis 7, 26 (2018).","journal-title":"Oncogenesis"},{"key":"1554_CR36","doi-asserted-by":"publisher","first-page":"3952","DOI":"10.7150\/thno.30814","volume":"9","author":"D Hao","year":"2019","unstructured":"Hao, D. et al. Non-classical estrogen signaling in ovarian cancer improves chemo-sensitivity and patients outcome. Theranostics 9, 3952\u20133965 (2019).","journal-title":"Theranostics"},{"key":"1554_CR37","doi-asserted-by":"publisher","first-page":"2081","DOI":"10.7150\/ijbs.80952","volume":"19","author":"J Li","year":"2023","unstructured":"Li, J. et al. Metabolic modulation of CtBP dimeric status impacts the repression of DNA damage repair genes and the platinum sensitivity of ovarian cancer. Int J. Biol. Sci. 19, 2081\u20132096 (2023).","journal-title":"Int J. Biol. Sci."},{"key":"1554_CR38","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1158\/0008-5472.CAN-14-1561","volume":"75","author":"JB Addison","year":"2015","unstructured":"Addison, J. B. et al. KAP1 promotes proliferation and metastatic progression of breast cancer cells. Cancer Res. 75, 344\u2013355 (2015).","journal-title":"Cancer Res."},{"key":"1554_CR39","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1186\/s12929-017-0374-4","volume":"24","author":"P Czerwinska","year":"2017","unstructured":"Czerwinska, P., Mazurek, S. & Wiznerowicz, M. The complexity of TRIM28 contribution to cancer. J. Biomed. Sci. 24, 63 (2017).","journal-title":"J. Biomed. Sci."},{"key":"1554_CR40","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1016\/j.molcel.2007.11.012","volume":"28","author":"AV Ivanov","year":"2007","unstructured":"Ivanov, A. V. et al. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28, 823\u2013837 (2007).","journal-title":"Mol. Cell"},{"key":"1554_CR41","doi-asserted-by":"publisher","first-page":"902","DOI":"10.1038\/s41418-018-0169-5","volume":"26","author":"L Lionnard","year":"2019","unstructured":"Lionnard, L. et al. TRIM17 and TRIM28 antagonistically regulate the ubiquitination and anti-apoptotic activity of BCL2A1. Cell Death Differ. 26, 902\u2013917 (2019).","journal-title":"Cell Death Differ."},{"key":"1554_CR42","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1016\/j.cell.2015.01.034","volume":"160","author":"CT Pineda","year":"2015","unstructured":"Pineda, C. T. et al. Degradation of AMPK by a cancer-specific ubiquitin ligase. Cell 160, 715\u2013728 (2015).","journal-title":"Cell"},{"key":"1554_CR43","doi-asserted-by":"publisher","first-page":"3279","DOI":"10.1038\/sj.emboj.7600791","volume":"24","author":"C Wang","year":"2005","unstructured":"Wang, C. et al. MDM2 interaction with nuclear corepressor KAP1 contributes to p53 inactivation. EMBO J. 24, 3279\u20133290 (2005).","journal-title":"EMBO J."},{"key":"1554_CR44","doi-asserted-by":"publisher","first-page":"963","DOI":"10.1016\/j.molcel.2010.08.029","volume":"39","author":"JM Doyle","year":"2010","unstructured":"Doyle, J. M., Gao, J., Wang, J., Yang, M. & Potts, P. R. MAGE\u2013RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell 39, 963\u2013974 (2010).","journal-title":"Mol. Cell"},{"key":"1554_CR45","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-05911-0","volume":"9","author":"RK Zwick","year":"2018","unstructured":"Zwick, R. K. et al. Adipocyte hypertrophy and lipid dynamics underlie mammary gland remodeling after lactation. Nat. Commun. 9, 3592 (2018).","journal-title":"Nat. Commun."},{"key":"1554_CR46","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms2438","volume":"4","author":"LJ Di","year":"2013","unstructured":"Di, L. J. et al. Genome-wide profiles of CtBP link metabolism with genome stability and epithelial reprogramming in breast cancer. Nat. Commun. 4, 1449 (2013).","journal-title":"Nat. Commun."},{"key":"1554_CR47","doi-asserted-by":"publisher","first-page":"6841","DOI":"10.1073\/pnas.1217692110","volume":"110","author":"Y Yang","year":"2013","unstructured":"Yang, Y. et al. Acetylated Hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy. Proc. Natl Acad. Sci. USA 110, 6841\u20136846 (2013).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1554_CR48","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1038\/s41580-022-00529-z","volume":"24","author":"L Wang","year":"2023","unstructured":"Wang, L., Klionsky, D. J. & Shen, H.-M. The emerging mechanisms and functions of microautophagy. Nat. Rev. Mol. Cell Biol. 24, 186\u2013203 (2023).","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"1554_CR49","doi-asserted-by":"publisher","first-page":"295","DOI":"10.4161\/auto.4144","volume":"3","author":"JF Dice","year":"2007","unstructured":"Dice, J. F. Chaperone-mediated autophagy. Autophagy 3, 295\u2013299 (2007).","journal-title":"Autophagy"},{"key":"1554_CR50","doi-asserted-by":"publisher","first-page":"2038","DOI":"10.1080\/15548627.2016.1217371","volume":"12","author":"S Devkota","year":"2016","unstructured":"Devkota, S. et al. Functional characterization of EI24-induced autophagy in the degradation of RING-domain E3 ligases. Autophagy 12, 2038\u20132053 (2016).","journal-title":"Autophagy"},{"key":"1554_CR51","doi-asserted-by":"publisher","first-page":"4082","DOI":"10.1016\/j.cell.2022.09.001","volume":"185","author":"Q Zheng","year":"2022","unstructured":"Zheng, Q. et al. Calcium transients on the ER surface trigger liquid-liquid phase separation of FIP200 to specify autophagosome initiation sites. Cell 185, 4082\u20134098 (2022).","journal-title":"Cell"},{"key":"1554_CR52","doi-asserted-by":"publisher","first-page":"1344","DOI":"10.1126\/science.1193497","volume":"330","author":"JD Rabinowitz","year":"2010","unstructured":"Rabinowitz, J. D. & White, E. J. S. Autophagy and metabolism. Science 330, 1344\u20131348 (2010).","journal-title":"Science"},{"key":"1554_CR53","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1016\/j.cell.2008.11.044","volume":"136","author":"P Nicklin","year":"2009","unstructured":"Nicklin, P. et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136, 521\u2013534 (2009).","journal-title":"Cell"},{"key":"1554_CR54","doi-asserted-by":"publisher","first-page":"4794","DOI":"10.1038\/s41467-021-25033-4","volume":"12","author":"Y Qin","year":"2021","unstructured":"Qin, Y. et al. TRIM28 SUMOylates and stabilizes NLRP3 to facilitate inflammasome activation. Nat. Commun. 12, 4794 (2021).","journal-title":"Nat. Commun."},{"key":"1554_CR55","doi-asserted-by":"publisher","first-page":"626","DOI":"10.1038\/nsmb.1416","volume":"15","author":"L Zeng","year":"2008","unstructured":"Zeng, L. et al. Structural insights into human KAP1 PHD finger\u2013bromodomain and its role in gene silencing. Nat. Struct. Mol. Biol. 15, 626\u2013633 (2008).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"1554_CR56","doi-asserted-by":"publisher","first-page":"W325","DOI":"10.1093\/nar\/gku383","volume":"42","author":"Q Zhao","year":"2014","unstructured":"Zhao, Q. et al. GPS-SUMO: a tool for the prediction of sumoylation sites and SUMO-interaction motifs. Nucleic Acids Res. 42, W325\u2013W330 (2014).","journal-title":"Nucleic Acids Res."},{"key":"1554_CR57","doi-asserted-by":"publisher","first-page":"3483","DOI":"10.1093\/bioinformatics\/btv403","volume":"31","author":"G Beauclair","year":"2015","unstructured":"Beauclair, G., Bridier-Nahmias, A., Zagury, J. F., Sa\u00efb, A. & Zamborlini, A. JASSA: a comprehensive tool for prediction of SUMOylation sites and SIMs. Bioinformatics 31, 3483\u20133491 (2015).","journal-title":"Bioinformatics"},{"key":"1554_CR58","doi-asserted-by":"publisher","first-page":"734","DOI":"10.1002\/iub.113","volume":"60","author":"M Drag","year":"2008","unstructured":"Drag, M. & Salvesen, G. S. DeSUMOylating enzymes\u2014SENPs. IUBMB Life 60, 734\u2013742 (2008).","journal-title":"IUBMB Life"},{"key":"1554_CR59","doi-asserted-by":"crossref","unstructured":"Bellesis, A. G., Jecrois, A. M., Hayes, J. A., Schiffer, C. A. & Royer, W. E. Jr Assembly of human C-terminal binding protein (CtBP) into tetramers. J. Biol. Chem. 293, 9101\u20139112 (2018).","DOI":"10.1074\/jbc.RA118.002514"},{"key":"1554_CR60","doi-asserted-by":"publisher","first-page":"1406","DOI":"10.1038\/nsmb.1941","volume":"17","author":"LJ Di","year":"2010","unstructured":"Di, L. J., Fernandez, A. G., De Siervi, A., Longo, D. L. & Gardner, K. Transcriptional regulation of BRCA1 expression by a metabolic switch. Nat. Struct. Mol. Biol. 17, 1406\u20131413 (2010).","journal-title":"Nat. Struct. Mol. Biol."},{"key":"1554_CR61","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1038\/nrc2748","volume":"10","author":"JS Desgrosellier","year":"2010","unstructured":"Desgrosellier, J. S. & Cheresh, D. A. Integrins in cancer: biological implications and therapeutic opportunities. Nat. Rev. Cancer 10, 9\u201322 (2010).","journal-title":"Nat. Rev. Cancer"},{"key":"1554_CR62","doi-asserted-by":"publisher","first-page":"5296","DOI":"10.1128\/MCB.22.15.5296-5307.2002","volume":"22","author":"JD Hildebrand","year":"2002","unstructured":"Hildebrand, J. D. & Soriano, P. Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol. Cell. Biol. 22, 5296\u20135307 (2002).","journal-title":"Mol. Cell. Biol."},{"key":"1554_CR63","doi-asserted-by":"publisher","first-page":"12119","DOI":"10.1073\/pnas.1100160108","volume":"108","author":"Z Xie","year":"2011","unstructured":"Xie, Z. et al. Smad6 promotes neuronal differentiation in the intermediate zone of the dorsal neural tube by inhibition of the Wnt\/\u03b2-catenin pathway. Proc. Natl Acad. Sci. USA 108, 12119\u201312124 (2011).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"1554_CR64","doi-asserted-by":"publisher","first-page":"8549","DOI":"10.1074\/jbc.273.15.8549","volume":"273","author":"U Schaeper","year":"1998","unstructured":"Schaeper, U., Subramanian, T., Lim, L., Boyd, J. M. & Chinnadurai, G. Interaction between a cellular protein that binds to the C-terminal region of adenovirus E1A (CtBP) and a novel cellular protein is disrupted by E1A through a conserved PLDLS motif. J. Biol. Chem. 273, 8549\u20138552 (1998).","journal-title":"J. Biol. Chem."},{"key":"1554_CR65","doi-asserted-by":"publisher","first-page":"6181","DOI":"10.1128\/MCB.21.18.6181-6188.2001","volume":"21","author":"N Vo","year":"2001","unstructured":"Vo, N., Fjeld, C. & Goodman, R. H. Acetylation of nuclear hormone receptor-interacting protein RIP140 regulates binding of the transcriptional corepressor CtBP. Mol. Cell. Biol. 21, 6181\u20136188 (2001).","journal-title":"Mol. Cell. Biol."},{"key":"1554_CR66","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1038\/nature01550","volume":"422","author":"Y Shi","year":"2003","unstructured":"Shi, Y. et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735\u2013738 (2003).","journal-title":"Nature"},{"key":"1554_CR67","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1128\/MCB.01077-07","volume":"28","author":"M Kuppuswamy","year":"2008","unstructured":"Kuppuswamy, M. et al. Role of the PLDLS-binding cleft region of CtBP1 in recruitment of core and auxiliary components of the corepressor complex. Mol. Cell. Biol. 28, 269\u2013281 (2008).","journal-title":"Mol. Cell. Biol."},{"key":"1554_CR68","doi-asserted-by":"publisher","first-page":"623","DOI":"10.1016\/j.cell.2009.02.037","volume":"137","author":"RA Phelps","year":"2009","unstructured":"Phelps, R. A. et al. A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137, 623\u2013634 (2009).","journal-title":"Cell"},{"key":"1554_CR69","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1042\/BC20100067","volume":"103","author":"CN Birts","year":"2010","unstructured":"Birts, C. N. et al. Expression of CtBP family protein isoforms in breast cancer and their role in chemoresistance. Biol. Cell 103, 1\u201319 (2010).","journal-title":"Biol. Cell"},{"key":"1554_CR70","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1038\/s41556-018-0065-8","volume":"20","author":"J Cai","year":"2018","unstructured":"Cai, J. et al. CK1\u03b1 suppresses lung tumour growth by stabilizing PTEN and inducing autophagy. Nat. Cell Biol. 20, 465\u2013478 (2018).","journal-title":"Nat. Cell Biol."},{"key":"1554_CR71","doi-asserted-by":"publisher","first-page":"e113987","DOI":"10.15252\/embj.2023113987","volume":"42","author":"K Nikolatou","year":"2023","unstructured":"Nikolatou, K. et al. PTEN deficiency exposes a requirement for an ARF GTPase module for integrin-dependent invasion in ovarian cancer. EMBO J. 42, e113987 (2023).","journal-title":"EMBO J."},{"key":"1554_CR72","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1038\/nrm3332","volume":"13","author":"VW Hsu","year":"2012","unstructured":"Hsu, V. W., Bai, M. & Li, J. Getting active: protein sorting in endocytic recycling. Nat. Rev. Mol. Cell Biol. 13, 323\u2013328 (2012).","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"1554_CR73","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1038\/ncb2501","volume":"14","author":"RT Bottcher","year":"2012","unstructured":"Bottcher, R. T. et al. Sorting nexin 17 prevents lysosomal degradation of \u03b21 integrins by binding to the \u03b21-integrin tail. Nat. Cell Biol. 14, 584\u2013592 (2012).","journal-title":"Nat. Cell Biol."},{"key":"1554_CR74","doi-asserted-by":"publisher","first-page":"1554","DOI":"10.1016\/j.cub.2012.06.060","volume":"22","author":"C Margadant","year":"2012","unstructured":"Margadant, C., Kreft, M., de Groot, D. J., Norman, J. C. & Sonnenberg, A. Distinct roles of talin and kindlin in regulating integrin \u03b15\u03b21 function and trafficking. Curr. Biol. 22, 1554\u20131563 (2012).","journal-title":"Curr. Biol."},{"key":"1554_CR75","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1016\/j.bbamcr.2012.11.018","volume":"1833","author":"JM Hyttinen","year":"2013","unstructured":"Hyttinen, J. M., Niittykoski, M., Salminen, A. & Kaarniranta, K. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochim. Biophys. Acta 1833, 503\u2013510 (2013).","journal-title":"Biochim. Biophys. Acta"},{"key":"1554_CR76","doi-asserted-by":"publisher","first-page":"977","DOI":"10.1038\/nmeth979","volume":"3","author":"I Remy","year":"2006","unstructured":"Remy, I. & Michnick, S. W. A highly sensitive protein\u2013protein interaction assay based on Gaussia luciferase. Nat. Methods 3, 977\u2013979 (2006).","journal-title":"Nat. Methods"},{"key":"1554_CR77","doi-asserted-by":"publisher","first-page":"1500","DOI":"10.1074\/mcp.M700166-MCP200","volume":"6","author":"M Jarvius","year":"2007","unstructured":"Jarvius, M. et al. In situ detection of phosphorylated platelet-derived growth factor receptor \u03b2 using a generalized proximity ligation method. Mol. Cell Proteom. 6, 1500\u20131509 (2007).","journal-title":"Mol. Cell Proteom."},{"key":"1554_CR78","doi-asserted-by":"publisher","first-page":"995","DOI":"10.1038\/nmeth947","volume":"3","author":"O S\u00f6derberg","year":"2006","unstructured":"S\u00f6derberg, O. et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995\u20131000 (2006).","journal-title":"Nat. Methods"},{"key":"1554_CR79","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1038\/nmeth.3047","volume":"11","author":"NE Sanjana","year":"2014","unstructured":"Sanjana, N. E., Shalem, O. & Zhang, F. Improved vectors and genome-wide libraries for CRISPR screening. Nat. Methods 11, 783\u2013784 (2014).","journal-title":"Nat. Methods"},{"key":"1554_CR80","first-page":"2828","volume":"53","author":"I Plante","year":"2011","unstructured":"Plante, I., Stewart, M. K. & Laird, D. W. Evaluation of mammary gland development and function in mouse models. J. Vis. Exp. 53, 2828 (2011).","journal-title":"J. Vis. Exp."},{"key":"1554_CR81","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1007\/s11154-021-09633-5","volume":"22","author":"G Colleluori","year":"2021","unstructured":"Colleluori, G., Perugini, J., Barbatelli, G. & Cinti, S. Mammary gland adipocytes in lactation cycle, obesity and breast cancer. Rev. Endocr. Metab. Disord. 22, 241\u2013255 (2021).","journal-title":"Rev. Endocr. Metab. Disord."},{"key":"1554_CR82","doi-asserted-by":"publisher","DOI":"10.1186\/1480-9222-13-4","volume":"13","author":"JN McGinley","year":"2011","unstructured":"McGinley, J. N. & Thompson, H. J. Quantitative assessment of mammary gland density in rodents using digital image analysis. Biol. Proced. Online 13, 4 (2011).","journal-title":"Biol. Proced. Online"},{"key":"1554_CR83","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1080\/01902148.2018.1543368","volume":"44","author":"E Wawryk-Gawda","year":"2018","unstructured":"Wawryk-Gawda, E. et al. CB2R agonist prevents nicotine induced lung fibrosis. Exp. Lung Res. 44, 344\u2013351 (2018).","journal-title":"Exp. Lung Res."},{"key":"1554_CR84","doi-asserted-by":"publisher","first-page":"1159","DOI":"10.1038\/s41556-018-0198-9","volume":"20","author":"L Fort","year":"2018","unstructured":"Fort, L. et al. Fam49\/CYRI interacts with Rac1 and locally suppresses protrusions. Nat. Cell Biol. 20, 1159\u20131171 (2018).","journal-title":"Nat. Cell Biol."},{"key":"1554_CR85","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-12412-1","volume":"10","author":"I Godet","year":"2019","unstructured":"Godet, I. et al. Fate-mapping post-hypoxic tumor cells reveals a ROS-resistant phenotype that promotes metastasis. Nat. Commun. 10, 4862 (2019).","journal-title":"Nat. Commun."},{"key":"1554_CR86","doi-asserted-by":"publisher","first-page":"eabb1307","DOI":"10.1126\/sciadv.abb1307","volume":"6","author":"F Niu","year":"2020","unstructured":"Niu, F., Sun, K., Wei, W., Yu, C. & Wei, Z. F-actin disassembly factor MICAL1 binding to myosin Va mediates cargo unloading during cytokinesis. Sci. Adv. 6, eabb1307 (2020).","journal-title":"Sci. Adv."}],"container-title":["Nature Structural & Molecular Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41594-025-01554-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41594-025-01554-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41594-025-01554-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,6]],"date-time":"2025-09-06T16:55:48Z","timestamp":1757177748000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41594-025-01554-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,15]]},"references-count":86,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2025,8]]}},"alternative-id":["1554"],"URL":"https:\/\/doi.org\/10.1038\/s41594-025-01554-0","relation":{},"ISSN":["1545-9993","1545-9985"],"issn-type":[{"value":"1545-9993","type":"print"},{"value":"1545-9985","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,15]]},"assertion":[{"value":"7 December 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 April 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 May 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}